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Schistosomiasis screening of travelers to Corsica, France.

To the Editor: As members of the French Ministry of Health Working Group on autochthonous urinary schistosomiasis, we read with interest the 2 recently published articles regarding schistosomiasis screening of travelers to Corsica, France (1,2). Surprisingly, the authors of both articles lacked evidence to support the diagnosis of schistosomiasis in most of what they referred to as confirmed cases. The diagnostic standard for confirmation of urinary schistosomiasis is identification of eggs by microscopic examination of urine samples (3-5). If this criterion were applied in both reports, only 1 patient of the 7 allegedly confirmed cases would actually be confirmed.

The low sensitivity of microscopy is well known. Therefore, different serologic tests have been developed, including Western blot (WB). In the study based on travelers from Italy (1), the SCHISTO II WB IgG test (LDBIO Diagnostics, Lyon, France) was used. This test, available since 2015, is based on both Schistosoma haematobium and S. mansoni antigens and has not been evaluated by anyone other than the manufacturer. Moreover, the authors did not report any details regarding the molecular weight and number of specific bands observed on the strip.

In the study by authors from the GeoSentinel Surveillance Network (2), both cases that could have been infected after 2013, since exposure occurred only in 2014, and 4 cases which reported bathing in rivers in Corsica other than the Cavu River had just 1 weakly positive serologic screening test. Hence, irrespective of the criteria for a confirmed case of schistosomiasis described above, it appears difficult to conclude that confirmation could rely on only 1 positive serologic test, even a WB.

Altogether, these 2 studies identified only 1 patient with parasitological evidence of infection that was attributable to the already known 2013 focus in Cavu River. Therefore, these articles do not provide evidence of transmission of schistosomiasis in Corsica after 2013 or outside the Cavu River.

Antoine Berry, Luc Paris, Jerome Boissier, Eric Caumes

Author affiliations: Toulouse University Hospital, Toulouse, France (A. Berry); Public Assistance Hospitals of Paris, Paris, France (L. Paris, E. Caumes); University of Perpignan Via Domitia, Perpignan, France; National Centre of Scientific Research, Perpignan (J. Boissier)

DOI: http://dx.doi.org/10.3201/eid2201.151290

References

(1.) Beltrame A, Zammarchi L, Zuglian G, Gobbi F, Angheben A, Marchese V, et al. Schistosomiasis screening of travelers from Italy with possible exposure in Corsica, France. Emerg Infect Dis. 2015;21:1887-9. http://dx.doi.org/10.3201/eid2110.150869

(2.) Gautret P, Mockenhaupt FP, von Sonnenburg F, Rothe C, Libman M, Van De Winkel K, et al. Local and international implications of schistosomiasis acquired in Corsica, France. Emerg Infect Dis. 2015;21:1865-8. http://dx.doi.org/10.3201/eid2110.150881

(3.) Gryseels B, Strickland GT. Schistosomiasis. In: Magill AJ, Ryan ET, Hill DR, Solomon T, editors. Hunter's tropical medicine and emerging infectious diseases, 9th ed. London: Elsevier Saunders; 2013. p. 868-83.

(4.) Maguire JH. Trematodes. Schistosomes and other flukes. In: Mandell GL, Bennett JE, Dolin JE, editors. Mandell, Douglas, and Bennett's principles and practice of infectious diseases, 7th ed. Philadelphia: Churchill Livingstone Elsevier Philadelphia; 2010. p. 3595-3606.

(5.) World Health Organization. WHO recommended surveillance standards. 2nd ed. WHO/CDS/CSR/ISR/99/2/EN. Geneva: The Organization; 2015. p 107 [cited 2015 July 22]. http://www.who.int/csr/resources/publications/surveillance/WHO_CDS_CSR_ISR_99_2_EN/en

Address for correspondence: Antoine Berry, Service de Parasitologie-Mycologie, IFB, Hopital Purpan, Centre Hospitalier Universitaire de Toulouse, TSA 40031-31059 Toulouse, CEDEX 9, France; email: berry.a@chu-toulouse.fr

In Response:

Anna Beltrame, Lorenzo Zammarchi, Gianluca Zuglian, Federico Gobbi, Andrea Angheben, Valentina Marchese, Monica Degani, Antonia Mantella, Leila Bianchi, Carlotta Montagnani, Luisa Galli, Matteo Bassetti, Alessandro Bartoloni, Zeno Bisoffi

