Severe Strongyloidiasis in Corticosteroid-Treated Patients: Case Series and Literature Review

Journal of Infection (2007) 54,18e27

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Severe strongyloidiasis in corticosteroid-treated patients: Case series and literature review

Laurence Fardet*, Thierry Ge´ne´reau, Jean-Louis Poirot, Bertrand Guidet, Adrien Kettaneh, Jean Cabane

Hopital Saint-Antoine, Internal Medicine, Parasitology and Intensive Care Department, 184 rue du Fbg Saint-Antoine, 75012 Paris, France

Accepted 22 January 2006 Available online 14 March 2006

KEYWORDS Summary Objective: To describe the main features of severe strongyloidiasis in Strongyloidiasis; corticosteroid-treated patients Strongyloides Methods: We report on 3 cases of corticosteroid-treated patients with severe stron- stercoralis; gyloidiasis and review cases of severe strongyloidiasis in corticosteroid-treated Corticosteroids patients reported in the literature. Results: One hundred and fifty-one cases of severe strongyloidiasis complicated a therapy with corticosteroids were evaluated. The mean age of the patients was 48 17 years and 71% were men. Corticosteroids were given for hematological malignancies in 34 (23%), systemic lupus erythematosus or vasculitis in 27 (18%), and nephropathy or renal transplantation in 32 (21%). At time of infection, the mean daily dosage of prednisone-equivalent was 52 42 mg (median: 40 mg) and 84% of patients had received a cumulative dosage of prednisone-equivalent higher than 1000 mg. The total duration of treatment ranged from 4 days to 20 years (6 months or less: 69%). Non-specific gastro-intestinal symptoms were reported in 91% of these patients associated or not with pulmonary complaints. Low-grade fever was present in 54% of patients. Fifty-nine patients (39%) experienced severe bacterial or yeast infection during the course of severe strongyloidiasis. Peripheral eosinophilia was detected at presentation in 32% of patients. Strongyloidiasis was usually confirmed by repeated stool examinations. Thiabendazole was the treatment the more widely used. Eighty-nine patients (59%) deceased during the course of the disease. Conclusions: Severe strongyloidiasis is a risk in every corticosteroid-treated patient who has traveled to a soil-infested country, even if the contact was 30 years prior. This diagnosis should be suspected in patients who either experience unusual gastro-intestinal or pulmonary symptoms or suffer from unexplained Gram-negative bacilli sepsis. ª 2006 The British Infection Society. Published by Elsevier Ltd. All rights reserved.

* Corresponding author. Tel.: þ33149282373. E-mail address: [email protected] (L. Fardet).

Introduction ‘‘strongyloidiasis’’ or ‘‘Strongyloides stercoralis’’. Bibliographies of all articles were scanned for ref- Strongyloides stercoralis (Ss) is an ubiquitous intes- erences not identified in the initial search. For the tinal nematode endemic in sub-Saharan Africa, present analysis we included only the references in Southeast Asia, Latin America as well as in parts of English or French reporting patients treated with south-eastern United States and some European corticosteroids. Data were summarized using countries.1,2 This worm has a complex parasitic a standardized data form, including age, gender, life cycle that causes a long-lived auto-infection origin, current dosage and cumulative dosage of in the host.2 Many patients chronically infected corticosteroids at the time of Ss infection, dura- with Ss are asymptomatic or exhibit only minor tion of corticosteroids therapy at time of cutaneous (larva currens), pulmonary (cough) or infection, symptoms, specimens positive for gastro-intestinal (abdominal bloating and an- Strongyloides larvae, associated infection, eosino- orexia) symptoms. Thus, Ss can persist for decades philia, treatment and evolution. without being diagnosed. Under some conditions, Strongyloidiasis was classified as severe in case Ss can trigger the so-called hyperinfection syn- of (1) severe and persistent gastro-intestinal drome and the life-threatening disseminated forms symptoms with fever and/or marked asthenia, or of strongyloidiasis. The term ‘‘hyperinfection’’ has (2) extra-intestinal symptoms induced by Ss, or (3) been used to denote an increase in the auto-infec- presence of the parasite in extra-intestinal regions. tion cycle resulting in a massive invasion by filari- Inclusion was limited to patients with severe stron- form larvae.3 In these patients, most of whom are gyloidiasis treated by corticosteroids before the symptomatic, worms are easily detectable in bowels onset of strongyloidiasis symptoms, with larvae of Ss and often in lungs. The term ‘‘disseminated’’ has evidenced on biological samples (feces, gastric been used to describe a form of the disease in aspiration, bronchoalveolar lavage, etc.). which worms are also located in extra-intestinal and extra-pulmonary sites. However, these two Case reports forms are clinically difficult to distinguish. These severe forms of the disease are usually associated Case 1 with immunosuppressive or debilitating disorders. In October 2000 an 80-year-old white woman was Long-term corticosteroid therapy, leading to some hospitalized for abdominal pain, vomiting and suppression of inflammatory and immunologic re- diarrhea of 1 month duration. She had been treated 1 sponses and altering the hosteparasite equilibrium, with prednisone (80 mg d ) since August for giant is a well-known condition that predisposes the cell arteritis. The striking findings were fever patient to the occurrence of severe strongyloidiasis. (37.9 C) and a distended painful abdomen with To clarify the spectrum of clinical and biological predominant epigastric tenderness. No cutaneous features of Ss infection in patients receiving lesions were observed. Peripheral blood count 1 1 corticosteroids, we report herein 3 patients and showed 730 mL eosinophils and 12 000 mL reviewed the English and French language medical neutrophils. A blood culture was positive for literatures. Escherichia coli. Stool examinations showed numerous Strongyloides larvae. Upper gastro-intestinal endoscopy showed marked gastritis and duodenitis. Patients and methods Biopsies revealed an acute inflammatory infiltrate and the presence of many Ss ova and larvae, mainly We reviewed data for all patients with severe in the gastric glands. Chest X-rays were normal. She strongyloidiasis associated with corticosteroids was successively treated with antibiotics and thia- therapy admitted to our department between bendazole (2 g d1, 5 days). All symptoms improved January 2000 and January 2005. and repeated stool examinations were assessed We also performed a MEDLINE search, using the without evidence of any parasite. The patient was following terms, for cases reported in the litera- discharged 1 month after her admission. Ss was ture during 1966e2004: ‘‘immunocompromised’’, thought to be imported from Vietnam where the pa- ‘‘immunodepression’’, ‘‘corticosteroids’’, ‘‘gluco- tient lived between 1950 and 1960, without any corticoids’’, ‘‘steroids’’, ‘‘prednisone’’, ‘‘prednis- tropical journey thereafter. olone’’, ‘‘methylprednisolone’’, ‘‘asthma’’, ‘‘leukaemia’’, ‘‘lymphoma’’, ‘‘graft’’, ‘‘vasculi- Case 2 tis’’, ‘‘lupus erythematosus’’, ‘‘rheumatoid arthri- An 85-year-old man who had immigrated from tis’’, ‘‘sarcoidosis’’, ‘‘giant cell arteritis’’, ‘‘crohn Vietnam 40 years previously was diagnosed in March disease’’ or ‘‘ulcerative colitis’’ in addition to 2003 with giant cell arteritis. A treatment with 20 L. Fardet et al.

