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      Diagnostic Accuracy of Five Serologic Tests for Strongyloides stercoralis Infection

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          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          Background

          The diagnosis of Strongyloides stercoralis ( S. stercoralis) infection is hampered by the suboptimal sensitivity of fecal-based tests. Serological methods are believed to be more sensitive, although assessing their accuracy is difficult because of the lack of sensitivity of a fecal-based reference (“gold”) standard.

          Methods

          The sensitivity and specificity of 5 serologic tests for S. stercoralis (in-house IFAT, NIE-ELISA and NIE-LIPS and the commercially available Bordier-ELISA and IVD-ELISA) were assessed on 399 cryopreserved serum samples. Accuracy was measured using fecal results as the primary reference standard, but also using a composite reference standard (based on a combination of tests).

          Results

          According to the latter standard, the most sensitive test was IFAT, with 94.6% sensitivity (91.2–96.9), followed by IVD-ELISA (92.3%, 87.7–96.9). The most specific test was NIE-LIPS, with specificity 99.6% (98.9–100), followed by IVD-ELISA (97.4%, 95.5–99.3). NIE-LIPS did not cross-react with any of the specimens from subjects with other parasitic infections. NIE-LIPS and the two commercial ELISAs approach 100% specificity at a cut off level that maintains ≥70% sensitivity.

          Conclusions

          NIE-LIPS is the most accurate serologic test for the diagnosis of S. stercoralis infection. IFAT and each of the ELISA tests are sufficiently accurate, above a given cut off, for diagnosis, prevalence studies and inclusion in clinical trials.

          Author Summary

          The diagnosis of Strongyloides stercoralis infection is usually made by finding larvae of the parasite in the feces. The larval output is orders of magnitude lower than, say, the egg output of Ancylostoma duodenale, therefore the sensitivity of conventional techniques is poor. Sensitivity is enhanced by specific techniques, but the infection can still be missed. Several serologic methods ( Strongyloides antibody detection in blood) are considered more sensitive, but they have been assessed so far with fecal tests as the gold standard, which is obviously unsatisfactory considering, precisely, their suboptimal sensitivity. Using a bank of sera from patients surely infected, not infected or doubtful, we assessed the accuracy of five different serologic tests also using a composite reference standard, obtained by combining the results of different tests. The recently developed NIE-LIPS resulted virtually 100% specific, with sensitivity >80%. Two commercially available ELISA tests were also highly specific above a given cut-off. Cross reactions with other parasitic infections were rarer than in previous studies. In conclusion, serologic tests are accurate tools, both for diagnostic purposes and for prevalence studies. Whether or not they can also be reliable markers of cure is currently under study.

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          Most cited references 9

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          A Public Health Response against Strongyloides stercoralis: Time to Look at Soil-Transmitted Helminthiasis in Full

          Strongyloides stercoralis infections have a worldwide distribution with a global burden in terms of prevalence and morbidity that is largely ignored. A public health response against soil-transmitted helminth (STH) infections should broaden the strategy to include S. stercoralis and overcome the epidemiological, diagnostic, and therapeutic challenges that this parasite poses in comparison to Ascaris lumbricoides, Trichuris trichiura, and hookworms. The relatively poor sensitivity of single stool evaluations, which is further lowered when quantitative techniques aimed at detecting eggs are used, also complicates morbidity evaluations and adequate drug efficacy measurements, since S. stercoralis is eliminated in stools in a larval stage. Specific stool techniques for the detection of larvae of S. stercoralis, like Baermann's and Koga's agar plate, despite superiority over direct techniques are still suboptimal. New serologies using recombinant antigens and molecular-based techniques offer new hopes in those areas. The use of ivermectin rather than benzimidazoles for its treatment and the need to have curative regimens rather than lowering the parasite burden are also unique for S. stercoralis in comparison to the other STH due to its life cycle, which allows reproduction and amplification of the worm burden within the human host. The potential impact on STH of the benzimidazoles/ivermectin combinations, already used for control/elimination of lymphatic filariasis, should be further evaluated in public health settings. While waiting for more effective single-dose drug regimens and new sensitive diagnostics, the evidence and the tools already available warrant the planning of a common platform for STH and S. stercoralis control.
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            Efficacy of stool examination for detection of Strongyloides infection.