Author affiliations: Sacro Cuore Hospital, Negrar, Italy (A. Beltrame, F. Gobbi, A. Angheben, V. Marchese, M. Degani, Z. Bisoffi); Santa Maria Misericordia University Hospital of Udine, Udine, Italy (G. Zuglian, M. Bassetti); University of Florence School of Medicine, Florence, Italy (L. Zammarchi, A. Mantella, A. Bartoloni); Anna Meyer Children's University Hospital, Florence, Italy (L. Bianchi, C. Montagnani, L. Galli)

DOI: http://dx.doi.org/10.3201/eid2201.151590

In Response: Regarding the comments by Berry et al. (1) on our previously published letter, we acknowledge that, in strict parasitological terms, confirmation of the diagnosis of urogenital schistosomiasis requires the identification of eggs by microscopic examination of urine. Nevertheless, we aimed at an operational case definition, providing criteria for identifying cases most likely to be true infections. We should not forget that microscopy has an unacceptably low sensitivity (2). We should also consider that currently available serologic tools are hampered by both a poor sensitivity and a poor specificity for Schistosoma haematobium (3). Regarding immunoblot, Berry et al. are correct in saying that there is not yet any formally published evidence of its accuracy for S. haematobium and that the high specificity declared, close to 100%, is based on data provided by the manufacturer. A formal study on the accuracy of this test is underway at the Centre for Tropical Diseases of Sacro Cuore Hospital. This assay has been less extensively assessed than that in which purified S. mansoni antigen is used, as described previously, which has shown very high accuracy (4). However, Western blot is already accepted as a diagnostic standard for the identification of other infectious diseases, including parasitic infections such as cysticercosis (for which, indeed, the direct parasitological confirmation is often impossible), and has become the test of choice for the latter (5).

Moreover, the population in our study was composed of persons not exposed to other parasites. Therefore, cross-reactions with other helminths would be extremely unlikely.

In conclusion, although we recognize that, by a strictly semantic definition, the term "confirmed" should be reserved for cases for which there is a parasitological proof, in operational terms, we could not rely on a direct test that has such a poor sensitivity in this particular patient population. Had we done so, we would have found a subestimated, and therefore totally incorrect, picture of the true prevalence, leading to inappropriate conclusions and actions (or lack thereof).

References

(1.) Berry A, Paris L, Boissier J, Caume E. Schistosomiasis screening of travelers to Corsica, France. Emerg Infect Dis. 2015; 22;159.

(2.) Bierman WF, Wetsteyn JC, van Gool T. Presentation and diagnosis of imported schistosomiasis: relevance of eosinophilia, microscopy for ova, and serology. J Travel Med. 2005; 12:9-13. http://dx.doi.org/10.2310/7060.2005.00003

(3.) Kinkel HF, Dittrich S, Baumer B, Weitzel T. Evaluation of eight serological tests for diagnosis of imported schistosomiasis. Clin Vaccine Immunol. 2012; 19:948-53. http://dx.doi.org/10.1128/CVI.05680-11

(4.) Sulahian A, Garin YJ, Izri A, Verret C, Delaunay P, van Gool T, et al. Development and evaluation of a Western Blot Kit for diagnosis of schistosomiasis. Clin Diagn Lab Immunol. 2005; 12:548-51. http://dx.doi.org/10.1128/CDLI.12.4548-551.2005

(5.) Del Brutto OH, Rajshekhar V, White AC, Tsang VCW, Nash TE, Takayanagui OM, et al. Proposed diagnostic criteria for neurocysticercosis. Neurology. 2001; 57:177-83. http://dx.doi.org/10.1212/WNL.57.2.177

Address for correspondence: Anna Beltrame, Centre for Tropical Diseases, Sacro Cuore Hospital, Via Sempreboni 5, 37024 Negrar, Italy; email: anna.beltrame@sacrocuore.it

In Response:

Philippe Gautret, Frank P. Mockenhaupt, Frank von Sonnenburg, Camilla Rothe, Michael Libman, Kristina Van De Winkel, Emmanuel Bottieau, Martin P. Grobusch, Davidson H. Hamer, Douglas H. Esposito, Philippe Parola, and Patricia Schlagenhauf, for the GeoSentinel Surveillance Network