35 mg d1 of prednisone was initiated. Moreover, be- Literature cases cause of the patient’s origins (and without stool examination), a systematic prophylaxis of Ss infection A total of 163 corticosteroid-treated patients with was prescribed (2 courses of thiabendazole, total: severe Ss infection were found in literature. 1 4 g). While on prednisone 30 mg d , the patient Fifteen of them were not included because of e came back to our department in June 2003 because poorly documented clinical history (n ¼ 5),4 8 on- of persistent abdominal pain of 1 month duration set of strongyloidiasis symptoms prior to steroid e associated with diarrhea, weight loss and the recur- therapy (n ¼ 8),9 17 duplicated case (n ¼ 1)18 or rence of biological inflammatory syndrome. Blood unavailable paper (n ¼ 1)19 leaving 148 patients pressure and heart rate were normal and tempera- corresponding to 108 papers.20e128 ture was 37.7 C. Examination of chest, abdomen The 3 cases mentioned above were merged with and central nervous system was also normal. Hemo- 148 cases retrieved in the literature for an overall 1 globin concentration was 11 g dL , white blood analysis. 1 1 cell count was 12 500 mL with 500 eosinophils mL . The general characteristics of these 151 pa- 1 C-reactive protein was higher than 100 mg L , tients are summarized in Table 1. All patients but 3 1 fibrinogen was 7 g L . Chest roentgenogram was received oral corticosteroids (parenteral pulse: 2 normal as well as films of the abdomen. Fresh stool patients, subconjunctival injections of dexameth- examination showed numerous larvae of Ss. Oral asone: 1 patient122). The total duration of cortico- 1 thiabendazole (2 g d , 10 days) was started immedi- steroid therapy at time of infection was available ately and the patient condition improved remark- in 137 patients and the daily dosage of corticoste- ably. He was discharged 1 month after admission. roids in 112. A cumulative dosage could be esti- mated in 102 cases (67%). The results of these Case 3 data at time of strongyloidiasis are reported in A 46-year-old woman, who had immigrated from Table 1. Interestingly, 4 patients developed symp- Guinea 20 years previously, had chemotherapy toms a few days86,106,119 or weeks (5 weeks)62 after from September 1999 to May 2000 for an HTLV-1- the corticosteroids were stopped and no other associated non-Hodgkin’s lymphoma. Because of immunosuppressive therapy was added or pursued. the recurrence of lymphoma, the patient received Corticosteroids were associated with other immu- a new combination therapy in July 2000 associating nosuppressive therapy in 53 (35%) of these arsenic, interferon and prednisone (30 mg d1). patients. One of these patients was infected by Four weeks later, a blood culture grew Enterobacter the Human Immunodeficiency Virus.41 cloacae. Antibiotherapy was initiated and provided Clinical symptoms at presentation are described subsequent improvement. Two weeks later, the pain Table 1. Almost all patients (91%) presented tient developed acute abdominal pain associated with gastro-intestinal symptoms which were pre- with diarrhea and acute respiratory failure requir- dominantly abdominal pain, vomiting and diar- ing mechanical ventilation. Her blood pressure rhea. Patients presented usually with cough and/ was 110/70 mmHg, pulse 120/min and temperature or dyspnea associated with gastro-intestinal symp- 38 C. Other physical findings included diffuse bilat- toms, except in 17 patients in whom respiratory eral crackles associated with purulent sputum and symptoms were isolated. Fever was observed in a distended, diffusely tender abdomen. Neurologi- 81 patients (54%) and was mostly mild (mean: cal and cutaneous examinations were normal. Lab- 37.9 C). In 38 of these patients, cutaneous mani- oratory findings included a hemoglobin concentration festations such as transient rash or persistent of 7.3 g dL1 and white blood cell count of 8100 mL1 purpuric lesions were reported. with no eosinophils. Chest roentgenogram demon- Associated infections were common (Table 2). strated newly developed bilateral alveolo-intersti- Fifty-nine patients (39%) had evidence of severe tial changes. Examination of bronchoalveolar bacterial or yeast infection including bacteraemia lavage (BAL) fluid identified many Strongyloides (44 cases) associated or not with meningitis (23 filariform larvae and adult Ss females. Stool exami- cases). The organisms cultured were mainly nation failed to isolate these organisms. Treatment Gram-negative bacilli (82%). Six patients were in- with thiabendazole (3 g d1, 5 days) was then initi- fected with anaerobic bacteria (n ¼ 2), candide- ated but did not lead to eradication of the larvae mia (n ¼ 3) or disseminated aspergillosis (n ¼ 1). from the lungs (another lavage performed 7 days Serologic status regarding concomitant HTLV-1 in- later was again positive). Despite ventilatory and fection was reported in only 4 patients (3 positive). hemodynamic supports, the patient gradually dete- Peripheral eosinophilia (>500 mL1) was de- riorated and died 10 days after intubation. tected at presentation in 38 of the 118 patients Severe strongyloidiasis and Corticosteroids 21

Table 1 Characteristics of patients and corticoste- Table 2 Associated infections roid therapy at time of diagnosis of severe Number of patients strongyloidiasis Site of infectiona Gender, male/female 107 (71%)/44 (29%) Blood 44 Mean age SD 48 17 Years Central nervous system 23 Underlying disease Lung 5 Hematological 34 (23%) Peritoneum 3 malignancies Sub-cutaneous abscess 3 Nephropathy or renal 32 (21%) transplantation Organismsb Systemic lupus 27 (18%) E. coli 45 erythematosus or Klebsiella 11 vasculitis Pseudomonas/Serratia/ 10 Others 58 (38%) Enterobacter/Proteus Streptococcus bovis or 4 Mean daily dosage of 52 42 mg Streptococcus viridans equivalent Enterococcus 4 prednisone SD Staphylococcus aureus or 2 Staphylococcus epidermis Total duration of corticosteroid therapy Anaerobia 2 e Range 4 Days 20 years Candida species 3 Less than 15 days 12 (9%) e a A patient may be infected in more than one site. 15 30 Days 24 (17%) b 1e6 Months 68 (50%) A patient may be infected with more than one organism. More than 6 months 33 (24%)

