Role of Phlebotomy in the Management of Hemoglobin SC Disease: Case Report and Review of the Literature
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1 American Journal of Hematology 73: (2003) Role of Phlebotomy in the Management of Hemoglobin SC Disease: Case Report and Review of the Literature Merry Jennifer Markham, 2 Richard Lottenberg, 1,2 and Marc Zumberg 1,2 * 1 Division of Hematology/Oncology, University of Florida, Gainesville, Florida 2 Department of Medicine, University of Florida, Gainesville, Florida Marked variability is a keynote in the disease course of patients with hemoglobin SC (Hb SC) and hemoglobin S/ + -thalassemia (Hb S/ + -thal), with some patients having a frequency of complications and painful episodes similar to patients with homozygous sickle cell (Hb SS) disease. One possible explanation is that the higher hematocrit in these syndromes may contribute to an increase in blood viscosity, leading to vaso-occlusive pain episodes as well as an increased incidence of thromboembolic complications and retinopathy. We present a patient with Hb SC disease with an excellent baseline functional status who developed splenic infarction at a high altitude. Following splenectomy, the patient developed a sustained increase in hematocrit, an increase in the frequency of painful episodes, as well as new-onset dizziness and malaise. We initiated a therapeutic phlebotomy program in order to lower the hematocrit to pre-splenectomy values, as well as to induce iron deficiency. Repeated phlebotomy resulted in a dramatic decrease in symptoms. Our patient no longer requires narcotic analgesics for pain, has resolution of constitutional symptoms, and has not required further hospitalizations for vasoocclusive pain crises. The correlation between symptoms and hematocrit levels supports the importance of blood viscosity in contributing to this patient s symptoms. A trial of phlebotomy to reduce viscosity in patients with higher hematocrit values should be considered as an intervention for symptomatic patients with sickle cell disease. Am. J. Hematol. 73: , Wiley-Liss, Inc. Key words: sickle cell; hemoglobin SC; phlebotomy; viscosity INTRODUCTION In homozygous sickle cell disease (hemoglobin SS) many factors including infection, leukocytosis, low fetal hemoglobin, pregnancy, and cold weather are known to correlate with an increased frequency of vaso-occlusive pain crises and some with mortality as well [1,2,3,16,17]. Baum et al. in a study of 391 homozygous sickle cell patients also noted an increased incidence of painful events in males with hemoglobin SS having Hb levels over 8.5 g/dl [2]. Platt et al. have also shown that the rate of vaso-occlusive events varies directly with the hematocrit [3]. In explaining their findings, these authors have speculated that sickle cell patients with more severe anemia have a lower blood viscosity, lessening the severity of vaso-occlusive episodes [2,3]. Due to the heterozygosity of hemoglobin S, patients with Hb SC and Hb S/ + -thalassemia are generally characterized as having a milder clinical course with fewer vaso-occlusive episodes despite higher hematocrit values 2003 Wiley-Liss, Inc. than those with Hb SS [1,4]. The hematocrit of patients with homozygous Hb SS is typically 20 30%, while that of patients with Hb SC is typically 30 36%. Patients with Hb S/ + -thalassemia usually have a hematocrit falling in between these two ranges [5]. An increase in blood viscosity, secondary to the elevated hematocrit, is thought to contribute to the increased thromboembolic complications, retinopathy, and renal papillary necrosis in Hb SC patients [4]. Vaso-occlusive events may also be due to an increase in viscosity. It is speculated that increased blood *Correspondence to: Marc Zumberg, M.D., Division of Hematology/ Oncology, P.O. Box , Gainesville, Florida zumbems@medicine.ufl.edu Received for publication 10 August 2002; Accepted 15 February 2003 Published online in Wiley InterScience ( DOI: /ajh.10328
