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1.  Strongyloides stercoralis in the Immunocompromised Population 
Clinical Microbiology Reviews  2004;17(1):208-217.
Strongyloides stercoralis is an intestinal nematode of humans that infects tens of millions of people worldwide. S. stercoralis is unique among intestinal nematodes in its ability to complete its life cycle within the host through an asexual autoinfective cycle, allowing the infection to persist in the host indefinitely. Under some conditions associated with immunocompromise, this autoinfective cycle can become amplified into a potentially fatal hyperinfection syndrome, characterized by increased numbers of infective filariform larvae in stool and sputum and clinical manifestations of the increased parasite burden and migration, such as gastrointestinal bleeding and respiratory distress. S. stercoralis hyperinfection is often accompanied by sepsis or meningitis with enteric organisms. Glucocorticoid treatment and human T-lymphotropic virus type 1 infection are the two conditions most specifically associated with triggering hyperinfection, but cases have been reported in association with hematologic malignancy, malnutrition, and AIDS. Anthelmintic agents such as ivermectin have been used successfully in treating the hyperinfection syndrome as well as for primary and secondary prevention of hyperinfection in patients whose exposure history and underlying condition put them at increased risk.
doi:10.1128/CMR.17.1.208-217.2004
PMCID: PMC321465  PMID: 14726461
2.  Strongyloidiasis in Transplant Patients 
Strongyloides stercoralis is an intestinal nematode that can persist in the human host for decades after the initial infection and can progress to fulminant hyperinfection syndrome in immunocompromised hosts. We describe a patient who died of Strongyloides hyperinfection syndrome 2 months after orthotopic heart transplantation and discuss approaches to prevention, diagnosis, and treatment. Current practice guidelines recommend screening for and treatment of Strongyloides infection before transplantation, but physicians in the United States often miss opportunities to identify patients with chronic strongyloidiasis. Screening tests have limitations, and clinical suspicion remains an important component of the evaluation before transplantation. After immunocompromised patients develop hyperinfection syndrome, diagnosis is often delayed and mortality is high, so emphasis must be placed on screening and treatment before transplantation. We review current strategies for prevention, diagnosis, and treatment of chronic intestinal strongyloidiasis in patients who will undergo transplantation and discuss the clinical features and management of Strongyloides hyperinfection syndrome in transplant recipients.
doi:10.1086/630201
PMCID: PMC2913967  PMID: 19807271
3.  Regulatory T Cell Expansion in HTLV-1 and Strongyloidiasis Co-infection Is Associated with Reduced IL-5 Responses to Strongyloides stercoralis Antigen 
Background
Human strongyloidiasis varies from a chronic but limited infection in normal hosts to hyperinfection in patients treated with corticosteroids or with HTLV-1 co-infection. Regulatory T cells dampen immune responses to infections. How human strongyloidiasis is controlled and how HTLV-1 infection affects this control are not clear. We hypothesize that HTLV-1 leads to dissemination of Strongyloides stercoralis infection by augmenting regulatory T cell numbers, which in turn down regulate the immune response to the parasite.
Objective
To measure peripheral blood T regulatory cells and Strongyloides stercoralis larval antigen-specific cytokine responses in strongyloidiasis patients with or without HTLV-1 co-infection.
Methods
Peripheral blood mononuclear cells (PBMCs) were isolated from newly diagnosed strongyloidiasis patients with or without HTLV-1 co-infection. Regulatory T cells were characterized by flow cytometry using intracellular staining for CD4, CD25 and FoxP3. PBMCs were also cultured with and without Strongyloides larval antigens. Supernatants were analyzed for IL-5 production.
Results
Patients with HTLV-1 and Strongyloides co-infection had higher parasite burdens. Eosinophil counts were decreased in the HTLV-1 and Strongyloides co-infected subjects compared to strongyloidiasis-only patients (70.0 vs. 502.5 cells/mm3, p = 0.09, Mann-Whitney test). The proportion of regulatory T cells was increased in HTLV-1 positive subjects co-infected with strongyloidiasis compared to patients with only strongyloidiasis or asymptomatic HTLV-1 carriers (median = 17.9% vs. 4.3% vs. 5.9 p<0.05, One-way ANOVA). Strongyloides antigen-specific IL-5 responses were reduced in strongyloidiasis/HTLV-1 co-infected patients (5.0 vs. 187.5 pg/ml, p = 0.03, Mann-Whitney test). Reduced IL-5 responses and eosinophil counts were inversely correlated to the number of CD4+CD25+FoxP3+ cells.
Conclusions
Regulatory T cell counts are increased in patients with HTLV-1 and Strongyloides stercoralis co-infection and correlate with both low circulating eosinophil counts and reduced antigen-driven IL-5 production. These findings suggest a role for regulatory T cells in susceptibility to Strongyloides hyperinfection.