Cumulative dosage of equivalent prednisone (mucosal edema, erosions or ulcer) or duodenitis Range 200e20 000 mg in all but one. Less than 1000 mg 16 (16%) Diagnosis of strongyloidiasis was performed after More than 1000 mg 85 (84%) death in 25 patients who were not given anthelmintic treatment. In the 126 others, the main pre- Gastro-intestinal symptoms 138 (91%) scribed drug was thiabendazole (105 patients). The Abdominal pain 102 (68%) most prescribed regimen was 25 mg kg d1 during Nausea/vomiting 61 (40%) 5e7 days. Nevertheless, daily dosage of that mole- Diarrhea 54 (36%) cule varied between patients (in adults, range Gastro-intestinal bleeding 30 (20%) 100 mg d1 38 to 7000 mg d1 33,42) as well as dura- Pulmonary symptoms 55 (36%) tion of treatment (range 2 days33e1 month85). Cutaneous manifestations 38 (25%) Fever 81 (54%) Albendazole (12 patients) or ivermectine (9 patients) were also used. Interestingly, one of our patients and 22 literature patients developed an invasive infection despite of having received a for whom this data were available (32%). The prophylactic treatment with thiabendazole. The median eosinophil count was 950 mL1. Sixteen mortality rate was high, 89 patients (59%) died percent of the patients who died exhibited an eo- during the course of strongyloidiasis. sinophil count greater than 500 mL1 versus 38% of the patients who survived (p ¼ 0.002). The diagnosis of Ss infection was made before death in 126 Discussion patients. Among 89 (71%) of these patients, Ss was evidenced by microscopic examination of stool Several studies have shown that the dormant or specimens. The parasite was found in sputum or carrier state of Ss may persist for very long periods bronchoalveolar lavage in 63 patients (50%) and of time (more than 30 years) without the de- in duodenal aspirate of 43 patients (34%). Ss was velopment of clinical disease.28,62,82 The develop- also found in skin (9 patients), peritoneal fluid ment of clinical manifestations is, in many cases, (7 patients) or cerebro-spinal fluid (2 patients). attributed to a decrease in host resistance caused Chest X-ray reported in 83 patients was normal by a debilitating disease, malnutrition or immuno- in only 16% of them. A bilateral lung infiltrate was suppressive drugs. Symptomatic strongyloidiasis is common among the others. Result of gastroscopy then an often fatal opportunistic infection for im- was available for 35 patients showing gastritis munocompromised hosts, in particular for those 22 L. Fardet et al. receiving corticosteroids. Moreover, the diagnosis men work outdoor more often than women, and of strongyloidiasis is often difficult to perform in thus might be exposed to Ss larvae for greater these patients whereas an early diagnosis is essen- periods of time. tial to allow early specific treatment. As point out by this review, clinical symptoms Epidemiologically, corticosteroids increase the reported by patients are non-specific. Gastro- risk of being infected with Ss. In the study of Berk intestinal symptoms are very common in patients et al.,129 patients infected with Ss were signifi- with severe strongyloidiasis (receiving or not cantly more likely to have received corticosteroids corticosteroids136) and symptomatic or occult gas- than those who were not infected. Nucci et al.130 tro-intestinal bleeding is a frequent sign at presen- retrospectively studied 343 consecutive patients tation (56% in the series of Adedayo et al.136). with hematological malignancies and showed that Fever at presentation is generally mild, probably the use of corticosteroids was one of the predic- blunted by corticosteroids. Lastly, we would tive factors for strongyloidiasis (OR, 2.29). In underline that symptoms associated with Ss infec- a caseecontrol study, Davidson et al.131 identified tion may mimic an exacerbation of the underlying a threefold increase of the relative risk of Ss disease and may led to an inappropriate increase infection in patients treated recently with cortico- of corticosteroid dosage. This point was observed steroids. However, little is known about the mech- for 29 patients we report. anisms by which corticosteroids are involved in the This series and others57,136 show that bacterial susceptibility to severe Ss infection. While most or yeast infections were frequently associated authors hypothesize that corticosteroids predis- with severe strongyloidiasis. The postulated mech- pose the patient to parasitic infection through anism for sepsis in these cases is transmission of their immunosuppressive effects (and particularly enteric bacteria through the bowel wall by invad- their effects on eosinophils, important mediators ing filariform larvae.57,140 Sepsis with Gram- of the immune response to Ss larvae,132,133) it has negative bacilli was a frequent presentation for been suggested134 that corticosteroids may have these patients and was frequently the cause of a direct effect on the parasites, precipitating dis- death. So, it has to be kept in mind that such a semination of Ss. sepsis in corticosteroid-treated patients with gastro- Interestingly, HTLV-1 co-infection, observed in intestinal symptoms may reflect an underlying in- one of our patients, is a well-known risk factor for fection with Ss and repeated stool examinations Ss infection.135 In the paper of Adedayo et al.136 have to be performed to not to misdiagnose the reviewing 27 patients with HS, 24 patients were parasitic infection. tested for HTLV-1 and 17 (71%) had positive test No Ss specific serology being available, the results. HTLV-1 may favor Ss infection by decreas- detection of this parasitic infection in patients ing IL-5 and IgE responses, by inducing a switch scheduled to receive steroids is still based on from Th2 to Th1 immunological response137 leading eosinophil count and stool examination, with to a pro-Ss synergy with corticosteroid therapy. poor diagnostic performances and the risk of not Since the geographic distribution of both infec- detecting the underlying infection. In asymptom- tions is largely overlapping, HTLV-1 should be atic patients, it has been shown that a single stool searched in every patient with Ss and reciprocally. examination fails to detect larvae in up to 70% of The preponderance of males in the current cases. Repeated stool examinations improved the series was similar to that reported by Adedayo chances of finding parasites (diagnostic sensitivity et al.136 in which patients developing an hyperin- approximately 100% with 7 samples).141 Even in the fective strongyloidiasis were not treated by corti- Baermann method, the Harada-Mori filter paper costeroids (27 patients, 18 males). It is possible and especially the agar-plate culture method are that hyperinfective strongyloidiasis be preponder- much more sensitive than single stool-smear,142 ant among males because males are widely in- they are not standard procedures in most clinical fected by the nematode. Indeed, in a second parasitology laboratories and have to be clearly study, Sanchez et al.138 described the epidemiol- required once the diagnosis suspected. Moreover, ogy and clinical features of 152 prospectively iden- the rate of eosinophilia was low in our series tified cases of strongyloidiasis (patients receiving (lower than in others which report an hypereosino- or not corticosteroids) and found a male/female philia among more than 50% of patients,129,131,139) ratio of 3/1. A third study139 reviewing 3271 stool may be because of the eosinophil-lowering role of examinations (52 patients infected with Ss), this corticosteroids. Taken together, this points out the ratio was 2/1. In another,131 men had a 3.9 difficulties in the diagnosis of severe strongyloidia- [1.24e11.41] greater risk of having Ss infection sis and explains why Ss infection was treated than women. One possible explanation was that before death in only 83% of patients. Severe strongyloidiasis and Corticosteroids 23

