Hematopoietic Growth Factors for the Treatment of Severe Chronic Neutropenia
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1 Hematopoietic Growth Factors for the Treatment of Severe Chronic Neutropenia David C. Dale Department of Medicine, University of Washington, Seattle, Washington, USA Key Words. Neutropenia Chronic neutropenia Granulocyte colony-stimulating factor G-CSFIFilgrastim Kostmann s syndrome Cyclic neutropenia Idiopathic neutropenia Cytokine therapy Abstract. Severe chronic neutropenia (SCN) is a rare but important cause of recurrent fevers, oropharyngeal ulcerations and severe infections. In three forms of SCN, i.e., congenital neutropenia (Kostmann s syndrome and related syndromes), idiopathic neutropenia (both childhood and adult), and cyclic neutropenia, it is now established that long-term treatment with the hematopoietic growth factor, recombinant human granulocyte colony stimulating factor (rhuc-csf or Filgrastim), can elevate blood neutrophil counts to the normal range in most patients, with a concomitant reduction in infection-related events including fever, oral ulcerations, antibiotic use and symptoms of inflammation. Treatment with this growth factor causes an increase in the number and maturity of marrow cells of the neutrophilic series; other cell lines are largely unaffected. Marrow stimulation and expansion are reflected by the occurrence of bone pain early in therapy, as well as some increase in spleen size in most cases. Adverse effects of therapy are infrequent in both children and adults, and long-term treatment with daily or every-other-day S.C. injections of rhuc-csf are well accepted. Because of the risk that some patients with chronic neutropenia may have or develop myelodysplasia and/or leukemia, careful pretreatment evaluations (blood, bone marrow and cytogenetics) and longterm observations are extremely important. An international registry for patients with SCN has been established to maintain records and further investigate these conditions. Correspondence: Dr. David C. Dale, Department of Medicine RG-22, University of Washington Medical Center, Seattle, WA USA. Received August 24, 1994; accepted for publication August 24, OAlphaMed Press /95/$5.00/0 Introduction Neutropenia is associated with a predictable pattern of fever and oropharyngeal, gastrointestinal, perianal and cutaneous infections; the risk is greater with progressively lower counts. Ordinarily neutropenia is defied as a blood neutrophil count below 1.8 x 109/1, although some healthy individuals and some specific populations, particularly people of African origin, may normally have neutrophil counts of 1.0 x 109/1 without apparent ill effects. The association of neutropenia and infections is clearest for individuals with counts sustained below 0.5 x 109/1, and most problems occur when counts are below 0.2 X 109/l. The duration of neutropenia and the function of the neutrophils, as well as the intactness of other host defenses, are vitally important in determining when infections occur. Although superficial infection and inflammation such as oral ulcerations, gingivitis and painful inflammation of other tissues are a cause for considerable morbidity in patients with neutropenia, it is the deeper tissue infections of the sinuses, lungs, liver and blood which are truly life-threatening. The repetitive use of antibiotics is the major reason for infections with resistant bacteria, yeast and fungi in these patients [ The hematopoietic growth factors have rapidly revolutionized our approach to neutropenia [5, 61. Many of the problems associated with neutropenia following cancer chemotherapy and bone marrow transplantation are now prevented by the use of granulocyte colony-stimulating factor (G-CSF) and granulocytemacrophage CSF (GM-CSF) [6]. Their use for neutropenia occuning as an idiosyncratic reaction to drugs, i.e., antibiotics, psychotropic agents, antithyroid drugs, etc., is not yet supported by STEM CELLS 1995;13:94-100
