Autologous versus allogeneic hematopoietic stem cell transplantation
Autologous and allogeneic hematopoietic stem cell transplantation (HSCT) have some common and some clearly distinct goals. Both permit the application of high dose chemo-radiotherapy up to the dose limiting extramedullary toxicity; allogeneic HSCT in addition can replace a diseased host hematopoiesis, including the immune system, with a healthy donor hemopoiesis. In the case of an autoimmune disease, the necessary goal to be achieved still remains a matter of debate. High dose immunoablation can reset ontogenesis of the immune system in animal models of experimental encephalomyelitis as well as in clinical HSCT for multiple sclerosis in humans. In view of its significantly lower transplant-related mortality, autologous HSCT currently remains the preferred choice in clinical studies.
Hematopoietic stem cell transplantation (HSCT) has become the treatment of choice for many patients with severe congenital or acquired malignant or non-malignant disorders of the hematopoietic system, and for chemo-, radio-, or immuno-sensitive malignancies [1, 2]. Experimental animal studies, incidental reports from patients with HSCT for another indication but concomitant autoimmune disorders, and results from pilot studies have documented that complete remissions can be obtained in situations of severe treatment-refractory autoimmune disorders [3-6]. Animal data give clear indications that some forms of congenital autoimmune diseases can only be cured by allogeneic HSCT. Other forms of animal autoimmune diseases, considered as acquired immune disorders can just as clearly be cured by autologous HSCT alone [4, 5]. The situation is less clear in humans. Generally, autoimmune disorders in humans are considered to be induced by three independent components: a) inherited factors such as certain defined HLA-antigens, b) environmental factors such as smoking in rheumatoid arthritis and, c) chance phenomena [7].
These considerations make it clear that autologous HSCT cannot eradicate the congenital factor; it might, however, be sufficient to control the inflammatory component that was induced by chance through environmental factors in an individual patient. As such, the situation in autoimmune disorders is not so much different from the case of clonally aberrant lymphoid reactions in patients with lymphoid malignancies. In some of these high dose chemotherapy is sufficient for control of the disease; in others, an allogeneic healthy novel immune system might be required. These concepts were already well known more than ten years ago, when the European Group for Blood and Marrow Transplantation (EBMT) and the European League Against Rheumatism (EULAR) released a joint statement on the potential use of HSCT for treatment of patients with severe autoimmune disorders: the disease should be severe enough to justify the risk, the disease should not be so advanced not to permit clinical benefit for the patient, autologous HSCT should be the preferred choice, and standard techniques should be used [6, 9].
This view has not changed since. The experience from more than 200,000 HSCT procedures worldwide give some clear indications as to the potential benefits and risks of both allogeneic and autologous HSCT. Allogeneic HSCT is always linked with immunological complications, graft rejection (Host-versus-Graft reaction; HvG) and the reverse, rejection of the recipient by the immunocompetent transplanted immune system (Graft-versus-Host disease; GvHD). Furthermore, time to recovery of complete immuno-competence is considerably longer in allogeneic HSCT than in autologous HSCT. The reasons for this delayed immune recovery are probably manifold: donor-host interaction is required for competent immune response, and immunosuppression is needed to suppress both HvG reaction and GvHD. This combined and prolonged immuno-incompetence is associated with a prolonged higher risk for bacterial, fungal, viral, and parasitic infections in allogeneic, compared to autologous HSCT. For these reasons, allogeneic HSCT is associated with higher transplant related mortality (TRM) in the early as well as in the late post-transplantation period. As a benefit, allogeneic HSCT is devoid of malignant (in the case of HSCT for a malignant disease) or autoreactive (in the case of autoimmune disease) stem, precursor, or effector cells. The risk of relapse is significantly higher after autologous HSCT in all disease categories examined. The net balance of benefit and detrimental effects between autologous and allogeneic HSCT is not easy to assess. It can be very clear in some congenital or high-risk malignancies. In others, years may elapse until the beneficial effects of reduced relapse become higher than the early years of life lost after allogeneic HSCT. Overall, the best results are always obtained with syngeneic HSCT; if there is a syngeneic donor, HSCT is the preferred choice. This is true despite the fact that syngeneic twins possess an inherent risk of developing the same disease as their twin. This disease concordance for twins has clearly been shown in autoimmune disorders and in hematological malignancies [1, 10, 11].
The discordant effects of major histocompatibility antigens holds true as well for minor histocompatibility antigens (mHAg). This has been shown for the H-Y encoded mHAg. Male stem cells are more likely to be rejected by female recipients; female donors are more likely to induce more GvHD in male recipients. The detrimental effects of increased TRM in the female donor-male recipient situation never outweigh the benefits of a reduced relapse rate. Hence it is unlikely that beneficial allogeneic effects, whatever their mechanism, will outweigh the negative impact [12]. The situation in severe autoimmune disorders is even more complicated than after allogeneic HSCT for a malignancy. Some clinical features of chronic GvHD are indistinguishable from some autoimmune disorders [13]. Specifically, chronic GvHD was first described based on its resemblance with Sjögren’s syndrome, systemic sclerosis, or primary biliary cirrhosis [14]. Last but not least, late altered immunity has recently been described as a new late effect after allogeneic HSCT [15]. This syndrome includes some clinical and laboratory aspects of autoimmunity.
The introduction of reduced intensity conditioning transplants (RIC HSCT) has revolutionized clinical HSCT, expanded HSCT to patients with co-morbidities, and has abolished age limits [16]. It has also created big expectations that RIC HSCT might favor the clinical applicability of allogeneic HSCT for patients with severe autoimmune disorders. Indeed, RIC HSCT was recommended via a joint statement on allogeneic HSCT by an international panel [17]. However, experience over the last ten years with RIC HSCT for hematological malignancies does not support such expectations. Explanations are simple. The main reasons for death after an allogeneic HSCT are relapse, immunological complications (HvG and GvHD), infectious complications, and the toxicity of the conditioning regimen.
Conditioning regimens
The contribution to toxicity of the conditioning regimen is therefore just about one quarter of all toxicity. Earlier experience had clearly shown that increased conditioning intensity could reduce relapse risk, but only at the expense of higher TRM. The reverse is now the case. Reduced conditioning can reduce deaths from toxicity of the conditioning; it cannot reduce the risk of immunological complications. It does so at the expense of an increased relapse rate. The net benefit is in favor of the RIC HSCT early on, e.g., at day 100. It is lost at five-year follow up. RIC HSCT does not alter the inherent risk of the key pre-transplant patient factors as established by the EBMT risk score: age of the patient, disease stage, time interval from diagnosis to transplant, donor type, and donor recipient gender combination [11].
In summary, all current available information suggests that autologous HSCT should remain the standard approach to clinical HSCT for patients with severe autoimmune disorders including multiple sclerosis [18]. Syngeneic twin donors, if they exist, are preferred. Allogeneic HSCT can be discussed in rare patients with specific features that they are likely to benefit more, e.g., young patients with no co-morbidities and hematological autoimmune cytopenias [19].
References
1. Copelan EA. Hematopoietic stem-cell transplantation. N Engl J Med. 2006;27:1813-26. pmid: 16641398.
2. Gratwohl A, Baldomero H, Aljurf M, et al. Hematopoietic stem cell transplantation: a global perspective. JAMA. 2010;303:1617-24. pmid: 20424252.
5. Van Bekkum DW. Stem cell transplantation for autoimmune disorders. Preclinical experiments. Best Pract Res Clin Haematol. 2004;17:201-22. doi: 10.1016/j.beha.2004.04.003.
7. Davidson A, Diamond B. Autoimmune diseases. N Engl J Med. 2001;345:340-50. pmid: 11484692.
8. Ringdén O, Karlsson H, Olsson R, Omazic B, Uhlin M. The allogeneic graft-versus-cancer effect. Br J Haematol. 2009;147:614-33. doi: 10.1111/j.1365-2141.2009.07886.x.
9. Marmont A, Tyndall A, Gratwohl A, Vischer T. Haemopoietic precursor-cell transplants for autoimmune diseases. Lancet. 1995;345:978.
10. Gratwohl A. Risk assessment in haematopoietic stem cell transplantation. Best Pract Res Clin Haematol. 2007;20:119-124. doi: 10.1016/j.beha.2006.10.011.
11. Gratwohl A, Stern M, Brand R et al. Risk score for outcome after alloge¬neic hematopoietic stem cell transplantation: a Retrospective Analysis. Cancer. 2009;115:4715-26. doi: 10.1002/cncr.24531.
13. Filipovich AH, Weisdorf D, Pavletic S, et al. National Institutes of Health consensus development project on criteria for clinical trials in chronic graft-versus-host disease: I. Diagnosis and staging working group report. Biol Blood Marrow Transplant. 2005;11:945-56.
14. Gratwohl AA, Moutsopoulos HM, Chused TM, Akizuki M, Wolf RO, Sweet JB, Deisseroth AB. Sjögren-type syndrome after allogeneic bone-marrow transplantation. Ann Intern Med. 1977;87:703-6. pmid: 22306.
16. Bacigalupo A, Ballen K, Rizzo D, Giralt S, Lazarus H, Ho V, Apperley J, Slavin S, Pasquini M, Sandmaier BM, Barrett J, Blaise D, Lowski R, Horowitz M. Defining the intensity of conditioning regimens: working definitions. Biol Blood Marrow Transplant. 2009;15:1628-33. doi: 10.1016/j.bbmt.2009.07.004.
18. Farge D, Labopin M, Tyndall A, et al. Autologous hematopoietic stem cell transplantation for autoimmune diseases: an observational study on 12 years' experience from the European Group for Blood and Marrow Transplantation Working Party on Autoimmune Diseases. Haematologica. 2010;95:284-92.
19. Daikeler T, Hügle T, Farge D, et al. Allogeneic hematopoietic SCT for patients with autoimmune diseases. Bone Marrow Transplant. 2009;44:27-33. doi:10.1038/bmt.2008.424.
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Autologous and allogeneic hematopoietic stem cell transplantation (HSCT) have some common and some clearly distinct goals. Both permit the application of high dose chemo-radiotherapy up to the dose limiting extramedullary toxicity; allogeneic HSCT in addition can replace a diseased host hematopoiesis, including the immune system, with a healthy donor hemopoiesis. In the case of an autoimmune disease, the necessary goal to be achieved still remains a matter of debate. High dose immunoablation can reset ontogenesis of the immune system in animal models of experimental encephalomyelitis as well as in clinical HSCT for multiple sclerosis in humans. In view of its significantly lower transplant-related mortality, autologous HSCT currently remains the preferred choice in clinical studies.
Hematopoietic stem cell transplantation (HSCT) has become the treatment of choice for many patients with severe congenital or acquired malignant or non-malignant disorders of the hematopoietic system, and for chemo-, radio-, or immuno-sensitive malignancies [1, 2]. Experimental animal studies, incidental reports from patients with HSCT for another indication but concomitant autoimmune disorders, and results from pilot studies have documented that complete remissions can be obtained in situations of severe treatment-refractory autoimmune disorders [3-6]. Animal data give clear indications that some forms of congenital autoimmune diseases can only be cured by allogeneic HSCT. Other forms of animal autoimmune diseases, considered as acquired immune disorders can just as clearly be cured by autologous HSCT alone [4, 5]. The situation is less clear in humans. Generally, autoimmune disorders in humans are considered to be induced by three independent components: a) inherited factors such as certain defined HLA-antigens, b) environmental factors such as smoking in rheumatoid arthritis and, c) chance phenomena [7].
These considerations make it clear that autologous HSCT cannot eradicate the congenital factor; it might, however, be sufficient to control the inflammatory component that was induced by chance through environmental factors in an individual patient. As such, the situation in autoimmune disorders is not so much different from the case of clonally aberrant lymphoid reactions in patients with lymphoid malignancies. In some of these high dose chemotherapy is sufficient for control of the disease; in others, an allogeneic healthy novel immune system might be required. These concepts were already well known more than ten years ago, when the European Group for Blood and Marrow Transplantation (EBMT) and the European League Against Rheumatism (EULAR) released a joint statement on the potential use of HSCT for treatment of patients with severe autoimmune disorders: the disease should be severe enough to justify the risk, the disease should not be so advanced not to permit clinical benefit for the patient, autologous HSCT should be the preferred choice, and standard techniques should be used [6, 9].
This view has not changed since. The experience from more than 200,000 HSCT procedures worldwide give some clear indications as to the potential benefits and risks of both allogeneic and autologous HSCT. Allogeneic HSCT is always linked with immunological complications, graft rejection (Host-versus-Graft reaction; HvG) and the reverse, rejection of the recipient by the immunocompetent transplanted immune system (Graft-versus-Host disease; GvHD). Furthermore, time to recovery of complete immuno-competence is considerably longer in allogeneic HSCT than in autologous HSCT. The reasons for this delayed immune recovery are probably manifold: donor-host interaction is required for competent immune response, and immunosuppression is needed to suppress both HvG reaction and GvHD. This combined and prolonged immuno-incompetence is associated with a prolonged higher risk for bacterial, fungal, viral, and parasitic infections in allogeneic, compared to autologous HSCT. For these reasons, allogeneic HSCT is associated with higher transplant related mortality (TRM) in the early as well as in the late post-transplantation period. As a benefit, allogeneic HSCT is devoid of malignant (in the case of HSCT for a malignant disease) or autoreactive (in the case of autoimmune disease) stem, precursor, or effector cells. The risk of relapse is significantly higher after autologous HSCT in all disease categories examined. The net balance of benefit and detrimental effects between autologous and allogeneic HSCT is not easy to assess. It can be very clear in some congenital or high-risk malignancies. In others, years may elapse until the beneficial effects of reduced relapse become higher than the early years of life lost after allogeneic HSCT. Overall, the best results are always obtained with syngeneic HSCT; if there is a syngeneic donor, HSCT is the preferred choice. This is true despite the fact that syngeneic twins possess an inherent risk of developing the same disease as their twin. This disease concordance for twins has clearly been shown in autoimmune disorders and in hematological malignancies [1, 10, 11].