Author Summary
Human strongyloidiasis varies from a mild, controlled infection to a severe frequently fatal disseminated infection depending on the hosts. Patients infected with the retrovirus HTLV-1 have more frequent and more severe forms of strongyloidiasis. It is not clear how human strongyloidiasis is controlled by the immune system and how HTLV-1 infection affects this control. We hypothesize that HTLV-1 leads to dissemination of Strongyloides stercoralis by augmenting regulatory T cell numbers, which in turn down regulate the immune response to the parasite. In our study, patients with HTLV-1 and Strongyloides co-infection had higher parasite burdens than patients with only strongyloidiasis. Eosinophils play an essential role in control of strongyloidiasis in animal models, and eosinophil counts were decreased in the HTLV-1 and Strongyloides stercoralis co-infected subjects compared to patients with only strongyloidiasis. The proportion of T cells with a regulatory cell phenotype was increased in HTLV-1 positive subjects co-infected with strongyloidiasis compared to patients with only strongyloidiasis. IL-5 is a key host molecule in stimulating eosinophil production and activation, and Strongyloides stercoralis antigen-specific IL-5 responses were reduced in strongyloidiasis/HTLV-1 co-infected patients. Reduced IL-5 responses and eosinophil counts were inversely correlated to the number of regulatory T cells. These findings suggest a role for regulatory T cells in susceptibility to Strongyloides hyperinfection.
doi:10.1371/journal.pntd.0000456
PMCID: PMC2686100  PMID: 19513105
4.  Intestinal strongyloidiasis and hyperinfection syndrome 
In spite of recent advances with experiments on animal models, strongyloidiasis, an infection caused by the nematode parasite Strongyloides stercoralis, has still been an elusive disease. Though endemic in some developing countries, strongyloidiasis still poses a threat to the developed world. Due to the peculiar but characteristic features of autoinfection, hyperinfection syndrome involving only pulmonary and gastrointestinal systems, and disseminated infection with involvement of other organs, strongyloidiasis needs special attention by the physician, especially one serving patients in areas endemic for strongyloidiasis. Strongyloidiasis can occur without any symptoms, or as a potentially fatal hyperinfection or disseminated infection. Th2 cell-mediated immunity, humoral immunity and mucosal immunity have been shown to have protective effects against this parasitic infection especially in animal models. Any factors that suppress these mechanisms (such as intercurrent immune suppression or glucocorticoid therapy) could potentially trigger hyperinfection or disseminated infection which could be fatal. Even with the recent advances in laboratory tests, strongyloidiasis is still difficult to diagnose. But once diagnosed, the disease can be treated effectively with antihelminthic drugs like Ivermectin. This review article summarizes a case of strongyloidiasis and various aspects of strongyloidiasis, with emphasis on epidemiology, life cycle of Strongyloides stercoralis, clinical manifestations of the disease, corticosteroids and strongyloidiasis, diagnostic aspects of the disease, various host defense pathways against strongyloidiasis, and available treatment options.
doi:10.1186/1476-7961-4-8
PMCID: PMC1538622  PMID: 16734908
5.  Strongyloides stercoralis: there but not seen 
Purpose of review
Diagnosis of S. stercoralis is often delayed due to patients presenting with non-specific gastrointestinal complaints, a low parasite load and irregular larval output. Although several diagnostic methods exist to detect the presence of S. stercoralis there is no gold standard. In immunocompromised hosts (patients with malignancy, organ transplantation or concurrent HTLV-1 infection or those on corticosteroid therapy), autoinfection can go unchecked where large numbers of invasive Strongyloides larvae disseminate widely and cause hyperinfection with dissemination, which can be fatal. This review will highlight current published research on improved diagnostic methods for S. stercoralis and the immune mechanisms thought to be responsible for hyperinfection syndrome.
Recent findings
Recent advances in diagnosis of Strongyloides stercoralis include a luciferase immunoprecipitation system that shows increased sensitivity and specificity to detect S. stercoralis specific antibodies and a real time quantitative PCR method to detect S. stercoralis in fecal samples. The severe clinical manifestations of S. stercoralis observed in HTLV-1 co-infected patients has been associated to an increased proportion of regulatory T cells that may be responsible for blunting otherwise effective granulocyte responses.
Summary
Strongyloidiasis is a major global health challenge that is underestimated in many countries. Novel diagnostic methods are expected to improve epidemiological studies and control efforts for prevention and treatment of strongyloidiasis. More studies are needed to unveil the mechanisms of severe clinical manifestations of human strongyloidiasis.
doi:10.1097/QCO.0b013e32833df718
PMCID: PMC2948977  PMID: 20733481
Strongyloides stercoralis; strongyloidiasis; diagnosis; hyperinfection; immunology
6.  A Case of Gastric and Duodenal Strongyloidiasis 
Strongyloides stercoralis is a nematode parasite which causes a protracted asymptomatic intestinal infection. It is considered a life threatening condition in immunocompromised patients when hyperinfection is associated with disseminated disease. The diagnosis by routine stool examination is very limited since the larval output in stools is very low. We present the case of a 52 year-old Omani man from Salalah, in the southern region of Oman, with a 15-year history of type 2 diabetes mellitus and recently discovered to have hairy cell leukaemia, who complained of nausea, abdominal pain, loss of appetite and loss of weight. An oesophagogastroduodoscopic biopsy was obtained and histopathologic examination revealed gastrointestinal strongyloidiasis.
PMCID: PMC3074720  PMID: 21509240
Strongyloides stercoralis; intestinal infection; Case report; Oman
7.  Strongyloides stercoralis Transmission by Kidney Transplantation in Two Recipients from a Common Donor 
Strongyloides stercoralis hyperinfection in an immunocompromised host has a high mortality rate but may initially present with non-specific pulmonary and gastrointestinal symptoms. Donor-derived S. stercoralis by kidney transplantation is an uncommon diagnosis and difficult to prove. We report two renal allograft recipients on different immunosuppressive maintenance regimens that developed strongyloidiasis after transplantation from the same donor. Recipient 1 presented with a small bowel obstruction. Larvae were demonstrated on a duodenal biopsy and isolated from gastric, pulmonary, and stool samples. Serologic testing for S. stercoralis was negative at a referral laboratory but positive at the Centers for Disease Control. The patient's hospital course was complicated by a hyperinfection syndrome requiring subcutaneous ivermectin due to malabsorption. Recipient 1 survived but the allograft failed. Recipient 2 had larvae detected in stool samples after complaints of diarrhea and was treated. On retrospective testing for S. stercoralis, pre-transplant serum collected from the donor and Recipient 1 was positive and negative, respectively. Donor-derived strongyloidiasis by renal transplantation is a preventable disease that may be affected by the immunosuppressive maintenance regimen. Subcutaneous ivermectin is an option in the setting of malabsorption. Finally, routine screening for S. stercoralis infection in donors from endemic areas may prevent future complications.
