Pneumococcemia as the Presenting Feature of Multiple Myeloma
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1 American Journal of Hematology 77: (2004) Pneumococcemia as the Presenting Feature of Multiple Myeloma Daniel B. Costa, 1 Byol Shin, 1 and Dennis L. Cooper 1,2 * 1 Department of Internal Medicine, Yale University School of Medicine, New Haven, Connecticut 2 Section of Medical Oncology, Yale University School of Medicine, New Haven, Connecticut Multiple myeloma is associated with a susceptibility to bacterial infections, specifically for encapsulated organisms such as Streptococcus pneumoniae. However, severe bacterial infection as the initial presentation of this disease has been rarely reported. The most common presenting features are anemia, lytic lesions, hypercalcemia, and renal failure. We report two cases of pneumococcal bacteremia as the initial manifestation of an underlying multiple myeloma. The first case is of a 68-year-old woman with pneumococcal pneumonia and bacteremia, presenting with a white blood cell count of 900/mL andmildanemia. Further work-up disclosed monoclonal IgG kappa and 50% plasma cells in bone marrow. Her course was complicated by acute renal failure requiring hemodialysis. The second patient is a 57-year-old man presenting with acute pneumococcal meningitis and bacteremia. Due to prior bacterial epiglottitis, further work-up disclosed IgG lambda monoclonal spike and 40% plasma cells in bone marrow. Both cases responded to antibiotic therapy without complications. These two cases add to the few patients described in the literature with pneumococcemiaasthefirstsignofmultiplemyeloma.featuresthatwerecommoninmostofthese cases, and that should lead to a suspicion of myeloma in an otherwise asymptomatic patient, are S. pneumoniae bacteremia, leukopenia, mild anemia, history of prior bacterial infections, and indirect evidence of a paraproteinemia, such as increased total protein levels with low albumin. Am. J. Hematol. 77: , ª 2004 Wiley-Liss, Inc. Key words: multiple myeloma; pneumococcemia; Streptococcus pneumoniae; bacterial infections INTRODUCTION Multiple myeloma is a malignancy characterized by proliferation of a single clone of plasma cells derived from B cells, which produce a monoclonal protein [1,2]. This neoplasm is frequently associated with recurrent infections as part of the natural history of the disease, commonly with encapsulated organisms such as Streptococcus pneumoniae [3 8]. However, the presence of infection at the time of diagnosis or as the initial clinical presentation is seldom reported [9]. The most current review of presenting symptoms and signs of the disease in a cohort of 1,027 patients at Mayo clinic by Kyle et al. identifies anemia, bone pain from lytic lesions, hypercalcemia, and renal failure as the most common findings [2]. No mention is made to infectious processes at time of diagnosis [2,5 8]. We report two cases of pneumococcal bacteremia as the initial manifestation of an underlying multiple ª 2004 Wiley-Liss, Inc. myeloma, one with pneumonia as the source and the other with meningitis. A review of the published literature regarding the subject is also presented. CASE REPORTS Case 1 The patient is a 68-year-old white female in her usual state of good health up to 3 days prior to hospitalization. She presented with fever, chills, *Correspondence to: Dennis L. Cooper, M.D., Yale University, Department of Internal Medicine, Section of Medical Oncology, 333 Cedar Street, WWW 220, New Haven, CT dennis.cooper@yale.edu Received for publication 23 February 2004; Accepted 25 April 2004 Published online in Wiley InterScience ( DOI: /ajh.20158