In 2000, the Centers for Disease Control and prevention of disseminated disease. Rev Infect Dis 1989; Prevention, the Infectious Disease Society of 11(5):755e67. America, and the American Society of Blood and 2. Siddiqui AA, Berk SL. Diagnosis of Strongyloides stercoralis infection. Clin Infect Dis 2001;33(7):1040e7. Marrow Transplantation recommended oral iver- 3. Scowden EB, Schaffner W, Stone WJ. Overwhelming stron- 1 mectin 200 mgkg daily for 2 consecutive days gyloidiasis: an unappreciated opportunistic infection. (alternative: oral albendazole 400 mg daily for 3 Medicine (Baltimore) 1978;57(6):527e44. days or thiabendazole 25 mg kg1 2 times/day for 4. Bank DE, Grossman ME, Kohn SR, Rabinowitz AD. The thumbprint sign: rapid diagnosis of disseminated strongy- 2 days) for the prevention of strongyloidiasis in e 143 loidiasis. J Am Acad Dermatol 1990;23(2 Pt 1):324 6. immunosuppressed patients. In 2003, an Austra- 5. Chaudhary K, Smith RJ, Himelright IM, Baddour LM. Case lian team recommended to treat unexplained pul- report: purpura in disseminated strongyloidiasis. Am J monary infiltrates, fever, abdominal pain or septic Med Sci 1994;308(3):186e91. shock in immunosuppressed patients (including pa- 6. Leelarasamee A, Nimmannit S, Na Nakorn S, Aswapokee N, tients receiving 0.5 mg kg d1 of prednisolone or Aswapokee P, Benjasuratwong Y. Disseminated strongyloidiasis: report of seven cases. Southeast Asian J Trop Med the equivalent for longer than 14 days) with an Public Health 1978;9(4):539e42. 1 oral ivermectin 200 mgkg on day 0, 1 and 7, 8 7. Pagliuca A, Layton DM, Allen S, Mufti GJ. Hyperinfection regimen.144 Nevertheless, the only available stud- with Strongyloides after treatment for adult T cell leukae- ies which corroborate these recommendations miaelymphoma in an African immigrant. BMJ 1988; e were performed in immunocompetent popula- 297(6661):1456 7. 145 8. Wagenvoort JH, Houben HG, Boonstra GL, Scherpbier J. tions. Gann et al. showed that 1 dose of iver- Pulmonary superinfection with Strongyloides stercoralis 1 mectin (200 mgkg in a single dose) provides in an immunocompromised retired coal miner. Eur J Clin safety and efficacy equivalent to thiabendazole Microbiol Infect Dis 1994;13(6):518e9. (50 mg kg d1 for 3 consecutive days) with a much 9. Civantos F, Robinson MJ. Fatal strongyloidiasis following e lower prevalence of side effects. Others showed corticosteroid therapy. Am J Dig Dis 1969;14(9):643 51. 10. de Goede E, Martens M, Van Rooy S, VanMoerkerke I. A case of e 1 that ivermectin (150 200 mgkg in a single systemic strongyloidiasis in an ex-coal miner with idiopathic 1 dose) was superior to albendazole (400 mg d for colitis. Eur J Gastroenterol Hepatol 1995;7(8):807e9. 3 days) in the treatment of uncomplicated strong- 11. Klein RA, Cleri DJ, Doshi V, Brasitus TA. Disseminated yloidiasis.146e148 To our knowledge, only one study Strongyloides stercoralis: a fatal case eluding diagnosis. e is available in immunocompromised hosts. This South Med J 1983;76(11):1438 40. 12. Leung VK, Liew CT, Sung JJ. Fatal strongyloidiasis in a study tested the efficacy of thiabendazole for the patient with ulcerative colitis after corticosteroid therapy. prophylaxis of strongyloidiasis in 103 patients Am J Gastroenterol 1997;92(8):1383e4. (patients immunosuppressed by hematological 13. Mariotta S, Pallone G, LiBianchi E, Gilardi G, Bisetti A. Strong- diseases or benign condition treated with cortico- yloides stercoralis hyperinfection in a case of idiopathic e steroids) and showed that the drug was not supe- pulmonary fibrosis. Panminerva Med 1996;38(1):45 7. 14. Massey AC, Weinstein DL, Petri WA, Williams ME, Hess CE. rior to placebo (incidence rate of strongyloidiasis ATLL complicated by strongyloidiasis and isosporiasis: case 149 2% versus 7%, p ¼ 0.36). However, the statistical report. Va Med Q 1990;117(7):311e6. power of these study was lower than projected 15. Pansegrouw D. Strongyloides stercoralis infestation 80%. Therefore, to date, ivermectine is the best masquerading as steroid resistant asthma. Monaldi Arch e prophylactic and therapeutic option and thiaben- Chest Dis 1994;49(5):399 402. 16. Yim Y, Kikkawa Y, Tanowitz H, Wittner M. Fatal strongyloi- dazole should no longer be used. diasis in Hodgkin’s disease after immunosuppressive ther- In this work, we did not distinguish patients with apy. J Trop Med Hyg 1970;73(10):245e9. hyperinfection syndrome and those with criteria 17. Gill GV, Beeching NJ, Khoo S, Bailey JW, Partridge S, for disseminated disease. Indeed, we believe that Blundell JW, et al. A British Second World War veteran these 2 forms of the disease are not always with disseminated strongyloidiasis. Trans R Soc Trop Med Hyg 2004;98(6):382e6. distinguishable among alive patients and represent 18. Pagliuca A. Strongyloides hyperinfection in adult T-cell probably the same entity at different stages of leukaemia/lymphoma. Br J Haematol 1999;105(1):1. evolution. Because the treatment of these 2 forms 19. Wilkinson R, Leen CL. Chronic lymphocytic leukaemia and is the same we agree with Siddiqui and Berk2 and overt presentation of underlying Strongyloides stercoralis e Grove,150 that it would be simpler to categorized infection. J Infect 1993;27(1):99 100. 20. Adam M, Morgan O, Persaud C, Gibbs WN. Hyperinfection strongyloidiasis as ‘‘uncomplicated’’ (the purely syndrome with Strongyloides stercoralis in malignant lym- digestive and most frequent form of the disease) phoma. BMJ 1973;1(5848):264e6. and ‘‘complicated’’ or ‘‘severe’’. 21. Ainley CC, Clarke DG, Timothy AR, Thompson RP. Strongy- loides stercoralis hyperinfection associated with cimeti- dine in an immunosuppressed patient: diagnosis by References endoscopic biopsy. Gut 1986;27(3):337e8. 22. Ali-Khan Z, Seemayer TA. Fatal bowel infarction and sep- 1. Genta RM. Global prevalence of strongyloidiasis: sis: an unusual complication of systemic strongyloidiasis. critical review with epidemiologic insights into the Trans R Soc Trop Med Hyg 1975;69(5e6):473e6. 24 L. Fardet et al.

