Literature DB >> 26401824

Schistosomiasis Screening of Travelers from Italy with Possible Exposure in Corsica, France.

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.   

Abstract

Entities:  

Keywords:  Corsica; Europe; France; Schistosoma haematobium; exposure; parasites; schistosomiasis; screening; surveillance; travelers

Mesh:

Year:  2015        PMID: 26401824      PMCID: PMC4593455          DOI: 10.3201/eid2110.150869

Source DB:  PubMed          Journal:  Emerg Infect Dis        ISSN: 1080-6040            Impact factor:   6.883


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To the Editor: Since 2014, many cases of urogenital schistosomiasis acquired in Corsica, France, have been described (–). The infections, which all occurred in persons who had bathed in the Cavu River in 2011 or 2013, represent the first cases of autochthonous Schistosoma haematobium infection acquired in Europe since the last reported case in Portugal in 1965 (). In June 2014, France established a screening program for persons reporting exposure to the Cavu River during 2011–2013. By March 2015, a national surveillance journal had reported 110 autochthonous urogenital schistosomiasis cases in residents of France (). We describe the diagnostic work-up for and clinical management of persons from Italy who reported bathing in the Cavu River at least once during 2011–2014. All of the patients had requested screening after learning of the risk for acquiring schistosomiasis after freshwater exposure in Corsica. Exclusion criteria for the study included residence in or travel to a country where schistosomiasis is endemic. At least 3 months after their last exposure to the Cavu River, each participant had a filtered terminal urine sample and a serum sample tested for schistosomiasis. Different commercial tests were used, depending on local availability: 3 different ELISAs and an indirect immunofluorescent antibody test (IIFAT). All serum samples were tested in parallel in a laboratory in Florence, Italy, by using 2 Western blots (WBs): a Schistosoma WB IgG kit containing antigens from adult S. mansoni worms and a second kit containing S. mansoni and S. haematobium antigens from a crude adult extract (LDBio Diagnostics, Lyon, France). Confirmed urogenital schistosomiasis was defined by confirmation of S. haematobium eggs in urine by microscopy, positive WB result, or both. Probable urogenital schistosomiasis was defined by positive serologic test results. Possible urogenital schistosomiasis was defined by signs or symptoms suggestive of schistosomiasis (i.e., urogenital symptoms), eosinophilia (>0.4 × 109 cells/L of blood), or both (). All participants who met the case definition received 1 oral dose of praziquantel (40 mg/kg). Forty-three persons were consecutively enrolled during January 2014–January 2015; of these, 15 (34%) had confirmed (6 patients), probable (2 patients), or possible (7 patients) urogenital schistosomiasis (Table). Of these 15 patients, 7 (47%) reported repeat visits to Cavu River over a period of at least 2 years. The mean eosinophil count was 295 (range 40–1,540) cells/μL of blood; 6 (40%) patients had eosinophilia. Genitourinary symptoms were reported by 7 (47%) patients, and blood was detected by dipstick in the urine of 1 patient. Schistosoma eggs were not found in any urine samples.
Table

Demographic, epidemiologic, clinical, and laboratory data for 15 patients with urogenital schistosomiasis acquired after bathing in the Cavu River, Corsica, France*

Patient age, y/sexYear exposedPrevious symptomsEosinophils, cells/μL†No. samples tested for ovaELISA‡IFATWB§Infection definition
12/M2012Urgency to urinate2103 NegNeg: T1, T2NDNeg: WB1, WB2Possible
12/M2012None5503 NegNeg: T1, T2NDNeg: WB1, WB2Possible
68/M2012Acute prostatitis1903 NegNeg: T1, T2NDNeg: WB1, WB2Possible
5/M2011, 2012, 2013None5603 NegNeg: T2NDNeg: WB1, WB2Possible
64/M1990–2013Macroscopic hematuria, hematospermia1401 NegPos: T1; Neg: T2NDNeg: WB1, WB2Probable
57/M1997, 1998, 2006–2014NoneND1 NegNeg: T1, T2NDNeg: WB1, WB2Possible
58/F1997, 1998, 2006–2014Macroscopic hematuria1,5401 NegPos: T1; Neg: T2NDNeg: WB1, WB2Probable
37/M2013None3801 NegNDNegNeg: WB1; Pos: WB2Confirmed
54/M2011None1101 NegNDNegNeg: WB1; Pos: WB2Confirmed
60/F2014None1901 NegNDNegNeg: WB1; Pos: WB2Confirmed
58/M2011, 2012, 2013None4001 NegNDNegNeg: WB1; Pos: WB2Confirmed
11/F2011, 2012, 2013Vaginal discharge5003 NegNDNegNeg: WB1; Pos: WB2Confirmed
39/M1980–2013Urolithiasis403 NegNDNegNeg: WB1, WB2Possible
29/M2014Hematospermia1304 NegNDNegNeg: WB1, WB2Possible
10/M2011None4371 NegNDNegNeg: WB1, WB2Possible

