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1 CASE REPORT Disseminated Cryptococcosis Complicated with Bilateral Pleural Effusion and Ascites during Corticosteroid Therapy for Organizing Pneumonia with Myelodysplastic Syndrome Hiroyuki Kamiya 1, Rie Ishikawa 1, Atsuko Moriya 1,AikoArai 1, Kozo Morimoto 1, Tsunehiro Ando 1, Soichiro Ikushima 1, Masaru Oritsu 1 and Tamiko Takemura 2 Abstract An 83-year-old man with myelodysplastic syndrome was admitted to our hospital due to dyspnea and abnormal shadows on chest X-ray films during corticosteroid therapy for organizing pneumonia. He was diagnosed as having disseminated cryptococcosis with pulmonary lesions after detecting Cryptococcus neoformans. Both bilateral pleural effusion with or without ipsilateral pulmonary lesions and ascites ensued, and it was assumed that both direct involvement and serositis were associated with the fluid accumulation. Cryptococcal yeast was only detected in the right pleural effusion, and the titer of cryptococcal antigen was quite different between body cavities, even though it was positive in all sites. Key words: disseminated cryptococcosis, pleural effusion, ascites, serositis, cryptococcal antigen (Inter Med 47: , 2008) () Introduction It is well recognized that cryptococcosis occurs in immunocompromised patients (1), and is often disseminated. Although the lungs, central nervous system, and skin are often involved, pleural effusion (2, 3) and ascites (4) are rare. Here, we report a case of disseminated cryptococcosis complicated with pulmonary lesions, bilateral pleural effusion, and ascites, and also discuss the significance of cryptococcal antigen. Case Report An 83-year-old man was admitted to our hospital for further evaluation of dyspnea on exertion and newly detected abnormal shadows on chest X-ray films. The patient had never experienced a serious disease until a diagnosis of myelodysplastic syndrome (MDS) was made at a near-by hospital 6 months before admission. Three months before admission, he had presented with low-grade fever, and chest X-ray films had revealed bilateral infiltrative shadows, which had been pathologically diagnosed as organizing pneumonia (OP) by transbronchial lung biopsy (TBLB). Both his symptoms and radiological findings were remarkably improved after initiating corticosteroid therapy (methylprednisolone 500 mg/day for three consecutive days followed by prednisolone 1 mg/kg/day), which was gradually tapered at an outpatient department. No special treatment had been undertaken to treat the MDS with the exception of hormonal drug (metenolone) and vitamin K2 before the previous admission. He had never had previous exposure to birds. Physical examination on admission showed that he was afebrile, and his percutaneous saturated oxygen level was almost normal (97% at room air). Although palpebral conjunctive was slightly anemic, no other abnormal findings including nuchal rigidity were identified. Laboratory findings on admission showed that the inflammatory reaction was slightly elevated as the white blood cell count was 9,900/μL and C-reactive protein was 7.63 mg/dl (Table 1). Chest X- ray films showed infiltrative shadows in the right middle lung field (Fig. 1). A computed tomography (CT) scan of the chest showed consolidation together with ground-glass Respiratory, Japanese Red Cross Medical Center, Tokyo and Pathology, Japanese Red Cross Medical Center, Tokyo Received for publication January 8, 2008; Accepted for publication July 3, 2008 Correspondence to Dr. Hiroyuki Kamiya, mlb04194@nifty.com 1981
2 Table1. LaboratoryFindingsonAdmision Figure1. ChestX-rayfilmsshowinginfiltrativeshadowsin therightmiddlelungfield. opacity (GGO) in the right lower lobe and right pleural effusion (Fig. 2). His symptoms, inflammatory reactions, and radiological findings gradually worsened regardless of both antibiotic therapy including carbapenem and newquinolone and corticosteroid pulse therapy on suspicion of bacterial pneumonia Figure2. CTscanofthechestshowingconsolidationwith ground-glasopacity(ggo)intherightlowerlobeandright pleuralefusion. or recurrence of OP. Cryptococcus neoformans was identified in a blood culture, and serum cryptococcal antigen (by latex agglutinated procedure) showed positivity with a titer of 1 : Furthermore, the specimen obtained by TBLB from pulmonary lesions on the right lower lobe revealed multiple yeasts in alveolar spaces (Fig. 3), which led to a diagnosis of dissemination from pulmonary cryptococcosis. Lumbar puncture was not undertaken because of the anxiety 1982
