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Saudi Journal of Kidney Diseases and Transplantation
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CASE REPORT  
Year : 2015  |  Volume : 26  |  Issue : 1  |  Page : 98-102
Strongyloides stercoralis infection in kidney transplant recipients


Department of Pathology and Laboratory Medicine, Multi-Organ Transplant Center, Department of Internal Medicine, King Fahad Specialist Hospital, Dammam, Saudi Arabia

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Date of Web Publication8-Jan-2015
 

   Abstract 

Strongyloides stercoralis is an uncommon infection in Saudi Arabia. It can establish latency and cause an autoinfection in humans that lasts for years. The infection can get reactivated during immunosuppression and can result in a life-threatening Strongyloides hyperinfection syndrome. We present three cases of renal transplant recipients who developed Strongyloides infection following transplantation. A bronchoalveolar lavage specimen, a duodenal biopsy and/or a stool specimen from these patients revealed evidence of S. stercoralis larvae. The first two patients received kidneys from the same deceased donor, a native of Bangladesh, an area that is highly endemic for S. stercoralis. The data suggest that the first two cases might be donor derived. High-risk donors and recipients should be screened for Strongyloides infection to initiate treatment before transplantation thus reducing morbidity and mortality.

How to cite this article:
Abdalhamid BA, Al Abadi AM, Al Saghier MI, Joudeh AA, Shorman MA, Amr SS. Strongyloides stercoralis infection in kidney transplant recipients. Saudi J Kidney Dis Transpl 2015;26:98-102

How to cite this URL:
Abdalhamid BA, Al Abadi AM, Al Saghier MI, Joudeh AA, Shorman MA, Amr SS. Strongyloides stercoralis infection in kidney transplant recipients. Saudi J Kidney Dis Transpl [serial online] 2015 [cited 2019 Nov 14];26:98-102. Available from: http://www.sjkdt.org/text.asp?2015/26/1/98/148752

   Introduction Top


Infection caused by Strongyloides stercoralis is common in South East Asia but not in Saudi Arabia. [1],[2],[3] S. stercoralis can cause autoinfection, which may result in chronic infections. [4],[5] It can cause severe life-threatening infections known as Strongyloides hyperinfection syndrome (SHS) due to reactivation in immu nocompromised patients, which is associated with a high mortality rate approaching 70%. [4],[6],[7]

Cases of S. stercoralis infections in organ transplant recipients and transmission of S. stercoralis from deceased donors have been documented in the literature. [4],[7],[8] We report a series of case studies of S. stercoralis infections in transplant patients in a tertiary care hospital in Saudi Arabia. In two cases, we believe that the donor graft could be the source of S. stercoralis in our patients. To the best of our knowledge, this is the first reported case suggesting donor-derived S. stercoralis infection in kidney transplant patients.


   Case Reports Top


Case 1

A 59-year-old Saudi male with end-stage renal disease (ESRD) secondary to long-standing diabetes and hypertension underwent deceaseddonor renal transplantation from a Bangladeshi donor. The pre-transplant laboratory evaluation showed negative hepatitis B surface antigen (HBsAg), positive hepatitis B surface antibody (HBsAb), positive hepatitis B core (HBc) IgG and normal eosinophil count in blood and negative ova and parasites on stool examination.

The patient received basiliximab and methylprednisolone for induction; 250 mg of methylprednisolone during surgery followed by a tapering dose of prednisone, reaching 20 mg by the end of the first week. Basiliximab was given in two doses of 20 mg on day-zero and day-four post-transplantation. On the eighth day after the transplantation, he received three extra doses of methylprednisolone for acute cellular rejection (ACR) classified as Grade IIA (ACR Banff IIa). The maintenance immunosuppression included tacrolimus, mycophenolate and prednisone.