23. Almasidou D, Maniatis M, Vassiou K, Damani E, Vakalis N, 42. Dwork KG, Jaffe JR, Lieberman HD. Strongyloidiasis with Fesoulidis I, et al. Strongyloides hyperinfection in a patient massive hyperinfection. N Y State J Med 1975;75(8):1230e4. with sarcoidosis. Respirology 2003;8(1):105e6. 43. Fagundas LA, Busato O, Brentano L. Strongyloidiasis: fatal 24. Aydin H, Doppl W, Battmann A, Bohle RM, Klor HU. Oppor- complication of renal transplantation. Lancet 1971; tunistic Strongyloides stercoralis hyperinfection in lym- 2(7721):439e40. phoma patients undergoing chemotherapy and/or 44. Finkielman JD, Grinberg AR, Paz LA, Plana JL, radiotherapy e report of a case and review of the litera- Benchetrit GA, Nicastro MA, et al. Case report: reactive ture. Acta Oncol 1994;33(1):78e80. hemophagocytic syndrome associated with disseminated 25. Berenson CS, Dobuler KJ, Bia FJ. Fever, petechiae, and strongyloidiasis. Am J Med Sci 1996;312(1):37e9. pulmonary infiltrates in an immunocompromised Peruvian 45. Fowler CG, Lindsay I, Levin J, Sweny P, Fernando ON, man. Yale J Biol Med 1987;60(5):437e45. Moorhead JF. Recurrent hyperinfestation with Strongy- 26. Berger R, Kraman S, Paciotti M. Pulmonary stronglyoidiasis loides stercoralis in a renal allograft recipient. BMJ complicating therapy with corticosteroids. Report of 1982;285(6352):1394. a case with secondary bacterial infections. Am J Trop 46. Genta RM, Miles P, Fields K. Opportunistic Strongyloides Med Hyg 1980;29(1):31e4. stercoralis infection in lymphoma patients. Report of 27. Bezares RF, Carreras LO, Marin CA, Rodriguez Fuchs CA, de a case and review of the literature. Cancer 1989;63(7): Tezanos Pinto M, Nunez EN. Fatal Strongyloides stercoralis 1407e11. hyperinfection in acute leukaemia. Lancet 1983;1(8322): 47. Ghoshal UC, Saha J, Ghosal U, Ray BK, Santra A, Naik S, 481. et al. Pigmented nails and Strongyloides stercoralis infes- 28. Boram LH, Keller KF, Justus DE, Collins JP. Strongyloidiasis tation causing clinical worsening in a patient treated for in immunosuppressed patients. Am J Clin Pathol 1981; immunoproliferative small intestinal disease: two unusual 76(6):778e81. observations. J Diarrhoeal Dis Res 1999;17(1):43e5. 29. Bradley SL, Dines DE, Brewer NS. Disseminated Strongy- 48. Goldman DE, Grier JF, Ball BE, Abreo F, Abreo KD. A 72- loides stercoralis in an immunosuppressed host. Mayo year-old woman with non-Hodgkin’s lymphoma, dyspnea, Clin Proc 1978;53(5):332e5. vomiting, diarrhea, and eosinophilia. J La State Med Soc 30. Casati A, Cornero G, Muttini S, Tresoldi M, Gallioli G, 1995;147(6):243e50. Torri G. Hyperacute pneumonitis in a patient with over- 49. Gordon SM, Gal AA, Solomon AR, Bryan JA. Disseminated whelming Strongyloides stercoralis infection. Eur J Anaes- strongyloidiasis with cutaneous manifestations in an im- thesiol 1996;13(5):498e501. munocompromised host. J Am Acad Dermatol 1994;31(2 31. Case records of the Massachusetts General Hospital. Pt 1):255e9. Weekly clinicopathological exercises, Case 47e1987. A 50. Hakim SZ, Genta RM. Fatal disseminated strongyloidiasis in 79-year-old Cuban native with asthma, weight loss, vomit- a Vietnam war veteran. Arch Pathol Lab Med 1986;110(9): ing, eosinophilia, and past meningitis. N Engl J Med 1987; 809e12. 317(21):1332e42. 51. Harris Jr RA, Musher DM, Fainstein V, Young EJ, Clarridge J. 32. Chabannon C, Peyrond F, Faure H, Sotto JJ. Malignant an- Disseminated strongyloidiasis. Diagnosis made by sputum guilluliasis with digestive localization in an immunosup- examination. JAMA 1980;244(1):65e6. pressed patient. Gastroenterol Clin Biol 1989;13(12): 52. Hayden GM, Atlas SA. Strongyloidiasis masquerading as in- 1090e1. flammatory bowel disease in a patient with lupus erythe- 33. Chaudhuri B, Nanos S, Soco JN, McGrew EA. Disseminated matosis: a case report. Conn Med 1995;59(11):649e50. Strongyloides stercoralis infestation detected by sputum 53. Hennequin C, Pialoux G, Taillet-Bellemere C, Caujolle B, cytology. Acta Cytol 1980;24(4):360e2. Petite JP. Anguilluliasis hyperinfection in a patient receiv- 34. Chu E, Whitlock WL, Dietrich RA. Pulmonary hyperinfec- ing corticosteroids: hepatic and biliary involvement. tion syndrome with Strongyloides stercoralis. Chest Gastroenterol Clin Biol 1991;15(1):87e8. 1990;97(6):1475e7. 54. Higenbottam TW, Heard BE. Opportunistic pulmonary 35. Cook GA, Rodriguez H, Silva H, Rodriguez-Iturbe B, Bohor- strongyloidiasis complicating asthma treated with ste- quez de Rodriguez H. Adult respiratory distress secondary roids. Thorax 1976;31(2):226e33. to strongyloidiasis. Chest 1987;92(6):1115e6. 55. Hirschmann JV, Plorde JJ, Ochi RF. Fever and pulmonary 36. Coulter C, Walker DG, Gunsberg M, Brown IG, Bligh JF, infiltrates in a patient with a renal transplant. West J Prociv P. Successful treatment of disseminated strongyloi- Med 1984;140(6):914e20. diasis. Med J Aust 1992;157(5):331e2. 56. Huang MS, Hwang KP, Chiang PC, Hwang JJ. Pulmonary 37. Cruz T, Reboucas G, Rocha H. Fatal strongyloidiasis in pa- hyperinfection with Strongyloides stercoralis. J Formos tients receiving corticosteroids. N Engl J Med 1966; Med Assoc 1996;95(7):551e4. 275(20):1093e6. 57. Igra-Siegman Y, Kapila R, Sen P, Kaminski ZC, Louria DB. 38. Cuni LJ, Rosner F, Chawla SK. Fatal strongyloidiasis. In im- Syndrome of hyperinfection with Strongyloides stercora- munosuppressed patients. N Y State J Med 1977;77(13): lis. Rev Infect Dis 1981;3(3):397e407. 2109e13. 58. Jaramillo D, Leon W, Cardenas V, Cortes A. Reiter’s syn- 39. Czachor JS, Jonas AP. Transmission of Strongyloides ster- drome, immunodepression and strongyloidiasis. Report of acolis person to person. J Travel Med 2000;7(4):211e2. a fatal case. J Cutan Pathol 1978;5(4):200e8. 40. Daubenton JD, Buys HA, Hartley PS. Disseminated strongy- 59. Kaslow JE, Novey HS, Zuch RH, Spear GS. Disseminated loidiasis in a child with lymphoblastic lymphoma. J Pediatr strongyloidiasis: an unheralded risk of corticosteroid ther- Hematol Oncol 1998;20(3):260e3. apy. J Allergy Clin Immunol 1990;86(1):138. 41. Dutcher JP, Marcus SL, Tanowitz HB, Wittner M, 60. Kebede D. Strongyloidiasis and glucocorticoids: case Fuks JZ, Wiernik PH. Disseminated strongyloidiasis with report. V Med 1986;113(2):104e5. central nervous system involvement diagnosed antemor- 61. Kim YK, Kim H, Park YC, Lee MH, Chung ES, Lee SJ, et al. tem in a patient with acquired immunodeficiency syn- A case of hyperinfection with Strongyloides stercoralis in drome and Burkitts lymphoma. Cancer 1990;66(11): an immunosuppressed patient. Korean J Intern Med 2417e20. 1989;4(2):165e70. Severe strongyloidiasis and Corticosteroids 25