doi:10.1111/ajt.12390
PMCID: PMC3785548  PMID: 23919410
Strongyloides stercoralis; donor-derived infection; hyperinfection syndrome; kidney transplantation
8.  The Transcriptome Analysis of Strongyloides stercoralis L3i Larvae Reveals Targets for Intervention in a Neglected Disease 
Background
Strongyloidiasis is one of the most neglected diseases distributed worldwide with endemic areas in developed countries, where chronic infections are life threatening. Despite its impact, very little is known about the molecular biology of the parasite involved and its interplay with its hosts. Next generation sequencing technologies now provide unique opportunities to rapidly address these questions.
Principal Findings
Here we present the first transcriptome of the third larval stage of S. stercoralis using 454 sequencing coupled with semi-automated bioinformatic analyses. 253,266 raw sequence reads were assembled into 11,250 contiguous sequences, most of which were novel. 8037 putative proteins were characterized based on homology, gene ontology and/or biochemical pathways. Comparison of the transcriptome of S. strongyloides with those of other nematodes, including S. ratti, revealed similarities in transcription of molecules inferred to have key roles in parasite-host interactions. Enzymatic proteins, like kinases and proteases, were abundant. 1213 putative excretory/secretory proteins were compiled using a new pipeline which included non-classical secretory proteins. Potential drug targets were also identified.
Conclusions
Overall, the present dataset should provide a solid foundation for future fundamental genomic, proteomic and metabolomic explorations of S. stercoralis, as well as a basis for applied outcomes, such as the development of novel methods of intervention against this neglected parasite.
Author Summary
Strongyloides stercoralis (Nematoda) is an important parasite of humans, causing Strongyloidiasis, considered as one of the most neglected diseases, affecting more than 100 million people worldwide. Chronic infections in endemic areas can be maintained for decades through the autoinfective cycle with the L3 filariform larvae. In these areas, misdiagnosis, inadequate treatment and the facilitation of hyperinfection syndrome by immunosupression are frequent and contribute to a high mortality rate. Among the affected areas, chronic patients have been described in the Valencian Mediterranean coastal region of Spain. Despite its serious impact, very little is known about this parasite and its relationship with its hosts at the molecular level, and more effective diagnostic tests and treatments are needed. Next generation sequencing technologies now provide unique opportunities to rapidly advance in these areas. In this study, we present the first transcriptome of S. stercoralis L3i using 454 sequencing followed by semi-automated bioinformatic analyses. Our study identifies 8037 putative proteins based on homology, gene ontology, and/or biochemical pathways, including putative excretory/secretory proteins as well as potential drug targets. The present dataset provides a useful resource and adds greatly to our understanding of a human parasite affecting both developed and developing countries.
doi:10.1371/journal.pntd.0001513
PMCID: PMC3289599  PMID: 22389732
9.  Survival in a case of diffuse alveolar hemorrhage due to Strongyloides stercoralis hyperinfection 
Strongyloides stercoralis is an intestinal nematode endemic to tropical and sub-tropical regions. Although infection is typically asymptomatic or self-limited, immunocompromised individuals can develop a severe form of disease marked by hyperinfection. Pulmonary involvement accompanies hyperinfection in a majority of cases, though manifestations range from asymptomatic infiltrates to diffuse alveolar hemorrhage (DAH) and respiratory failure. When complicated by DAH, the hyperinfection syndrome is usually fatal. We report a case of a 65-year-old Guatemalan woman with chronic inflammatory demyelinating polyneuropathy (CIDP) treated with chronic steroids who presented with Escherichia coli urosepsis. She was initially treated with antibiotics and corticosteroids. She subsequently developed DAH due to disseminated strongyloidiasis. She was treated with oral and subcutaneous ivermectin and had complete recovery.
doi:10.1016/j.rmedc.2011.12.002
PMCID: PMC3920423
Pulmonary Strongyloides stercoralis; Diffuse alveolar hemorrhage; Hyperinfection; BAL, bronchoalveolar lavage; CIDP, chronic inflammatory demyelinating polyneuropathy; DAH, diffuse alveolar hemorrhage; ICU, intensive care unit; WBC, white blood cell
10.  Bacteriophage-Fused Peptides for Serodiagnosis of Human Strongyloidiasis 
Background
Strongyloidiasis, a human intestinal infection caused by the nematode Strongyloides stercoralis, is frequently underdiagnosed and although its high prevalence is still a neglected parasitic disease because conventional diagnostic tests based on parasitological examination (presence of Strongyloides larvae in stool) are not sufficiently sensitive due to the low parasitic load and to the irregular larval output. There is an urgent need to improve diagnostic assays, especially for immunocompromised patients with high parasitic load as consequence of self-infection cycle, which can disseminate throughout the body, resulting in a potentially fatal hyperinfection syndrome often accompanied by sepsis or meningitis.
Methods/Principal Findings
We have performed Phage Display technology to select peptides that mimic S. stercoralis antigens, capable of detecting a humoral response in patients with strongyloidiasis. The peptides reactivity was investigated by Phage-ELISA through different panels of serum samples. We have successfully selected five peptides with significant immunoreactivity to circulating IgG from patients' sera with strongyloidiasis. The phage displayed peptides C9 and C10 presented the highest diagnostic potential (AUC>0.87) with excellent sensitivity (>85%) and good specificity (>77.5%), suggesting that some S. stercoralis antigens trigger systemic immune response.