2 122 Case Report: Markham et al. viscosity causes decreased oxygen concentration within very small caliber blood vessels, leading to tissue hypoxia and subsequent painful episodes [1]. To further support this concept, we present a patient with a rising hematocrit who developed new onset dizziness, malaise, fatigue, and an increased frequency of painful episodes. CASE REPORT The patient is a 26-year-old male with Hb SC disease (hemoglobin electrophoresis: 53% Hb S and 47% Hb C). His prior medical history is significant for childhood pneumonia, painful episodes, a laparoscopic cholecystectomy for symptomatic gallstones at age 18, and avascular necrosis of both femoral heads diagnosed by plain films at age 20. Between the ages of 18 and 19 years, he had received 6 units of packed red blood cells. He had no prior history of stroke, acute chest syndrome, or retinopathy. The patient did relatively well into his adult years except for intermittent painful events requiring three hospitalizations (all during a 3-month period in 1997). His typical painful episodes consisted of upper and lower extremity bone pain, occasionally associated with chest wall and lower back pain. At the age of 22, the patient was driving his commercial truck at an altitude of 6,100 feet when he developed acute, left upper quadrant (LUQ) abdominal pain. He was subsequently diagnosed with splenic infarction by computerized tomography. Initial management was conservative and consisted of intravenous fluids and analgesics. He was transferred to our institution when medically stable. He was subsequently hospitalized twice more over the following 2 months: once for a typical painful event and persistent LUQ abdominal pain and a second time for a typical painful episode. Three months following the diagnosis of splenic infarct, due to continued LUQ abdominal pain, elective splenectomy was performed. The patient developed a painful event beginning on post-operative day 5 and was subsequently discharged with oral narcotic analgesics 3 days later. There were no further complications, and he received no peri-operative blood transfusions. Incidentally, 6 months later, during the investigation of a heart murmur detected on physical exam, an atrial septal defect (ASD) was found by echocardiography. There was no clinical evidence of hypoxemia, right-sided heart failure, or pulmonary hypertension. One month following diagnosis, he underwent pre-operative red cell exchange transfusion followed by surgical repair of the ASD. He remained hemodynamically stable throughout the hospitalization without complications. Following the splenectomy, the patient developed an increased frequency of painful events involving pain in his extremities and lower back. He required three hospital admissions over the next year for typical sickle cell TABLE I. Laboratory Data, February 2000 (Prior to Start of Phlebotomy Program) Parameter Result (reference range) Hb (g/dl) 14.1 ( ) Hct (%) 43.2 (41 53) MCV (fl) 88.4 (80 100) MCHC (g/dl) 32.7 (31 37) RDW (%) 14.1 ( ) Reticulocytes (%) 3.4 ( ) WBC ( 10 3 / L) 8.1 (4.5 11) RBC ( 10 6 / L) 4.89 ( ) Platelets ( 10 3 / L) 510 ( ) BUN (mg/dl) 9.0 (9 20) Creatinine (mg/dl) 0.6 ( ) AST (U/L) 64 (15 46) ALT (U/L) 31 (11 66) Total bilirubin (mg/dl) 1.6 ( ) painful episodes and was treated with increased frequency in the outpatient clinic. He also began to experience frequent episodes of new-onset dizziness and generalized malaise. A neurological workup including a magnetic resonance (MR) imaging exam of the head and an MR angiogram of the cerebral circulation was performed to exclude a central nervous system cause of his symptoms. Neither exam revealed any source for the patient s dizziness, although MR imaging of the brain incidentally revealed a small, old infarct in the left caudate. Several months after splenectomy, because of his perceived worsening state of health, this previously active patient filed for disability from his job as a truck driver. Table I summarizes his laboratory evaluation at that time, including complete blood count, renal, and liver chemistries. As we thought the increase in frequency of painful episodes and new-onset constitutional symptoms were related to the sustained elevation in hematocrit, a phlebotomy program was instituted 18 months after splenectomy. The target hematocrit was 35%, the patient s prior baseline value previous to splenectomy. The mean hematocrit data for the periods of time prior to splenic infarction, after infarction but prior to splenectomy, postsplenectomy, and