One week following the transplantation, the patient complained of frequent vomiting and heartburn, which was relieved by symptomatic treatment and reduction of the dose of mycophenolate. After discharge, the patient suffered several bouts of nausea and vomiting and was treated for these symptoms. The patient was readmitted to the hospital six weeks post-transplantation with intractable vomiting and constipation, which were complicated by aspiration pneumonia and sepsis due to gram-negative organisms (Escherichia coli and Klebsiella pneumoniae). The patient did not improve significantly despite the initiation of piperacillin- tazobactam (tazocin), levofloxacin, pentamidine and ganciclovir. He was intubated for respiratory failure and severe pneumonia. A chest X-ray revealed mid-zonal and basal reticulonodular infiltrates [Figure 1]A. A bronchoscopy was performed and bronchoalveolar lavage revealed parasitic larvae consistent with S. stercoralis [Figure 1]B. He had no significant travel history outside the Kingdom of Saudi Arabia (KSA). Albendazole (400 mg bid) was commenced, given through the nasogastric tube. Ivermectin was not initiated as it was not available in the hospital. The patient did not improve and died a few days later with the diagnosis of SHS complicated by gramnegative septicemia.
Figure 1: Strongyloides stercoralis infections in kidney transplant patients: (A) chest X-ray showing bilateral mid-zonal and basal reticulonodular infiltrates. Strongyloides stercoralis larvae are shown with original magnification ×40 in (B) broncheoalveolar lavage [hematoxylin and eosin (H&E]) stain, (C) duodenum (H&E stain), (D) rectum (H&E stain), (E) stool (wet mount) and (F) stool (trichrome stain).

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Case 2

A 47-year-old Saudi female with ESRD secondary to hypertension received a cadaveric kidney from the same Bangladeshi donor as the first patient on the same day. She was on dialysis for two years prior to the transplant. There was no diabetes mellitus, any chronic infection or recent travel. Her pre-transplant work up revealed no ova or parasite in stool, negative Strongyloides IgG, negative HBsAb and borderline leukocytosis and eosinophilia in the blood. Induction immunosuppression was with thymoglobulin and methylprednisolone. She received three doses of thymoglobulin, with the total dose being 4.5 mg/kg. Because of detectable donor-specific antibodies (DSAs), she received intravenous immunoglobulin G (IVIg) followed by eight sessions of plasma exchange and IVIg starting from the second day post-operation, with the total dose of IVIg administered being 4.5 g/kg. In addition, the patient received a three-day regimen of methylprednisolone 10 days after the transplantation for suspected ACR. As mentioned above, maintenance immunosuppression consisted of tacrolimus, mycophenolate and prednisone. Five months after the transplant, the patient complained of fatigue, persistent vomiting, diarrhea and loss of weight (15 kg). The laboratory results were similar to those of the pretransplant work-up. The patient did not respond to a reduction in the dose of mycophenolate and the adjustment of dose of proton pump inhibitors. The patient underwent an upper gastrointestinal (UGI) endoscopy and a duodenal biopsy, which revealed the presence of S. stercoralis larvae [Figure 1] C). Her symptoms subsided after starting a two-week course of albendazole (400 mg bid).

Case 3

A 38-year-old Saudi male was diagnosed with ESRD of unknown etiology and was started on hemodialysis. His past medical and travel history as well as pre-transplant work up were not significant. He received kidney transplantation from a deceased Bangladeshi donor; induction immunosuppression was with thymoglobulin and methylprednisolone. The maintenance immunosuppressive treatment included tacrolimus, mycophenolate and prednisone. Four months post-transplantation, the patient complained of nausea, vomiting, abdominal bloating and significant weight loss, which did not improve with reduction of the dose of mycophenolate or switching to mycophenolic acid, or later to azathioprine. The UGI endoscopy did not reveal any significant findings. Colonoscopy revealed mucosal inflammation involving the whole colon, extending from the terminal ileum to the rectum with parasitic larvae infiltrates typical of S. stercoralis [Figure 1]D. This was confirmed by the presence of a large number of S. stercoralis larvae on fecal examination [Figure 1]E. These findings were associated with blood eosinophilia and positive Strongyloides IgG by the enzyme-linked immunosorbent assay (ELISA). The patient was started on a regimen of albendazole (400 mg, bid) for three weeks. Repeated colonoscopies, eosinophil counts and stool examinations were normal after treatment. After six months, the patient's routine follow-up revealed eosinophilia in blood and Strongyloides larvae on stool examination. The laboratory findings returned back to normal after initiation of a twoweek regimen of albendazole.


