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  Table of Contents    
CASE REPORT  
Year : 2018  |  Volume : 61  |  Issue : 1  |  Page : 109-112
Strongyloides stercoralis hyperinfection in an unconscious diabetic patient with dermatomyositis


1 Department of Medical Parasitology and Mycology, School of Medicine, Guilan University of Medical Sciences, Rasht, Iran
2 Emergency Department of Emam Reza Hospital, Qom Medical Center, Social Security Organization, Qom, Iran
3 Department of Medical Parasitology and Mycology, Amol Faculty of Paramedics, Mazandaran University of Medical Sciences, Sari, Iran
4 Center for Research of Endemic Parasites of Iran, Tehran University of Medical Sciences; Department of Medical Parasitology and Mycology, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran

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Date of Web Publication22-Mar-2018
 

   Abstract 


A case of Strongyloides stercoralis hyperinfection in a patient with dermatomyositis and diabetes mellitus is herein reported. The case was a 60-year-old female admitted due to watery diarrhea and unconsciousness. She had a 10-year history of chronic immunosuppressive therapy including methotrexate and prednisolone for dermatomyositis. Stool parasitological examination revealed numerous rhabditiform larvae of threadworm “S. stercoralis.” Larva in stool sample was characterized by sequencing of mitochondrial DNA. After treatment with ivermectin, the patient recovered without evidence of S. stercoralis in follow-up stool samples. In endemic areas, stool examination for detection of S. stercoralis should be performed on a regular basis for all patients receiving immunosuppressive therapy, as early detection and treatment are necessary to minimize complications of severe strongyloidiasis.

Keywords: Dermatomyositis, diabetes mellitus, immunosuppression, Strongyloides stercoralis, strongyloidiasis hyperinfection, threadworm

How to cite this article:
Sharifdini M, Hesari A, Mahdavi SA, Alipour A, Kia EB. Strongyloides stercoralis hyperinfection in an unconscious diabetic patient with dermatomyositis. Indian J Pathol Microbiol 2018;61:109-12

How to cite this URL:
Sharifdini M, Hesari A, Mahdavi SA, Alipour A, Kia EB. Strongyloides stercoralis hyperinfection in an unconscious diabetic patient with dermatomyositis. Indian J Pathol Microbiol [serial online] 2018 [cited 2019 Dec 11];61:109-12. Available from: http://www.ijpmonline.org/text.asp?2018/61/1/109/228191





   Introduction Top


Strongyloidiasis is one of the important neglected tropical diseases and caused by the intestinal nematode, Strongyloides stercoralis.[1] The parasite is prevalent in tropical and some temperate countries in the world; however, migration and globalization have changed this distribution.[2] It is estimated that 30–100 million people are infected worldwide.[2] Strongyloidiasis has various clinical presentations, ranging in severity from asymptomatic infections in immunocompetent individuals to gastrointestinal, cutaneous, or pulmonary symptoms with or without fever.[2],[3] Most infected immunocompetent individuals present only with eosinophilia, but the parasite can produce internal autoinfection leading to hyperinfection and life-threatening disseminated strongyloidiasis in immunocompromised patients.[2],[3]

The parasite is usually limited to the gastrointestinal and respiratory tracts in chronic and acute strongyloidiasis; however, it migrates away from the lung and gastrointestinal tract into other organ systems in disseminated infections.[4] This type of infection has a fatality rate of almost 100% if left untreated.[4]

Treatment with corticosteroid and immunosuppressive drugs (in cases of, e.g., multiple myeloma, ulcerative colitis, dermatomyositis, lymphocytic leukemia, kidney and bone marrow transplantation) or having diseases such as diabetes mellitus, human T-cell lymphotropic virus-1, HIV and hypogammaglobulinemia are recognized predisposing conditions for the hyperinfection syndrome and disseminated strongyloidiasis.[2]

We present a case of strongyloidiasis hyperinfection in a patient with diabetes mellitus and dermatomyositis.