The discordant effects of major histocompatibility antigens holds true as well for minor histocompatibility antigens (mHAg). This has been shown for the H-Y encoded mHAg. Male stem cells are more likely to be rejected by female recipients; female donors are more likely to induce more GvHD in male recipients. The detrimental effects of increased TRM in the female donor-male recipient situation never outweigh the benefits of a reduced relapse rate. Hence it is unlikely that beneficial allogeneic effects, whatever their mechanism, will outweigh the negative impact [12]. The situation in severe autoimmune disorders is even more complicated than after allogeneic HSCT for a malignancy. Some clinical features of chronic GvHD are indistinguishable from some autoimmune disorders [13]. Specifically, chronic GvHD was first described based on its resemblance with Sjögren’s syndrome, systemic sclerosis, or primary biliary cirrhosis [14]. Last but not least, late altered immunity has recently been described as a new late effect after allogeneic HSCT [15]. This syndrome includes some clinical and laboratory aspects of autoimmunity.
The introduction of reduced intensity conditioning transplants (RIC HSCT) has revolutionized clinical HSCT, expanded HSCT to patients with co-morbidities, and has abolished age limits [16]. It has also created big expectations that RIC HSCT might favor the clinical applicability of allogeneic HSCT for patients with severe autoimmune disorders. Indeed, RIC HSCT was recommended via a joint statement on allogeneic HSCT by an international panel [17]. However, experience over the last ten years with RIC HSCT for hematological malignancies does not support such expectations. Explanations are simple. The main reasons for death after an allogeneic HSCT are relapse, immunological complications (HvG and GvHD), infectious complications, and the toxicity of the conditioning regimen.
Conditioning regimens
The contribution to toxicity of the conditioning regimen is therefore just about one quarter of all toxicity. Earlier experience had clearly shown that increased conditioning intensity could reduce relapse risk, but only at the expense of higher TRM. The reverse is now the case. Reduced conditioning can reduce deaths from toxicity of the conditioning; it cannot reduce the risk of immunological complications. It does so at the expense of an increased relapse rate. The net benefit is in favor of the RIC HSCT early on, e.g., at day 100. It is lost at five-year follow up. RIC HSCT does not alter the inherent risk of the key pre-transplant patient factors as established by the EBMT risk score: age of the patient, disease stage, time interval from diagnosis to transplant, donor type, and donor recipient gender combination [11].
In summary, all current available information suggests that autologous HSCT should remain the standard approach to clinical HSCT for patients with severe autoimmune disorders including multiple sclerosis [18]. Syngeneic twin donors, if they exist, are preferred. Allogeneic HSCT can be discussed in rare patients with specific features that they are likely to benefit more, e.g., young patients with no co-morbidities and hematological autoimmune cytopenias [19].
References
1. Copelan EA. Hematopoietic stem-cell transplantation. N Engl J Med. 2006;27:1813-26. pmid: 16641398.
2. Gratwohl A, Baldomero H, Aljurf M, et al. Hematopoietic stem cell transplantation: a global perspective. JAMA. 2010;303:1617-24. pmid: 20424252.
5. Van Bekkum DW. Stem cell transplantation for autoimmune disorders. Preclinical experiments. Best Pract Res Clin Haematol. 2004;17:201-22. doi: 10.1016/j.beha.2004.04.003.
7. Davidson A, Diamond B. Autoimmune diseases. N Engl J Med. 2001;345:340-50. pmid: 11484692.
8. Ringdén O, Karlsson H, Olsson R, Omazic B, Uhlin M. The allogeneic graft-versus-cancer effect. Br J Haematol. 2009;147:614-33. doi: 10.1111/j.1365-2141.2009.07886.x.
9. Marmont A, Tyndall A, Gratwohl A, Vischer T. Haemopoietic precursor-cell transplants for autoimmune diseases. Lancet. 1995;345:978.
10. Gratwohl A. Risk assessment in haematopoietic stem cell transplantation. Best Pract Res Clin Haematol. 2007;20:119-124. doi: 10.1016/j.beha.2006.10.011.
11. Gratwohl A, Stern M, Brand R et al. Risk score for outcome after alloge¬neic hematopoietic stem cell transplantation: a Retrospective Analysis. Cancer. 2009;115:4715-26. doi: 10.1002/cncr.24531.
13. Filipovich AH, Weisdorf D, Pavletic S, et al. National Institutes of Health consensus development project on criteria for clinical trials in chronic graft-versus-host disease: I. Diagnosis and staging working group report. Biol Blood Marrow Transplant. 2005;11:945-56.
14. Gratwohl AA, Moutsopoulos HM, Chused TM, Akizuki M, Wolf RO, Sweet JB, Deisseroth AB. Sjögren-type syndrome after allogeneic bone-marrow transplantation. Ann Intern Med. 1977;87:703-6. pmid: 22306.
16. Bacigalupo A, Ballen K, Rizzo D, Giralt S, Lazarus H, Ho V, Apperley J, Slavin S, Pasquini M, Sandmaier BM, Barrett J, Blaise D, Lowski R, Horowitz M. Defining the intensity of conditioning regimens: working definitions. Biol Blood Marrow Transplant. 2009;15:1628-33. doi: 10.1016/j.bbmt.2009.07.004.
18. Farge D, Labopin M, Tyndall A, et al. Autologous hematopoietic stem cell transplantation for autoimmune diseases: an observational study on 12 years' experience from the European Group for Blood and Marrow Transplantation Working Party on Autoimmune Diseases. Haematologica. 2010;95:284-92.
19. Daikeler T, Hügle T, Farge D, et al. Allogeneic hematopoietic SCT for patients with autoimmune diseases. Bone Marrow Transplant. 2009;44:27-33. doi:10.1038/bmt.2008.424.
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Вся имеющаяся в настоящее время информация предполагает, что аутологичные ТГСК должны оставаться стандартным подходом в клинической трансплантации для лечения больных с тяжелыми аутоиммунными заболеваниями, в том числе – при рассеянном склерозе. Выбор в пользу аллогенных ТГСК должен рассматриваться у немногих больных с особыми характеристиками, при которых, возможно, выгоднее использовать аллогенную ТГСК, например, для молодых пациентов без сопутствующих заболеваний и гематологических аутоиммунных цитопений.
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High-dose immunosuppressive therapy with hemopoietic stem cell transplantation (HSCT) was already introduced into the management of multiple sclerosis (MS) in 1995 [8]. The method was based on the concept of an immunological “renewal” after (near)-complete eradication of the aberrant immune system responsible for the development of the disease. Experimental hemopoietic transplants in an animal model of MS, experimental autoimmune encephalomyelitis (EAE), performed in Israel and in the Netherlands, showed that the induction of profound and long-lasting immunosuppression followed by allogeneic or syngeneic or (pseudo)-autologous HSCT can actually have a beneficial impact on the course of EAE [3]. At that time, there was a need for new effective treatments for MS; in particular for the rapidly progressing, therapy-resistant cases, as the results of the existing standard therapies, namely interferon-beta and glatiramer acetate, were rather moderate to poor and their effect on the progression of disability was only marginal.
In order to eradicate the immune system and in view of the lack of a purely immunotoxic regimen, the proposal was for MS patients to be treated with high-dose chemotherapeutic agents (carmustin/ etoposide/ araC/ melphalan or busulfan/ cyclophosphamide) or total body irradiation (TBI), in the way patients with lymphoma or leukemia are conditioned for HSCT. To rescue the patient, autologous grafts were used, purged of T cells or CD34+ cell-selected. These were harvested from peripheral blood stem cells mobilized by cyclophosphamide plus G-CSF prior to HSCT. Intravenous anti-lymphocyte globulins (ALG, ATG) were also administered in the peri-transplant period in order to further eradicate any auto-reactive lymphocytes surviving the conditioning regimen or re-infused with the autologous graft. The “debulking” of autoreactive clones followed by reconstitution of the immune system in the presence of auto-antigens was speculated to bring about, apart from the abrogation of inflammation, qualitative changes as well, which might induce a degree of self-tolerance.
Since 1995, a number of centers in the European Union, Russia, Israel, China, USA, Canada, and Latin America have reported their experience in treating progressing, mainly advanced-stage and standard-therapy-resistant MS with high-dose immunosuppression and HSCT [9]. It is estimated that more than 400 patients have so far been treated worldwide, and favorable results have been reported with certain spectacular and long-lasting beneficial outcomes. However, after fourteen years of experience, the number of centers performing HSCT for MS still remains limited and few patients are referred for this kind treatment, which has not yet been accepted as an established therapy for aggressive MS because the neurological communities have constantly kept a skeptical attitude towards it. The reason lies mainly in the toxic complications of HSCT, especially in the risk of mortality associated with the procedure, which may be elevated in improperly selected patients [25]. This attitude has, unfortunately, prevented the accomplishment of comparative studies that were initiated in Europe (ASTIMS) and the USA (MIST, HALTMS) [11] some years ago and have not yet been finalized. In the meantime, other therapies emerged that were claimed to give good results in MS, e.g., mitoxantrone, alemtuzumab, rituximab, and natalizumab.
HSCT has been shown to be a most powerful immunosuppressive and anti-inflammatory treatment. Since 2000, all communications have consistently reported a dramatic, almost 100%, reduction in, or disappearance of, disease activity (inflammation) on magnetic resonance imaging (MRI) which is retained with time and has not been observed as an outcome of any other MS treatment [16, 26, 10, 23]. Also, brain atrophy, which seems to continue after HSCT as a result of edema resolution, slows down after the 2nd post-HSCT year [22, 12]. Consequently, patients with a lot of inflammation in the CNS experience substantial improvement of their disability status. On the other hand, patients with long-standing disease and those with primary progressive MS, i.e., cases in which the neurodegenerative component of the disease prevails, may not respond to HSCT [4]. This has been detected clinically and also in histopathological examinations of autopsy material, which show ongoing demyelination and axonal damage despite marked suppression of inflammation [19].
With regard to the clinical results of HSCT, it must first be noted that the great majority of the patient series treated worldwide had advanced disease with median EDSS scores of 6 to 6.5, while about 20% of the patients had primary progressive MS. All patients had evidence of disease progression over the twelve months preceding HSCT and/or gadolinium-enhancing lesions in MRI. After HSCT, improvement of disability scores by 1 to 4 steps was observed with a great reduction in the yearly relapse rate and a probability of disease progression-free survival (PFS) of 60–80% at three years [9, 25, 11, 10, 18]. At 10 years post-HSCT, PFS was around 65% for secondary and 40% for primary progressive MS (Fassas, unpublished data). Moreover, the patients’ quality of life and the physical and mental health have also been reported to improve [24]. The most dramatic effect, however, was seen in the so-called “malignant” cases of MS, which have a devastating course unresponsive to any standard therapy. In such cases, HSCT has been shown to be life-saving, with meaningful clinical improvement and long-standing disease stabilization [17, 14, 21, 15, 7].
From the immunological point of view, the effects of HSCT, especially the long-term ones on disease stabilization or on reduction in activity, do not seem to derive only from the immunosuppressive effect of the conditioning regimen, i.e., the “debulking” of auto-reactive clones, because MBP-recognizing T cells usually reappear within a year after HSCT [27, 6]. Immunological studies have shown that the speculated immunological remodulation can actually become a fact after HSCT. Expansion of naive CD4+ cells of thymic origin, decrease of memory T cells, reconstitution of broad clonal diversity, and renewal of clonal specificities have been described to occur after HSCT using high-intensity conditioning regimens (e.g. busulfan 16mg/kg.b.wt. or TBI) [20]. These changes may possibly create tolerance or tip the immunological balance towards suppression of autoimmunity and explain the long-standing beneficial effects of HSCT. Recently, there has been a tendency to use “light” conditioning regimens, e.g., cyclophosphamide 200mg/k.b.wt. plus alemtuzumab or ATG in order to diminish the procedure-related mortality risk. Low-intensity conditioning regimens are, too, capable of inducing immune changes, like the renewal of the balance between CD4+25+FoxP3 regulatory and other T cells or like the deviation of a proinflammatory phenotype of autoimmune cells to a tolerant one [2, 1]. There seems to be a difference in the kind of immune reconstitution brought about by the two types of conditioning, high and low, and we still do not know whether this difference might have the same or a different (better or worse) impact on the clinical outcome. It has been reported, however, that, although “light” conditioning regimens do have less toxicity, they are also associated with more autoimmune relapse after HSCT, compared to “strong” regimens [5, 13]. The regimen of cyclophosphamide plus ATG is less toxic than others but does not appear to have the same good impact on MRI compared to the intermediate-intensity BEAM (carmustine/ etoposide/ araC/ melphalan) [18]. The number of relapses after HSCT with cyclophosphamide plus alemtuzumab or ATG appears somewhat elevated [5], and it is still too early to conclude on the long-term effects on disease progression.
HSCT is a toxic treatment with a variety of complications depending on the intensity of the conditioning regimen [9, 25]. Although a patient may undergo HSCT without any problems, it not unusual for infections, organ damage, and transient neurological worsening to develop during the early post-transplant period. Secondary autoimmune phenomena may also appear late after HSCT. In the two EBMT reports of 2002 and 2006, the procedure-related mortality was 6% in 85 cases [9] and 5.3% in 185 cases [25], respectively. However, the mortality has dropped considerably from 7.3% in transplants before the year 2000 to 1.3% after the year 2000 [18]. This is the result of better patient selection, reserving HSCT for younger, ambulatory, not too-disabled patients, and avoiding the use of too “strong” and too intensive conditioning regimens, i.e., ex-vivo plus in-vivo, and lymphocyte depletion.
In summary, the analyses of the EBMT registry cases have shown that HSCT is active in the inflammatory phases of MS and is capable of slowing down the progression of the disease in relapsing/remitting cases and in patients that have recently entered the secondary progressive phase. Younger patients with low disability scores are more likely to benefit from this therapy. HSCT can be life-saving in desperate cases of very aggressive, rapidly progressing disease, which is refractory to any other therapy. HSCT is not curative, but it may offer prolonged periods of clinical disease stabilization or may change an aggressive disease course. It is not a therapy for the general population of MS patients, as the benefit does not justify the morbidity and mortality risks in cases of already stable disease, in primary progressive or long-standing secondary progressive MS, in cases without gadolinium-positive (inflammatory) lesions on MRI, and in wheelchair-bound patients (EDSS score ≥7) with low performance status and medical co-morbidities. In contrast, the best candidates, in whom the benefit of HSCT outweighs the risks, are young (below 40 years of age), who are still ambulatory, have active and rapidly progressing disease with inflammatory lesions in the CNS, and are in relapsing/remitting or recent secondary progressive phase without much disability. If such MS patients have no accompanying medical co-morbidities precluding transplantation, they may undergo HSCT with a practically zero mortality risk and a good outlook for clinical improvement and/or long disease stability.