*Only 1 patient, the 10-year-old male, had microscopic hematuria. IIFAT, indirect immunofluorescent antibody test; ND, not done; Neg, negative; Pos, positive; WB, Western blot.
†Absolute cell count.
‡T1 indicates the ELISA used in Udine and Brescia, Italy, and T2 indicates the ELISA used in Negrar, Italy.
§WB1 contained Schistosomiasis mansoni soluble antigens; WB2 contained S. haematobium plus S. mansoni soluble antigens.

*Only 1 patient, the 10-year-old male, had microscopic hematuria. IIFAT, indirect immunofluorescent antibody test; ND, not done; Neg, negative; Pos, positive; WB, Western blot.
†Absolute cell count.
‡T1 indicates the ELISA used in Udine and Brescia, Italy, and T2 indicates the ELISA used in Negrar, Italy.
§WB1 contained Schistosomiasis mansoni soluble antigens; WB2 contained S. haematobium plus S. mansoni soluble antigens. Schistosomiasis screening has been suggested for persons with exposure to the Cavu River (); however, clinical history and clinical evaluation alone and eosinophilia, have low sensitivity for the diagnosis of urogenital schistosomiasis (,). Asymptomatic infection has been reported in 25%–36% of persons with travel-associated schistosomiasis, and eosinophilia was present in 50% of the patients (,). In screenings in France, only 27% of schistosomiasis-positive patients reported genitourinary symptoms (). For the diagnosis of urogenital schistosomiasis, serologic testing is more sensitive than detection of eggs in urine, particularly in mild infections (–). Many asymptomatic family members of the index case-patients who acquired infection in Corsica tested positive only by serologic testing (–). However, commercial serologic tests for schistosomiasis have low sensitivity (). Kinkel et al. () showed that sensitivity of an IIFAT and 3 ELISAs for S. haematobium ranged from 21.4% to 71.4%. In the Corsica outbreak, serologic testing may be even less sensitive because of the hybrid nature of the schistosoma (S. haematobium/S. bovis) (). In our study, only 2 patients had positive ELISA results. Combinations of >2 serologic tests can markedly increase testing sensitivity to almost 78.6% (). Sulahian et al. () found that a WB containing S. mansoni antigens had 89.5% sensitivity and 100% specificity for S. mansoni. In our study, no patients with urogenital schistosomiasis tested positive by WB containing S. mansoni antigens, but 6 patients tested positive by WB containing S. haematobium antigens. In mild infections, the absence of schistosoma antibodies cannot exclude a diagnosis of urogenital schistosomiasis (). Therefore, we provided treatment to patients with possible urogenital schistosomiasis; our decision to treat these patients considered the tolerability of praziquantel and the possible severe genitourinary complications of untreated infections (e.g., bladder carcinoma, infertility). Our findings suggest that a sensitive screening strategy for urogenital schistosomiasis consists of a patient’s travel history (exposure in multiple years), clinical history (any new genitourinary complaints after freshwater exposure), eosinophil count, and serologic testing. Because of the failure of commercial ELISA and IIFAT methods, we emphasize that a WB containing S. haematobium antigen should also be used for screening. Of note, a confirmed urogenital schistosomiasis case acquired after a single exposure in 2014 was never reported (–,). The risk for delayed diagnosis of this insidious, neglected disease, which has recently reappeared in Europe, must be reduced. To accomplish this, information regarding the risk for schistosomiasis after freshwater exposure in Corsica must be disseminated to physicians worldwide.
  8 in total

1.  Evaluation of eight serological tests for diagnosis of imported schistosomiasis.

Authors:  Hans-Friedemann Kinkel; Sabine Dittrich; Britta Bäumer; Thomas Weitzel
Journal:  Clin Vaccine Immunol       Date:  2012-03-21

2.  Development and evaluation of a Western blot kit for diagnosis of schistosomiasis.

Authors:  Annie Sulahian; Yves Jean François Garin; Arezki Izri; Caroline Verret; Pascal Delaunay; Tom van Gool; Francis Derouin
Journal:  Clin Diagn Lab Immunol       Date:  2005-04

3.  [Urinary schistosomiasis contracted in a child in Corsica].