62. Kimmelstiel F, Lange M. Fatal systemic strongyloidiasis 83. Polenakovik H, Polenakovik S, Weinstein J, Pelstring RJ. following corticosteroid therapy. N Y State J Med 1984; New-onset purpura in a patient with recently diagnosed tem- 84(8):399e401. poral arteritis. Clin Infect Dis 2003;37(2):238e40, 299-301. 63. Kinjo T, Tsuhako K, Nakazato I, et al. Extensive intra-alve- 84. Pollock TW, Perencevich EN. Hyperinfection with Strongy- olar haemorrhage caused by disseminated strongyloidiasis. loides stercoralis in a patient with Hodgkin’s disease. JAm Int J Parasitol 1998;28(2):323e30. Osteopath Assoc 1976;76(3):171e5. 64. Kothary NN, Muskie JM, Mathur SC. Strongyloides stercor- 85. Powell RW, Moss JP, Nagar D, Melo JC, Boram LH, alis hyperinfection. Radiographics 1999;19(4):1077e81. Anderson WH, et al. Strongyloidiasis in immunosuppressed 65. Kuberski TT, Gabor EP, Boudreaux D. Disseminated stron- hosts. Presentation as massive lower gastrointestinal bleed- gyloidiasis. A complication of the immunosuppressed ing. Arch Intern Med 1980;140(8):1061e3. host. West J Med 1975;122(6):504e8. 86. Powles AC. Strongyloides stercoralis hyperinfection: case 66. Lemos LB, Qu Z, Laucirica R, Fred HL. Hyperinfection syn- report. N Z Med J 1973;77(490):169e71. drome in strongyloidiasis: report of two cases. Ann Diagn 87. Rassiga AL, Lowry JL, Forman WB. Diffuse pulmonary Pathol 2003;7(2):87e94. infection due to Strongyloides stercoralis. JAMA 1974; 67. Liepman M. Disseminated Strongyloides stercoralis.A 230(3):426e7. complication of immunosuppression. JAMA 1975;231(4): 88. Reddy TS, Myers JW. Syndrome of inappropriate secretion 387e8. of antidiuretic hormone and nonpalpable purpura in 68. Link K, Orenstein R. Bacterial complications of strongyloi- a woman with Strongyloides stercoralis hyperinfection. diasis: Streptococcus bovis meningitis. South Med J 1999; Am J Med Sci 2003;325(5):288e91. 92(7):728e31. 89. Reiman S, Fisher R, Dodds C, Trinh C, Laucirica R, 69. Livneh A, Coman EA, Cho SH, Lipstein-Kresch E. Strongy- Whigham CJ. Mesenteric arteriographic findings in a loides stercoralis hyperinfection mimicking systemic patient with Strongyloides stercoralis hyperinfection. lupus erythematosus flare. Arthritis Rheum 1988;31(7): J Vasc Interv Radiol 2002;13(6):635e8. 930e1. 90. Rivals A, Rouquet RM, Recco P, Linas MD, Leophonte P, 70. Marsan C, Marais MH, Sollet JP, Le Turdu F, Guerin PH, Didier A. A rare cause of asthma exacerbation: systemic Garcia R, et al. Disseminated strongyloidiasis: a case anguilluliasis. Rev Mal Respir 2000;17(1):99e102. report. Cytopathology 1993;4(2):123e6. 91. Rivera E, Maldonado N, Velez-Garcia E, Grillo AJ, 71. McNeely DJ, Inouye T, Tam PY, Ripley SD. Acute respiratory Malaret G. Hyperinfection syndrome with Strongyloides failure due to strongyloidiasis in polymyositis. J Rheumatol stercoralis. Ann Intern Med 1970;72(2):199e204. 1980;7(5):745e50. 92. Rodrigues MA, Froes RC, Anefalos A, Kobayasi S. Invasive 72. Mejia JH, Denis M, Leleu G, Roux P, Mayaud C, Akoun G. enteritis by Strongyloides stercoralis presenting as acute Acute respiratory insufficiency caused by hyperinfestation abdominal distress under corticosteroid therapy. Rev with Strongyloides. BALF diagnosis and favourable out- Hosp Clin Fac Med Sao Paulo 2001;56(4):103e6. come. Rev Pneumol Clin 1992;48(2):75e8. 93. Rogers Jr WA, Nelson B. Strongyloidiasis and malignant 73. Meyers AM, Shapiro DJ, Milne FJ, Myburgh JA, Rabkin R. lymphoma. ‘‘Opportunistic infection’’ by a nematode. Strongyloides stercoralis hyperinfection in a renal allo- JAMA 1966;195(8):685e7. graft recipient. S Afr Med J 1976;50(33):1301e2. 94. Ronan SG, Reddy RL, Manaligod JR, Alexander J, Fu T. 74. Morgan JS, Schaffner W, Stone WJ. Opportunistic strongy- Disseminated strongyloidiasis presenting as purpura. J loidiasis in renal transplant recipients. Transplantation Am Acad Dermatol 1989;21(5 Pt 2):1123e5. 1986;42(5):518e24. 95. Sarubbi FA. Hyperinfection with Strongyloides during 75. Mori S, Konishi T, Matsuoka K, Deguchi M, Ohta M, treatment of Pemphigus vulgaris. Arch Dermatol 1987; Mizuno O, et al. Strongyloidiasis associated with nephrotic 123(7):864e5. syndrome. Intern Med 1998;37(7):606e10. 96. Schindzielorz A, Edberg SC, Bia FJ. Strongyloides stercora- 76. Morimoto J, Kaneoka H, Sasatomi Y, Sato YN, Murata T, lis hyperinfection and central nervous system involvement Ogahara S, et al. Disseminated strongyloidiasis in ne- in a patient with relapsing polychondritis. South Med J phrotic syndrome. Clin Nephrol 2002;57(5):398e401. 1991;84(8):1055e7. 77. Nagalotimath SJ, Ramaprasad AV, Chandrashekhar NK. 97. Scoggin CH, Call NB. Acute respiratory failure due to dis- Fatal strongyloidiasis in a patient receiving corticoste- seminated strongyloidiasis in a renal transplant recipient. roids. Indian J Pathol Bacteriol 1974;17(3):190e2. Ann Intern Med 1977;87(4):456e8. 78. Neefe LI, Pinilla O, Garagusi VF, Bauer H. Disseminated 98. Seabury JH, Abadie S, Savoy Jr F. Pulmonary strongyloidi- strongyloidiasis with cerebral involvement. A complication asis with lung abscess. Ineffectiveness of thiabendazole of corticosteroid therapy. Am J Med 1973;55(6):832e8. therapy. Am J Trop Med Hyg 1971;20(2):209e11. 79. Ossorio MA, Brown PE, Fields CL, Roy TM. Exacerbation of 99. Sekhar U, Madan M, Ranjitham M, Abraham G, Eapen G. chronic obstructive pulmonary disease due to hyperinfec- Strongyloides hyperinfection syndrome e an unappreci- tion with Strongyloides stercoralis. J Ky Med Assoc 1990; ated opportunistic infection. J Assoc Physicians India 88(5):233e7. 2000;48(10):1017e9. 80. Palau LA, Pankey GA. Strongyloides hyperinfection in a 100. Sen P, Gil C, Estrellas B, Middleton JR. Corticosteroid- renal transplant recipient receiving cyclosporine: possible induced asthma: a manifestation of limited hyperinfection Strongyloides stercoralis transmission by kidney trans- syndrome due to Strongyloides stercoralis. South Med J plant. Am J Trop Med Hyg 1997;57(4):413e5. 1995;88(9):923e7. 81. Panyathanya R, Sriumpai S, Tantranond R. Fatal strongyloi- 101. Setoyama M, Fukumaru S, Takasaki T, Yoshida H, diasis in Siriraj Hospital, Bangkok, Thailand. Southeast Kanzaki T. SLE with death from acute massive pulmonary Asian J Trop Med Public Health 1983;14(3):294e7. hemorrhage caused by disseminated strongyloidiasis. 82. Pasqualini L, Crotti D, Scarponi A, Vaudo G, Mannarino E. Scand J Rheumatol 1997;26(5):389e91. Strongyloides stercoralis infection in a patient with 102. Sim TC, Alam R, Grant JA. Refractory wheezing and septi- Crohn’s disease. Eur J Clin Microbiol Infect Dis 1997; cemia in a 57-year-old man with asthma. Ann Allergy 1990; 16(5):401e3. 65(3):180e4. 26 L. Fardet et al.