2 278 Case Report: Costa et al. nausea, increased weakness, and pleuritic chest pain with a productive cough. A detailed review of systems was otherwise unremarkable. There was a history of hypertension and dyslipidemia, for which she was receiving a stable dose of Benazepril and Atorvastatin, respectively. She did not take over-the-counter medications and denied use of tobacco products, alcoholic beverages, or illicit drugs. The family history was negative for hypertension, coronary artery disease, diabetes, and cancer. No recent laboratory tests had been done, and she had not received the pneumococcal vaccine. On admission she was febrile to F, blood pressure was 130/76 mmhg, pulse 120 min 1, respirations 22 min 1, and transcutaneous oxygen saturation was 84% on room air and 97% on a 100% non-rebreather mask. She appeared tired and in moderate respiratory distress with shallow breathing. Pertinent findings included dry mucous membrane and mild conjunctival pallor. There was no lymphadenopathy or thyromegaly. She had decreased breath sounds, egophony, and increased tactile fremitus over the right lower lobe with bilateral basilar crackles. Heart revealed a tachycardic rhythm with no rub or murmur. Her abdominal examination was unremarkable and without hepatosplenomegaly. Extremities demonstrated no edema. There were no focal neurological findings or meningeal signs on examination. Admission laboratory values were notable for white blood cell count (wbc) of 900/mL with an absolute neutrophil count of 717/mL, hemoglobin 9.8 g/dl, hematocrit 28.8%, and platelet count 180,000/mL. Serum values were as follows: sodium, 138 mmol/l; potassium, 3.5 mmol/l; chloride, 108 mmol/l; bicarbonate, 23 mmol/l; BUN, 47 mmol/l; creatinine, 2.0 mmol/l; and calcium, 8.0 mg/dl. The total bilirubin was 1.2 mg/dl, ALT 195 U/L, AST 306 U/L, and alkaline phosphatase 40 U/L. Total protein was 10 g/dl, and albumin was 2.4 g/dl. An arterial blood gas revealed a ph of 7.37, pco 2 of 39 mmhg, and po 2 of 84 mmhg. A chest radiograph demonstrated no cardiomegaly with right lower lobe collapse and infiltrate with small pleural effusion as well as left lower lobe infiltrate. Urinalysis was positive for 1+ protein and negative for glucose, ketones, nitrites, and leukocyte esterase. Due to hypoxia on admission, she was continued on a 100% non-rebreather mask and was initially treated with gatifloxacin for presumed communityacquired pneumonia. On the subsequent day, two blood cultures were positive for penicillin resistant S. pneumoniae. Because of the discrepancy between elevated total protein and albumin levels and acute renal failure, a serum protein electrophoresis (SPEP) was obtained revealing a discrete abnormal band measuring 6.5 g/dl in the gamma region. Serum and urine immunofixation electrophoresis identified a monoclonal IgG kappa. IgA level was decreased, and IgM was not detected. A bone marrow biopsy disclosed diffuse infiltrate of plasma cells that comprised 50% of the cellular elements. All the above were consistent with multiple myeloma. The b 2 - microglobulin level was 12.5 mg/l. Due to worsening renal function with progressive fluid imbalances, the patient was started on hemodialysis on the second hospital day, at which time the serum creatinine was 3.3 mg/dl. On the third hospital day, she was started on a 5-day course of plasmapheresis with intravenous immunoglobulin replacement after each session. On the sixth hospital day, she was afebrile and had an improvement of her pulmonary function with resolving infiltrates on chest radiography, and decreased oxygen requirements. Two sets of subsequent blood cultures were negative. She completed a 14-day course of antibiotic treatment. After a week, hemodialysis was discontinued and creatine stabilized at around 1.6 mg/dl. On hospital day 8, she was started on thalidomide in combination with dexamethasone. She is receiving monthly IVIg infusions, and was vaccinated with the pneumococcal vaccine. Case 2 The patient is a 57-year-old white male in his usual good health up to 4 days prior to presentation. He had fever and chills for 3 days, followed by a severe headache in the day prior to admission associated with nausea, vomiting, and altered level of consciousness. At the day of admission, the patient became lethargic. A detailed review of systems was otherwise unremarkable. There was a history of diabetes, for which he was receiving a stable dose of glyburide. He did not take over-the-counter medications and denied recent use of tobacco products. The family history was negative for cancer. Of note, in the 6 months preceding admission, the patient had been diagnosed twice with epiglottitis, requiring antibiotics. No prior laboratory tests were available, and he had not received the pneumococcal vaccine. On admission, he was febrile to F, blood pressure was 138/70 mmhg, pulse 104 min 1, respirations 17 min 1, and the transcutaneous oxygen saturation was 93% on room air. He was lethargic and only arousable to painful stimuli. Pertinent findings included mild conjunctival pallor, reactive pupils, and no papilledema in fundoscopic exam. There was no lymphadenopathy or thyromegaly. His chest was clear to percussion and auscultation. The heart revealed a tachycardic rhythm with no rub or murmur. His