2 95 Treatment of Severe Chronic Neutropenia randomized controlled trials but has become common practice [7-91. Many other uses for these colony stimulating factors and other growth factors are under investigation. Recently controlled trials established the benefit of recombinant human (rhu)g-csf for the treatment of severe chronic neutropenia (SCN) [lo], and it has been approved for marketing andor clinical use for this indication in the US and many other countries. Approval for this indication has just been granted by the U. S. Food and Drug Administration. Disorders Causing SCN Chronic neutropenia is a general term for conditions with neutrophil counts less than 1.8 x 109/1 lasting for months or years; with SCN, counts are regularly or recurrently less than 0.5 x 109A. Chronic neutropenia is caused by a variety of hematological, immunological, metabolic and infectious diseases (Table I). For most of these conditions, the precise genetic and cellular mechanisms of neutropenia have not been delineated [ 11. Most are considered to be disorders of production, but some immunological and infectious diseases causing neutropenia are due to alterations of cell kinetics and accelerated utilization or a combination of mechanisms. Investigations of the use of the hematopoietic growth factors for treatment of the chronic neutropenias has proceeded largely on an empirical basis driven by the inadequacy of other therapies and the severe clinical problems of these patients. Clinical Trials in Congenital, Cyclic and Idiopathic Neutropenia Clinical trials of the treatment of congenital,cyclic and idiopathic neutropenia with G-CSF and GM-CSF began in Two open-label, single-center phase 1/11 trials in children with severe congenital neutropenia demonstrated that rhug-csf in doses of 3 to 60 pg/kg/day increased blood neutrophil levels and reduced chronic infection and inflammation [ 1 1, 121. The responses often took several days to occur because of the time required for neutrophil formation and maturation in the bone marrow. In some patients Table I. Causes of chronic neutropenia Hematological diseases ImmunoIogicaI Diseases Nutritional and metabolic diseases Infections Other Congenital neutropenia Kostmann s syndrome Schwachman-Diamond syndrome Cyclic neutropenia Childhood idiopathic neutropenia Adult idiopathic neutropenia Aplastic anemia Myelodysplastic syndrome Congenital immunodeficiency syndromes (SCID) Isoimmune neonatal neutropenia Autoimmune neutropenia Autoimmune diseases with neutropenia - rheumatoid arthritis, SjBgren s syndrome Systemic lupus erythematosus Vitamin BIZ, folate deficiency Glycogen storage disease type Ib Gaucher s disease Transcobalamin deficiency Human immunodeficiency virus Parvovirus Hepatitis viruses Malaria Kala azar Chemotherapy Radiation therapy
3 Dale 96 even modest increases in neutrophils were associated with clinical improvement. In a few patients, platelet decreases were noted, generally not necessitating discontinuation of treatment. Treatment of cyclic neutropenia was first reported for six patients administered 3 to 10 pg/kg/day (i.v. or s.c.) for periods of two months or more [13]. This study showed that in cyclic neutropenia oscillations of the blood neutrophil levels persisted on therapy, but the cycle length shifted from 21 to 14 days with marked abbreviation of the duration of severe neutropenia. Other blood cells also oscillated on therapy, and this regular cycling persisted indefinitely. Clinical benefit was demonstrated by a reduction in the episodes of fever and the occurrence and severity of mouth ulcers. Increased marrow cellularity with increased percentages of marrow neutrophils, normal blood half-life for the cells produced in response to G-CSF, and normal inflammatory responses utilizing the skin chamber technique were also reported [ 131. In a case report, one patient with chronic idiopathic neutropenia responded rapidly to daily S.C. G-CSF with reductions in episodes of fevers, hospitalizations and antibiotic treatments [ 141. Subsequently, numerous additional cases have been reported [ Concomitant with these trials, a somewhat smaller number of patients with congenital, cyclic and idiopathic neutropenia were treated with rhugm-csf [12, 18-20]. Available data suggest that neutrophil responses occur less frequently and were of smaller magnitude than with rhug-csf. Eosinophilia and a variety of inflammatory symptoms (local skin reactions, fever and myalgias) were also reported. On the basis of this information almost all subsequent trials have used rhug-csf. With