Conclusions/Significance
These novel antigens are interesting serum biomarkers for routine strongyloidiasis screenings due to the easy production and simple assay using Phage-ELISA. Such markers may also present a promising application for therapeutic monitoring.
Author Summary
Strongyloidiasis is one of the most neglected helminthic infections and can cause disseminated disease in immunocompromised hosts, which can be fatal. Given the unsatisfactory results of current parasitological and serological tests, there is a need for more efficient diagnostic tools. Therefore we have used phage display technology and bioppaning procedure to select sensitive and specific mimotopes ready to be used in immunodiagnostic tests. These mimotopes allows a cheap and fast clear-cut diagnosis of Strongyloides stercoralis infections. The field applicability of the assay using the phage clones obtained is really promising. The main advantage is that phage-based ELISA is the reproducible, simple, rapid and low-cost for production of recombinant antigens, and such tests may be of interest for massive screening in developing countries. Our results indicate that the mimotopes selected and tested here are potential biomarkers for the diagnosis of human strongyloidiasis.
doi:10.1371/journal.pntd.0002792
PMCID: PMC4038474  PMID: 24874206
11.  Development of a Rapid Serological Assay for the Diagnosis of Strongyloidiasis Using a Novel Diffraction-Based Biosensor Technology 
Background
Strongyloidiasis is a persistent human parasitic infection caused by the intestinal nematode, Strongyloides stercoralis. The parasite has a world-wide distribution, particularly in tropical and subtropical regions with poor sanitary conditions. Since individuals with strongyloidiasis are typically asymptomatic, the infection can persist for decades without detection. Problems arise when individuals with unrecognized S. stercoralis infection are immunosuppressed, which can lead to hyper-infection syndrome and disseminated disease with an associated high mortality if untreated. Therefore a rapid, sensitive and easy to use method of diagnosing Strongyloides infection may improve the clinical management of this disease.
Methodology/Principal Findings
An immunological assay for diagnosing strongyloidiasis was developed on a novel diffraction-based optical bionsensor technology. The test employs a 31-kDa recombinant antigen called NIE derived from Strongyloides stercoralis L3-stage larvae. Assay performance was tested using retrospectively collected sera from patients with parasitologically confirmed strongyloidiasis and control sera from healthy individuals or those with other parasitoses including schistosomiasis, trichinosis, echinococcosis or amebiasis who were seronegative using the NIE ELISA assay. If we consider the control group as the true negative group, the assay readily differentiated S. stercoralis-infected patients from controls detecting 96.3% of the positive cases, and with no cross reactivity observed in the control group These results were in excellent agreement (κ = 0.98) with results obtained by an NIE-based enzyme-linked immunosorbent assay (ELISA). A further 44 sera from patients with suspected S. stercoralis infection were analyzed and showed 91% agreement with the NIE ELISA.
Conclusions/Significance
In summary, this test provides high sensitivity detection of serum IgG against the NIE Strongyloides antigen. The assay is easy to perform and provides results in less than 30 minutes, making this platform amenable to rapid near-patient screening with minimal technical expertise.
Author Summary
A rapid and sensitive serodiagnostic assay for strongyloidiasis based on a 31-kDa recombinant antigen from Strongyloides stercoralis (NIE) was developed using a novel diffraction-based optical biosensor technology. Assay performance was tested using retrospectively collected sera from patients with parasitologically confirmed strongyloidiasis (n = 54) and control sera from healthy individuals (n = 7) or those with other parasitoses including schistosomiasis, trichinosis, echinococcosis or amebiasis (n = 40). If we consider the control group as the true negative group, the assay readily differentiated S. stercoralis-infected patients from controls detecting 96.3% of the positive cases, and with no cross reactivity observed in the control group. These results were in excellent agreement (κ = 0.98) with results obtained by an NIE-based enzyme-linked immunosorbent assay (ELISA). A further 44 sera from patients with suspected S. stercoralis infection were analyzed and showed 91% agreement with the NIE ELISA. This test provides high sensitivity detection of serum IgG against the NIE Strongyloides antigen. The assay is easy to perform and provides results in less than 30 minutes, making this platform amenable to rapid near-patient screening with minimal technical expertise.
doi:10.1371/journal.pntd.0003002
PMCID: PMC4125104  PMID: 25102174
12.  Efficacy and Safety of Single and Double Doses of Ivermectin versus 7-Day High Dose Albendazole for Chronic Strongyloidiasis 
Background
Strongyloidiasis, caused by an intestinal helminth Strongyloides stercoralis, is common throughout the tropics. It remains an important health problem due to autoinfection, which may result in hyperinfection and disseminated infection in immunosuppressed patients, especially patients receiving chemotherapy or corticosteroid treatment. Ivermectin and albendazole are effective against strongyloidiasis. However, the efficacy and the most effective dosing regimen are to be determined.
Methods
A prospective, randomized, open study was conducted in which a 7-day course of oral albendazole 800 mg daily was compared with a single dose (200 microgram/kilogram body weight), or double doses, given 2 weeks apart, of ivermectin in Thai patients with chronic strongyloidiasis. Patients were followed-up with 2 weeks after initiation of treatment, then 1 month, 3 months, 6 months, 9 months, and 1 year after treatment. Combination of direct microscopic examination of fecal smear, formol-ether concentration method, and modified Koga agar plate culture were used to detect strongyloides larvae in two consecutive fecal samples in each follow-up visit. The primary endpoint was clearance of strongyloides larvae from feces after treatment and at one year follow-up.