   Discussion Top


To the best of our knowledge, these are the first reported cases suggesting donor-derived S. stercoralis infection in kidney transplant patients in a tertiary care hospital in Saudi Arabia. This report reveals the difficulty in identifying and treating the infection in immunocompromised patients. The cutaneous manifestations, which are typically peri-umbilical petechia seen in disseminated strongyloidiasis, were absent in these patients. [9] To the best of our knowledge, this the first report of SHS in the absence of cutaneous manifestations. Therefore, clinicians should be aware that the absence of cutaneous findings does not rule out SHS.

We believe that the donor graft was possibly the source of Strongyloides in the first two cases because the donor for the paired kidneys had lived in Bangladesh (Southeast Asia), an area in which Strongyloides is endemic. The disease is not common in Saudi Arabia and the patients' travel histories did not reflect any visits to the endemic areas. [3] Unfortunately, no blood samples were available from the deceased donor for performing retrospective serological tests for Strongyloides IgG.

It is recommended to screen high-risk donors and recipients for Strongyloides as it is a life-threatening disease in immunocompromised patients. Screening tests should include stool examination for ova and parasites, serology for Strongyloides IgG and eosinophil count in peripheral blood. The diagnosis of S. stercoralis depends on the detection of larvae in stool specimens. However, a single stool examination detects larvae in only 30% of the cases, and multiple stool specimens should be examined to increase the sensitivity of the test. [10] ELISA is used to detect S. stercoralis antigen, which has a sensitivity of 83-95% and specificity of 95-97%. [10],[11],[12] The ELISA test can detect symptomatic and asymptomatic strongyloidiasis. [3],[12] Eosinophilia is encountered in 70% of immunocompetent patients with Strongyloides, but that percentage is reduced to only 20% in immunocompromised patients. [13] Eosinophilia was not a reliable indicator in the mentioned cases as the first patient had consistent low-to-normal eosinophil count and consistent eosinophilia was encountered in the second case. In the third case, the patient's normal eosinophil count shifted to high levels four months post-transplantation.

The eradication of the infection is the main aim in the management of the S. stercoralis infection. In immunocompetent patients, albendazole, 400 mg orally twice daily for seven days, or ivermectin 200 μg/kg orally twice daily for one to two days, is usually sufficient. [3],[6] In such populations of patients, ivermectin has been shown to be more effective than albendazole. [4],[14] In disseminated disease or hyperinfection syndrome, it is recommended to administer ivermectin for five to seven days. [3],[4] The efficacy of treatment must be documented after two weeks by stool examination or anti-Strongyloides antibody detection. [3] We treated our patients with albendazole because ivermectin was not available in the pharmacy formulary. Microbiologic clearance of Strongyloides larvae occurred within two weeks of albendazole initiation, which is within the normal range (3-21 days). [4] However, monotherapy with albendazole may not be enough, especially in immunocompromised patients. One of our patients had reactivation probably due to impaired immune response, and this patient was treated with albendazole for an additional two weeks. There is a lack of information and studies on the efficacy of combination therapy with ivermectin and albendazole compared with monotherapy. [3] There are no alternative well-documented therapeutic protocols to oral therapy in patients with severe diarrhea or malabsorption. [8] Although a few studies have revealed some success using parenteral ivermectin for such cases, parenteral ivermectin for humans has not been approved by the Food and Drug Authority yet. [8]

These cases spread light on the importance of implementing strategies to prevent Strongyloides in transplant patients. Donors and recipients from endemic areas or with a history of unexplained gastrointestinal complaints, unexplained eosinophilia or other helminthic infections should be screened for Strongyloides infections before transplantation. Diagnostic screening tests include serology in peripheral blood using ELISA to detect S. stercoralis IgG and stool examination for ova and parasites in order to detect Strongyloides larvae. Patients with positive stool or ELISA should be treated before transplantation. It is recommended to have a follow-up protocol to control stool, serology and eosinophil count after Stronglyoidiasis treatment and discharge from the hospital. This study also recommends that ivermectin be made available in the pharmacy formulary.