the very encouraging results with rhug-csf in phase I/II trials, a phase 111 randomized, controlled trial was conducted in the US. beginning in late 1988 [21]. Patients eligible for enrollment had a minimum of six months of severe neutropenia with at least three measurements of the absolute neutrophil count (ANC) less than 0.5 x 109/l. The diagnosis of cyclic neutropenia required documentation of regularly recurrent episodes of counts below this level at approximately 2 1 -day intervals. Patients enrolled also had a history of at least three infections in the last 12 months or a single life-threatening infection. Patients with marrow or chromosomal evidence of a myeloid malignancy were excluded, but patients with idiopathic neutropenia associated with large granular lymphocytes (less than 5.0 x 109/1) were included. Patients with Felty s syndrome and other autoimmune disorders, severe anemia and/or thrombocytopenia, and concomitant treatment with other drugs which might influence the blood neutrophil level were excluded. The trial enrolled 123 patients (60 congenital, 21 cyclic and 42 idiopathic); the age range was 0.6 to 76 years, median 12 years. One hundred twenty of these patients had evaluable responses. The results strongly supported the conclusions of the phase I/II studies [21]. Defining a complete response as maintenance of median neutrophil count of greater than 1.5 x 109/1, 90% of the patients showed a complete response to treatment, and almost all patients improved in some way during the initial four months of treatment (Table 11). The median increase in blood neutrophil levels was 16-fold over the baseline count. There was also a statistically significant reduction in the occurrence of fever, mouth ulcers, infections and requirement for antibiotics (Table 111, [21]). Table 11. rhug-csf phase I11 trial: response rates Idiopathic Cyclic Congenital Total Complete Response (ANC > 1,500/mm3) Partial Response (500 S ANC S1,500/mm3) No Response (ANC < 500/mm3) Total rhug-csf = recombinant human granulocyte colony-stimulating factor; ANC = absolute neutrophil count
4 91 Treatment of Severe Chronic Neutropenia Table 111. The relative frequency of fever and other signs and symptoms for patients in the phase 111 trial of rhug-csf Fever Stomatitis Sore throat Lymphadenopathy Abdominal pain Cellulitis Pustules Diarrhea Rash Headache Bone pain Pain Untreated rhug-csf rhug-csf (MO6.0-5) (Mos. 5-17) 17% 60% 18% 11% 15% 8% 6% 18% 4% 24% 6% 27% 20% 4% 9% 2% 1% 15% 35% 17% 25% 28% 11% 4% 1% 2% 8% 6% 24% 5% 11% G-CSF doses required to achieve these responses varied by patient group, as was noted in the phase I/II trials. Patients with idiopathic neutropenia and cyclic neutropenia, who tend to have milder marrow abnormalities and somewhat higher blood neutrophil counts, responded to the lowest doses of rhug-csf, usually. 1 to 5 pgkglday. Patients with congenital neutropenia often required higher doses of G-CSF, i.e., 5 to 15 pglkglday, administered once or twice per day. The hematological effects of long-term rhug-csf included increased marrow cellularity, with increases in both mature neutrophils and their precursors. The percentage of early myeloid cells, i.e., myeloblasts, was not increased significantly in marrow or blood. Cells of the erythroid series were generally unaffected. Platelet counts diminished to less than 1 x lo5 per mmz in about of patients on long-term therapy; lower levels were very uncommon [21]. The mechanisms of thrombocytopenia, i.e., altered production versus altered turnover, were not investigated. Other hematologic effects included bone pain during the early phases of treatment and increased spleen size, generally detectable only by magnetic resonance imaging (MRI) or computerized tomography (CT). Other adverse events in the phase I/II and phase 111 trials were infrequent (Table 111). These included headaches (generally early in treatment), vasculitis, hematuria and osteopenia. As a result, most patients beginning rhug-csf treatment have continued long-term maintenance. Withdrawal from therapy has resulted in recurrence of neutropenia in almost all cases. Long-Term Treatment Results There are now observations of patients given daily rhug-csf for up to seven years. More than 200 patients have