103. Simpson WG, Gerhardstein DC, Thompson JR. Dissemi- 124. Willis AJ, Nwokolo C. Steroid therapy and strongyloidiasis. nated Strongyloides stercoralis infection. South Med J Lancet 1966;1(7452):1396e8. 1993;86(7):821e5. 125. Wong TY, Szeto CC, Lai FF, Mak CK, Li PK. Nephrotic 104. Smedts Walters H, Bader-Meunier B, Dommergues JP. He- syndrome in strongyloidiasis: remission after eradication mophagocytic syndrome associated with strongyloidiasis with anthelmintic agents. Nephron 1998;79(3):333e6. in a child treated for acute lymphoblastic leukemia. Arch 126. Wurtz R, Mirot M, Fronda G, Peters C, Kocka F. Short Pediatr 1998;5(3):346e7. report: gastric infection by Strongyloides stercoralis. Am 105. Soman R, Vaideeswar P, Shah H, Almeida AF. A 34-year-old J Trop Med Hyg 1994;51(3):339e40. renal transplant recipient with high-grade fever and progres- 127. Yee A, Boylen CT, Noguchi T, Klatt EC, Sharma OP. Fatal sive shortness of breath. J Postgrad Med 2002;48(3):191e6. Strongyloides stercoralis infection in a patient receiving 106. Sreenivas DV, Kumar A, Kumar YR, Bharavi C, Sundaram C, corticosteroids. West J Med 1987;146(3):363e4. Gayathri K. Intestinal strongyloidiasis e a rare opportunis- 128. Yun HR, Yoo DH, Lee HS, Kim TH, Ahn MH, Min Dy, et al. tic infection. Indian J Gastroenterol 1997;16(3):105e6. Fatal Strongyloides hyper-infection in a patient with rheu- 107. Stewart JB, Heap BJ. Fatal disseminated strongyloidiasis matoid arthritis. Clin Exp Rheumatol 2001;19(2):224. in an immunocompromised former war prisoner of the 129. Berk SL, Verghese A, Alvarez S, Hall K, Smith B. Clinical Japanese. J R Army Med Corps 1985;131(1):47e9. and epidemiologic features of strongyloidiasis. A prospec- 108. Suvajdzic N, Kranjcic-Zec I, Jovanovic V, Popovic D, tive study in rural Tennessee. Arch Intern Med 1987; Colovic M. Fatal strongyloidosis following corticosteroid 147(7):1257e61. therapy in a patient with chronic idiopathic thrombocyto- 130. Nucci M, Portugal R, Pulcheri W, Spector N, Ferreira SB, de penia. Haematologia (Budap) 1999;29(4):323e6. Castro MB, et al. Strongyloidiasis in patients with hemato- 109. Suzuki T, Nara N, Miyake S, Eishi Y, Sugiyama E, Aoki N. Fa- logic malignancies. Clin Infect Dis 1995;21(3):675e7. tal strongyloidiasis latent over 42 years in the antineoplas- 131. Davidson RA, Fletcher RH, Chapman LE. Risk factors for tic chemotherapy of a case with malignant lymphoma. Jpn strongyloidiasis. A caseecontrol study. Arch Intern Med J Med 1989;28(1):96e9. 1984;144(2):321e4. 110. Tabacof J, Feher O, Katz A, Simon SD, Gansl RC. Strongy- 132. Brigandi RA, Rotman HL, Leon O, Nolan TJ, Schad GA, loides hyperinfection in two patients with lymphoma, pu- Abraham D. Strongyloides stercoralis host-adapted third- rulent meningitis, and sepsis. Cancer 1991;68(8):1821e3. stage larvae are the target of eosinophil-associated 111. Tankanow L, Eichenhorn MS. Disseminated Strongyloides immune-mediated killing in mice. J Parasitol 1998;84(2): stercoralis and Aspergillus fumigatus presenting as diffuse 440e5. interstitial pneumonitis in a steroid-dependent chronic ob- 133. Herbert DR, Lee JJ, Lee NA, Nolan TJ, Schad GA, structive pulmonary disease patient. Henry Ford Hosp Med Abraham D. Role of IL-5 in innate and adaptive immunity J 1988;36(1):41e3. to larval Strongyloides stercoralis in mice. J Immunol 112. Tarr PE, Miele PS, Peregoy KS, Smith MA, Neva FA, 2000;165(8):4544e51. Lucey DR. Case report: rectal adminstration of ivermectin 134. Genta RM. Dysregulation of strongyloidiasis: a new hypoth- to a patient with Strongyloides hyperinfection syndrome. esis. Clin Microbiol Rev. 1992;5(4):345e55. Am J Trop Med Hyg 2003;68(4):453e5. 135. Courouble G, Rouet F, Herrmann-Strock C, Nicolas M, 113. Thomas MC, Costello SA. Disseminated strongyloidiasis Candolﬁ E, Deloumeaux J, et al. Epidemiologic study of arising from a single dose of dexamethasone before ste- the association between human T-cell lymphotropic virus reotactic radiosurgery. Int J Clin Pract 1998;52(7):520e1. type 1 and Strongyloides stercoralis infection in female 114. Thompson JR, Berger R. Fatal adult respiratory distress blood donors (Guadeloupe, French West Indies). West syndrome following successful treatment of pulmonary Indian Med J 2004;53(1):3e6. strongyloidiasis. Chest 1991;99(3):772e4. 136. Adedayo O, Grell G, Bellot P. Hyperinfective strongyloidia- 115. Ting YM. Pulmonary strongyloidiasis e case report of 2 sis in the medical ward: review of 27 cases in 5 years. cases. Kaohsiung J Med Sci 2000;16(5):269e74. South Med J 2002;95(7):711e6. 116. Venizelos PC, Lopata M, Bardawil WA, Sharp JT. Respira- 137. Porto AF, Neva FA, Bittencourt H, Lisboa W, Thompson R, tory failure due to Strongyloides stercoralis in a patient Alcantara L, et al. HTLV-1 decreases Th2 type of immune with a renal transplant. Chest 1980;78(1):104e6. response in patients with strongyloidiasis. Parasite Immu- 117. Vishwanath S, Baker RA, Mansheim BJ. Strongyloides in- nol 2001;23(9):503e7. fection and meningitis in an immunocompromised host. 138. Sanchez PR, Guzman AP, Guillen SM, Adell RI, Estruch AM, Am J Trop Med Hyg 1982;31(4):857e8. Gonzalo IN, et al. Endemic strongyloidiasis on the Spanish 118. von Kuster LC, Genta RM. Cutaneous manifestations of Mediterranean coast. QJM 2001;94(7):357e63. strongyloidiasis. Arch Dermatol 1988;124(12):1826e30. 139. Milder JE, Walzer PD, Kilgore G, Rutherford I, Klein M. Clin- 119. Vulser C, Cousin MT. Malignant anguilluliasis. A fatal case ical features of Strongyloides stercoralis infection in an following corticoid therapy in a diabetic. Cah Anesthesiol endemic area of the United States. Gastroenterology 1990;38(3):187e90. 1981;80(6):1481e8. 120. Wachter RM, Burke AM, MacGregor RR. Strongyloides ster- 140. Ghoshal UC, Ghoshal U, Jain M, Kumar A, Aggarwal R, coralis hyperinfection masquerading as cerebral vasculitis. Misra A, et al. Strongyloides stercoralis infestation associ- Arch Neurol 1984;41(11):1213e6. ated with septicemia due to intestinal transmural migration 121. Webster E, Ballinger Jr WE, Panush RS. A case of a patient of bacteria. J Gastroenterol Hepatol 2002;17(12):1331e3. with deteriorating multisystem disease. Ann Allergy 1984; 141. Nielsen PB, Mojon M. Improved diagnosis of Strongyloides 52(6):399e400. 423e7. stercoralis by seven consecutive stool specimens. Zen- 122. West BC, Wilson JP. Subconjunctival corticosteroid ther- tralbl Bakteriol Mikrobiol Hyg [A] 1987;263(4):616e8. apy complicated by hyperinfective strongyloidiasis. Am J 142. Jongwutiwes S, Charoenkorn M, Sitthichareonchai P, Ophthalmol 1980;89(6):854e7. Akaraborvorn P, Putaporntip C. Increased sensitivity of 123. White JV, Garvey G, Hardy MA. Fatal strongyloidiasis after routine laboratory detection of Strongyloides stercoralis renal transplantation: a complication of immunosuppres- and hookworm by agar-plate culture. Trans R Soc Trop sion. Am Surg 1982;48(1):39e41. Med Hyg 1999;93(4):398e400. Severe strongyloidiasis and Corticosteroids 27