Results
Ninety patients were included in the analysis (30, 31 and 29 patients in albendazole, single dose, and double doses ivermectin group, respectively). All except one patient in this study had at least one concomitant disease. Diabetes mellitus, systemic lupus erythrematosus, nephrotic syndrome, hematologic malignancy, solid tumor and human immunodeficiency virus infection were common concomitant diseases in these patients. The median (range) duration of follow-up were 19 (2–76) weeks in albendazole group, 39 (2–74) weeks in single dose ivermectin group, and 26 (2–74) weeks in double doses ivermectin group. Parasitological cure rate were 63.3%, 96.8% and 93.1% in albendazole, single dose oral ivermectin, and double doses of oral ivermectin respectively (P = 0.006) in modified intention to treat analysis. No serious adverse event associated with treatment was found in any of the groups.
Conclusion/Significance
This study confirms that both a single, and a double dose of oral ivermectin taken two weeks apart, is more effective than a 7-day course of high dose albendazole for patients with chronic infection due to S. stercoralis. Double dose of ivermectin, taken two weeks apart, might be more effective than a single dose in patients with concomitant illness.
Trial Registration
ClinicalTrials.gov NCT00765024
Author Summary
Strongyloidiasis, caused by an intestinal helminth Strongyloides stercoralis, is common throughout the tropics. We conducted a prospective, clinical study to compare the efficacy and safety of a 7-day course of oral albendazole with a single dose of oral ivermectin, or double doses, given 2 weeks apart, of ivermectin in Thai patients who developed this infection. Patients were regularly followed-up after initiation of treatment, until one year after treatment. Ninety patients were studied (30, 31 and 29 patients in albendazole, single dose, and double doses ivermectin group, respectively). The average duration of follow-up were 19 (range 2–76) weeks in albendazole group, 39 ( range 2–74) weeks in single dose ivermectin group, and 26 ( range 2–74) weeks in double doses ivermectin group. Parasitological cure rate were 63.3%, 96.8% and 93.1% in albendazole, single dose oral ivermectin, and double doses of oral ivermectin respectively. No serious adverse event associated with treatment was found in any of the groups. Therefore this study confirms that both a single, and a double dose of oral ivermectin taken two weeks apart, is more effective than a 7-day course of high dose albendazole for patients with chronic infection due to S. stercoralis.
doi:10.1371/journal.pntd.0001044
PMCID: PMC3091835  PMID: 21572981
13.  Strongyloidiasis—An Insight into Its Global Prevalence and Management 
Background
Strongyloides stercoralis, an intestinal parasitic nematode, infects more than 100 million people worldwide. Strongyloides are unique in their ability to exist as a free-living and autoinfective cycle. Strongyloidiasis can occur without any symptoms or as a potentially fatal hyperinfection or disseminated infection. The most common risk factors for these complications are immunosuppression caused by corticosteroids and infection with human T-lymphotropic virus or human immunodeficiency virus. Even though the diagnosis of strongyloidiasis is improved by advanced instrumentation techniques in isolated and complicated cases of hyperinfection or dissemination, efficient guidelines for screening the population in epidemiological surveys are lacking.
Methodology and Results
In this review, we have discussed various conventional methods for the diagnosis and management of this disease, with an emphasis on recently developed molecular and serological methods that could be implemented to establish guidelines for precise diagnosis of infection in patients and screening in epidemiological surveys. A comprehensive analysis of various cases reported worldwide from different endemic and nonendemic foci of the disease for the last 40 years was evaluated in an effort to delineate the global prevalence of this disease. We also updated the current knowledge of the various clinical spectrum of this parasitic disease, with an emphasis on newer molecular diagnostic methods, treatment, and management of cases in immunosuppressed patients.
Conclusion
Strongyloidiasis is considered a neglected tropical disease and is probably an underdiagnosed parasitic disease due to its low parasitic load and uncertain clinical symptoms. Increased infectivity rates in many developed countries and nonendemic regions nearing those in the most prevalent endemic regions of this parasite and the increasing transmission potential to immigrants, travelers, and immunosuppressed populations are indications for initiating an integrated approach towards prompt diagnosis and control of this parasitic disease.
doi:10.1371/journal.pntd.0003018
PMCID: PMC4133206  PMID: 25121962
14.  Strongyloides stercoralis infection in marmosets: replication of complicated and uncomplicated human disease and parasite biology 
Parasites & Vectors  2014;7(1):579.
Background
Strongyloides stercoralis can undergo an alternative autoinfective life cycle in the host, which, in some individuals can lead to a lethal infection. However, due to a number of factors, such as, the majority of those infected are from low-income backgrounds and the limitation in experimental models for studying human S. stercoralis, strongyloidiasis remains neglected. Improved knowledge of animal models that are susceptible to this parasite is needed in order to investigate the immunological mechanisms involved during infection and in particular to further understand the natural history of the autoinfective cycle.
Methods
Callithrix penicillata were inoculated subcutaneously with 100 (n = 2), 300 (n = 4) or 500 (n = 9) third-stage infective larvae (L3i) of S. stercoralis of human origin. Three marmosets received smaller inocula (i.e., one received 100 and two received 300 L3i) to ensure a greater capacity to withstand the infection after immunosuppression, which was triggered by administration of dexamethasone during early patency. Qualitative faecal analyses began at 7 days post-infection (DPI), and semi-quantitative tests were also performed for the dexamethasone-treated primates and the three matched controls. During the necropsies, specimens of S. stercoralis were recovered and tissue fragments were processed for histopathology.