3 Figure3. (HematoxylinandEosinstaining, 10).Specimen obtainedfrom pulmonarylesionsontherightlowerlobeby TBLBrevealingfoamymacrophageswithmultipleyeastsin alveolarspaces,butlackinggranulomatousreactionswitha fewinfiltrationsofinflammatorycels. Figure4. (Giemsastain, 100).Cryptococcusyeastswere detectedinthesmearofrightpleuralefusion. Table2. CharacteristicsofFluidsinBodyCavities Right pleural effusion Left pleural effusion Ascites Cerebrospinal fluid (Day53) (Day54) (Day60) (Day53) Yellowish Yellowish Yellowish No color, Transparent ph 7.2 ph 7.2 ph 7.6 Protein 60 Protein 2.8 Protein 2.2 Protein 1.9 Glucose 100 (Ratio to serum 0.72) (Ratio to serum 0.56) (Ratio to serum 0.49) Cell 4/3mm 3 (lymphocyte) LDH 295 LDH 253 LDH 246 Cryptococcal antigen 256 (Ratio to serum 0.72) (Ratio to serum 0.63) (Ratio to serum 0.67) Glucose 169 Glucose 110 Glucose 74 Cryptococcal antigen 4096 Cryptococcal antigen 256 Cryptococcal antigen 512 of bleeding due to MDS although a complication of meningitis was highly suspected. After initiation of anti-fungal therapy consisting of lyposomal amphotericin B (L-AMB) (5 mg/kg/day), Cryptococcus neoformans disappeared from his blood, and both his symptoms and laboratory findings improved gradually, although antibiotic therapy including carbapenem, vancomycin, and newquinolone had to be instituted to treat a recurrence of high grade fever after a shorttime clinical improvement, which was later found to have been caused by a complication of bacteremia due to both Enterococcus faecalis and Staphylococcus epidermidis. The infiltrative shadows on chest X-ray films remained, and the bilateral pleural effusion and ascites gradually worsened even after administration of a total dose of 4.35 g of L-AMB until renal dysfunction became a complication. Lumbar puncture, thoracentesis and abdominocentesis were undertaken to evaluate the extent of cryptococcal dissemination and the effectiveness of the treatment. These procedures demonstrated that cryptococcal antigen in the cerebrospinal fluid, left pleural effusion and ascites was positive with a titer of 1 : 256 or 1 : 512, but it was much lower than in the right pleural effusion which had a titer of 1 : 4096, a titer that was the same as in the serum. Furthermore, Cryptococcus neoformans was never detected in any sites other than in the right pleural effusion (Fig. 4), and there was no increase in the cell count in cerebrospinal fluid (Table 2). In consid- 1983
4 Figure5. Clinicalcourseafteradmision.ABPC:ampicilin,CLDM:clindamycin,CPFX:ciprofloxacinhydrochloride,DRPM:doripenem hydrate,f-flcz:fosfluconazole,l-amb:lyposomal amphotericinb,mpsl:methylprednisolonesodium succinate,vcm:vancomycinhydrochloride eration of these findings, it was assumed that L-AMB was effective, although the treatment should have been continued slightly longer. Cryptococcus neoformans disappeared from the right pleural effusion, and his condition improved temporarily by continuing fosfluconazole (F-FLCZ) administration (initiated with a dose of 200 mg/day followed by 100 mg/day) after discontinuing L-AMB because of renal dysfunction. However, the patient gradually became malnourished, and died of respiratory failure after a complication of aspiration and renal failure regardless of antibiotic therapy (Fig. 5). Discussion This is a case of disseminated cryptococcosis, which developed in an immunocompromised patient, and it is worthy of being presented here because of its rarity in that both pleural effusion and ascites were complicated as the result of cryptococcal serositis, and cryptococcal antigen titer was elevated in all body cavities including bilateral pleural effusion, ascites and cerebrospinal fluid. Cryptococcosis is one of the most common fungal infections (5), and often develops in immunocompromised patients (1). Considering that the patient in the present case was suffering from hematological disorders and receiving steroid therapy for