143. Centers for Disease Control and Prevention, Infectious Dis- 147. Marti H, Haji HJ, Savioli L, Chwaya HM, Mgeni AF, Ameir JS, ease Society of America, American Society of Blood and et al. A comparative trial of a single-dose ivermectin ver- Marrow Transplantation. Guidelines for preventing oppor- sus three days of albendazole for treatment of Strongy- tunistic infections among hematopoietic stem cell trans- loides stercoralis and other soil-transmitted helminth plant recipients. MMWR Recomm Rep 2000 Oct;49(RR-10): infections in children. Am J Trop Med Hyg 1996;55(5): 1e125, CE1e7. 477e81. 144. Davis JS, Currie BJ, Fisher DA, Huffam SE, Anstey NM, 148. Datry A, Hilmarsdottir I, Mayorga-Sagastume R, Lyagoubi M, Price RN, et al. Prevention of opportunistic infections in im- Gaxotte P, Biligui S, et al. Treatment of Strongyloides ster- munosuppressed patients in the tropical top end of the coralis infection with ivermectin compared with albenda- Northern Territory. Commun Dis Intell 2003;27(4):526e32. zole: results of an open study of 60 cases. Trans R Soc Trop 145. Gann PH, Neva FA, Gam AA. A randomized trial of single- Med Hyg 1994;88(3):344e5. and two-dose ivermectin versus thiabendazole for treat- 149. Portugal R, Schaffel R, Almeida L, Spector N, Nucci M. ment of strongyloidiasis. J Infect Dis 1994;169(5):1076e9. Thiabendazole for the prophylaxis of strongyloidiasis in im- 146. Toma H, Sato Y, Shiroma Y, Kobayashi J, Shimabukuro I, munosuppressed patients with hematological diseases: Takara M. Comparative studies on the efﬁcacy of three an- a randomized double-blind placebo-controlled study. thelminthics on treatment of human strongyloidiasis in Haematologica 2002;87(6):663e4. Okinawa, Japan. Southeast Asian J Trop Med Public Health 150. Grove DI. Human strongyloidiasis. Adv Parasitol 1996;38: 2000;31(1):147e51. 251e309.