received more than three years of daily or intermittent therapy [ 10, 22 and Dale et al., unpublished data]. These data suggest that most patients can be maintained on a stable dose of rhug-csf without a significant alteration of their hematological responses, evidence for exhaustion of precursor populations, changes in other cell types, progression of splenic enlargement or the development of antibodies to the rhug-csf. To date, growth and development of children on long-term rhug-csf, maturation of adolescents during puberty and menarche, and the clinical courses of older adults, potentially at greater risk for adverse cardiovascular, pulmonary or neurological events, appear to be unaffected by longterm rhug-csf therapy. The acceptance of patients of the requirement for daily S.C. injections of rhug-csf is also noteworthy [23,24]. From the inception of trials of long-term growth factor treatment of neutropenia, there have been concerns whether this treatment might be associated with hematologic toxicities and the evolution of myeloid malignancies. Prior to the availability of the hematopoietic growth factors, it was recognized that myeloid malignancies, particularly acute myeloid leukemia (AML), occurs in congenital aplastic anemia and several forms of SCN [ The precise incidence or lifetime risk of leukemia or myelodysplasia in these conditions, however, is not known. For the patients with cyclic and
5 Dale 98 congenital neutropenia enrolled in phase 1/11 trials between August 1987 and March 1990, 3 of 54 patients have developed leukemia or myelodysplastic syndrome (MDS) over a period of four to seven years of treatment [22]. In the randomized controlled trial in the U.S. with 123 patients enrolled, four patients had evidence of leukemia and/or myelodysplasia prior to treatment, but no new cases were observed during the initial five months on therapy when treatment was randomly assigned. Longer term, six patients from this population have evolved to have chromosomal abnormalities, and two have developed AML [unpublished data]. In a few other cases treated outside defined protocols, evolution to MDS or AML has been noted, but the total number of patients receiving such treatment is not known. It is important to note that almost all of these cases have evolved in patients with severe congenital neutropenia, most categorized as Kostmann s syndrome. Patients with cyclic or idiopathic neutropenia (children and adults) have generally not shown evidence of evolution. These observations suggest that it is the underlying marrow disease or interaction of the growth factor with a premalignant marrow, rather than the growth factor itself, which is the cause for the transformations that have been observed. On the basis of these data, some current recommendations for the use of rhug-csf for SCN follow: 1. Recombinant human G-CSF is an effective therapy for SCN, serving to elevate blood neutrophils and to reduce the occurrence of fever, mouth ulcers and recurrent infections. Some patients without symptoms despite severe neutropenia may not require treatment but may be observed expectantly. 2. When rhug-csf is started, there may be a delay of up to a week or ten days before the blood neutrophil response. This occurs because most patients with SCN have few or no mature neutrophils in the marrow to release into the blood, and their production takes several days. 3. The dose of rhug-csf to achieve a normal blood neutrophil count varies substantially, from less than 0.5 pg/kg/day to greater than 100 pglkglday, but most patients (i.e., more than 90%) respond to doses of 1 to 12 pg/kg/day. In patients who are not severely ill, it is reasonable to start with a low dose working upwards at intervals of one to two weeks rather than to start with a high dose and then reduce it. This approach will probably help to avoid bone pain. For patients with idiopathic or cyclic neutropenia (children and adults), a starting dose of 1 to 3 pg/kg/day is suitable in most cases, although 3 to 5 pg/kg/day will generally not cause an excessive response. For congenital neutropenia, a dose of 5 to 10 pgtkglday (either as a single or divided dose) is recommended. In severely ill patients, a higher starting dose, i.e., 5 to 20 pglkglday, may be beneficial, but this has not been studied systematically. There is probably a physiological limit to how rapidly the neutrophils can occur, but the limits of this response are also not known. 