3 Case Report: Pneumococcemia as the Presenting Feature of MM 279 abdominal exam was unremarkable without hepatosplenomegaly. Extremities demonstrated no edema. There was significant nuchal rigidity and Kernig s sign. The remaining neurological exam was non-focal, but the patient was disoriented and poorly responsive to tactile stimuli. Admission labs were notable for a WBC of 13,100/mL with 95% neutrophils; hemoglobin 9.7 g/dl, hematocrit 28.2%; and platelet count 161,000/mL. Serum values were as follows: sodium, 133 mmol/l; potassium, 3.8 mmol/l; chloride, 103 mmol/l; bicarbonate, 20.8 mmol/l; BUN, 20 mmol/l; creatinine, 1.4 mmol/l; glucose, 349 mg/dl; and calcium, 8.1 mg/dl. The total bilirubin 0.3 mg/dl, ALT 41 U/L, AST 22 U/L, and alkaline phosphatase 102 U/L. Total protein was 7.3 g/dl, and albumin was 2.2 g/dl. An arterial blood gas revealed a ph of 7.49, pco 2 of 25 mmhg, po 2 of 97 mmhg. Urinalysis was positive for 3+ protein and glucose and negative for ketones, nitrites, and leukocyte esterase. A chest radiograph demonstrated no cardiomegaly without significant infiltrates. A computer tomography of the head demonstrated no intracerebral mass or hemorrhage. Cerebral spinal fluid (CSF) analysis was pertinent for 3,500 nucleated cells being 85% granulocytes, a glucose of 22 mg/dl, protein of 985 mg/dl, Gram stain with Gram-positive cocci in pairs. Due to altered sensorium in the setting of presumed acute bacterial meningitis, the patient was intubated and ceftriaxone was started. On the subsequent day, the CSF and two blood cultures were positive for penicillin resistant S. pneumoniae with intermediate sensitivity to Ceftriaxone. Vancomycin was added to the antibiotic scheme. Given the patient s life-threatening infection and the two prior episodes of bacterial epiglottitis, the etiopathogenesis was further explored with the following studies: serum protein electrophoresis (SPEP) revealed a discrete abnormal band measuring 2.57 g/dl in the gamma region. Serum and urine immunofixation electrophoresis identified monoclonal IgG lambda. IgA and IgM levels were diminished. Bone marrow biopsy revealed diffuse infiltrate of plasma cells that comprised 45% of the cellular elements, which were all consistent with multiple myeloma. A skeletal survey disclosed two small lytic lesions in his right humerus. A b 2 -microglobulin level was 4.9 mg/dl, and cytogenetic analysis was pertinent for loss of Y chromosome in 16 of 30 metaphases. On hospital day 3, the patient regained full mentation and was extubated. At that point, he was afebrile. The patient completed a 14-day course of antibiotics, and his hospital course was complicated by one episode of tonic clonic seizure, which was attributed to the pneumococcal meningitis. He received IVIg infusions monthly for 1 year after the episode of meningitis and was vaccinated for pneumococcus and Haemophilus influenza type B. Dexamethasone and thalidomide were started. No further bacterial infections occurred. His course was further complicated by a peripheral polyneuropathy attributed to his underlying myeloma. DISCUSSION There is a known association of multiple myeloma and a diverse array of infections [4 6]. An analysis of infection rate in patients with multiple myeloma done by Twoney et al. demonstrated higher incidence when compared to an age-matched cohort of patients [5]. Most of the infections are of bacterial origin [3 6], and the most serious infectious are septicemia, meningitis, or pneumonia. The mostly common found organisms in 1950s and 1960s were polysaccharideencapsulated bacteria, and there is a specific