Author affiliations: Institut Hospitalo-Universitaire Mediterranee Infection, Marseille, France (P. Gautret, P. Parola); Aix Marseille Universite, Marseille (P. Gautret, P. Parola); Charite-Universitatsmedizin Berlin, Berlin, Germany (F.P. Mockenhaupt); University of Munich, Munich, Germany (F. von Sonnenburg); University Clinic Hamburg-Eppendorf, Hamburg, Germany (C. Rothe); McGill University, Montreal, Quebec, Canada (M. Libman); University Hospital, Ghent, Belgium (K. Van De Winkel); Institute of Tropical Medicine, Antwerp, Belgium (E. Bottieau); University of Amsterdam, Amsterdam, the Netherlands (M.P. Grobusch); Boston University School of Public Health, Boston, Massachusetts, USA (D.H. Hamer); Boston Medical Center, Boston (D.H. Hamer); Centers for Disease Control and Prevention, Atlanta, Georgia, USA (D.H. Esposito); University of Zurich Centre for Travel Medicine, Zurich, Switzerland (P. Schlagenhauf)

DOI: http://dx.doi.org/10.3201/eid2201.151606

In Response: We agree with Berry et al. (1) that the diagnostic standard for confirmation of urinary schistosomiasis is the identification of eggs by microscopic examination of urine, especially in patients living in endemic areas with high schistosome loads. However, this approach may not apply to travelers who have low parasite loads and in whom the diagnosis relies mainly on serologic testing (2,3). Given the very poor sensitivity of egg detection in non-schistosomiasis-endemic settings, most tropical and travel medicine clinics in Europe use conventional microscopy systematically combined with 2 different (commercial or in-house) serologic tests (2). The sensitivity of this approach (i.e., diagnosis of infection if combined ELISA and hemagglutination inhibition assay or an indirect fluorescent antibody test are positive) is >78% for chronic urinary schistosomiasis; specificity is 75%-98% when using various in-house and commercial kits (3). Future availability of promising ultra-sensitive tests (e.g., PCR and antigenic tests) may overcome the limitations associated with conventional microscopy and serologic testing for low-parasite load schistosomiasis.

As stated in our manuscript, we cannot exclude the possibility that our case definition generated false-positives; the potential limitations of our findings have already been discussed (4). Furthermore, we were cautious with our interpretation of the serologic test results and, therefore, claimed only 2 confirmed cases (4), 1 on the basis of egg detection and the other on positive serologic test results by using 2 different methods. We believe, on the basis of our findings (4) and in accordance with the European Centre for Disease Control experts (5), that the possibility of transmission in the Cavu River during the summer of 2014 cannot be excluded. We also want to reiterate the possibility of transmission in other rivers in Corsica, including the Solenzara, Osu, and Tarcu rivers, where Bulinus snails, which can serve as intermediate hosts for Schistosoma haematobium, were found during a malacological survey in 2014 (5).

References

(1.) Berry A, Paris L, Boissier J, Caumes E. Schistosomiasis screening of travelers to Corsica, France. Emerg Infect Dis. 2016; 22:159.

(2.) Clerinx J, Van Gompel A. Schistosomiasis in travelers and migrants. Travel Med Infect Dis. 2011; 9:6-24. http://dx.doi.org/10.1016/j.tmaid.2010.11.002

(3.) Kinkel HF, Dittrich S, Baumer B, Weitzel T. Evaluation of eight serological tests for diagnosis of imported schistosomiasis. Clin Vaccine Immunol. 2012; 19:948-53. http://dx.doi.org/10.1128/CVI.05680-11

(4.) Gautret P, Mockenhaupt FP, von Sonnenburg F, Rothe C, Libman M, Van De Winkel K, et al. Local and international implications of schistosomiasis acquired in Corsica, France. Emerg Infect Dis. 2015; 21:1865-8. http://dx.doi.org/10.3201/eid2110.150881

(5.) European Centre for Disease Prevention and Control. Rapid risk assessment: local transmission of Schistosoma haematobium in Corsica, France. Stockholm: The Centre; 2015 [cited 2015 Jul 30]. http://ecdc.europa.eu/en/publications/Publications/risk-assessment-Schistosoma%20haematobiumCorsica-update_TOR1N6.pdf

Address for correspondence: Philippe Gautret, CHU Nord, Chemin des Bourrely, 13915 Marseille, France; email: philippe.gautret@club-internet.fr
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Title Annotation:LETTERS
Author:Berry, Antoine; Paris, Luc; Boissier, Jerome; Caumes, Eric
Publication:Emerging Infectious Diseases
Article Type:Letter to the editor
Geographic Code:4EUFR
Date:Jan 1, 2016
Words:1867
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