It is well known that MS is a very difficult disease in which to show the efficacy of a therapy. Despite the very interesting outcomes of HSCT in treatment of MS, it is only in comparative trials that its superiority over other therapies can be demonstrated. Therefore, it is absolutely necessary to complete the running randomized studies comparing HSCT with mitoxantrone (ASTIMS) or other standard therapies. Unless such trials yield their final results, HSCT will never be approved as an established therapy for MS patients, who may therefore miss the opportunity of receiving an active, powerful immunosuppressive and immunomodulating treatment having a long-term beneficial impact on the course of the disease.
References
1. Abrahamsson SV, et al. Effects of immunosupressive conditioning regimens on immune reconstitution after haematopoietic stem cell transplantation in patients with MS. Mult Scler. 2007;P814.
2. Abrahamsson S. and Muraro PA. Immune re-education following autologous hematopoietic stem cell transplantation. Autoimmunity. 2008;41:577-584.
3. van Bekkum DW. Stem cell transplantation for autoimmuine disorders. Preclinical experiments. Best Pract Res Clin Haematol. 2004;17:201-222.
5. Burt RK, et al. Autologous non-myeloablative haemopoietic stem cell transplantation in relapsing-remitting multiple sclerosis: a phase I/II study. Lancet Neurol. 2009;8:244-253.
6. Dubinsky AN, et al. T-cell clones persisting in the circulation after autologous hematopoietic SCT are undetectable in the peripheral CD34+ selected graft. Bone Marrow Transplant. 2009 June 22 [Epub ahead of print].
7. Fagius J, et al. Early highly aggressive MS successfully treated by hematopoietic stem cell transplantation. Mult Scler. 2009;15:229-237.
9. Fassas A, et al. for the Autoimmune Disease Working Party of the EBMT (European Group for Blood and Marrow Transplantation): Hematopoietic stem cell transplantation for multiple sclerosis: a retrospective multicenter study. J Neurol. 2002;249:1088-1097.
10. Fassas A. and Nash R. Stem cell transplantation for autoimmune disorders. Multiple sclerosis. Best Pract Res Clin Haematol. 2004;17:247-262.
11. Fassas A. and Mancardi GL. Autologous hemopoietic stem cell transplantation for multiple sclerosis: is it worthwile? Autoimmunity. 2008;41:601-610.
13. Hamerschlak N, et al. Brazilian experience with two conditioning regimens in patients with multiple sclerosis: BEAM/horse ATG and CY/rabbit ATG. Bone Marrow Transplant. 2009 Jul6. [Epub ahead of print].
14. Havrdova E. Aggressive multiple sclerosis - is there a role for stem cell transplantation? J Neurol. 2005;252[Suppl 3]:III/34-III37.
15. Kimiskidis V, et al. Treatment of a malignant form of multiple sclerosis with immune ablation and autologous stem cell transplantation. Mult Scler. 2008;14:278-283.
16. Mancardi GL, et al. and the Italian GITMO-NEURO Intergroup on Autologous Hematopoietic Stem Cell Transplantation for Multiple Sclerosis: Autologous hematopoietic stem cell transplantation suppresses Gd-enhanced MRI activity in MS. Neurology. 2001;57:62-68.
17. Mancardi GL, et al. Autologous stem cell transplantation as rescue therapy in malignant forms of multiple sclerosis. Mult Scler. 2005;11:367-371.
18. Mancardi G. and Saccardi R. Autologous haematopoetic stem-cell transplantation in multiple sclerosis. Lancet Neurol. 2008;7:626-636.
21. Portaccio E, et al. Autologous hematopoietic stem cell transplantation for very active relapsing-remitting multiple sclerosis: report of two cases. Mult Scler. 2007;13:676-678.
23. Roccatagliata L, et al. Italian GITMO-NEURO Intergroup on Autologous Stem Cell Transplantation. The long-term effect of AHSCT on MRI measures of MS evolution: a five-year follow-up study. Mult Scler. 2007;13:1068-1070.
25. Saccardi R, et al. Autologous stem cell transplantation for progressive multiple sclerosis: update of the European Group for Blood and Marrow Transplantation autoimmune diseases working party database. Mult Scler. 2006;12:814-823.
26. Saiz A, et al. Clinical and MRI outcome after autologous hemtopoietic stem cell transplantation in MS. Neurology. 2004;62:282-284.
27. Sun W, et al. Characteristics of T-cell receptor repertoire and myelin-reactive T cells reconstituted from autologous haematopoietic stem-cell grafts in multiple sclerosis. Brain. 2004;127:996-1008.
On the evolution of high-dose immunosuppressive therapy with autologous stem cell transplantation in multiple sclerosis
High-dose immunosuppressive therapy with hemopoietic stem cell transplantation (HSCT) was already introduced into the management of multiple sclerosis (MS) in 1995 [8]. The method was based on the concept of an immunological “renewal” after (near)-complete eradication of the aberrant immune system responsible for the development of the disease. Experimental hemopoietic transplants in an animal model of MS, experimental autoimmune encephalomyelitis (EAE), performed in Israel and in the Netherlands, showed that the induction of profound and long-lasting immunosuppression followed by allogeneic or syngeneic or (pseudo)-autologous HSCT can actually have a beneficial impact on the course of EAE [3]. At that time, there was a need for new effective treatments for MS; in particular for the rapidly progressing, therapy-resistant cases, as the results of the existing standard therapies, namely interferon-beta and glatiramer acetate, were rather moderate to poor and their effect on the progression of disability was only marginal.
In order to eradicate the immune system and in view of the lack of a purely immunotoxic regimen, the proposal was for MS patients to be treated with high-dose chemotherapeutic agents (carmustin/ etoposide/ araC/ melphalan or busulfan/ cyclophosphamide) or total body irradiation (TBI), in the way patients with lymphoma or leukemia are conditioned for HSCT. To rescue the patient, autologous grafts were used, purged of T cells or CD34+ cell-selected. These were harvested from peripheral blood stem cells mobilized by cyclophosphamide plus G-CSF prior to HSCT. Intravenous anti-lymphocyte globulins (ALG, ATG) were also administered in the peri-transplant period in order to further eradicate any auto-reactive lymphocytes surviving the conditioning regimen or re-infused with the autologous graft. The “debulking” of autoreactive clones followed by reconstitution of the immune system in the presence of auto-antigens was speculated to bring about, apart from the abrogation of inflammation, qualitative changes as well, which might induce a degree of self-tolerance.
Since 1995, a number of centers in the European Union, Russia, Israel, China, USA, Canada, and Latin America have reported their experience in treating progressing, mainly advanced-stage and standard-therapy-resistant MS with high-dose immunosuppression and HSCT [9]. It is estimated that more than 400 patients have so far been treated worldwide, and favorable results have been reported with certain spectacular and long-lasting beneficial outcomes. However, after fourteen years of experience, the number of centers performing HSCT for MS still remains limited and few patients are referred for this kind treatment, which has not yet been accepted as an established therapy for aggressive MS because the neurological communities have constantly kept a skeptical attitude towards it. The reason lies mainly in the toxic complications of HSCT, especially in the risk of mortality associated with the procedure, which may be elevated in improperly selected patients [25]. This attitude has, unfortunately, prevented the accomplishment of comparative studies that were initiated in Europe (ASTIMS) and the USA (MIST, HALTMS) [11] some years ago and have not yet been finalized. In the meantime, other therapies emerged that were claimed to give good results in MS, e.g., mitoxantrone, alemtuzumab, rituximab, and natalizumab.
HSCT has been shown to be a most powerful immunosuppressive and anti-inflammatory treatment. Since 2000, all communications have consistently reported a dramatic, almost 100%, reduction in, or disappearance of, disease activity (inflammation) on magnetic resonance imaging (MRI) which is retained with time and has not been observed as an outcome of any other MS treatment [16, 26, 10, 23]. Also, brain atrophy, which seems to continue after HSCT as a result of edema resolution, slows down after the 2nd post-HSCT year [22, 12]. Consequently, patients with a lot of inflammation in the CNS experience substantial improvement of their disability status. On the other hand, patients with long-standing disease and those with primary progressive MS, i.e., cases in which the neurodegenerative component of the disease prevails, may not respond to HSCT [4]. This has been detected clinically and also in histopathological examinations of autopsy material, which show ongoing demyelination and axonal damage despite marked suppression of inflammation [19].
With regard to the clinical results of HSCT, it must first be noted that the great majority of the patient series treated worldwide had advanced disease with median EDSS scores of 6 to 6.5, while about 20% of the patients had primary progressive MS. All patients had evidence of disease progression over the twelve months preceding HSCT and/or gadolinium-enhancing lesions in MRI. After HSCT, improvement of disability scores by 1 to 4 steps was observed with a great reduction in the yearly relapse rate and a probability of disease progression-free survival (PFS) of 60–80% at three years [9, 25, 11, 10, 18]. At 10 years post-HSCT, PFS was around 65% for secondary and 40% for primary progressive MS (Fassas, unpublished data). Moreover, the patients’ quality of life and the physical and mental health have also been reported to improve [24]. The most dramatic effect, however, was seen in the so-called “malignant” cases of MS, which have a devastating course unresponsive to any standard therapy. In such cases, HSCT has been shown to be life-saving, with meaningful clinical improvement and long-standing disease stabilization [17, 14, 21, 15, 7].
From the immunological point of view, the effects of HSCT, especially the long-term ones on disease stabilization or on reduction in activity, do not seem to derive only from the immunosuppressive effect of the conditioning regimen, i.e., the “debulking” of auto-reactive clones, because MBP-recognizing T cells usually reappear within a year after HSCT [27, 6]. Immunological studies have shown that the speculated immunological remodulation can actually become a fact after HSCT. Expansion of naive CD4+ cells of thymic origin, decrease of memory T cells, reconstitution of broad clonal diversity, and renewal of clonal specificities have been described to occur after HSCT using high-intensity conditioning regimens (e.g. busulfan 16mg/kg.b.wt. or TBI) [20]. These changes may possibly create tolerance or tip the immunological balance towards suppression of autoimmunity and explain the long-standing beneficial effects of HSCT. Recently, there has been a tendency to use “light” conditioning regimens, e.g., cyclophosphamide 200mg/k.b.wt. plus alemtuzumab or ATG in order to diminish the procedure-related mortality risk. Low-intensity conditioning regimens are, too, capable of inducing immune changes, like the renewal of the balance between CD4+25+FoxP3 regulatory and other T cells or like the deviation of a proinflammatory phenotype of autoimmune cells to a tolerant one [2, 1]. There seems to be a difference in the kind of immune reconstitution brought about by the two types of conditioning, high and low, and we still do not know whether this difference might have the same or a different (better or worse) impact on the clinical outcome. It has been reported, however, that, although “light” conditioning regimens do have less toxicity, they are also associated with more autoimmune relapse after HSCT, compared to “strong” regimens [5, 13]. The regimen of cyclophosphamide plus ATG is less toxic than others but does not appear to have the same good impact on MRI compared to the intermediate-intensity BEAM (carmustine/ etoposide/ araC/ melphalan) [18]. The number of relapses after HSCT with cyclophosphamide plus alemtuzumab or ATG appears somewhat elevated [5], and it is still too early to conclude on the long-term effects on disease progression.
HSCT is a toxic treatment with a variety of complications depending on the intensity of the conditioning regimen [9, 25]. Although a patient may undergo HSCT without any problems, it not unusual for infections, organ damage, and transient neurological worsening to develop during the early post-transplant period. Secondary autoimmune phenomena may also appear late after HSCT. In the two EBMT reports of 2002 and 2006, the procedure-related mortality was 6% in 85 cases [9] and 5.3% in 185 cases [25], respectively. However, the mortality has dropped considerably from 7.3% in transplants before the year 2000 to 1.3% after the year 2000 [18]. This is the result of better patient selection, reserving HSCT for younger, ambulatory, not too-disabled patients, and avoiding the use of too “strong” and too intensive conditioning regimens, i.e., ex-vivo plus in-vivo, and lymphocyte depletion.
In summary, the analyses of the EBMT registry cases have shown that HSCT is active in the inflammatory phases of MS and is capable of slowing down the progression of the disease in relapsing/remitting cases and in patients that have recently entered the secondary progressive phase. Younger patients with low disability scores are more likely to benefit from this therapy. HSCT can be life-saving in desperate cases of very aggressive, rapidly progressing disease, which is refractory to any other therapy. HSCT is not curative, but it may offer prolonged periods of clinical disease stabilization or may change an aggressive disease course. It is not a therapy for the general population of MS patients, as the benefit does not justify the morbidity and mortality risks in cases of already stable disease, in primary progressive or long-standing secondary progressive MS, in cases without gadolinium-positive (inflammatory) lesions on MRI, and in wheelchair-bound patients (EDSS score ≥7) with low performance status and medical co-morbidities. In contrast, the best candidates, in whom the benefit of HSCT outweighs the risks, are young (below 40 years of age), who are still ambulatory, have active and rapidly progressing disease with inflammatory lesions in the CNS, and are in relapsing/remitting or recent secondary progressive phase without much disability. If such MS patients have no accompanying medical co-morbidities precluding transplantation, they may undergo HSCT with a practically zero mortality risk and a good outlook for clinical improvement and/or long disease stability.
It is well known that MS is a very difficult disease in which to show the efficacy of a therapy. Despite the very interesting outcomes of HSCT in treatment of MS, it is only in comparative trials that its superiority over other therapies can be demonstrated. Therefore, it is absolutely necessary to complete the running randomized studies comparing HSCT with mitoxantrone (ASTIMS) or other standard therapies. Unless such trials yield their final results, HSCT will never be approved as an established therapy for MS patients, who may therefore miss the opportunity of receiving an active, powerful immunosuppressive and immunomodulating treatment having a long-term beneficial impact on the course of the disease.
References
1. Abrahamsson SV, et al. Effects of immunosupressive conditioning regimens on immune reconstitution after haematopoietic stem cell transplantation in patients with MS. Mult Scler. 2007;P814.
2. Abrahamsson S. and Muraro PA. Immune re-education following autologous hematopoietic stem cell transplantation. Autoimmunity. 2008;41:577-584.
3. van Bekkum DW. Stem cell transplantation for autoimmuine disorders. Preclinical experiments. Best Pract Res Clin Haematol. 2004;17:201-222.
5. Burt RK, et al. Autologous non-myeloablative haemopoietic stem cell transplantation in relapsing-remitting multiple sclerosis: a phase I/II study. Lancet Neurol. 2009;8:244-253.
6. Dubinsky AN, et al. T-cell clones persisting in the circulation after autologous hematopoietic SCT are undetectable in the peripheral CD34+ selected graft. Bone Marrow Transplant. 2009 June 22 [Epub ahead of print].