4. The goal of therapy is to prevent infections by maintaining a normal or near normal blood neutrophil level. It is possible that maintaining neutrophils at a level of 0.5 to 1.5 x 109/1 will be sufficient to prevent bacterial infections, but this lower threshold has not been studied carefully. Assessment of the response to rhug-csf treatment requires careful follow-up with regular measurements of the complete blood counts (CBCs). The CBC should be measured two to three times per week for the first two to three weeks of treatment and then once per week for one to two months. Thereafter, less frequent monitoring, probably on a monthly basis, is recommended. Dosing should be adjusted on the basis of serial counts measuring the blood neutrophils just before the next scheduled dose. Because blood neutrophil counts vary considerably in these patients, it is best to make dose adjustments based upon a series of counts rather than single values and to try to keep the dosing reasonably constant. 5. Most patients have been treated with daily S.C. therapy; other dosing schedules and longterm i.v. treatment have not yet been carefully studied. Many patients, however, have
6 99 Treatment of Severe Chronic Neutropenia received rhug-csf on an every-other-day to three-times-a-week schedule (Monday, Wednesday, Friday). These schedules appear to work satisfactorily, avoiding daily injections and requiring less total drug to be administered. Generally, it is best to switch to an alternate day schedule only after the effectiveness of daily treatment has been established. For patients with cyclic neutropenia, treatment just before the nadir of counts appears not to work very well because treatment changes the periodicity (cycle length) for these patients and, thus, very frequent counts are required to know when the nadir of the counts will occur. 6. The long-term risk of rhug-csf is not known. In patients with aplastic anemia and severe congenital neutropenia, there have been cases evolving to myelodysplasia and acute myeloleukemia while on therapy, a pattern of evolution also observed before rhug-csf and other growth factors were introduced into medical practice. Patients should be cautioned about these and other adverse effects. It is also important to observe patients regularly with periodic blood cell and bone marrow examinations. Pretreatment cytogenetic examination and expert review of the marrow histology are strongly recommended before therapy is initiated. It is now clear that the long-term use of rhug-csf markedly improves the well-being of patients with SCN, but many questions remain regarding the mechanisms of these diseases and the long-term safety of this therapy. Recently an international registry for patients with SCN was established to extend our knowledge of these conditions. It will serve as a focus for research and long-term monitoring of the efficacy and safety of rhug-csf and other therapies. In addition there remain many questions about the use of recombinant growth factors for the treatment of other forms of chronic neutropenia. It is not yet known if rhug-csf or other growth factors are equally effective for patients with chronic neutropenia due to autoimmune mechanisms, other marrow failure states, metabolic disorders or chronic infectious diseases such as the human immunodeficiency virus (HIV). Experience with treatment of congenital, idiopathic and cyclic neutropenia suggest that clinical trials in these populations may prove to be very rewarding. For further information on the Severe Chronic Neutropenia (SCN) International Registry contact: Audrey Anna Bolyard, R.N., References 1 Dale DC. Neutropenia. In: Williams WJ et al., eds. Hematology, 5th Ed. New York: McGraw-Hill, January Pincus SH, Boxer LA, Stossel TP. Chronic neutropenia in childhood: analysis of 16 cases and a review of the literature. Am J Med 1976;61: Dale DC, Guerry D, Werwerka JR et al. Chronic neutropenia. Medicine 1979;58: Weetman RM, Boxer LA. Childhood neutropenia. Pediatr Clin North Am 1980;27: Metcalf D. The colony stimulating factors: discovery, development