   Case Report Top


A 60-year-old woman was admitted to hospital with watery diarrhea and unconsciousness starting 12 h earlier. She was a resident of Mazandaran Province in Northern Iran, a region endemic of S. stercoralis. On admission to the emergency room, the patient was unconscious, febrile, hypotensive, and tachycardic. Neurological examination was unremarkable. On physical examination, her abdomen was soft and generally tender with no sign of hepatosplenomegaly. Chest X-ray and electrocardiography were normal. She had been diagnosed with dermatomyositis and had received chronic immunosuppressive therapy, including methotrexate and prednisolone, for the past 10 years. The patient also had a steroid-induced diabetes mellitus for 5 years ago and was receiving treatment with glibenclamide and metformin.

Laboratory findings showed leukocytosis (16,700 mm 3) with eosinophilia (18%), an erythrocyte sedimentation rate of 22 mm/h, a C-reactive protein (CRP) value of + 3, uremia (76 mg/dl), and hyponatremia (133 mEq/L) as a result of diarrhea and hyperglycemia (170 mg/dl). Stool consistency was that of watery diarrhea. Stool bacteriological culture was negative for enteric bacterial pathogens, but parasitological examination including evaluation by direct smear and formalin-ether concentration revealed numerous rhabditiform larvae of S. stercoralis [Figure 1].
Figure 1: Rhabditiform larva of Strongyloides stercoralis in the patient stool sample

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Treatment with ivermectin was prescribed as the drug of choice, 12 mg (4 × 3 mg tablets), for 2 days. After treatment, symptoms of diarrhea waned, and following liquid and insulin therapy, the patient recovered from uremia and hyperglycemia, leaving hospital in good general condition. During following up 3 months later, she was found asymptomatic for strongyloidiasis, with no evidence of larva in stool as revealed by formalin-ether concentration and agar plate culture techniques.

For molecular characterization of S. stercoralis, stool sample with rhabditiform larvae was preserved in 70% ethanol at room temperature. Total genomic DNA was extracted from the sample using an in-house method described by Sharifdini et al. and stored at −20°C until use.[5] The mitochondrial cytochrome C oxidase subunit 1 (cox 1) gene was amplified using forward (COX F: 5'-TGG TTT GGG TAC TAG TTG-3') and reverse (COX R: 5'-GAT GAG CTC AAA CTA CAC A-3') primers. PCR amplification was performed by the protocol reported by Sharifdini et al.[5] The PCR product was electrophoresed on a 1.5% agarose gel and visualized after ethidium bromide staining [Figure 2]. DNA sequencing was performed using an ABI 3130xlplatform (Applied Biosystems, Foster City, California, USA). Sequence results were edited and analyzed by the Geneious software (www.geneious.com) and compared with sequences deposited in GenBank by the BLAST algorithm (http://www.ncbi.nlm.nih.gov/). The sequence obtained in the current study was identified as S. stercoralis and deposited in GenBank under the accession number KP663661.
Figure 2: Agarose-gel electrophoresis of polymerase chain reaction products amplified with genomic DNA from stool sample. Lanes 1: Negative control; lane 2: Polymerase chain reaction product of stool sample positive for Strongyloides stercoralis; M = 100-bp DNA marker

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   Discussion Top


The clinical course of strongyloidiasis is dependent on host immune response. S. stercoralis hyperinfection and disseminated disease are known to be associated with immunosuppression, including treatment with corticosteroids.[2]

The present case of S. stercoralis hyperinfection was observed in a resident of mazandaran province, northern Iran, known to be endemic for S. stercoralis with several documented cases of hyperinfection, including fatal cases.[3],[6],[7],[8],[9],[10] The area has a humid, temperate climate, suitable for the transmission of soil-transmitted helminthes.[3],[11] It is considered that differences exist between S. stercoralis strains from tropical and moderate climatic zones.[12] In the present study, the isolate from a temperate area was compared with isolates from other geographical areas of the world using molecular characterization and sequencing of mitochondrial DNA. Molecular analysis revealed high similarity with S. stercoralis sequences from Laos and Cambodia that are available in GenBank.