7. Fagius J, et al. Early highly aggressive MS successfully treated by hematopoietic stem cell transplantation. Mult Scler. 2009;15:229-237.
9. Fassas A, et al. for the Autoimmune Disease Working Party of the EBMT (European Group for Blood and Marrow Transplantation): Hematopoietic stem cell transplantation for multiple sclerosis: a retrospective multicenter study. J Neurol. 2002;249:1088-1097.
10. Fassas A. and Nash R. Stem cell transplantation for autoimmune disorders. Multiple sclerosis. Best Pract Res Clin Haematol. 2004;17:247-262.
11. Fassas A. and Mancardi GL. Autologous hemopoietic stem cell transplantation for multiple sclerosis: is it worthwile? Autoimmunity. 2008;41:601-610.
13. Hamerschlak N, et al. Brazilian experience with two conditioning regimens in patients with multiple sclerosis: BEAM/horse ATG and CY/rabbit ATG. Bone Marrow Transplant. 2009 Jul6. [Epub ahead of print].
14. Havrdova E. Aggressive multiple sclerosis - is there a role for stem cell transplantation? J Neurol. 2005;252[Suppl 3]:III/34-III37.
15. Kimiskidis V, et al. Treatment of a malignant form of multiple sclerosis with immune ablation and autologous stem cell transplantation. Mult Scler. 2008;14:278-283.
16. Mancardi GL, et al. and the Italian GITMO-NEURO Intergroup on Autologous Hematopoietic Stem Cell Transplantation for Multiple Sclerosis: Autologous hematopoietic stem cell transplantation suppresses Gd-enhanced MRI activity in MS. Neurology. 2001;57:62-68.
17. Mancardi GL, et al. Autologous stem cell transplantation as rescue therapy in malignant forms of multiple sclerosis. Mult Scler. 2005;11:367-371.
18. Mancardi G. and Saccardi R. Autologous haematopoetic stem-cell transplantation in multiple sclerosis. Lancet Neurol. 2008;7:626-636.
21. Portaccio E, et al. Autologous hematopoietic stem cell transplantation for very active relapsing-remitting multiple sclerosis: report of two cases. Mult Scler. 2007;13:676-678.
23. Roccatagliata L, et al. Italian GITMO-NEURO Intergroup on Autologous Stem Cell Transplantation. The long-term effect of AHSCT on MRI measures of MS evolution: a five-year follow-up study. Mult Scler. 2007;13:1068-1070.
25. Saccardi R, et al. Autologous stem cell transplantation for progressive multiple sclerosis: update of the European Group for Blood and Marrow Transplantation autoimmune diseases working party database. Mult Scler. 2006;12:814-823.
26. Saiz A, et al. Clinical and MRI outcome after autologous hemtopoietic stem cell transplantation in MS. Neurology. 2004;62:282-284.
27. Sun W, et al. Characteristics of T-cell receptor repertoire and myelin-reactive T cells reconstituted from autologous haematopoietic stem-cell grafts in multiple sclerosis. Brain. 2004;127:996-1008.
Атанасиос Фассас
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Во всех сообщениях, начиная с 2000 г., отмечается существенное (почти на 100%) снижение, или полное исчезновение признаков заболевания (воспаления), выявляемое с помощью метода ядерно-магнитного резонанса, и этот эффект сохраняется в течение длительного времени, в отличие от всех других методов лечения РС. Несмотря на весьма впечатляющие результаты применения HSCT для лечения РС, её преимущества были продемонстрированы только в сравнительных исследованиях. Поэтому представляется абсолютно необходимым завершить текущие рандомизированные исследования по сравнению HSCT с митоксантроном (ASTIMS) или с другими стандартными методами терапии. Пока не будут получены окончательные результаты этих исследований, HSCT не может быть принят как общепризнанный метод лечения больных с РС, которые могут быть лишены возможности получить действительно эффективную иммуносупрессивную и иммуномодулирующую терапию с длительным положительным воздействием на течение болезни.
Athanasios Fassas
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Было показано, что HSCT является здесь наиболее эффективной иммуносупрессивной и противовоспалительной терапией. <br /><br />Во всех сообщениях, начиная с 2000 г., отмечается существенное (почти на 100%) снижение, или полное исчезновение признаков заболевания (воспаления), выявляемое с помощью метода ядерно-магнитного резонанса, и этот эффект сохраняется в течение длительного времени, в отличие от всех других методов лечения РС. Несмотря на весьма впечатляющие результаты применения HSCT для лечения РС, её преимущества были продемонстрированы только в сравнительных исследованиях. Поэтому представляется абсолютно необходимым завершить текущие рандомизированные исследования по сравнению HSCT с митоксантроном (ASTIMS) или с другими стандартными методами терапии. Пока не будут получены окончательные результаты этих исследований, HSCT не может быть принят как общепризнанный метод лечения больных с РС, которые могут быть лишены возможности получить действительно эффективную иммуносупрессивную и иммуномодулирующую терапию с длительным положительным воздействием на течение болезни. </p>" ["TYPE"]=> string(4) "HTML" } ["DESCRIPTION"]=> string(0) "" ["VALUE_ENUM"]=> NULL ["VALUE_XML_ID"]=> NULL ["VALUE_SORT"]=> NULL ["~VALUE"]=> array(2) { ["TEXT"]=> string(2360) "Высокодозная иммуносупрессивная терапия и трансплантация аутологичных гемопоэтических стволовых клеток (HSCT) была введена в практику лечения больных рассеянным склерозом (РС) в 1995 г. Было показано, что HSCT является здесь наиболее эффективной иммуносупрессивной и противовоспалительной терапией.
Во всех сообщениях, начиная с 2000 г., отмечается существенное (почти на 100%) снижение, или полное исчезновение признаков заболевания (воспаления), выявляемое с помощью метода ядерно-магнитного резонанса, и этот эффект сохраняется в течение длительного времени, в отличие от всех других методов лечения РС. Несмотря на весьма впечатляющие результаты применения HSCT для лечения РС, её преимущества были продемонстрированы только в сравнительных исследованиях. Поэтому представляется абсолютно необходимым завершить текущие рандомизированные исследования по сравнению HSCT с митоксантроном (ASTIMS) или с другими стандартными методами терапии. Пока не будут получены окончательные результаты этих исследований, HSCT не может быть принят как общепризнанный метод лечения больных с РС, которые могут быть лишены возможности получить действительно эффективную иммуносупрессивную и иммуномодулирующую терапию с длительным положительным воздействием на течение болезни.
Высокодозная иммуносупрессивная терапия и трансплантация аутологичных гемопоэтических стволовых клеток (HSCT) была введена в практику лечения больных рассеянным склерозом (РС) в 1995 г. Было показано, что HSCT является здесь наиболее эффективной иммуносупрессивной и противовоспалительной терапией.
Во всех сообщениях, начиная с 2000 г., отмечается существенное (почти на 100%) снижение, или полное исчезновение признаков заболевания (воспаления), выявляемое с помощью метода ядерно-магнитного резонанса, и этот эффект сохраняется в течение длительного времени, в отличие от всех других методов лечения РС. Несмотря на весьма впечатляющие результаты применения HSCT для лечения РС, её преимущества были продемонстрированы только в сравнительных исследованиях. Поэтому представляется абсолютно необходимым завершить текущие рандомизированные исследования по сравнению HSCT с митоксантроном (ASTIMS) или с другими стандартными методами терапии. Пока не будут получены окончательные результаты этих исследований, HSCT не может быть принят как общепризнанный метод лечения больных с РС, которые могут быть лишены возможности получить действительно эффективную иммуносупрессивную и иммуномодулирующую терапию с длительным положительным воздействием на течение болезни.
Introduction
Stem cell therapy for severe autoimmune diseases (AD), generally as hematopoietic stem cell transplantation (HSCT), both allogeneic and autologous, but also more recently as gene therapy-assisted autologous HSCT, has become one of the hottest areas of clinical immunology. It has been developing progressively in the last decades, and has generated “excitement and promise as well as confusion and at times contradictory results in the lay and scientific literature” [6]. The utilization of stem cells to promote regenerative medicine must be distinguished from the purpose of suppressing autoimmune cellular and humoral aggression. This does not mean that both areas aren’t tightly connected, since supplying new pancreatic beta cells to patients with type I diabetes, whether by islet cell transplantation or by boosting their numbers by reprogramming pancreatic acinar cells, cannot resolve the disease if the autoimmune process is not eliminated [61]. In some clinical entities both effects coincide. An appropriate example is aplastic anemia (AA) and some of its minor variants (pure red cell aplasia-PRCA, pure white cell aplasia-PWCA), in which allogeneic HSCT both suppresses autoimmunity and provides new HSC [62]. In all the other autoimmune conditions this double effect has not been demonstrated conclusively.
The utilization of HSCT, overwhelmingly of the autologous modality, has been growing impressively in the last few years, and is still increasing steadily [28, 47]. Autologous HSCT (ASCT) relies on an extensive debulking of the autoaggressive immune system, followed by the re-infusion of the patients’ HSC (commonly identified as CD34+ cells). The allogeneic procedure is based on the substitution of the faulty immune system by a new healthy one, theoretically capable of eradicating the autoimmune clones by means of the classical combination of high-dose immunosuppressive therapy and a Graft-versus-Autoimmunity (GVA) effect, which will be discussed later. Whether this last intervention will be capable of achieving the Holy Grail of self-tolerance [15] is still not established, given the complexity of the pathogenesis of ADs, including the persisting antigenicity of altered “self” proteins [12] and some paradoxical post-transplant relapses despite full donor chimerism, which will be discussed later.
A brief historical recapitulation
Two streams of research, experimental and clinical, are at the origin of the increasing utilization of HSCT, autologous and allogeneic, for SADs [34]. The first animal studies had shown that the transfer of spleen and/or whole marrow cells to immunosuppressed mice could reproduce murine lupus. The culprit cells were shown to be stem or lymphoid progenitors. The next step was to ascertain whether, contrarily, healthy HSC were capable of curing experimental ADs. Human blood SC were capable of suppressing antibody production in lupus mice, perhaps the first demonstration of a curative effect by xenogeneic HSCT. More recently, it has elegantly been shown that the nonmyeloablative transplantation of purified allogeneic HSC not only prevented, but also induced stabilization or reversal of lupus symptoms in NZB mice [50]. Durable mixed chimerism was also efficacious, a point that will be discussed later. A further experimental improvement has been the intra-bone injection of HSC [21].
The resolution of experimental ADs by means of healthy, compatible allo-SCT was to be expected, considering the overwhelming genetic predisposition of inbred strains of mice, which differs from the intricacies of human ADs, in which there is a complex relationship between genetic, environmental and regulatory factors, and where impaired mechanisms of thymic selection interact, in still poorly elucidated ways, with genetic factors. As already mentioned, a GVA effect has been postulated [33], and theoretically dissected in 6 different mechanisms [53], with immune-mediated abrogation of autoreactive clones in the foreground. In practice, donor-derived immune cells are capable of mediating an anti-autoimmune effect either specifically, or as a part of a more general alloimmune reaction. In experimental autoimmune encephalomyelitis (EAE) it was shown that active alloreactivity was associated with the greatest GVA effect [60]. The second stream in favor of allo-SCT came from the clinical observation of patients affected by coincidental diseases, that is patients with ADs having developed a hematologic malignancy for which they received an allo-SCT, and were ultimately cured of both diseases [35]. There were even cases in which allo-BMT transferred the AD of the donor to the recipient, but cured the latter of his former AD.
The rationale for an apparently paradoxical procedure such as autologous HSCT, in which the patients’ immune cells, despite varying degrees of HSC depletion in vitro and/or in vivo, are administered back to them, came from the pioneering studies by van Bekkum and his group, who were able to cure EAE and adjuvant arthritis (AA), both models of human multiple sclerosis (MS) and rheumatoid arthritis (RA), by means of autologous (“pseudoautologous”) HSCT [58]. These results considerably strengthened the philosophy of autologous HSCT for human ADs, even if it was pointed out later that in animal models the abnormality of the antigen-induced type seems to reside in immunocompetent T/B cells but not in the HSC, and therefore ASCT may be curative, while in spontaneous ADs new, unaffected HSC were necessary to achieve a cure [22]. In any case, the utilization of ASCT is now widely accepted for treating severe, refractory ADs.
A powerful immunosuppressive therapy for SADs has been developed at Johns Hopkins University in Baltimore, where such patients are treated with high-dose cyclophosphamide (CY) alone, with an inevitable delay of marrow and blood reconstitution, but with results that do not differ significantly from those obtained by ASCT [5].
Finally, two new approaches appear to be integrating this area. Mesenchymal stem cells (MSC) possess several immunomodulatory properties [44], have been shown to significantly ameliorate Graft-versus-Host Disease [25] (GVHD), and have been considered a valuable therapeutic option for SADs [56]. However the role of this kind of cellular therapy in human AD, whether associated with ASCT or not, is still to be established. Another fascinating approach is based on the idea of achieving antigen-specific tolerance to treat refractory ADs, even if translating such therapies from bench to bedside is still mainly theoretical. An approach combining HSCT and transduction of the culprit self-antigens in autologous HSCs in order to achieve central (thymic) tolerance has been developed by Alderuccio and his group [2], although only in animal experiments with organ-specific autoimmune conditions at this stage.
Autologous transplantation: progress and questions
In contrast to the long interval having taken place between the first allogeneic transplants for animal ADs and translational clinical trials, ASCT quickly followed the experimental investigations. It was proposed by myself for severe SLE in 1993 [36], and then for ADs in general in 1995 [30]. The first transplants were performed for a connective tissue disease [54] and for severe SLE [32]. The following utilization of ASCT for SADs grew almost exponentially, so much so that, besides the continually increasing registered transplants in the EBMT and CIBMTR registries, a recent study by Dominique Farge et al has analyzed 900 patients [14]. Excellent reviews of specific diseases have been published recently, and a monographic issue of Autoimmunity has just been devoted to this theme [28]. Here, I shall focus on the most significant and contemporary questions.