Results
The mean prepatency and patency periods were 16.1 ± 3.0 and 161.1 ± 72.2 DPI, respectively. The marmosets typically tolerated the infection well, but immunosuppressed individuals exhibited higher numbers of larvae in the faeces and progressive clinical deterioration with late disseminated infection. In these cases, the number of females recovered was significantly higher than the number of inoculated L3i. Large quantities of larvae were observed migrating through the host tissues, and histopathology revealed pulmonary and intestinal injuries consistent with those observed in human strongyloidiasis.
Conclusions
Both complicated and uncomplicated strongyloidiasis occur in C. penicillata that is described as a susceptible small non-human primate model for S. stercoralis. This host permits the maintenance of a human strain of the parasite in the laboratory and can be useful for experimental investigations of strongyloidiasis. In parallel, we discuss data related to the autoinfective cycle that provides new insights into the biology of S. stercoralis.
doi:10.1186/s13071-014-0579-2
PMCID: PMC4287166  PMID: 25499310
Strongyloides stercoralis; Neotropical primate model; Experimental infection; Glucocorticoid; Hyperinfection; Disseminated infection
15.  A case of Strongyloides hyperinfection associated with tuberculosis 
Strongyloidiasis is a parasitic infection that occurs in tropical regions. Hyperinfection, which is an accelerated autoinfection, is often associated with an immunosuppressive state, such as HTLV-1 infection or steroid use. Immunosuppression can also lead to reactivation of tuberculosis infection. These infections may have interacted as a result of impaired cellular immunity. A 28-year-old Nepali male was referred to our hospital for slight abdominal pain and high fever. An abdominal CT scan showed ascites and intestinal swelling. He was admitted with suspected gastroenteritis. Results of stool microscopy on the third day of hospitalization revealed abundant strongylid larvae. We diagnosed a Strongyloides hyperinfection and prescribed ivermectin. Although the numbers of strongylid organisms in the patient’s stool soon diminished, his temperature remained high. After receiving a second dose of ivermectin on day 17, he was transferred to a nearby hospital for observation, where he was noted to have massive pleural effusion. He returned to our hospital where his pleural effusion was found to be positive for adenosine deaminase (ADA), and he was diagnosed with a tuberculosis infection. Strongyloides hyperinfection can occur in a non-endemic region. It can be associated with tuberculosis infection possibly due to impaired cellular immunity. It is important to consider other possible infections when treating a patient with an infection associated with impaired cellular immunity.
doi:10.1186/2052-0492-1-7
PMCID: PMC4336266
Strongyloidiasis; Hyperinfection; Ivermectin; Tuberculosis; Cellular immunity
16.  Pulmonary Strongyloidiasis 
Strongyloides stercoralis is a unique parasite. It can complete its life cycle entirely within the human host. As a result, an autoinfection cycle is set up. As long as there is an intact immune system, the host can control the parasitic burden, and the organism may persist for years after the initial inoculum. Most infected individuals experience mild gastrointestinal or pulmonary symptoms that may fluctuate for years. When cell-mediated immunity becomes impaired (ie, corticosteroid use, malignancy, acquired immunodeficiency syndrome), the parasite burden will grow, disseminate, and cause hyperinfection. Strongyloidiasis is endemic in the tropical and subtropical areas of the world; additionally, it is also endemic in the southeastern United States. Strongyloidiasis is associated with asthma, preexisting lung disease, and immunosuppression, including acquired immunodeficiency syndrome. Eosinophilia is not a prerequisite; therefore, the diagnosis of strongyloidiasis requires a high index of suspicion.
doi:10.1097/01.cpm.0000107609.50629.69
PMCID: PMC2812430  PMID: 20111672
Strongyloides stercoralis; strongyloidiasis; autoinfection; hyperinfection; eosinophilia
17.  Duodenal obstruction - an unusual presentation of Strongyloides stercoralis enteritis: a case report 
Background
Intestinal obstruction is a poorly recognized and probably underreported complication of strongyloidiasis. We present herein an unusual case, of complete duodenal obstruction caused by S. stercoralis.
Methods
A systematic review of the literature examining the clinical course, diagnostic methods, and outcome of this rare complication of strongyloidiasis was performed.
Results
A 42-year-old woman presented with a 5-month history of abdominal pain, vomit, and weight loss. An abdominal CT scan showed an obstruction of the third part of the duodenum. Segmental intestinal resection was carried out and histopathology examination revealed heavy Strongyloides stercoralis infestation. Duodenal obstruction is a rare complication of S. stercoralis infection, with only 8 cases described in the literature since 1970. Most of the patients are males, middle-aged, and the diagnosis was made by duodenal aspirate/biopsy, or analysis of surgical specimen.
Conclusions
Duodenal obstruction is an unusual, but potential fatal, complication of S. stercoralis infection. The large spectrum of clinical manifestation and lack of classic clinical syndrome make the final diagnosis of strongyloidiasis extremely difficult. A high index of suspicion, mainly in patients from endemic areas, is needed for correct and early diagnosis of this uncommon presentation of Strogyloides stercoralis enteritis.
doi:10.1186/1749-7922-5-23
PMCID: PMC2925357  PMID: 20698992
18.  Fatal Strongyloides Hyperinfection Complicating a Gram-Negative Sepsis after Allogeneic Stem Cell Transplantation: A Case Report and Review of the Literature 
Case Reports in Hematology  2013;2013:860976.