susceptibility for infections with S. pneumoniae [6]. With the advent of chemotherapy and hospitalization for disease treatment a trend toward Gram-negative and Staphylococcus aureus infections was observed in the 1970s and 1980s [5,6]; however, S. pneumoniae continued to be the most common pathogen in the course of disease progression [6]. Morbidity and mortality in multiple myeloma is often attributed to life-threatening infections [3,10]. Major infections with the bacterial pathogens described above occur commonly months after the diagnosis of malignancy [3,8]. Hargreaves et al. in the United Kingdom observed that over three-quarters of all serious infections happened 3 months after the initial diagnosis [4]. Perri et al. reported the greatest risk of infection in the first 2 months after the start of chemotherapy and also found that renal failure and decreased polyclonal serum immunoglobulins predicted infection risk [7]. In the cohort by Savage et al., most of the infections with S. pneumoniae and H. influenza occurred in the first 8 months of disease, and almost all patients were receiving chemotherapy [6]. A defect in humoral immunity has been proposed for the predisposition to bacterial infections. The classical assumption is that inability to provide specific antibodies against bacteria, due to the known decrease in polyclonal immunoglobulin levels observed when the tumor secretes a monoclonal paraprotein, leads to ineffective protection and increased susceptibility to bacterial pathogens [3 7]. It has been noted that titers of anti-capsular polysaccharide antibodies to S. pneumonia, in non-vaccinated multiple myeloma patients, are below the tenth percentile of a normal adult cohort [11]. Chapel points out that in the stable disease phase, in which there is no progressive bone marrow suppression,
4 280 Case Report: Costa et al. humoral immune suppression persists, and bacterial infections are common [12]. However, other mechanisms have been identified. A defect in C3b binding capacity to S. pneumonia has been measured in serum from patients with multiple myeloma, and this correlated with the incidence of pneumococcal infections [13]. Since opsonization with complement is required to facilitate granulocyte interaction with the most common bacterial agents encountered in multiple myeloma: S. pneumoniae, H. influenza, S. aureus, and Escherichia coli; absence of a functional complement system may play a role toward infection susceptibility in these patients [13]. Most recently, there has been evidence of defects in cellular immune response, specifically of dendritic cells which, as potent antigen-presenting cells, stimulate T- and B-cell responses [14,15]. Dendritic cells from multiple myeloma patients demonstrate defective function in cell culture studies [14,16], possibly through mechanisms involving interleukin 10 [14] and interleukin 6 [16]. Of note, high levels of b 2 -microglobulin, commonly found in multiple myeloma, inhibit in vitro generation of functional dendritic cells [15]. A few case reports of S. pneumoniae bacteremia as the first sign of multiple myeloma have been reported in the literature [17,18]. In a case series of three patients from Israel, two were older then 70 years and had pneumonia as the presenting site of infection. All three patients had mild leukopenia (white blood cell counts of less than 4,500/mL); however, the response to antibiotic treatment was prompt [17]. In another single case report of fulminant pneumococcal infection with positive cultures from blood and cerebrospinal fluid, leukopenia was noted again [18]. Of note, all the four patients described above were in general good health prior to presentation and without symptoms ascribed to multiple myeloma [17,18]. Interestingly, a previous bacterial infection was recorded in two of those patients a year prior to the episode of pneumococcemia [17]. Even though Savage et al. indicate 11 out of 106 infections in their cohort as a presenting episode, those were defined as occurring before hospitalization, chemotherapy, or both within the first 8 months of disease; there is no mention if any was the initial presentation of the underlying myeloma [6]. A