1. Autologous HSCT for ADs has been considered a relatively safe procedure from its inception, but is it becoming safer?
Autoimmune diseases represent an extremely heterogenous spectrum of diseases, and in most of them severe-refractory forms have a poor prognosis and a greatly impaired quality of life. One cannot disagree, however, with Burt’s statement that “Treatment-related mortality needs to be very low for non-malignant diseases”1. Treatment-Related Mortality (TRM) reached 12% in the initial EBMT Registry, decreased to 7 +3% in 2005, and finally did not exceed 5% in the most recent EBMT study [14]. In this last study evidence was also found of a clear center effect, indicating that experienced teams that are well acquainted with the multi-organ involvement of SADs produce superior results. In the case of a single disease such as SLE, a collection of 162 patients transplanted in 30 Centers showed a TRM of 11% [29], However of 200 patients transplanted at Northwestern University, Chicago, the TRM using non-myeloablative conditioning regimens in 200 patients was 1.5% [8]. This does not mean, of course, that TRM cannot grow much higher in very severe conditions such as advanced scleroderma. Scleroderma-related organ disfunction contributed to treatment-related deaths [43]. In conclusion, the answer to this first question is that ASCT may be considered reasonably safe when performed by experienced teams, appropriate conditioning regimens, and on patients who are not too disease-compromised. These data need to be counterbalanced by mortality from disease progression, and require the adoption of inclusion and exclusion criteria for each category of diseases, which cannot be detailed here. Although the inclusion of patients within approved or investigational protocols is the best policy, it must be realized that, in selected patients with advanced, refractory SADs, the decision to perform ASCT will ultimately rely on a combination of clinical acumen, experienced teams, and a good patient-doctor relationship.
2. Which are the most appropriate mobilization and conditioning regimens?
The source of HSCs was initially the bone marrow (BM), but has now changed to the peripheral blood (PB) following mobilization procedures. In the previously mentioned EBMT study of 900 patients the source was PB in 827 cases [43]. The most popular mobilizing regimens generally consist of combinations of cyclophosphamide (CY) and G-CSF [47]. Mobilizing regimens incorporating CY (from 2 to 4g/m2) have the additional, significant advantage of acting as an important therapeutic procedure per se (therapeutic mobilization). In our own experience of 9 SLE patients the achievement of a complete remission (CR) following mobilization with CY 4g/m2 enabled us, in 2 cases, to dispense from performing the initially programmed ASCT.
A variety of conditioning regimens have been utilized, but it could be shown that high-intensity protocols were followed by a lower probability of disease progression, albeit with a higher risk of TRM [16]. The strategy of performing intense immunosuppression without affecting the whole of the hematopoietic system is most generally accepted, taking into account that biologics such as Rituximab have a longer immunosuppressive activity than any chemotherapeutic agent. A combination of both strategies, in which Rituximab 500 mg is given before and after the regular 200 mg/kg CY protocol (the “sandwich technique”), is being currently utilized at Northwestern University, Chicago (USA). Anti-CD20 immunotherapy for the control of relapse following ASCT in patients with rheumatoid arthritis (RA) had been already utilized with success [41], and the strategy of using an additional immunotherapy in this area is attractive. Unfortunately a devastating complication, progressive multifocal leukoencephalopathy (PML), due to the activation of the John Cunningham virus (JCV), has been reported in a disquieting proportion of patients having been immunosuppressed with biological agents (Natalizumab, Rituximab). A recent review reported 52 patients as having developed PML, 7 of which had received HSCT (3 allogeneic, 4 autologous) for lymphoproliferative diseases [9]. Awareness is obviously needed of the potential for PML among Rituximab-treated patients. Maximal immunosuppression produces greater benefits, but may at the same time be associated with unforeseen iatrogenic complications.
3. What significant changes in the immune system take place following ASCT ? Are we really curing autoimmunity ?
No other aspect of the ASCT-based procedures has been the object of so much research, controversy, enthusiasm, and skepticism. A prolonged depression of CD4+ CD45RA cells is a general finding, and takes place following both ASCT and high-dose immunosuppressive therapy (HDIS) alone. The type of immunomodulation which then follows has been called a “black box” by Muraro and Douek [42], but, thanks to their own and others’ investigations, is becoming increasingly clear. High-dose immunosuppression reduces the population of autoimmune cells to minimal residual autoimmune disease (MRAD). While the cure of oncohematological disease requires the eradication of cancer SC, a different view is entertained for ADs. Two basic mechanisms have been postulated.The first has been defined as a “re-education” of the faulty immune system [1], obtained by restoring a diverse antigen-specific repertoire through reactivation of the thymic output (“thymic rebound”), which has also been shown to persist in adults, albeit in lesser measure. In a recent study of ASCT in 7 SLE patients the Berlin group has found evidence for an overwhelming regeneration of the adoptive immune system and of the B-cell lineage, which became apparently tolerant to self-antigens [3]. The second mechanism is closely related, and consists in the reconstitution of the regulatory T-cell pool following ASCT. Tregs (CD4+ CD25+) expressing the transcription factor Foxp3 are crucial in preventing autoreactivity and restraining autoimmunity throughout life. Experimental and clinical studies have demonstrated the impact of the T regulatory network in inducing post-transplant immune tolerance in SLE [63].
Are these changes sufficient and stable enough to guarantee a rebuilding of the immune system, configured in a way that is less likely to redevelop autoimmunity? The abundant and sophisticated studies undeniably display some controversies. In a first study in autotransplanted MS patients the T cells recognizing myelin basic protein were indeed initially depleted by immunoablation, but then rapidly expanded from the reconstituted T cell repertoire in 12 months [52]. More recently, an early recovery of CD4 T-cell receptor diversity was found after “lymphoablative” conditioning and autologous CD34 cell transplantation in systemic sclerosis (SSc) patients, suggesting that the treatment is not completely T-cell ablative (or, more generally immune SC-ablative), and thus not ultimately curative [51]. This contrasts with another recent study which found that CD34+-selected progenitor cells had limited survival capacity and are therefore unlikely to be a major source of carryover of autoimmune T-cell expansions [11]. However, in a comprehensive recent study analyzing original and pooled data from autotransplanted MS patients, Mondria et al [40] found not only the previously known persistence of CSF oligoclonal bands in 88% of the reported cases, but also the persistence of the soluble lymphocyte activator CD27 – thus concluding that complete eradication of activated lymphocytes from the CNS had not been established, despite an intensive immunosuppressive regimen including ATG, CY and total body irradiation (TBI), in two fractions of 5 Gy a day at days –2 and –1. Active demyelinization and axonal damage have been found to continue after ASCT [39]. Our own clinical experience has included late (and very late) relapses, in a way that suggested a recapitulation of the natural history of lupus. So whether pressing the reset button will turn out to be immunologically curative is still uncertain.
4. What type of benefit, if any, does ASCT confer to severe, progressive, relapsing-refractory ADs?
In a recent, provocative editorial commenting on the utilization of ASCT for SADs, and more specifically for the rheumatic diseases, Illei [23] has posed the question, whether “the glass is half full or half empty”.
The effects of ASCT may be divided into two phases: the early suppression of ongoing, immuno-inflammatory events, and the later resetting of the autoimmune clock, which is closely related to the length and grade of remission. The first effect is clearly due to the immunosuppressive conditioning regimens, and is proportional to the dose intensity, and also independent from HSC rescue. No sophisticated dynamics occur here, besides the well-known combination of immunosuppression and abrogation of its attending inflammation. This first effect is responsible for its dramatic disease-arresting (“nosostatic”) properties, which have been observed in practically all actively aggressive SADs, and most demonstratively in SLE. This change occurs in the aggressive phases of disease, where ASCT may well be the most potent salvage therapy available. A clear distinction of the diverse sensitivity to ASCT according to the phases of disease has been recently made by Shevchenko et al [49], who have divided the transplant strategies for MS into “early”, “conventional” and “salvage-late” procedures. Among the many examples of this early, dramatic therapeutic effect are, besides the cancellation of systemic symptoms, the almost immediate clearance of inflammatory urinary sediments in lupus nephritis, the rapid improvement of nailfold capillaroscopy in SSc [4], and the early abrogation of Gadolinium-enhancing lesions in MS [27]. The striking disappearance of diffuse calcinosis in a child with overlap connective disease [13] and the regression of dermal fibrosis in patients with severe scleroderma [43] may be considered intermediate changes.
The impact of ASCT on SADs in the long run has been discussed in several contributions. In the most important study, Progression Free Survival (PFS), which may be considered as the most accurate estimated outcome of a therapeutic procedure, was 43% at 3 years [14]. Three apparently contrasting aspects emerge: first, that in the overwhelming majority of patients no authentic immunological cure may be realistically expected; second, that dramatic remissions occur, may be life-saving, and even long term. Thirdly, in most relapses the utilization of conventional therapies, to which the patients were formerly refractory, is generally possible.
5. Is ASCT the best available treatment for SADs?
ASCT is a powerful therapeutic procedure for SADs. But can it be regarded as the best treatment available, considering the increasing utilization of new pharmacological, prospective (phase III) clinical trials, which are being actively pursued for SSc (the ASTIS trial in Europe and the SCOT trial in North America), MS (ASTIMS, which is probably the most advanced one), Crohn’s disease (ASTIC), and SLE (ASTIL)? It is clear that this is the only way to obtain a scientifically correct answer. However, the pace of medical progress is such, that by the time that these laborious trials will have reached statistical significance, new agents may have superseded those utilized in the non-transplant arms. Furthermore, in a sizable proportion of these patients' ASCT may be integrated with other therapeutic interventions, including high-dose immunoglobulins (HDIG), biologics and possibly new, “intelligent” molecules.
Allogeneic transplantation facts and questions
More cogently than for the autologous procedure, animal experiments and results from coincidental disease patients had indicated a powerful instrument to cure autoimmunity in Allo-SCT. In an international workshop held in 2005, it was stated that “the potential for a 1-time delivery of a curative therapy is outstanding” [17]. But will it really be so? Many clinical trials are being pursued worldwide, but I shall confine myself only to published material and our personal experience.
Clinical results
A retrospective EBMT study [10] has collected 35 patients having received 38 allogeneic transplants for various ADs, hematological and non-hematological. The donors were identical siblings for 24 patients, matched unrelated donors (MUD) for 3, mismatched related for 2 and syngeneic for 3 patients. Treatment related mortality (TRM) was 22.1% at 2 years and 30.7 at 5, while death due to progression of disease was 3.2% at 2 years and 8.7% at 5. Of the 29 surviving patients 55% achieved complete clinical and laboratory remission, and 24% achieved a partial remission. The consensus is that nonmyeloablative (NST), reduced intensity conditioning regimens (RIC) should be utilized [46].
Immunological aspects
The substitution of an immune system which is behaving badly by a normal, healthy one is the rationale of the allogeneic approach, and its successful achievement is the prerequisite for embarking on a treatment which has been saddled with a 30% mortality after 5 years [17]. Although it is predictable that TRM following Allo-SCT, if further pursued, will probably become lower, both with an improvement of the learning curve and with optimized conditioning regimens, and effective GVHD control, the only legitimate motivation for performing it is achieving a cure.Allo-SCT is traditionally regarded as a “platform for immunotherapy” [24]. An exhaustive analysis of the mechanisms by which it might cure ADs has been performed by Sykes and Nikolic [53], who have placed the previously discussed GVA effect in the foreground. A retrospective study showed, in analogy to an established pattern in oncohematological diseases, that there were more relapses of coincidental ADs in patients transplanted for hematological malignancies with no GVHD, than in those who developed it [19]. However this effect could not be detected in the recent EBMT study [10], and a much greater clinical material would be necessary to obtain significant evidence.Efforts have been made, as already attempted in oncohematological diseases, to separate GVHD from GVA. A potent GVA effect was demonstrated in rat models of EAE. Clinically there is a group of patients who had been allotransplanted for SADs, in whom donor lymphocyte infusions (DLI) were necessary to achieve full donor chimerism, which ultimately ensured complete remissions of the SADs (lit in 11). These results are counterbalanced with others, which are in favor of the hypothesis that mixed chimerism might be capable of inducing long-term remissions [7]. However it has been shown that increasing mixed chimerism is conducive to graft loss in children transplanted for non-malignant disorders [45]. Full chimerism was present in two patients with rheumatoid arthritis [26] and in a 7-year old boy with Evans syndrome, in whom two autologous transplants had been previously unsuccessful [57].
Controversial evidence, however, comes from the analysis of relapsed patients. There appear to be two types of relapses. An example of the first type is the report of a failure of Allo-SCT to arrest disease activity in a patient with MS having been successfully transplanted because of coincidental chronic myeloid leukemia [38]. Even more disquieting are the aforementioned reports of patients with SADs having received Allo-SCT, but having subsequently relapsed despite full donor chimerism. The first and widely acknowledged case was a female patient with rheumatoid arthritis (RA), who received an HLA-identical transplant because of gold-induced aplastic anemia [55] and the second another patient with RA and multiple myeloma (MM), in whom the myeloma was cured but the RA relapsed [31]. The most demonstrative case is the one of a patient with severe Evans syndrome, who was transplanted from his HLA-identical sister but needed a series of DLI in order to achieve full donor chimerism and complete hematological remission. This patient unfortunately relapsed and died with a terminal hemolytic-uremic syndrome 5 years later [20]. The patient was male and had received the bone marrow of his HLA-identical sister. The immunoglobulins (IgG, IgM) eluted from his 100% XX expanded B cells were not the ones eluted from his Coombs-positive cells. It was hypothesized that the autoantibodies might have been secreted by long-lived host plasmacytes surviving in postulated marrow niches [18]. Even allowing for the hypothesis that relapses in donor cells in patients transplanted for leukemia might be less uncommon than generally thought to be, it is still an extremely rare event, having been identified in 14 out of 10,489 transplants in a recent survey [37]. In contrast, 3 relapses in the much smaller group of autoimmune allotransplanted patients inevitably causes some perplexity. Only further careful investigations will hopefully elucidate this unexpected problem.
Syngeneic transplants are a niche event. Three patients with RA received syngeneic transplants following high-dose immunosuppression. The first was a patient with severe seronegative RA, who enjoyed a long-term remission [59]. However a second patient with progressively erosive, rheumatoid factor positive RA, who was treated with high-dose CY and received an unmanipulated peripheral blood graft (PBSCT) from her identical twin sister, had a poor clinical response, associated with serological persistence64. A still unpublished case is the one of 45 year old lady with severe seropositive RA who was transplanted in Genoa from her identical twin sister on July 29, 2005. The conditioning regimen consisted of CY, 160 mg/Kg. Both rheumatoid factor and anti-cyclic citrulline peptide (CCP) titres decreased significantly (CCP from 234 to 2), but there was a clinical relapse with fever, polyarthritis and elevation of ESR, requiring further treatment.