OP, it was assumed that he may have been highly immunocompromised, and easily subject to Cryptococcus neoformans because cell-mediated immunity is the main defensive mechanism against cryptococcal infection (6). This was verified indirectly by the laboratory findings which indicated that the lymphocyte count, in particular the CD4 positive cells in the blood was extremely low at 200 to 300/μL and 100/μL to 150/μL, respectively in the entire clinical course (data not shown). Further, it was also verified directly by the pathological findings that granulomatous reactions to cryptoccocal yeasts, which should have been revealed if his immunity was preserved as previously reported (7), were never detected in the specimens by TBLB. Systemic dissemination is often observed in immunocompromised patients (5), but to date complications consisting of pleural effusion (8) or ascites (4) have rarely been reported. Because pleural effusion in most cases are reported to have been induced by an extension of inflammatory reactions on subpleural pulmonary lesions into the thoracic cavity (9), it is reasonable to assume that the pulmonary lesions were the primary site of infection in the present case, and it caused both the right pleural effusion and dissemination into the blood. It is apparent that Cryptococcus neoformans was the infection in the right thoracic cavity where the fungus was actually detected on the cytologic examination, while the cryptococcal infection in the cerebrospinal fluid, left thoracic and abdominal cavities was not definitely confirmed although the cryptococcal antigen titer was elevated at all sites. However, it is reasonable to think that the cryptococcal infection was present in the cerebrospinal cavity because cryptococcal antigen, which is regarded as highly sensitive and specific in the site (10), was positive, and the normal 1984
5 cell count in the cerebrospinal fluid can be explained by the fact that an anti-fungal drug had already been administered. On the other hand, it is possible that cryptococcal infection was not actually present in the left thoracic and abdominal cavities, and cryptococcal antigen had only penetrated from the blood because the fungus could not be detected in either cavity, and the utility of cryptococcal antigen in those sites was not established yet. However, it is also reasonable to think that both the left pleural effusion and ascites may have been induced by a kind of serositis following fungemia because they were all exudative, and there were no other findings to explain the accumulation of the fluids. Actually, pleural effusion is complicated with pulmonary lesions in many cases as described above, and ascites usually occurs in patients with some underlying liver disease such as cirrhosis (11) or continuous ambulatory peritoneal dialysis (12) through translocation from the intestine, but because there was neither a left pulmonary lesion nor an underlying liver disease in the present case, those lesions were considered to have been caused by dissemination. Some may think that the increase of pleural effusion and ascites even after administration of an anti-fungal drug indicates the existence of other causes of the fluids than cryptococcal infection, but it may be explained by the accumulation of transudative components due to malnutrition in addition to exudative components due to the infection. There were some differences in the cryptococcal antigen titers at the sites. It was highly positive only in the right thoracic cavity with identification of Cryptococcus neoformans, while it was lower in other body cavities including the left thoracic, abdominal and cerebrospinal cavities, which may indicate that no Cryptococcus neoformans was present. This difference in the amount of the organism is partly due to whether the organism is directly invasive into the body cavities or disseminated from the primary site. Another possibility is that the result could be influenced by the timing of the tests because an anti-fungal drug had already been administered to treat some clinical findings. It is reported that cryptococcal antigen is not useful for the evaluation of treatment (13, 14) because its level remains high for a long time after treatment, which was