Strongyloides stercoralis is an intestinal nematode that causes strongyloidiasis, which affects 30 to 100 million people worldwide. Risk factors for hyperinfection and disseminated disease include immunosuppressive drug therapy, human T-lymphotropic virus-1 (HTLV-1) infection, solid organ and bone marrow transplantation, hematologic malignant diseases, hypogammaglobulinemia, and severe malnutrition and associated conditions. The diagnosis can be difficult because a single stool examination fails to detect larvae in up to 70% of the cases, and the symptoms are nonspecific. Although eosinophilia is a common finding in patients with chronic Strongyloides infection, it is an unreliable predictor of hyperinfection. Furthermore, the lack of eosinophilia while receiving immunosuppressive therapy cannot reliably exclude the underlying chronic Strongyloides infection. We report here a fatal Strongyloides hyperinfection in a patient receiving allogeneic stem cell transplantation; risk factors and outcome in this clinical setting are discussed.
doi:10.1155/2013/860976
PMCID: PMC3722979  PMID: 23936693
19.  Possible Strongyloides stercoralis infection diagnosed by videocapsule endoscopy in an immunocompetent patient with devastating diarrhea 
Annals of Gastroenterology  2012;25(3):268-270.
Strongyloides stercoralis is an endemic parasitic infection of tropical areas, but it is rare in Europe. Most infected immunocompetent patients are asymptomatic, but may present with abdominal pain and diarrhea even several years after acquiring the infection. However, in immunocompromized patients, hyperinfection syndrome has a high mortality rate. Risk factors for the hyperinfection syndrome are corticosteroids and infection with human T lymphotropic virus type 1. Diagnosis of strongyloidiasis is usually made by identifying the larvae in the stool or in duodenal biopsies. There are only four published cases of strongyloidiasis in Greek patients, three of them were immunocompromized. In our patient videocapsule endoscopy identified rhabditiform larvae suggestive of strongyloidiasis. This case report illustrates the difficulty in establishing a diagnosis of the disease in immunocompetent patients.
PMCID: PMC3959373  PMID: 24713813
Strongyloides stercoralis; small bowel videocapsule endoscopy; strongyloidiasis; helminthic infections; diarrhea; human T lymphotropic virus type 1
20.  Endoscopic and histopathological study on the duodenum of Strongyloides stercoralis hyperinfection 
AIM: To investigate endoscopic and histopathological findings in the duodenum of patients with Strongyloides stercoralis (S. stercoralis) hyperinfection.
METHODS: Over a period of 23 years (1984-2006), we investigated 25 patients with S. stercoralis hyperinfection who had had an esophagogastroduodenoscopy before undergoing treatment for strongyloidiasis. The clinical and endoscopic findings were analyzed retrospectively.
RESULTS: Twenty-four (96%) of the patients investigated were under immunocompromised condition which was mainly due to a human T lymphotropic virus type 1 (HTLV-1) infection. The abnormal endoscopic findings, mainly edematous mucosa, white villi and erythematous mucosa, were observed in 23 (92%) patients. The degree of duodenitis including villous atrophy/destruction and inflammatory cell infiltration corresponded to the severity of the endoscopic findings. The histopathologic yield for identifying larvae was 71.4% by duodenal biopsy. The endoscopic findings of duodenitis were more severe in patients whose biopsies were positive for larvae than those whose biopsies were negative (Endoscopic severity score: 4.86 ± 2.47 vs 2.71 ± 1.38, P < 0.05).
CONCLUSION: Our study clearly demonstrates that, in addition to stool analysis, endoscopic observation and biopsies are very important. We also emphasize that S. stercoralis and HTLV-1 infections should be ruled out before immunosuppressive therapy is administered in endemic regions.
doi:10.3748/wjg.14.1768
PMCID: PMC2695917  PMID: 18350608
Strongyloides stercoralis; Strongyloidiasis; Hyperinfection; Endoscopy; Histopathology; Duodenum
21.  Syndrome of Inappropriate Antidiuretic Hormone Secretion (SIADH) in Strongyloides stercoralis Hyperinfection 
Strongyloides stercoralis (S. stercoralis) is a soil transmitted intestinal roundworm that has a unique ability to multiply within the human host and reinfect the human carrier by a process of autoinfection. By this property, S. stercoralis can persist as an occult infection for many decades. In situations of immunosuppression or other permissive gastrointestinal conditions, there occurs a massive increase in parasite multiplication. The parasites penetrate through the intestinal mucosa and are carried in circulation and can cause multisystem involvement. We report a case of a 76-year-old Columbian male who presented with intractable vomiting and hyponatremia who was then diagnosed to have syndrome of inappropriate antidiuretic hormone (SIADH). The patient's symptoms improved after treatment with two doses of ivermectin and his serum sodium levels returned to normal. S. stercoralis infection should be suspected in patients from endemic regions who present with gastrointestinal symptoms and unexplained hyponatremia.
doi:10.4103/0974-777X.127945
PMCID: PMC3982351  PMID: 24741227
Disseminated strongyloidiasis; Hyponatremia; Parasite; Strongyloides hyperinfection; Strongyloides stercoralis; Syndrome of inappropriate antidiuretic hormone secretion
22.  Strongyloides stercoralis Infection in the Immunocompromised Host 
Strongyloides stercoralis is an intestinal nematode acquired in the tropics or subtropics. Most often, it causes chronic, asymptomatic infection, but a change in immune status can increase parasite numbers, leading to hyperinfection syndrome, dissemination, and death if unrecognized. Corticosteroid use is most commonly associated with hyperinfection syndrome. Diagnosis of Strongyloides infection is based on serology and serial stool examinations for larvae. The treatment of choice for chronic, asymptomatic infection is oral ivermectin. Alternative pharmacologic agents include albendazole and thiabendazole. For hyperinfection syndrome, ivermectin remains the drug of choice, though therapy duration must be individualized with the end point being complete parasite eradication. Recurrent strongyloidiasis should prompt an evaluation for human T-cell lymphotropic virus type 1 coinfection. No test of cure is currently available, although immunoglobulin G antibody levels have been shown to decline within 6 months of successful treatment.