Concluding remarks
Is there, at the time of this writing, sufficient evidence to answer the question, as to whether HSCT, in its various paradigms, is and will be the best available therapy for SADs? There has been a tendency to place the cause of autoimmunity on a faulty immune system, thus assimilating ADs to the neoplastic lymphoproliferative diseases. However most ADs result from a combination of faulty immune systems and antigen (target organ) dysfunctions. The distinction between primary and secondary ADs, the first being sustained by primary immune defaults and the latter by a predominant antigenic trigger, has been considered as helpful for the evaluation of SCT interventions. However the interaction between immune system and target organ antigenicity is extremely tight.
The autologous procedure is being performed worldwide because of its combination of safety and efficacy. It is capable of arresting progressive, otherwise refractory ADs. In addition, if utilized early in appropriate patients, it favorably changes the course of disease, even allowing for varying degrees of regeneration. Whether the autoaggressive immune system is being re-educated or, more simply, reset, is still not fully clarified. With this background, I believe that Illei’s glass [39] is more full than empty, when ASCT is performed in an early stage of disease (fig. 1). However , independently from the results, I believe that there ultimately will be an integration between the two approaches, with careful selection of individual patients.
A word of caution must be said concerning the potential development not only of PML, as already discussed, but also of therapy-related myelodysplasia and leukemia (t-MDS, t-AML), which must be closely watched for when utilizing alkylating drugs and others. Fortunately, there haven’t been such reports in this area, and recourse to ASCT in patients with SADs should not be hindered by the fear of late malignant complications, although careful long-term surveillance is mandatory.
Great expectations have been associated with allogeneic SCT, but its position is still uncertain. Ongoing trials will hopefully offer some answers to the question, or hope, whether the total eradication of a faulty immune system will be sufficient, and whether there is solid evidence of a clinically exploitable GVA effect. The unexpected relapses despite full donor chimerism are still a problem, but further experience is needed.
Summary
Two different sets of investigation are at the origin of hematopoietic stem cell transplantation (HSCT) for severe autoimmune diseases (SADs). The experimental evidence consisted in the transfer/cure of animal SADs as murine lupus by means of allogeneic but also, almost paradoxically, autologous HSCT. The clinical arm comes from serendipitous reports of patients allotransplanted for coincidental diseases, and finally cured of both conditions. The encouraging results of ASCT in experimental ADs were enthusiastically translated into human therapy by clinicians hoping to achieve great results without incurring into the rigors associated with the allogeneic procedure.
Well over 1000 ASCT for SADs have been performed worldwide at this time with multiple sclerosis (MS) and connective tissue diseases in the foreground. Transplant-related mortality (TRM) and morbidity have decreased to well under 5%. A dramatic disease-arresting effect is a constant benefit, but the whole course of the disease appears to be influenced favorably. Profound changes of the autoimmune circuitry have been demonstrated, but no authentic eradication of disease (cure?) should realistically be expected. Important multicentric prospective trials are ongoing to compare ASCT to the best available non-transplant therapies, but it may be argued that in the end both approaches will be integrated for single patients, and that new agents will possibly alter present strategies.
Allogeneic STC is eliciting great expectations, but the burden of higher mortality and morbidity with GVHD in the first place, must be considered, even when making recourse to reduced conditioning regimens (RIC). Paradoxical relapses despite complete donor chimerism have been reported. Further experience is clearly needed, but the early enthusiasm for an attractive one-shot therapy must be tempered with a realistic evaluation, at least until new significant breakthroughs have been attained.
Acknowledgements
This article is based on the materials of the perspective article in the International Journal of Clinical Rheumatology 2009; 4(4):395-408.
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Introduction
Stem cell therapy for severe autoimmune diseases (AD), generally as hematopoietic stem cell transplantation (HSCT), both allogeneic and autologous, but also more recently as gene therapy-assisted autologous HSCT, has become one of the hottest areas of clinical immunology. It has been developing progressively in the last decades, and has generated “excitement and promise as well as confusion and at times contradictory results in the lay and scientific literature” [6]. The utilization of stem cells to promote regenerative medicine must be distinguished from the purpose of suppressing autoimmune cellular and humoral aggression. This does not mean that both areas aren’t tightly connected, since supplying new pancreatic beta cells to patients with type I diabetes, whether by islet cell transplantation or by boosting their numbers by reprogramming pancreatic acinar cells, cannot resolve the disease if the autoimmune process is not eliminated [61]. In some clinical entities both effects coincide. An appropriate example is aplastic anemia (AA) and some of its minor variants (pure red cell aplasia-PRCA, pure white cell aplasia-PWCA), in which allogeneic HSCT both suppresses autoimmunity and provides new HSC [62]. In all the other autoimmune conditions this double effect has not been demonstrated conclusively.
The utilization of HSCT, overwhelmingly of the autologous modality, has been growing impressively in the last few years, and is still increasing steadily [28, 47]. Autologous HSCT (ASCT) relies on an extensive debulking of the autoaggressive immune system, followed by the re-infusion of the patients’ HSC (commonly identified as CD34+ cells). The allogeneic procedure is based on the substitution of the faulty immune system by a new healthy one, theoretically capable of eradicating the autoimmune clones by means of the classical combination of high-dose immunosuppressive therapy and a Graft-versus-Autoimmunity (GVA) effect, which will be discussed later. Whether this last intervention will be capable of achieving the Holy Grail of self-tolerance [15] is still not established, given the complexity of the pathogenesis of ADs, including the persisting antigenicity of altered “self” proteins [12] and some paradoxical post-transplant relapses despite full donor chimerism, which will be discussed later.
A brief historical recapitulation
Two streams of research, experimental and clinical, are at the origin of the increasing utilization of HSCT, autologous and allogeneic, for SADs [34]. The first animal studies had shown that the transfer of spleen and/or whole marrow cells to immunosuppressed mice could reproduce murine lupus. The culprit cells were shown to be stem or lymphoid progenitors. The next step was to ascertain whether, contrarily, healthy HSC were capable of curing experimental ADs. Human blood SC were capable of suppressing antibody production in lupus mice, perhaps the first demonstration of a curative effect by xenogeneic HSCT. More recently, it has elegantly been shown that the nonmyeloablative transplantation of purified allogeneic HSC not only prevented, but also induced stabilization or reversal of lupus symptoms in NZB mice [50]. Durable mixed chimerism was also efficacious, a point that will be discussed later. A further experimental improvement has been the intra-bone injection of HSC [21].
The resolution of experimental ADs by means of healthy, compatible allo-SCT was to be expected, considering the overwhelming genetic predisposition of inbred strains of mice, which differs from the intricacies of human ADs, in which there is a complex relationship between genetic, environmental and regulatory factors, and where impaired mechanisms of thymic selection interact, in still poorly elucidated ways, with genetic factors. As already mentioned, a GVA effect has been postulated [33], and theoretically dissected in 6 different mechanisms [53], with immune-mediated abrogation of autoreactive clones in the foreground. In practice, donor-derived immune cells are capable of mediating an anti-autoimmune effect either specifically, or as a part of a more general alloimmune reaction. In experimental autoimmune encephalomyelitis (EAE) it was shown that active alloreactivity was associated with the greatest GVA effect [60]. The second stream in favor of allo-SCT came from the clinical observation of patients affected by coincidental diseases, that is patients with ADs having developed a hematologic malignancy for which they received an allo-SCT, and were ultimately cured of both diseases [35]. There were even cases in which allo-BMT transferred the AD of the donor to the recipient, but cured the latter of his former AD.
The rationale for an apparently paradoxical procedure such as autologous HSCT, in which the patients’ immune cells, despite varying degrees of HSC depletion in vitro and/or in vivo, are administered back to them, came from the pioneering studies by van Bekkum and his group, who were able to cure EAE and adjuvant arthritis (AA), both models of human multiple sclerosis (MS) and rheumatoid arthritis (RA), by means of autologous (“pseudoautologous”) HSCT [58]. These results considerably strengthened the philosophy of autologous HSCT for human ADs, even if it was pointed out later that in animal models the abnormality of the antigen-induced type seems to reside in immunocompetent T/B cells but not in the HSC, and therefore ASCT may be curative, while in spontaneous ADs new, unaffected HSC were necessary to achieve a cure [22]. In any case, the utilization of ASCT is now widely accepted for treating severe, refractory ADs.
A powerful immunosuppressive therapy for SADs has been developed at Johns Hopkins University in Baltimore, where such patients are treated with high-dose cyclophosphamide (CY) alone, with an inevitable delay of marrow and blood reconstitution, but with results that do not differ significantly from those obtained by ASCT [5].
Finally, two new approaches appear to be integrating this area. Mesenchymal stem cells (MSC) possess several immunomodulatory properties [44], have been shown to significantly ameliorate Graft-versus-Host Disease [25] (GVHD), and have been considered a valuable therapeutic option for SADs [56]. However the role of this kind of cellular therapy in human AD, whether associated with ASCT or not, is still to be established. Another fascinating approach is based on the idea of achieving antigen-specific tolerance to treat refractory ADs, even if translating such therapies from bench to bedside is still mainly theoretical. An approach combining HSCT and transduction of the culprit self-antigens in autologous HSCs in order to achieve central (thymic) tolerance has been developed by Alderuccio and his group [2], although only in animal experiments with organ-specific autoimmune conditions at this stage.
Autologous transplantation: progress and questions
In contrast to the long interval having taken place between the first allogeneic transplants for animal ADs and translational clinical trials, ASCT quickly followed the experimental investigations. It was proposed by myself for severe SLE in 1993 [36], and then for ADs in general in 1995 [30]. The first transplants were performed for a connective tissue disease [54] and for severe SLE [32]. The following utilization of ASCT for SADs grew almost exponentially, so much so that, besides the continually increasing registered transplants in the EBMT and CIBMTR registries, a recent study by Dominique Farge et al has analyzed 900 patients [14]. Excellent reviews of specific diseases have been published recently, and a monographic issue of Autoimmunity has just been devoted to this theme [28]. Here, I shall focus on the most significant and contemporary questions.
1. Autologous HSCT for ADs has been considered a relatively safe procedure from its inception, but is it becoming safer?
Autoimmune diseases represent an extremely heterogenous spectrum of diseases, and in most of them severe-refractory forms have a poor prognosis and a greatly impaired quality of life. One cannot disagree, however, with Burt’s statement that “Treatment-related mortality needs to be very low for non-malignant diseases”1. Treatment-Related Mortality (TRM) reached 12% in the initial EBMT Registry, decreased to 7 +3% in 2005, and finally did not exceed 5% in the most recent EBMT study [14]. In this last study evidence was also found of a clear center effect, indicating that experienced teams that are well acquainted with the multi-organ involvement of SADs produce superior results. In the case of a single disease such as SLE, a collection of 162 patients transplanted in 30 Centers showed a TRM of 11% [29], However of 200 patients transplanted at Northwestern University, Chicago, the TRM using non-myeloablative conditioning regimens in 200 patients was 1.5% [8]. This does not mean, of course, that TRM cannot grow much higher in very severe conditions such as advanced scleroderma. Scleroderma-related organ disfunction contributed to treatment-related deaths [43]. In conclusion, the answer to this first question is that ASCT may be considered reasonably safe when performed by experienced teams, appropriate conditioning regimens, and on patients who are not too disease-compromised. These data need to be counterbalanced by mortality from disease progression, and require the adoption of inclusion and exclusion criteria for each category of diseases, which cannot be detailed here. Although the inclusion of patients within approved or investigational protocols is the best policy, it must be realized that, in selected patients with advanced, refractory SADs, the decision to perform ASCT will ultimately rely on a combination of clinical acumen, experienced teams, and a good patient-doctor relationship.
2. Which are the most appropriate mobilization and conditioning regimens?
The source of HSCs was initially the bone marrow (BM), but has now changed to the peripheral blood (PB) following mobilization procedures. In the previously mentioned EBMT study of 900 patients the source was PB in 827 cases [43]. The most popular mobilizing regimens generally consist of combinations of cyclophosphamide (CY) and G-CSF [47]. Mobilizing regimens incorporating CY (from 2 to 4g/m2) have the additional, significant advantage of acting as an important therapeutic procedure per se (therapeutic mobilization). In our own experience of 9 SLE patients the achievement of a complete remission (CR) following mobilization with CY 4g/m2 enabled us, in 2 cases, to dispense from performing the initially programmed ASCT.
A variety of conditioning regimens have been utilized, but it could be shown that high-intensity protocols were followed by a lower probability of disease progression, albeit with a higher risk of TRM [16]. The strategy of performing intense immunosuppression without affecting the whole of the hematopoietic system is most generally accepted, taking into account that biologics such as Rituximab have a longer immunosuppressive activity than any chemotherapeutic agent. A combination of both strategies, in which Rituximab 500 mg is given before and after the regular 200 mg/kg CY protocol (the “sandwich technique”), is being currently utilized at Northwestern University, Chicago (USA). Anti-CD20 immunotherapy for the control of relapse following ASCT in patients with rheumatoid arthritis (RA) had been already utilized with success [41], and the strategy of using an additional immunotherapy in this area is attractive. Unfortunately a devastating complication, progressive multifocal leukoencephalopathy (PML), due to the activation of the John Cunningham virus (JCV), has been reported in a disquieting proportion of patients having been immunosuppressed with biological agents (Natalizumab, Rituximab). A recent review reported 52 patients as having developed PML, 7 of which had received HSCT (3 allogeneic, 4 autologous) for lymphoproliferative diseases [9]. Awareness is obviously needed of the potential for PML among Rituximab-treated patients. Maximal immunosuppression produces greater benefits, but may at the same time be associated with unforeseen iatrogenic complications.
3. What significant changes in the immune system take place following ASCT ? Are we really curing autoimmunity ?
No other aspect of the ASCT-based procedures has been the object of so much research, controversy, enthusiasm, and skepticism. A prolonged depression of CD4+ CD45RA cells is a general finding, and takes place following both ASCT and high-dose immunosuppressive therapy (HDIS) alone. The type of immunomodulation which then follows has been called a “black box” by Muraro and Douek [42], but, thanks to their own and others’ investigations, is becoming increasingly clear. High-dose immunosuppression reduces the population of autoimmune cells to minimal residual autoimmune disease (MRAD). While the cure of oncohematological disease requires the eradication of cancer SC, a different view is entertained for ADs. Two basic mechanisms have been postulated.The first has been defined as a “re-education” of the faulty immune system [1], obtained by restoring a diverse antigen-specific repertoire through reactivation of the thymic output (“thymic rebound”), which has also been shown to persist in adults, albeit in lesser measure. In a recent study of ASCT in 7 SLE patients the Berlin group has found evidence for an overwhelming regeneration of the adoptive immune system and of the B-cell lineage, which became apparently tolerant to self-antigens [3]. The second mechanism is closely related, and consists in the reconstitution of the regulatory T-cell pool following ASCT. Tregs (CD4+ CD25+) expressing the transcription factor Foxp3 are crucial in preventing autoreactivity and restraining autoimmunity throughout life. Experimental and clinical studies have demonstrated the impact of the T regulatory network in inducing post-transplant immune tolerance in SLE [63].