after initiation of phlebotomy are summarized in Table II. No iron studies were performed prior to the initiation of phlebotomy. Evaluation of iron status in May 2002 confirmed deficiency: ferritin 18.6 ng/ml (normal level: ng/ml), iron 24 g/dl (normal level: g/ml), total iron binding capacity 605 g/dl (normal level: g/dl), and percent saturation 4% (normal level: 20 55%). A reduction of the red cell MCV to 62 fl (normal level: fl) was also consistent with iron deficiency. In the 2 years after phlebotomy was begun, 23 singleunit manual phlebotomies were performed. No intravenous fluids were administered, but the patient increased
3 Case Report: Phlebotomy in Sickle Cell Disease 123 TABLE II. Selected Laboratory Data and Clinical Course* Prior to splenic infarct 1/96 6/98 Post-splenic infarction Post-splenectomy Phlebotomy program 7/98 10/98 a 11/98 3/00 a 3/00 3/02 Hct (%), mean ± SD 34.5 ± ± ± ± 2.9 Hct, range Hb (g/dl), mean ± SD 11.6 ± ± ± ± 1.2 Hb, range MCV (fl), mean ± SD 80.0 ± ± ± ± 10.4 MCV, range MCHC (g/dl), mean ± SD 33.7 ± ± ± ± 1.0 MCHC, range WBC ( 10 3 / L), mean ± SD 5.7 ± ± ± ± 1.2 WBC, range Platelets ( 10 3 / L),mean±SD 204±35 234±94 516± ±112 Platelets, range No. of hospital admissions per time period *Hct, hematocrit; Hb, hemoglobin; MCV, mean corpuscular volume; MCHC, mean corpuscular hemoglobin concentration; WBC, white blood cell count. a Hct and Hb data during the hospitalization for splenectomy and ASD repair are not included in the calculated means, SD, and ranges listed above. his oral intake of fluids with each phlebotomy. Soon after the initiation of phlebotomy his complaints of dizziness and malaise significantly decreased. He has not required additional hospitalizations due to painful episodes, and he no longer requires routine narcotic analgesics for pain control. In addition, 6 months after the initiation of phlebotomy, our patient returned to work full time as a truck driver. He continues to tolerate each phlebotomy without complication. Phlebotomy is performed every 6 8 weeks on the basis of hematocrit values or development of symptoms (headache, fatigue, arthralgias). DISCUSSION In Hb SS disease, increased hematocrit has been recognized as a risk factor for vaso-occlusive painful episodes [1,3]. A paucity of literature exists in Hb SC disease and Hb S/ + -thalassemia, however. It is hypothesized that increased viscosity leads to decreased oxygen delivery at the tissue level, leading to hypoxia and ensuing vaso-occlusion. It is known that in Hb AA red cells, oxygen delivery begins to decrease at hematocrit levels of 45 50%; however in blood containing hemoglobin S, oxygen delivery begins to decrease at hematocrit levels above 30 35% (and is significantly reduced at values above 45%) [1,18]. It is also known that the mean corpuscular hemoglobin concentration (MCHC) is higher in Hb SC patients than in those with Hb SS disease [4]. A higher MCHC has been speculated to contribute to an enhanced rate of Hb S polymerization [6,7]. In accordance with this theory, Rao et al. have noted that iron-deficient red cells have a lower MCHC, decreased ability for Hb S polymerization, and resistance to sickling [7]. In the presence of reduced oxygen tension, SC erythrocytes sickle with a rate similar to that of SS red cells [8]. Fabry and colleagues have reported that when the MCHC in Hb SC patients is reduced to that of normal cells by hydration, viscosity is dramatically reduced. These authors noted that the rates of sickling in Hb SC erythrocytes could be decreased to values similar to those of sickle cell trait (Hb AS) cells [8]. In a recent report of Hb SC disease, Koduri et al. noted a 19% incidence of acute splenic infarction in 106 Hb SC patients [9]. The consequences of splenectomy for these patients were not documented. Our patient experienced splenic infarction while driving at a high altitude. Four cases of splenic infarction in Hb SC patients following travel to altitudes of 9,000 12,000 feet in the Rocky Mountains have been documented; a fifth patient with Hb SC disease experienced splenic infarction 10 days after arriving at an altitude 5,280 feet above sea level [10]. Following splenectomy, our patient began to experience an increased frequency of