case of pneumococcal septic arthritis, without bacteremia, has also been described as the initial feature of an underlying IgG lambda secreting multiple myeloma [19]. Characteristics of the above reported cases and the current patients are plotted in Table I. In our first patient, with pneumococcal pneumonia and bacteremia, the initial laboratory tests were striking for leukopenia, anemia, and acute renal failure. The patients described from the prior case series had also leukopenia; however, renal failure requiring dialysis and anemia were not observed [17]. The high disease burden (as observed by 50% plasma cells in bone marrow specimen and high total protein titers), high levels of b 2 -microglobulin, and multiple end organ damage (renal insufficiency, anemia) might have contributed to the underlying defects of humoral and cellular immunity that led to susceptibility to encapsulated organisms. Our second patient, with pneumococcal meningitis and bacteremia, did not have leukopenia as in the previous cases [17,18]. However, he had a prior history of bacterial infections (epiglottitis) in the months prior to presentation. Response to appropriate antibiotics was prompt. Both patients had no symptoms attributed to multiple myeloma prior to the acute infectious process. The prevention of recurrent infections is controversial in patients with multiple myeloma. The use of routine vaccination with influenza, S. pneumoniae, and H. influenza type B is recommended [3 6]; however, vaccination does not increase titers of antibodies directed against the specific pathogens to protective levels [11] and only one randomized trial of clinical efficacy of influenza vaccination for multiple myeloma showed protective effects [20]. One possible explanation for the lack of response to usual doses of vaccines is the dysfunction encountered in dendritic cells (the main TABLE I. Characteristics of Cases of S. pneumonia Bacteremia as the Initial Presenting Feature of Multiple Myeloma*, Source Age (years) Gender Source of S. pneumonia Type of M-protein WBC (no./ml) Hgb (g/dl) Prior bacterial infection Barasch et al. [17] 50 Female Unknown IgG lambda 3, No Barasch et al. [17] 70 Female Pneumonia IgG kappa 3,400 Yes Barasch et al. [17] 70 Female Pneumonia IgG kappa 4, Yes Posner et al. [18] 59 Female Meningitis IgG kappa 2,600 No Patient 1 a 68 Female Pneumonia IgG kappa No Patient 2 a 57 Male Meningitis IgG lambda 13, Yes *Data for prior-reported cases obtained through a Medline search from 1966 to y Abbreviations: M-protein, monoclonal protein; WBC, white blood cell count; Hgb, hemoglobin. a Patients in this case report.
5 Case Report: Pneumococcemia as the Presenting Feature of MM 281 antigen-presenting cells) of patients with multiple myeloma [14]. Poor responses to vaccination also correlated with recent chemotherapy and autologous peripheral blood stem cell transplant [11]. The role of prophylactic IVIg is still debated [3,8,12]. One small randomized trial of the use of prophylactic IVIg in plateau-phase myeloma patients without prior infections, at a dose of 0.4 mg/kg body weight monthly for 1 year, demonstrated protective effects against lifethreatening bacterial infections and recurrent infections [3]. However, the use of this scheme in clinical practice has not been validated in other studies, and intravenous immunoglobulin is commonly reserved for prophylaxis in patients with confirmed recurrent bacterial infections, especially with polysaccharide-encapsulated bacteria [8]. In both of our patients, the use of IVIg was advocated due to the functional hypogammaglobulinemia and life-threatening pneumococcal infection at presentation. Even though there are only scattered case reports of pneumococcemia at the time of diagnosis of multiple myeloma, this clinical scenario might be more frequent as a possible red flag for underlying disease in patients without other risk factors for pneumococcal infection. In a Danish study following episodes of communityacquired pneumococcal pneumonia with bacteremia or pneumococcal meningitis, the incidence ratio of being diagnosed with multiple myeloma in subsequent years after the initial presentation was over 50 