PMCID: PMC3401551  PMID: 18462583
23.  Hyperinfection of Strongyloides stercoralis in an immunocompetent patient 
Tropical Parasitology  2012;2(2):135-137.
Strongyloides stercoralis is an intestinal nematode causing endemic infection, mostly in immunocompromised individuals, in tropical and subtropical regions. Herewith, we are reporting a rare case of this kind in immunocompetent patient. A 31-year-old male patient presented with chief complaints of chronic diarrhea and loss of weight since last 4 months. He reported passing watery and foul smelling stool. He also had loss of appetite since last 2 months and was diagnosed as diabetic since last 4 months but he was not given any treatment for this and his fasting blood sugar was 110 mg/dl. His HIV status was negative. Stool examination done on three occasions showed plenty of S. stercoralis larvae. Patient responded well to albendazole therapy. Strongyloidiasis is not always associated with compromise in immune status. It should be suspected in immunocompetent individuals with history of long-term diarrhea and weight loss.
doi:10.4103/2229-5070.105182
PMCID: PMC3680875  PMID: 23767024
Strongyloides stercoralis; immunocompetent; hyperinfection
24.  Strongyloides stercoralis hyperinfection in a patient with rheumatoid arthritis and bronchial asthma: a case report 
Objective
Strongyloides stercoralis is a soil-transmitted intestinal nematode that has been estimated to infect at least 60 million people, especially in tropical and subtropical regions. Strongyloides infection has been described in immunosupressed patients with lymphoma, rheumatoid arthritis, diabetes mellitus etc. Our case who has rheumatoid arthritis (RA) and bronchial asthma was treated with low dose steroids and methotrexate.
Methods
A 68 year old woman has bronchial asthma for 55 years and also diagnosed RA 7 years ago. She received immunusupressive agents including methotrexate and steroids. On admission at hospital, she was on deflazacort 5 mg/day and methotrexate 15 mg/week. On her physical examination, she was afebrile, had rhonchi and mild epigastric tenderness. She had joint deformities at metacarpophalengeal joints and phalanges but no active arthritis finding.
Results
Oesophagogastroduodenoscopy was performed and it showed hemorrhagic focus at bulbus. Gastric biopsy obtained and showed evidence of S.Stercoralis infection. Stool and sputum parasitological examinations were also all positive for S.stercoralis larvae. Chest radiography result had no pathologic finding. Albendazole 400 mg/day was started for 23 days. After the ivermectin was retrieved, patient was treated with oral ivermectin 200 μg once a day for 3 days. On her outpatient control at 15th day, stool and sputum samples were all negative for parasites.
Conclusion
S.stercoralis may cause mortal diseases in patients. Immunosupression frequently causes disseminated infections. Many infected patients are completely asymptomatic. Although it is important to detect latent S. stercoralis infections before administering chemotherapy or before the onset of immunosuppression in patients at risk, a specific and sensitive diagnostic test is lacking. In immunosupressed patients, to detect S.stercoralis might help to have the patient survived and constitute the exact therapy.
doi:10.1186/1476-0711-9-27
PMCID: PMC2949791  PMID: 20849666
25.  A Coproantigen Diagnostic Test for Strongyloides Infection 
Accurate diagnosis of infection with the parasite Strongyloides stercoralis is hampered by the low concentration of larvae in stool, rendering parasitological diagnosis insensitive. Even if the more sensitive agar plate culture method is used repeated stool sampling is necessary to achieve satisfactory sensitivity. In this manuscript we describe the development of a coproantigen ELISA for diagnosis of infection. Polyclonal rabbit antiserum was raised against Strongyloides ratti excretory/secretory (E/S) antigen and utilized to develop an antigen capture ELISA. The assay enabled detection of subpatent rodent S. ratti and human S. stercoralis infection. No cross-reactivity was observed with purified E/S from Schistosoma japonicum, the hookworms Ancylostoma caninum, A. ceylanicum, nor with fecal samples collected from rodents harboring Trichuris muris or S. mansoni infection. Strongyloides coproantigens that appear stable when frozen as formalin-extracted fecal supernatants stored at −20°C remained positive up to 270 days of storage, whereas supernatants stored at 4°C tested negative. These results indicate that diagnosis of human strongyloidiasis by detection of coproantigen is an approach worthy of further development.
Author Summary
Strongyloides stercoralis is almost unique among human nematode infections in its ability to replicate within a patient's body, potentially leading to life-long infections if left untreated. Given the potential for severe life threatening Strongyloides infections and the unsatisfactory results of current parasitologic and antibody tests, there is a need for more efficient diagnostic tools. In this study we generated an assay to specifically detect proteins expelled by Strongyloides. Initially this assay for Strongyloides detection was not specific for the parasite; however, after developing a methodology using formaldehyde preservation of feces we specifically detected Strongyloides antigens in rodent and human stool. This methodology was then tested for cross-reactivity with purified proteins from closely related parasites and furthermore for cross-reactivity against faeces collected from animals harbouring single parasitic infections. Using this approach we found no non-specific reactivity with host or to various parasite antigens, suggesting that this assay is truly specific for Strongyloides detection.
doi:10.1371/journal.pntd.0000955
PMCID: PMC3035667  PMID: 21347447

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