painful events as well as new-onset dizziness and generalized malaise. It was noted that his symptoms developed in temporal association to a post-splenectomy rise in hematocrit. We speculate that the increase in symptoms in our patient was due to an increase in viscosity, secondary to the elevation in hematocrit. Wright et al. have reported an increased frequency of painful episodes in homozygous Hb SS patients who underwent splenectomy [11]. No laboratory data were reported to establish if there was a correlation between symptoms and hematocrit values. Changes in other laboratory tests, including an increase in the white blood cell (WBC) count and platelet count, were also noted in our patient post-splenectomy (Table II). However, after phlebotomy was introduced, the platelet count continued to rise even as clinical symptoms resolved, thus making elevation in platelet count an unlikely contributor to symptoms. The WBC count also remained elevated above baseline values post-phlebotomy as our patient s symptoms resolved, thus making it an equally unlikely contributor. Phlebotomy can be used to decrease the hematocrit
4 124 Case Report: Markham et al. and subsequently reduce viscosity. In the mid-1990s Rombos et al. described the use of weekly phlebotomy in five patients with Hb S/ + -thalassemia who presented with frequent, severe vaso-occlusive events [12]. In the year prior to the phlebotomy program, one of the patients required two hospital admissions for painful sickle cell episodes, three patients had four admissions, and one patient had five admissions. During the observation period after phlebotomy was initiated, no patient required hospitalization. The hematocrit values subsequent to the initiation of phlebotomy were not reported. A more recent report by Rombos and colleagues updated their initial experience [19]. Thirteen patients with frequent painful episodes not ameliorated by conventional treatment were treated with weekly phlebotomy. A significant decrease in painful events requiring hospital admission (P ), treated in the outpatient clinic (P 0.02), or treated at home (P 0.01) were noted. No significant decreases in the hemoglobin, MCV, and MCHC were observed in this study. Bouchair et al. also reported a dramatic decrease in the number of hospital days subsequent to initiation of a phlebotomy program in four Hb SC and three Hb SS patients with frequent painful vasoocclusive events. The mean hemoglobin value had decreased from 10.7 g/dl to g/dl in these patients after initiation of phlebotomy [13]. These authors hypothesize that, by reducing the mean hemoglobin level in patients with sickling syndromes, viscosity was lowered and red cell rheology improved [13]. An additional reason for our patient s improvement in symptoms and quality of life may exist. As anticipated, he has become iron deficient as a consequence of multiple therapeutic phlebotomies. It has previously been noted by other authors that patients with sickle cell disease experience a decreased incidence of painful episodes and require fewer days of hospitalization when made iron deficient through phlebotomy [13 15,19]. Rao et al. describe a patient with Hb SS disease and concurrent iron deficiency who had a decreased number of sickled erythrocytes noted on examination of the peripheral blood smear [7]. After iron therapy was initiated, the percentage of sickled red cells seen on the peripheral blood smear increased. Bouchair et al. observed a reduction in the MCHC and hemoglobin levels subsequent to the initiation of a sequential phlebotomy program in seven sickle cell patients. These authors speculated that, as the MCHC is reduced through phlebotomy, Hb S polymerization is modulated, leading to a beneficial clinical effect [13]. Castro et al. noted that low serum iron levels lead to a reduced production of oxygen free radicals, thus preventing membrane oxidation [15]. However, a downside to iron deficiency has also been noted; iron-deficient red blood cells have been shown to have reduced membrane flexibility which may lead to decreased life span of young erythrocytes [19]. Our case provided an opportunity to discern the contribution of an increased hematocrit to clinical manifestations of sickle cell disease in a patient who