In the case presented here, the hyperinfection syndrome led to severe watery diarrhea and consequent shock due to dehydration. S. stercoralis infection causes a wide variety of abdominal manifestations such as perforation of the intestinal wall, colitis, malabsorption, nausea, and diarrhea.[3],[13],[14] Remarkably, two case studies reported patients with cholera-like diarrhea resulting in hypokalemia with cardiac and respiratory arrest.[15],[16] In immunocompetent individuals with uncomplicated strongyloidiasis, diarrhea does presumably not occur.[17] Watery or bloody diarrhea is a major manifestation in hyperinfection and disseminated strongyloidiasis.[15],[18] In such conditions, large numbers of filariform larvae, which penetrate the wall of the small and large intestine, lead to mucosal erosion, ulceration, interstitial edema, and hemorrhage. These lesions give rise to various gastrointestinal defects, such as malabsorption, exudation, and perturbed motility. In addition, mucosal discontinuity accelerates bacterial enterocolitis, resulting in severe diarrhea.[17]

Infection with S. stercoralis is typically associated with eosinophilia.[3] In a study in Guilan province in northern Iran, which is adjacent to Mazandaran province, 42% of patients with eosinophilia were found to be infected with S. stercoralis.[6] In a study involving a large series of strongyloidiasis cases, it was found that eosinophilia was the most common reason for suspecting the disease, ranging from 6% to 66%, and being common both in asymptomatic and symptomatic patients, but with significantly lower means in elderly and also symptomatic patients.[3] Hence, eosinophilia alone cannot be used to infer a diagnosis of strongyloidiasis since it is more common in early or acute infections and declines in chronic infection [19] and in complicated cases associated with hyperinfection syndrome [20] and disseminated strongyloidiasis due to suppressive effect of corticosteroids.[2],[21] Hays et al. showed a higher prevalence of eosinophilia in Strongyloides-seropositive diabetics. This might be due to reason that diabetic group have a greater incidence of acute or recent infections, resulting in a higher rate of eosinophilia, while this is at odds with chronic and immunomodulated infections, where eosinophilia is decreased.[22] In the present immunosuppressed case, peripheral blood eosinophilia amounted to 18% which is close to the level of eosinophilia in symptomatic patients as presented in a previous study reporting that the relative mean level of eosinophilia in symptomatic S. stercoralis-infected patients is lower than that of asymptomatic S. stercoralis-infected patients.[3]

Immunosuppressive treatment can lead to the development of hyperinfection syndrome in strongyloidiasis patients. The use of immunosuppressive drugs is associated with transformation of chronic strongyloidiasis to the hyperinfection syndrome and disseminated strongyloidiasis. These drugs induce hyperinfection by acute suppression of eosinophilia and lymphocyte activation. Keiser and Nutmanreported that corticosteroid drugs can directly affect S. stercoralis by accelerating the transformation of rhabditiform larvae into invasive, filariform larvae.[2] On the other hand, parasitic female worms produce more eggs in the presence of exogenous steroids.[23] With respect to the present case, the patient had been receiving immunosuppressive therapy including prednisolone and methotrexate for 10 years. To the best of our knowledge, this is the second report in the world of S. stercoralis hyperinfection in a patient with this type of underlying autoimmune disease. It was detected in time and responded properly to treatment with ivermectine. In the previous first report of associated dermatomyositis and Strongyloides hyperinfection, the patient had been treated on a long-term basis with systemic corticosteroids and methotrexate for dermatomyositis; however, the patient died following fatal disseminated strongyloidiasis and a protracted course of progressive muscle weakness and multiple hospital stays for respiratory distress leading to acute respiratory failure, septic shock, and rapid physical decline.[24]