proven in the present case by detecting a continuous high titer of cryptococcal antigen even after Cryptococcus neoformans disappeared from the blood and right pleural effusion. On the other hand, a high titer of cryptococcal antigen is considered to be related to a poor prognosis reflecting the rapid progression of the fungus (15), which was also demonstrated in the present case, and led us to recognize that proper medication is important, especially in disseminated cryptococcosis. Combined therapy consisting of amphotericin B (AMPH- B) with flucytosine is recommended as first line therapy for disseminated cryptococcosis (16), but patients with the disease are prone to have some underlying disease such as myelosuppression or complications such as renal dysfunction, as was the case here, which implies that we should refrain from administering these cytotoxic drugs. L-AMB is recognized as a variant to AMPH-B with few side effects, and it was demonstrated that L-AMB was as effective and tolerable as AMPH-B, even in the compromised patients, because Cryptococcus neoformans disappeared from blood cultures after it was initiated, and a total dose of 4.35 g of L- AMB was administered before serum creatinine became slightly elevated. These results suggest that L-AMB monotherapy may be a good option. Furthermore, because alternative usage of F-FLCZ in place of L-AMB led to the disappearance of Cryptococcus neoformans in the right pleural effusion and clinical improvement, F-FLCZ can be substituted for long-term therapy. References 1. Chang WC, Tzao C, Hsu HH, et al. Pulmonary cryptococcosis: comparison of clinical and radiographic characteristics in immunocompetent and immunocompromised patients. Chest 129: , Newman TG, Soni A, Acaron S, Huang CT. Pleural cryptococcosis in the acquired immune deficiency syndrome. Chest 91: , Katz AS, Niesenbaum L, Mass B. Pleural effusion as the initial manifestation of disseminated cryptococcosis in acquired immune deficiency syndrome. diagnosis by pleural biopsy. Chest 96: , Poblete RB, Kirby BD. Cryptococcal peritonitis: report of a case and review of the literature. Am J Med 82: , Perfect JR. Cryptococcus neoformans. In: Principles and Practice of Infectious Diseases. 6th ed. Mandell GL, Bennett JE, Dolin Raphael, Eds. Churchill Livingstone, New York, 2004: Syme RM, Wood CJ, Wong H, Mody CH. Both CD4+ and CD8+ human lymphocytes are activated and proliferate in response to Cryptococcus neoformans. Immunology 92: , Shibuya K, Hirata A, Omuta J, et al. Granuloma and cryptococcosis. J Infect Chemother 11: , Young EJ, Hirsh DD, Fainstein V, Williams TW. Pleural effusion due to Cryptococcus neoformans: a review of the literature and report of two cases with cryptococcal antigen determinations. Am Rev Respir Dis 121: , Salyer WR, Salyer DC. Pleural involvement in cryptococcosis. Chest 66: , Tanner DC, Weinstein MP, Fedorciw B, Joho KL, Thorpe JJ, Reller LB. Comparison of commercial kits for detection of cryptococcal antigen. J Clin Microbiol 32: , Mabee CL, Mabee SW, Kirkpatrick RB, Koletar SL. Cirrhosis: a risk factor for cryptococcal peritonitis. Am J Gastroenterol 90: , Yinnon AM, Solages A, Teanor JJ. Cryptococcal peritonitis: report of a case developing during continuous ambulatory peritoneal dialysis and review of the literature. Clin Infect Dis 17: , Aberg JA, Watson J, Segal M, Chang LW. Clinical utility of monitoring serum cryptococcal antigen (scrag) titers in patients with AIDS-related cryptococcal disease. HIV Clin Trials 1: 1-6, Powderly WG, Cloud GA, Dismukes WE, Saag MS. Measurement of cryptococcal antigen in serum and cerebrospinal fluid: value in 1985
6 the management of AIDS-associated cryptococcal meningitis. Clin Infect Dis 18: , Chuck SL, Sande MA. Infections with Cryptococcus neoformans in the acquired immunodeficiency syndrome. N Engl J Med 321: , Saag MS, Graybill RJ, Larsen RA, et al. Practice guidelines for the management of cryptococcal disease. Infectious Diseases Society of America. Clin Infect Dis 30: , The Japanese Society of Internal Medicine
Hiroyuki Kamiya 1), Soichiro Ikushima 1), Tetsu Sakamoto 1), Kozo Morimoto 1), Tsunehiro Ando 1), Masaru Oritsu 1), Atsuo Goto 2), Tamiko Takemura 3)
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