essentially served as his own control. He had been doing relatively well with a baseline hematocrit of 35%. He experienced a splenic infarction and subsequently required a splenectomy. Following splenectomy he experienced an increased frequency of painful episodes and developed new-onset malaise and dizziness. During that same period the hematocrit had increased, peaking at 46%. After starting a phlebotomy program, the patient noted an improvement in his quality of life, a decrease in pain, and resolution of malaise and dizziness. He has not required any hospitalizations for pain crisis and has returned to work full time. There were no other clinical interventions over this period of time. It is uncertain whether the patient s clinical improvement was due to the decrease in hematocrit, the induction of iron deficiency, or both. However, on the basis of our patient s response and upon reviewing the literature, we believe a clinical trial investigating the role of phlebotomy in patients with sickle cell syndromes who experience severe vaso-occlusive manifestations in the face of a persistently elevated hematocrit should be considered. REFERENCES 1. Rosse WF, Narla M, Petz LD, Steinberg MH. New views of sickle cell disease pathophysiology and treatment. In: Schecter GP, Berliner N, Telen MJ, editors. Hematology Washington, DC: The American Society of Hematology; p Baum KF, Dunn DT, Maude GH, Serjeant GR. The painful crisis of homozygous sickle cell disease. A study of risk factors. Arch Intern Med 1987;147: Platt OS, Thorington BD, Brambilla DJ, Milner PF, Rosse WF, Vichinsky E, Kinney TR. Pain in sickle cell disease. Rates and risk factors. N Engl J Med 1991;325: Ballas SK, Lewis CN, Noone AM, Krasnow SH, Kamarulzaman E, Burka ER. Clinical, hematological, and biochemical features of Hb SC disease. Am J Hematol. 1982;13: Glader BE. Anemia. In: Embury SH, Hebbel RP, Mohandas N, Steinberg MH, editors. Sickle cell disease: basic principles and clinical practice. New York: Raven Press, Ltd; p Embury SH, Steinberg MH. Genetic modulators of disease. In: Embury SH, Hebbel RP, Mohandas N, Steinberg MH, editors. Sickle cell disease: basic principles and clinical practice. New York: Raven Press, Ltd; p Rao KRP, Patel AR, Honig GR, Vida LN, McGinnis PR. Iron deficiency and sickle cell anemia. Arch Intern Med 1983;143: Fabry ME, Kaul DK, Raventos-Suarez C. SC erythrocytes have an abnormally high intracellular hemoglobin concentration. Pathophysiological consequences. J Clin Invest 1982;70: Koduri PR, Agbemadzo B, Nathan S. Hemoglobin SC disease revisited: clinical study of 106 adults. Am J Hematol 2001;68: Githens JH, Gross GP, Eife RF, Wallner SF. Splenic sequestration syndrome at mountain altitudes in sickle/hemoglobin C disease. J Pediatr 1977;90: Wright JG, Hambleton IR, Thomas PW, Duncan ND, Venugopal S, Serjeant GR. Post-splenectomy course in homozygous sickle cell disease. J Pediatr 1999;134:
5 Case Report: Phlebotomy in Sickle Cell Disease Rombos Y, Tassiopoulos T, Tzanetea R, Tsekoura C, Loukopoulos D. Clinical improvement of -thal-hbs anemia by iron deficiency [letter]. Am J Hematol 1995;50: Bouchair N, Manigne P, Kanfer A, Raphalen P, de Montalembert M, Hagege I, Verschuur A, Maier-Redelsperger M, Girot R. Prevention of sickle cell crises with multiple phlebotomies [French]. Arch Pediatr 2000;7: Haddy TB, Castro O. Overt iron deficiency in sickle cell disease. Arch Intern Med 1982;142: Castro O, Poillon WN, Finke H, Massac E, Kim BC. Improvement of sickle cell anemia by iron-limited erythropoiesis. Am J Hematol. 1994; 47: Platt OS, Brambilla DJ, Rosse WF, Milner PF, Castro O, Steinberg MH, Klug PP. Mortality in sickle cell disease. Life expectancy and risk factors for early death. N Engl J Med 1994;330: Steinberg MH. Management of sickle cell disease. N Engl J Med 1999;340: Schmalzer EA, Lee JO, Brown AK, Usami S, Chien S. Viscosity of mixtures of sickle and normal red cells at varying hematocrit levels. Implications for transfusion. Transfusion 1987;27: Rombos Y, Tzanetea R, Kalotychou V, Konstantopoulos K, Simitzis S, Tassiopoulos T, Aessopos A, Fessas P. Amelioration of painful crises in sickle cell disease by venesections. Blood Cells Mol Dis 2002;28:
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