To prevent complicated strongyloidiasis, early diagnosis of infection using sensitive and specific methods is crucial. Among the various available parasitological methods, agar plate culture is reported to be more effective for detection of S. stercoralis than conventional stool methods [5],[9] Nevertheless, parasitological methods are often insensitive when the parasitic load is low in stool samples. On the other hand, several studies reported that molecular methods offer high sensitivity and specificity for the detection of S. stercoralis in stool samples.[5],[25] However, their utility in rural and remote areas are limited by high cost and expertise. Therefore, in endemic areas before initiating immunosuppressive therapy, application of feasible and effective methods for detection of strongyloidiasis and eosinophil counts are suggested. Regular screening and early treatment of patients at such conditions are necessary to minimize complications of severe strongyloidiasis. Physicians should be aware about the risk factors of this infection, and request diagnostic tests on suspected cases to prevent lethal consequences of the disease.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Financial support and sponsorship

The financial support of this study was partly provided by Deputy of Research, Tehran University of Medical Sciences, Tehran, Iran through grant no 91-01-160-17294.

Conflicts of interest

There are no conflicts of interest.



 
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Sharifdini M, Mirhendi H, Ashrafi K, Hosseini M, Mohebali M, Khodadadi H, et al. Comparison of nested polymerase chain reaction and real-time polymerase chain reaction with parasitological methods for detection of Strongyloides stercoralis in human fecal samples. Am J Trop Med Hyg 2015;93:1285-91.  Back to cited text no. 5
    
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Sharifdini, M, Heidari, Z, Hesari, Z, Vatandoost, S, Kia, EB. Molecular Phylogenetics of Trichostrongylus Species (Nematoda: Trichostrongylidae) from Humans of Mazandaran Province, Iran. Korean J Parasitol 2017;55:279-85.  Back to cited text no. 11
    
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Romero-Cabello R, Villagroy Gómez J, Hernández González M, Romero Feregrino R. Hyperinfection with strongyloides stercoralis. BMJ Case Rep 2012;2012:1-5.  Back to cited text no. 13
    
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da Silva OA, Amaral CF, da Silveira JC, López M, Pittella JE. Hypokalemic respiratory muscle paralysis following Strongyloides stercoralis hyperinfection: A case report. Am J Trop Med Hyg 1981;30:69-73.  Back to cited text no. 16
    
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Kia EB, Rahimi HR, Mirhendi H, Nilforoushan MR, Talebi A, Zahabiun F, et al. A case of fatal strongyloidiasis in a patient with chronic lymphocytic leukemia and molecular characterization of the isolate. Korean J Parasitol 2008;46:261-3.  Back to cited text no. 20
    
21.
Gotuzzo E, Terashima A, Alvarez H, Tello R, Infante R, Watts DM, et al. Strongyloides stercoralis hyperinfection associated with human T cell lymphotropic virus type-1 infection in Peru. Am J Trop Med Hyg 1999;60:146-9.  Back to cited text no. 21
    
22.
Hays R, Thompson F, Esterman A, McDermott R. Strongyloides stercoralis, eosinophilia, and type 2 diabetes mellitus: The predictive value of eosinophilia in the diagnosis of S. stercoralis infection in an endemic community. Open Forum Infect Dis 2016;3:ofw029.  Back to cited text no. 22
    
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Hunter CJ, Petrosyan M, Asch M. Dissemination of Strongyloides stercoralis in a patient with systemic lupus erythematosus after initiation of albendazole: A case report. J Med Case Rep 2008;2:156.  Back to cited text no. 23
    
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25.
Verweij JJ, Canales M, Polman K, Ziem J, Brienen EA, Polderman AM, et al. Molecular diagnosis of Strongyloides stercoralis in faecal samples using real-time PCR. Trans R Soc Trop Med Hyg 2009;103:342-6.  Back to cited text no. 25
    

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Correspondence Address:
Eshrat Beigom Kia
Department of Medical Parasitology and Mycology, School of Public Health, Tehran University of Medical Sciences, P. O. Box: 14155-6446, Tehran
Iran
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/IJPM.IJPM_734_16

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