when compared to expected cases in their population data [21]. However, the absolute risk was low, with only 11 cases in 1,662 patient-years of follow-up [21]. Also, in a Spanish case-control analysis of patients with recurrent pneumococcal bacteremia, multiple myeloma was found in one quarter of studied subjects as the underlying sign of immunodeficiency [22]. The two cases reported in this article underscore the importance of considering multiple myeloma in a patient presenting with pneumococcal pneumonia or meningitis and bacteremia. Suspicion should be especially high when there is evidence of leukopenia, anemia, prior bacterial infections, renal failure, and indirect evidence of a paraproteinemia, such as increased total protein levels with low albumin. REFERENCES 1. The International Myeloma Working Group. Criteria for the classification of monoclonal gammopathies, multiple myeloma and related disorders: a report of the international myeloma group. Br J Haematol 2003;121: Kyle RA, Gertz MA, Witzig TE, et al. Review of 1027 patients with newly diagnosed multiple myeloma. Mayo Clin Proc 2003;78: Chapel HM, Lee M, Hargreaves R, et al. Randomised trial of intravenous immunoglobulin as prophylaxis against infection in plateau-phase multiple myeloma. Lancet 1994;343: Hargreaves R, Griffiths H, Faux J, et al. Infection and immunological responses in myeloma. Blood 1991;76(Suppl 1): Twoney JH. Infectious complicating multiple myeloma and chronic lymphocytic leukemia. Arch Intern Med 1973;132: Savage DG, Lindenbaum J, Garret TJ. Biphasic pattern of bacterial infection in multiple myeloma. Ann Intern Med 1982;96: Perri RT, Hebbel RP, Oken MM. Influence of treatment and response status on infection risk in multiple myeloma. J Am Med Assoc 1981;71: Snowdon L, Gibson J, Joshua DE. Frequency of infection in plateau-phase multiple myeloma. Lancet 1994;344: Anderson, KC. Multiple myeloma: how far have we come? Mayo Clin Proc 2003;78: Kapadia SB. Multiple myeloma: a clinic pathologic study of 62 consecutively autopsied cases. Medicine 1980;59(5): Robertson JD, Nagesh K, Jowitt SN, et al. Immunogenicity of vaccination against influenza, Streptococcus pneumoniae and Haemophilus influenza type B in patients with multiple myeloma. Br J Cancer 2000;82(7): Chapel HM, Lee M. The use of intravenous immune globulin in multiple myeloma. Clin Exp Immunol 1994;97(Suppl 1): Cheson BD, Walker HS, Heath ME, Gobel RJ, Janatova J. Defective binding of the third component of complement (C3) to Streptococcus pneumoniae in multiple myeloma. Blood 1984;63(4): Brown RD, Pope B, Murray A, et al. Dendritic cells from patients with myeloma are numerically normal but functionally defective as they fail to up-regulate CD80 (B7 1) expression after hucd40lt stimulation because of inhibition by transforming growth factor-b1 and interleukin-10. Blood 2001;98(10): Xie J, Wang Y, Freeman ME, Barlogie B, Qing Y. Beta-2-microglobulin as a negative regulator of the immune system: high concentrations of the protein inhibit in vitro generation of functional dendritic cells. Blood 2003;101(10): Ratta M, Fagnoni F, Curti A, et al. Dendritic cells are functionally defective in multiple myeloma: the role of interleukin-6. Blood 2002;100(1): Barasch E, Berger SA, Golan E, Sigman-Igra Y. Pneumococcaemia as a presenting sign in 3 cases of multiple myeloma. Scand J Haematol 1986;36: Posner MR, Berk SL, Rice PA. Pneumococcal bacteremia diagnosed by peripheral blood smear in multiple myeloma. Arch Intern Med 1978;138: Cuesta M, Bernard M, Espinosa A, Herranz P, Mola EM, Banos JG. Pneumococcal septic arthritis as the first manifestation of multiple myeloma. Clin Exp Rheum 1992;10(5): Musto P, Carotenuto M. Vaccination against influenza in multiple myeloma. Br J Haematol 1997;97: Gregersen H, Pedersen G, Svendsen N, Thulstrup AM, Sorensen HT, Schonheyder HC. Multiple myeloma following an episode of community-acquired pneumococcal bacteraemia or meningitis. APMIS 2001;109(11): Rodriguez-Creixems M, Munoz P, Miranda E, Pelaez T, Alonso R, Bouza E. Recurrent pneumococcal bacteremia. A warning of immunodeficiency. Arch Intern Med 1996;156(13):
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