and clinical applications. Cancer 1990;65: Lieschke GJ, Burgess AW. Granulocyte colonystimulating factor and granulocyte-macrophage colony-stimulating factor. N Engl J Med 1992;327:28-35; Teitelbaum AH, Bell AJ, Brown SL. Filgrastim (r-methug-csf) reversal of drug-induced agranulocytosis [letter]. Am J Med 1993;95: Balkin MS, Buchholtz M, Ortiz J et al. Propylthiouracil (PTU)-induced agranulocytosis treated with recombinant human granulocyte colony-stimulating factor (G-CSF). Thyroid 1993;3: Gerson SL, Gullion G, Yeh H-S et al. Granulocyte colony-stimulating factor for clozapine-induced agranulocytosis [letter]. Lancet 1992;340: Dale DC, Welte K. Severe Chronic Neutropenia: The Role of Haematopoietic Growth Factors. Macclesfield, Cheshire, U.K.: Gardiner-Caldwell Communications Ltd., Bonilfa MA, Gillio AP, Ruggeiro M et al. Effects of recombinant human granulocyte colony-stimulating factor on neutropenia in patients with congenital agranulocytosis. N Engl J Med 1989;320: Welte K, Zeidler C, Reiter A et al. Differential effects of granulocyte macrophage colony-stimulating factor in children with severe congenital neutropenia. Blood 1990;75:
7 Dale Hammond WP, Price TH, Souza LM et al. Treatment of cyclic neutropenia with granulocyte colony stimulating factor. N Engl J Med 1989;320: Jakubowski AA, Souza L, Kelly F et al. Effects of human granulocyte colony-stimulating factor in a patient with idiopathic neutropenia. N Engl J Med 1989;320: Freund M, Heussner P, Scandoval M. Granulocyte colony-stimulating factor (G-CSF) for the treatment of adult patients with chronic idiopathic neutropenia and cyclic neutropenia. Onkologie 1991 ;2: Furukawa T, Takahashi M, Moriyama Y et al. Successful treatment of chronic idiopathic neutropenia using recombinant granulocyte-colonystimulating factor. Ann Hematol 1991;62: Imashuku S, Tsuchida M, Sasaki M et al. Recombinant human granulocyte colony-stimulating factor in the treatment of patients with chronic benign granulocytopenia and congenital agranulocytosis (Kostmann s syndrome). Acta Paediatr 1992;81: Ganser A, Ottmann OG, Erdmann H et al. The effect of recombinant human granulocytemacrophage colony-stimulating factor on neutropenia and related morbidity in severe chronic neutropenia. Ann Intern Med 1989;111: Locatelli F, Pedrazzoli P, Zecca M et al. Recombinant human granulocyte-macrophage colony stimulating factor (r-hug-csf) in cyclic neutropenia. Haematologica 1991 ;76: Wright DG, Kenney RF, Oette DH et al. Treatment of childhood-onset cyclic neutropenia with recombinant human granulocyte-macrophage colonystimulating factor. Blood 1994;84: Dale DC, Bonilla MA, Davis MW et al. A randomized controlled phase I11 trial of recombinant human G-CSF for treatment of severe chronic neutropenia. Blood 1993;81: Bonilla MA, Dale DC, Zeidler C et al. Long-term treatment with recombinant human colony-stimulating factor in patients with severe chronic neutropenia. Br J Haematol 1994;88: Fazio MT, Glaspy JA. The impact of granulocyte colony-stimulating factor on quality of life in patients with severe chronic neutropenia. Oncol Nurs Forum 1991;18: Jones EA, Bolyard AA, Dale DC. Quality of life of patients with severe chronic neutropenia receiving long-term treatment with granulocyte colonystimulating factor. JAMA 1993;270: DeVries A, Peketh L, Joshua H. Leukaemia and agranulocytosis in a member of a family with hereditary leukopenia. Acta Med Orient 1958;17: Gilman PA, Jackson DP, Guild HG. Congenital agranulocytosis: prolonged survival and terminal acute leukemia. Blood 1970;36: Rosen RB, Kang S. Congenital agranulocytosis terminating in acute myelomonocytic leukemia. J Pediatr 1979;94: Woods WG, Roloff JS, Lukens JN et al. The occurrence of leukemia in patients with the Shwachman syndrome. J Pediatr 1981;99: de Planque MM, Kluin-Nelemans HC, van Krieken HJM et al. Evolution of acquired severe aplastic anaemia to myelodysplasia and subsequent leukaemia in adults. Br J Haematol 1988;70: Kojima S, Tsuchida M, Matsuyama T. Myelodysplasia and leukemia after treatment of aplastic anemia with G-CSF. N Engl J Med 1992;326: Socie G, Henry-Amar M, Bacigalupo A et al. Malignant tumors occuning after treatment of aplastic anemia. NEngl J Med 1993;329:
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