 
   References Top

1.
Mokaddas EM, Shati S, Abdulla A, et al. Fatal strongyloidiasis in three kidney recipients in Kuwait. Med Princ Pract 2009;18:414-7.  Back to cited text no. 1
    
2.
Basile A, Simzar S, Bentow J, et al. Disseminated Strongyloides stercoralis: Hyperinfection during medical immunosuppression. J Am Acad Dermatol 2010;63:896-902.  Back to cited text no. 2
    
3.
Shorman M, Al-Tawfiq JA. Strongyloides stercoralis hyperinfection presenting as acute respiratory failure and Gram-negative sepsis in a patient with astrocytoma. Int J Infect Dis 2009;13:e288-91.  Back to cited text no. 3
    
4.
Hamilton KW, Abt PL, Rosenbach MA, et al. Donor-derived Strongyloides stercoralis infections in renal transplant recipients. Transplantation 2011;91:1019-24.  Back to cited text no. 4
    
5.
Roxby AC, Gottlieb GS, Limaye AP. Strongyloidiasis in transplant patients. Clin Infect Dis 2009;49:1411-23.  Back to cited text no. 5
    
6.
Rajapurkar M, Hegde U, Rokhade M, Gang S, Gohel K. Respiratory hyperinfection with Strongyloides stercoralis in a patient with renal failure. Nat Clin Pract Nephrol 2007;3:573-7.  Back to cited text no. 6
    
7.
Mizuno S, Iida T, Zendejas I, et al. Strongyloides hyperinfection syndrome following simultaneous heart and kidney transplantation. Transpl Int 2009;22:251-3.  Back to cited text no. 7
[PUBMED]    
8.
Lichtenberger P, Rosa-Cunha I, Morris M, et al. Hyperinfection strongyloidiasis in a liver transplant recipient treated with parenteral ivermectin. Transpl Infect Dis 2009;11:137-42.  Back to cited text no. 8
    
9.
Bank DE, Grossman ME, Kohn SR, Rabinowitz AD. The thumbprint sign: Rapid diagnosis of disseminated strongyloidiasis. J Am Acad Dermatol 1990;23:324-6.  Back to cited text no. 9
    
10.
Siddiqui AA, Berk SL. Diagnosis of Strongyloides stercoralis infection. Clin Infect Dis 2001;33:1040-7.  Back to cited text no. 10
    
11.
Neva FA, Gam AA, Burke J. Comparison of larval antigens in an enzyme-linked immunosorbent assay for strongyloidiasis in humans. J Infect Dis 1981;144:427-32.  Back to cited text no. 11
[PUBMED]    
12.
Carroll SM, Karthigasu KT, Grove DI. Serodiagnosis of human strongyloidiasis by an enzyme-linked immunosorbent assay. Trans R Soc Trop Med Hyg 1981;75:706-9.  Back to cited text no. 12
[PUBMED]    
13.
Liu LX, Weller PF. Strongyloidiasis and other intestinal nematode infections. Infect Dis Clin North Am 1993;7:655-82.  Back to cited text no. 13
    
14.
Marti H, Haji HJ, Savioli L, et al. A comparative trial of a single-dose ivermectin versus three days of albendazole for treatment of Strongyloides stercoralis and other soiltransmitted helminth infections in children. Am J Trop Med Hyg 1996;55:477-81.  Back to cited text no. 14
    

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Correspondence Address:
Dr. Baha A Abdalhamid
Department of Pathology and Laboratory Medicine, King Fahad Specialist Hospital, P. O. Box 15215 MBC 35, Dammam 31444
Saudi Arabia
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DOI: 10.4103/1319-2442.148752

PMID: 25579724

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