Are these changes sufficient and stable enough to guarantee a rebuilding of the immune system, configured in a way that is less likely to redevelop autoimmunity? The abundant and sophisticated studies undeniably display some controversies. In a first study in autotransplanted MS patients the T cells recognizing myelin basic protein were indeed initially depleted by immunoablation, but then rapidly expanded from the reconstituted T cell repertoire in 12 months [52]. More recently, an early recovery of CD4 T-cell receptor diversity was found after “lymphoablative” conditioning and autologous CD34 cell transplantation in systemic sclerosis (SSc) patients, suggesting that the treatment is not completely T-cell ablative (or, more generally immune SC-ablative), and thus not ultimately curative [51]. This contrasts with another recent study which found that CD34+-selected progenitor cells had limited survival capacity and are therefore unlikely to be a major source of carryover of autoimmune T-cell expansions [11]. However, in a comprehensive recent study analyzing original and pooled data from autotransplanted MS patients, Mondria et al [40] found not only the previously known persistence of CSF oligoclonal bands in 88% of the reported cases, but also the persistence of the soluble lymphocyte activator CD27 – thus concluding that complete eradication of activated lymphocytes from the CNS had not been established, despite an intensive immunosuppressive regimen including ATG, CY and total body irradiation (TBI), in two fractions of 5 Gy a day at days –2 and –1. Active demyelinization and axonal damage have been found to continue after ASCT [39]. Our own clinical experience has included late (and very late) relapses, in a way that suggested a recapitulation of the natural history of lupus. So whether pressing the reset button will turn out to be immunologically curative is still uncertain.
4. What type of benefit, if any, does ASCT confer to severe, progressive, relapsing-refractory ADs?
In a recent, provocative editorial commenting on the utilization of ASCT for SADs, and more specifically for the rheumatic diseases, Illei [23] has posed the question, whether “the glass is half full or half empty”.
The effects of ASCT may be divided into two phases: the early suppression of ongoing, immuno-inflammatory events, and the later resetting of the autoimmune clock, which is closely related to the length and grade of remission. The first effect is clearly due to the immunosuppressive conditioning regimens, and is proportional to the dose intensity, and also independent from HSC rescue. No sophisticated dynamics occur here, besides the well-known combination of immunosuppression and abrogation of its attending inflammation. This first effect is responsible for its dramatic disease-arresting (“nosostatic”) properties, which have been observed in practically all actively aggressive SADs, and most demonstratively in SLE. This change occurs in the aggressive phases of disease, where ASCT may well be the most potent salvage therapy available. A clear distinction of the diverse sensitivity to ASCT according to the phases of disease has been recently made by Shevchenko et al [49], who have divided the transplant strategies for MS into “early”, “conventional” and “salvage-late” procedures. Among the many examples of this early, dramatic therapeutic effect are, besides the cancellation of systemic symptoms, the almost immediate clearance of inflammatory urinary sediments in lupus nephritis, the rapid improvement of nailfold capillaroscopy in SSc [4], and the early abrogation of Gadolinium-enhancing lesions in MS [27]. The striking disappearance of diffuse calcinosis in a child with overlap connective disease [13] and the regression of dermal fibrosis in patients with severe scleroderma [43] may be considered intermediate changes.
The impact of ASCT on SADs in the long run has been discussed in several contributions. In the most important study, Progression Free Survival (PFS), which may be considered as the most accurate estimated outcome of a therapeutic procedure, was 43% at 3 years [14]. Three apparently contrasting aspects emerge: first, that in the overwhelming majority of patients no authentic immunological cure may be realistically expected; second, that dramatic remissions occur, may be life-saving, and even long term. Thirdly, in most relapses the utilization of conventional therapies, to which the patients were formerly refractory, is generally possible.
5. Is ASCT the best available treatment for SADs?
ASCT is a powerful therapeutic procedure for SADs. But can it be regarded as the best treatment available, considering the increasing utilization of new pharmacological, prospective (phase III) clinical trials, which are being actively pursued for SSc (the ASTIS trial in Europe and the SCOT trial in North America), MS (ASTIMS, which is probably the most advanced one), Crohn’s disease (ASTIC), and SLE (ASTIL)? It is clear that this is the only way to obtain a scientifically correct answer. However, the pace of medical progress is such, that by the time that these laborious trials will have reached statistical significance, new agents may have superseded those utilized in the non-transplant arms. Furthermore, in a sizable proportion of these patients' ASCT may be integrated with other therapeutic interventions, including high-dose immunoglobulins (HDIG), biologics and possibly new, “intelligent” molecules.
Allogeneic transplantation facts and questions
More cogently than for the autologous procedure, animal experiments and results from coincidental disease patients had indicated a powerful instrument to cure autoimmunity in Allo-SCT. In an international workshop held in 2005, it was stated that “the potential for a 1-time delivery of a curative therapy is outstanding” [17]. But will it really be so? Many clinical trials are being pursued worldwide, but I shall confine myself only to published material and our personal experience.
Clinical results
A retrospective EBMT study [10] has collected 35 patients having received 38 allogeneic transplants for various ADs, hematological and non-hematological. The donors were identical siblings for 24 patients, matched unrelated donors (MUD) for 3, mismatched related for 2 and syngeneic for 3 patients. Treatment related mortality (TRM) was 22.1% at 2 years and 30.7 at 5, while death due to progression of disease was 3.2% at 2 years and 8.7% at 5. Of the 29 surviving patients 55% achieved complete clinical and laboratory remission, and 24% achieved a partial remission. The consensus is that nonmyeloablative (NST), reduced intensity conditioning regimens (RIC) should be utilized [46].
Immunological aspects
The substitution of an immune system which is behaving badly by a normal, healthy one is the rationale of the allogeneic approach, and its successful achievement is the prerequisite for embarking on a treatment which has been saddled with a 30% mortality after 5 years [17]. Although it is predictable that TRM following Allo-SCT, if further pursued, will probably become lower, both with an improvement of the learning curve and with optimized conditioning regimens, and effective GVHD control, the only legitimate motivation for performing it is achieving a cure.Allo-SCT is traditionally regarded as a “platform for immunotherapy” [24]. An exhaustive analysis of the mechanisms by which it might cure ADs has been performed by Sykes and Nikolic [53], who have placed the previously discussed GVA effect in the foreground. A retrospective study showed, in analogy to an established pattern in oncohematological diseases, that there were more relapses of coincidental ADs in patients transplanted for hematological malignancies with no GVHD, than in those who developed it [19]. However this effect could not be detected in the recent EBMT study [10], and a much greater clinical material would be necessary to obtain significant evidence.Efforts have been made, as already attempted in oncohematological diseases, to separate GVHD from GVA. A potent GVA effect was demonstrated in rat models of EAE. Clinically there is a group of patients who had been allotransplanted for SADs, in whom donor lymphocyte infusions (DLI) were necessary to achieve full donor chimerism, which ultimately ensured complete remissions of the SADs (lit in 11). These results are counterbalanced with others, which are in favor of the hypothesis that mixed chimerism might be capable of inducing long-term remissions [7]. However it has been shown that increasing mixed chimerism is conducive to graft loss in children transplanted for non-malignant disorders [45]. Full chimerism was present in two patients with rheumatoid arthritis [26] and in a 7-year old boy with Evans syndrome, in whom two autologous transplants had been previously unsuccessful [57].
Controversial evidence, however, comes from the analysis of relapsed patients. There appear to be two types of relapses. An example of the first type is the report of a failure of Allo-SCT to arrest disease activity in a patient with MS having been successfully transplanted because of coincidental chronic myeloid leukemia [38]. Even more disquieting are the aforementioned reports of patients with SADs having received Allo-SCT, but having subsequently relapsed despite full donor chimerism. The first and widely acknowledged case was a female patient with rheumatoid arthritis (RA), who received an HLA-identical transplant because of gold-induced aplastic anemia [55] and the second another patient with RA and multiple myeloma (MM), in whom the myeloma was cured but the RA relapsed [31]. The most demonstrative case is the one of a patient with severe Evans syndrome, who was transplanted from his HLA-identical sister but needed a series of DLI in order to achieve full donor chimerism and complete hematological remission. This patient unfortunately relapsed and died with a terminal hemolytic-uremic syndrome 5 years later [20]. The patient was male and had received the bone marrow of his HLA-identical sister. The immunoglobulins (IgG, IgM) eluted from his 100% XX expanded B cells were not the ones eluted from his Coombs-positive cells. It was hypothesized that the autoantibodies might have been secreted by long-lived host plasmacytes surviving in postulated marrow niches [18]. Even allowing for the hypothesis that relapses in donor cells in patients transplanted for leukemia might be less uncommon than generally thought to be, it is still an extremely rare event, having been identified in 14 out of 10,489 transplants in a recent survey [37]. In contrast, 3 relapses in the much smaller group of autoimmune allotransplanted patients inevitably causes some perplexity. Only further careful investigations will hopefully elucidate this unexpected problem.
Syngeneic transplants are a niche event. Three patients with RA received syngeneic transplants following high-dose immunosuppression. The first was a patient with severe seronegative RA, who enjoyed a long-term remission [59]. However a second patient with progressively erosive, rheumatoid factor positive RA, who was treated with high-dose CY and received an unmanipulated peripheral blood graft (PBSCT) from her identical twin sister, had a poor clinical response, associated with serological persistence64. A still unpublished case is the one of 45 year old lady with severe seropositive RA who was transplanted in Genoa from her identical twin sister on July 29, 2005. The conditioning regimen consisted of CY, 160 mg/Kg. Both rheumatoid factor and anti-cyclic citrulline peptide (CCP) titres decreased significantly (CCP from 234 to 2), but there was a clinical relapse with fever, polyarthritis and elevation of ESR, requiring further treatment.
Concluding remarks
Is there, at the time of this writing, sufficient evidence to answer the question, as to whether HSCT, in its various paradigms, is and will be the best available therapy for SADs? There has been a tendency to place the cause of autoimmunity on a faulty immune system, thus assimilating ADs to the neoplastic lymphoproliferative diseases. However most ADs result from a combination of faulty immune systems and antigen (target organ) dysfunctions. The distinction between primary and secondary ADs, the first being sustained by primary immune defaults and the latter by a predominant antigenic trigger, has been considered as helpful for the evaluation of SCT interventions. However the interaction between immune system and target organ antigenicity is extremely tight.
The autologous procedure is being performed worldwide because of its combination of safety and efficacy. It is capable of arresting progressive, otherwise refractory ADs. In addition, if utilized early in appropriate patients, it favorably changes the course of disease, even allowing for varying degrees of regeneration. Whether the autoaggressive immune system is being re-educated or, more simply, reset, is still not fully clarified. With this background, I believe that Illei’s glass [39] is more full than empty, when ASCT is performed in an early stage of disease (fig. 1). However , independently from the results, I believe that there ultimately will be an integration between the two approaches, with careful selection of individual patients.
A word of caution must be said concerning the potential development not only of PML, as already discussed, but also of therapy-related myelodysplasia and leukemia (t-MDS, t-AML), which must be closely watched for when utilizing alkylating drugs and others. Fortunately, there haven’t been such reports in this area, and recourse to ASCT in patients with SADs should not be hindered by the fear of late malignant complications, although careful long-term surveillance is mandatory.
Great expectations have been associated with allogeneic SCT, but its position is still uncertain. Ongoing trials will hopefully offer some answers to the question, or hope, whether the total eradication of a faulty immune system will be sufficient, and whether there is solid evidence of a clinically exploitable GVA effect. The unexpected relapses despite full donor chimerism are still a problem, but further experience is needed.
Summary
Two different sets of investigation are at the origin of hematopoietic stem cell transplantation (HSCT) for severe autoimmune diseases (SADs). The experimental evidence consisted in the transfer/cure of animal SADs as murine lupus by means of allogeneic but also, almost paradoxically, autologous HSCT. The clinical arm comes from serendipitous reports of patients allotransplanted for coincidental diseases, and finally cured of both conditions. The encouraging results of ASCT in experimental ADs were enthusiastically translated into human therapy by clinicians hoping to achieve great results without incurring into the rigors associated with the allogeneic procedure.
Well over 1000 ASCT for SADs have been performed worldwide at this time with multiple sclerosis (MS) and connective tissue diseases in the foreground. Transplant-related mortality (TRM) and morbidity have decreased to well under 5%. A dramatic disease-arresting effect is a constant benefit, but the whole course of the disease appears to be influenced favorably. Profound changes of the autoimmune circuitry have been demonstrated, but no authentic eradication of disease (cure?) should realistically be expected. Important multicentric prospective trials are ongoing to compare ASCT to the best available non-transplant therapies, but it may be argued that in the end both approaches will be integrated for single patients, and that new agents will possibly alter present strategies.
Allogeneic STC is eliciting great expectations, but the burden of higher mortality and morbidity with GVHD in the first place, must be considered, even when making recourse to reduced conditioning regimens (RIC). Paradoxical relapses despite complete donor chimerism have been reported. Further experience is clearly needed, but the early enthusiasm for an attractive one-shot therapy must be tempered with a realistic evaluation, at least until new significant breakthroughs have been attained.
Acknowledgements
This article is based on the materials of the perspective article in the International Journal of Clinical Rheumatology 2009; 4(4):395-408.