            To determine the efficacy of stool examination for detection of Strongyloides infection, 1,350 stool samples collected in Japan, Brazil, and Thailand were examined by four different methods (direct fecal smear, formalin-ether concentration. Harada-Mori filter paper culture, and agar plate culture). The newly developed agar plate culture method was highly effective; more than 96% of the positive cases were diagnosed by this method. The coprologic examination, however, was not sensitive enough for detecting chronic infections because more than 40% of the positive cases were overlooked even when persons with proven Strongyloides infection were re-examined several months later without intervening treatment. Therefore, it is essential to examine stool samples repeatedly to achieve a correct diagnosis, and even so, it is important to note that a negative result does not necessarily indicate the unequivocal absence of the infection.
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              Patterns of detection of Strongyloides stercoralis in stool specimens: implications for diagnosis and clinical trials.

              Reported efficacies of drugs used to treat Strongyloides stercoralis infection vary widely. Because diagnostic methods are insensitive, therapeutic trials generally require multiple negative posttreatment stool specimens as evidence of drug efficacy. However, only a single positive stool specimen is usually required for study enrollment. To determine the reproducibility of detection of S. stercoralis larvae in the stool, 108 asymptomatic infected men submitted 25 g of fresh stool once a week for eight consecutive weeks for examination by the Baermann technique. During the 8-week study, 239 (27.7%) of 864 stool specimens were positive for S. stercoralis. Rates of detection of larvae in the stool specimens ranged from eight of eight specimens in 3 (2.8%) men to none of eight specimens in 36 (33.3%) men. Of 43 men for whom S. stercoralis was detected in at least two of the first four stool specimens, only 1 (2.3%) man tested negative on all of the next four specimens. In comparison, of 29 men who had detectable larvae in only one of the first four specimens, 22 (75.9%) tested negative on all of the next four samples. Thus, if these 29 men had been enrolled in a therapeutic trial between the first and second sets of four specimens, the efficacy of a drug with no activity against this parasite would have been estimated to be 76%. These data suggest that patterns of S. stercoralis detection vary widely among infected persons and that intermittent larval shedding can lead to inflated estimates of drug efficacy. Before a patient is entered in a clinical trial of drug efficacy, four consecutive stool specimens should be examined for S. stercoralis; only persons with two or more positive specimens should be enrolled.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, USA )
                1935-2727
                1935-2735
                January 2014
                9 January 2014
                13 January 2014
                : 8
                : 1
                Affiliations
                [1 ]Center for Tropical Diseases (CTD), Sacro Cuore Hospital, Negrar, Verona, Italy
                [2 ]Coordinating Resources to Assess and Improve Health Status of Migrants from Latin America (COHEMI) Project Study Group, European Commission, Health Cooperation Work Programme, FP7 (GA-261495)
                [3 ]Department of Public Health, IRCCS - Mario Negri Institute for Pharmacological Research, Milan, Italy
                [4 ]National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Bethesda, Maryland, United States of America
                [5 ]Instituto de Investigaciones en Enfermedades Tropicales - Universidad Nacional de Salta/CONICET, Oran, Argentina
                [6 ]Barcelona Centre for International Health Research (CRESIB, Hospital Clinic-Universitat de Barcelona), Barcelona, Spain
                Texas Tech University Health Sciences Center, United States of America
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: ZB DB AJK MA TBN. Performed the experiments: RM ROC MG SB. Analyzed the data: ZB DB MS AA. Contributed reagents/materials/analysis tools: ZB RM ROC MG SB TBN. Wrote the paper: ZB DB . Performed literature review: JM ARM DB. Critically revised the manuscript: ARM JM TBN MA AA. Read and approved the final version of the manuscript: ZB DB MS RM ROC AJK MA MG SB AA ARM JM TBN. Contributed equally to the manuscript: ZB DB.

                Article
                PNTD-D-13-01124
                10.1371/journal.pntd.0002640
                3890421

                This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

                Page count
                Pages: 8
                Funding
                This work has been partly supported by the EC within the 7th Framework Programme under the COHEMI project - grant agreement no. FP7-GA-261495. We thank Bordier Affinity Products SA for donating the Bordier ELISA kits. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Medicine
                Diagnostic Medicine
                Test Evaluation
                Infectious Diseases
                Neglected Tropical Diseases

                Infectious disease & Microbiology

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