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Альберто М. Мармонт
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На ТАСК возлагаются большие надежды, но никогда нельзя забывать о её последствиях - высокой смертности и осложнениях, прежде всего, в результате РТПХ, даже если для профилактики используют режимы предварительного кондиционирования. </p> <h3>Ключевые слова</h3> <p>аутоиммунные болезни, трансплантация гемопоэтических стволовых клеток, аллогенная трансплантация, аутологичная трансплантация </p>" ["TYPE"]=> string(4) "HTML" } ["DESCRIPTION"]=> string(0) "" ["VALUE_ENUM"]=> NULL ["VALUE_XML_ID"]=> NULL ["VALUE_SORT"]=> NULL ["~VALUE"]=> array(2) { ["TEXT"]=> string(2741) "Для обоснования целесообразности трансплантации гемопоэтических стволовых клеток (ТГСК) при тяжёлых аутоиммунных болезнях (ТАБ) приводятся результаты двух различных серий исследований. Экспериментальные доказательства основываются на положительных результатах лечения ТАБ (волчанки) у мышей посредством трансплантации аллогенных, а также, что звучит почти невероятно, аутологичных гемопоэтических стволовых клеток. Клинические доказательства основываются на сообщениях о аллотрансплантациях, сделанных по поводу других заболеваний, в результате чего были успешно вылечены и сопуствующие ТАБ. В настоящее время продолжаются мультицентрические клинические исследования, результаты которых позволят сравнить лечебный эффект трансплантации аллогенных стволовых клеток (ТАСК) с уже наиболее положительно зарекомендовавшими себя схемами лечения ТАБ без применения ТГСК, хотя, не исключено, что в будущем, в каких-то конкретных клинических случаях могут быть использованы оба подхода, и существующая лечебная тактика будет скорректирована при появлении новых лечебных препаратов. На ТАСК возлагаются большие надежды, но никогда нельзя забывать о её последствиях - высокой смертности и осложнениях, прежде всего, в результате РТПХ, даже если для профилактики используют режимы предварительного кондиционирования.
Ключевые слова
аутоиммунные болезни, трансплантация гемопоэтических стволовых клеток, аллогенная трансплантация, аутологичная трансплантация
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autoimmune diseases, hematopoietic stem cell transplantation
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autoimmune diseases, hematopoietic stem cell transplantation
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Keywords
autoimmune diseases, hematopoietic stem cell transplantation
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Экспериментальные доказательства основываются на положительных результатах лечения ТАБ (волчанки) у мышей посредством трансплантации аллогенных, а также, что звучит почти невероятно, аутологичных гемопоэтических стволовых клеток. Клинические доказательства основываются на сообщениях о аллотрансплантациях, сделанных по поводу других заболеваний, в результате чего были успешно вылечены и сопуствующие ТАБ. В настоящее время продолжаются мультицентрические клинические исследования, результаты которых позволят сравнить лечебный эффект трансплантации аллогенных стволовых клеток (ТАСК) с уже наиболее положительно зарекомендовавшими себя схемами лечения ТАБ без применения ТГСК, хотя, не исключено, что в будущем, в каких-то конкретных клинических случаях могут быть использованы оба подхода, и существующая лечебная тактика будет скорректирована при появлении новых лечебных препаратов. На ТАСК возлагаются большие надежды, но никогда нельзя забывать о её последствиях - высокой смертности и осложнениях, прежде всего, в результате РТПХ, даже если для профилактики используют режимы предварительного кондиционирования. </p> <h3>Ключевые слова</h3> <p>аутоиммунные болезни, трансплантация гемопоэтических стволовых клеток, аллогенная трансплантация, аутологичная трансплантация </p>" ["TYPE"]=> string(4) "HTML" } ["DESCRIPTION"]=> string(0) "" ["VALUE_ENUM"]=> NULL ["VALUE_XML_ID"]=> NULL ["VALUE_SORT"]=> NULL ["~VALUE"]=> array(2) { ["TEXT"]=> string(2741) "Для обоснования целесообразности трансплантации гемопоэтических стволовых клеток (ТГСК) при тяжёлых аутоиммунных болезнях (ТАБ) приводятся результаты двух различных серий исследований. Экспериментальные доказательства основываются на положительных результатах лечения ТАБ (волчанки) у мышей посредством трансплантации аллогенных, а также, что звучит почти невероятно, аутологичных гемопоэтических стволовых клеток. Клинические доказательства основываются на сообщениях о аллотрансплантациях, сделанных по поводу других заболеваний, в результате чего были успешно вылечены и сопуствующие ТАБ. В настоящее время продолжаются мультицентрические клинические исследования, результаты которых позволят сравнить лечебный эффект трансплантации аллогенных стволовых клеток (ТАСК) с уже наиболее положительно зарекомендовавшими себя схемами лечения ТАБ без применения ТГСК, хотя, не исключено, что в будущем, в каких-то конкретных клинических случаях могут быть использованы оба подхода, и существующая лечебная тактика будет скорректирована при появлении новых лечебных препаратов. На ТАСК возлагаются большие надежды, но никогда нельзя забывать о её последствиях - высокой смертности и осложнениях, прежде всего, в результате РТПХ, даже если для профилактики используют режимы предварительного кондиционирования.
Ключевые слова
аутоиммунные болезни, трансплантация гемопоэтических стволовых клеток, аллогенная трансплантация, аутологичная трансплантация
" ["TYPE"]=> string(4) "HTML" } ["~DESCRIPTION"]=> string(0) "" ["~NAME"]=> string(29) "Описание/Резюме" ["~DEFAULT_VALUE"]=> array(2) { ["TEXT"]=> string(0) "" ["TYPE"]=> string(4) "HTML" } ["DISPLAY_VALUE"]=> string(2741) "Для обоснования целесообразности трансплантации гемопоэтических стволовых клеток (ТГСК) при тяжёлых аутоиммунных болезнях (ТАБ) приводятся результаты двух различных серий исследований. Экспериментальные доказательства основываются на положительных результатах лечения ТАБ (волчанки) у мышей посредством трансплантации аллогенных, а также, что звучит почти невероятно, аутологичных гемопоэтических стволовых клеток. Клинические доказательства основываются на сообщениях о аллотрансплантациях, сделанных по поводу других заболеваний, в результате чего были успешно вылечены и сопуствующие ТАБ. В настоящее время продолжаются мультицентрические клинические исследования, результаты которых позволят сравнить лечебный эффект трансплантации аллогенных стволовых клеток (ТАСК) с уже наиболее положительно зарекомендовавшими себя схемами лечения ТАБ без применения ТГСК, хотя, не исключено, что в будущем, в каких-то конкретных клинических случаях могут быть использованы оба подхода, и существующая лечебная тактика будет скорректирована при появлении новых лечебных препаратов. На ТАСК возлагаются большие надежды, но никогда нельзя забывать о её последствиях - высокой смертности и осложнениях, прежде всего, в результате РТПХ, даже если для профилактики используют режимы предварительного кондиционирования.
Ключевые слова
аутоиммунные болезни, трансплантация гемопоэтических стволовых клеток, аллогенная трансплантация, аутологичная трансплантация
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Alois Gratwohl
Department of Hematology, University of Basel, Switzerland
Autologous and allogeneic hematopoietic stem cell transplantation (HSCT) have some common and some clearly distinct goals. All current available information suggests that autologous HSCT should remain the standard approach to clinical HSCT for patients with severe autoimmune disorders, including multiple sclerosis. Allogeneic HSCT should be considered in rare patients with specific features that they are likely to benefit more from an allogeneic HSCT, e.g. young patients with no co-morbidities and hematological autoimmune cytopenias.
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[TEXT] => <p class="bodytext">Высокодозная иммуносупрессивная терапия и трансплантация аутологичных гемопоэтических стволовых клеток (HSCT) была введена в практику лечения больных рассеянным склерозом (РС) в 1995 г. Было показано, что HSCT является здесь наиболее эффективной иммуносупрессивной и противовоспалительной терапией. <br /><br />Во всех сообщениях, начиная с 2000 г., отмечается существенное (почти на 100%) снижение, или полное исчезновение признаков заболевания (воспаления), выявляемое с помощью метода ядерно-магнитного резонанса, и этот эффект сохраняется в течение длительного времени, в отличие от всех других методов лечения РС. Несмотря на весьма впечатляющие результаты применения HSCT для лечения РС, её преимущества были продемонстрированы только в сравнительных исследованиях. Поэтому представляется абсолютно необходимым завершить текущие рандомизированные исследования по сравнению HSCT с митоксантроном (ASTIMS) или с другими стандартными методами терапии. Пока не будут получены окончательные результаты этих исследований, HSCT не может быть принят как общепризнанный метод лечения больных с РС, которые могут быть лишены возможности получить действительно эффективную иммуносупрессивную и иммуномодулирующую терапию с длительным положительным воздействием на течение болезни.
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Во всех сообщениях, начиная с 2000 г., отмечается существенное (почти на 100%) снижение, или полное исчезновение признаков заболевания (воспаления), выявляемое с помощью метода ядерно-магнитного резонанса, и этот эффект сохраняется в течение длительного времени, в отличие от всех других методов лечения РС. Несмотря на весьма впечатляющие результаты применения HSCT для лечения РС, её преимущества были продемонстрированы только в сравнительных исследованиях. Поэтому представляется абсолютно необходимым завершить текущие рандомизированные исследования по сравнению HSCT с митоксантроном (ASTIMS) или с другими стандартными методами терапии. Пока не будут получены окончательные результаты этих исследований, HSCT не может быть принят как общепризнанный метод лечения больных с РС, которые могут быть лишены возможности получить действительно эффективную иммуносупрессивную и иммуномодулирующую терапию с длительным положительным воздействием на течение болезни.
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[TEXT] => <p class="bodytext">High-dose immunosuppressive therapy with hemopoietic stem cell transplantation (HSCT) was already introduced into the management of multiple sclerosis (MS) in 1995. HSCT has been shown to be a most powerful immunosuppressive and anti-inflammatory treatment. Since 2000, all communications have consistently reported a dramatic, almost 100%, reduction in, or disappearance of, disease activity (inflammation) on magnetic resonance imaging (MRI), which is retained over time and has not been observed as an outcome of any other MS treatment. Despite the very interesting outcomes of HSCT in treatment of MS, it is only in comparative trials that its superiority over other therapies can be demonstrated. Therefore, it is absolutely necessary to complete the running randomized studies comparing HSCT with mitoxantrone (ASTIMS) or other standard therapies. Unless such trials yield their final results, HSCT will never be approved as an established therapy for MS patients who may so miss the opportunity of receiving an active, powerful immunosuppressive and immunomodulating treatment having a long-term beneficial impact on the course of the disease.
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Athanasios Fassas
Department of Hematology and Bone Marrow Transplantation Unit, Cell and Gene Therapy Unit, George Papanicolaou Hospital, Thessaloniki, Greece
High-dose immunosuppressive therapy with hemopoietic stem cell transplantation (HSCT) was already introduced into the management of multiple sclerosis (MS) in 1995. HSCT has been shown to be a most powerful immunosuppressive and anti-inflammatory treatment. Since 2000, all communications have consistently reported a dramatic, almost 100%, reduction in, or disappearance of, disease activity (inflammation) on magnetic resonance imaging (MRI), which is retained over time and has not been observed as an outcome of any other MS treatment. Despite the very interesting outcomes of HSCT in treatment of MS, it is only in comparative trials that its superiority over other therapies can be demonstrated. Therefore, it is absolutely necessary to complete the running randomized studies comparing HSCT with mitoxantrone (ASTIMS) or other standard therapies. Unless such trials yield their final results, HSCT will never be approved as an established therapy for MS patients who may so miss the opportunity of receiving an active, powerful immunosuppressive and immunomodulating treatment having a long-term beneficial impact on the course of the disease.
Reviews
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[TEXT] => <p class="bodytext">Для обоснования целесообразности трансплантации гемопоэтических стволовых клеток (ТГСК) при тяжёлых аутоиммунных болезнях (ТАБ) приводятся результаты двух различных серий исследований. Экспериментальные доказательства основываются на положительных результатах лечения ТАБ (волчанки) у мышей посредством трансплантации аллогенных, а также, что звучит почти невероятно, аутологичных гемопоэтических стволовых клеток. Клинические доказательства основываются на сообщениях о аллотрансплантациях, сделанных по поводу других заболеваний, в результате чего были успешно вылечены и сопуствующие ТАБ. В настоящее время продолжаются мультицентрические клинические исследования, результаты которых позволят сравнить лечебный эффект трансплантации аллогенных стволовых клеток (ТАСК) с уже наиболее положительно зарекомендовавшими себя схемами лечения ТАБ без применения ТГСК, хотя, не исключено, что в будущем, в каких-то конкретных клинических случаях могут быть использованы оба подхода, и существующая лечебная тактика будет скорректирована при появлении новых лечебных препаратов. На ТАСК возлагаются большие надежды, но никогда нельзя забывать о её последствиях - высокой смертности и осложнениях, прежде всего, в результате РТПХ, даже если для профилактики используют режимы предварительного кондиционирования.
</p>
<h3>Ключевые слова</h3>
<p>аутоиммунные болезни, трансплантация гемопоэтических стволовых клеток, аллогенная трансплантация, аутологичная трансплантация
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Ключевые слова
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[TEXT] => <p class="bodytext">Two different sets of investigation are at the origin of hematopoietic stem cell transplantation (HSCT) for severe autoimmune diseases (SADs). The experimental evidence consisted in the transfer/cure of animal SADs as murine lupus by means of allogeneic but also, almost paradoxically, autologous HSCT. The clinical arm comes from serendipitous reports of patients allotransplanted for coincidental diseases, and ultimately cured of both conditions. Important multicentric prospective trials are ongoing to compare ASCT to the best available non-transplant therapies, but it may be argued that in the end both approaches will be integrated for single patients, and that new agents will possibly alter present strategies. Allogeneic STC is eliciting great expectations, but the burden of higher mortality and morbidity as a result of GVHD in the first place must be considered, even when making recourse to reduced conditioning regimens (RIC).
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<h3>Keywords</h3>
<p>autoimmune diseases, hematopoietic stem cell transplantation </p>
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autoimmune diseases, hematopoietic stem cell transplantation
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Alberto M. Marmont
II Division of Hematology and Stem Cell Transplantation, Center Azienda Ospedaliera-Universitaria S. Martino, Genoa, Italy
Two different sets of investigation are at the origin of hematopoietic stem cell transplantation (HSCT) for severe autoimmune diseases (SADs). The experimental evidence consisted in the transfer/cure of animal SADs as murine lupus by means of allogeneic but also, almost paradoxically, autologous HSCT. The clinical arm comes from serendipitous reports of patients allotransplanted for coincidental diseases, and ultimately cured of both conditions. Important multicentric prospective trials are ongoing to compare ASCT to the best available non-transplant therapies, but it may be argued that in the end both approaches will be integrated for single patients, and that new agents will possibly alter present strategies. Allogeneic STC is eliciting great expectations, but the burden of higher mortality and morbidity as a result of GVHD in the first place must be considered, even when making recourse to reduced conditioning regimens (RIC).
Keywords
autoimmune diseases, hematopoietic stem cell transplantation