Authors:  P-M Patard; C Debuisson; S Mouttalib; A Berry; A Garnier; P Galinier; O Abbo
Journal:  Arch Pediatr       Date:  2015-01-20       Impact factor: 1.180

4.  Schistosoma haematobium infections acquired in Corsica, France, August 2013.

Authors:  M C Holtfreter; H Moné; I Müller-Stöver; G Mouahid; J Richter
Journal:  Euro Surveill       Date:  2014-06-05

5.  An unusual case of hematuria in a French family returning from Corsica.

Authors:  Julie Brunet; Alexander W Pfaff; Yves Hansmann; Guillaume Gregorowicz; Bernard Pesson; Ahmed Abou-Bacar; Ermanno Candolfi
Journal:  Int J Infect Dis       Date:  2014-11-06       Impact factor: 3.623

6.  Schistosomiasis presenting in travellers: a 15 year observational study at the Hospital for Tropical Diseases, London.

Authors:  Cordelia E M Coltart; Anastasia Chew; Neill Storrar; Margaret Armstrong; Natalie Suff; Leila Morris; Peter L Chiodini; Christopher J M Whitty
Journal:  Trans R Soc Trop Med Hyg       Date:  2015-01-08       Impact factor: 2.184

7.  Schistosomiasis in Travelers and Expatriates.

Authors: 
Journal:  J Travel Med       Date:  1996-09-01       Impact factor: 8.490

8.  Schistosomiasis haematobium, Corsica, France.

Authors:  Antoine Berry; Hélène Moné; Xavier Iriart; Gabriel Mouahid; Olivier Aboo; Jérôme Boissier; Judith Fillaux; Sophie Cassaing; Cécile Debuisson; Alexis Valentin; Guillaume Mitta; André Théron; Jean-François Magnaval
Journal:  Emerg Infect Dis       Date:  2014-09       Impact factor: 6.883

  8 in total
  8 in total

1.  The diagnosis and treatment of urogenital schistosomiasis in Italy in a retrospective cohort of immigrants from Sub-Saharan Africa.

Authors:  Marta Tilli; Federico Gobbi; Francesca Rinaldi; Jacopo Testa; Silvio Caligaris; Paola Magro; Dora Buonfrate; Monica Degani; Andrea Minervini; Marco Carini; Agostino Tuccio; Simone Sforza; Maurizio Gulletta; Francesco Castelli; Simone Agostini; Filippo Parretti; Joachim Richter; Piero Olliaro; Zeno Bisoffi; Alessandro Bartoloni; Lorenzo Zammarchi
Journal:  Infection       Date:  2019-01-21       Impact factor: 3.553

2.  Spectrum and burden of neglected tropical diseases observed in an infectious and tropical diseases unit in Florence, Italy (2000-2015).

Authors:  Lorenzo Zammarchi; Iacopo Vellere; Leonardo Stella; Filippo Bartalesi; Marianne Strohmeyer; Alessandro Bartoloni
Journal:  Intern Emerg Med       Date:  2017-01-04       Impact factor: 5.472

3.  Schistosomiasis Screening of Travelers to Corsica, France.

Authors:  Antoine Berry; Luc Paris; Jérôme Boissier; Eric Caumes
Journal:  Emerg Infect Dis       Date:  2016-01       Impact factor: 6.883

4.  Difficulties in Schistosomiasis Assessment, Corsica, France.

Authors:  Hélène Moné; Martha C Holtfreter; Gabriel Mouahid; Joachim Richter
Journal:  Emerg Infect Dis       Date:  2016-04       Impact factor: 6.883

5.  Accuracy of parasitological and immunological tests for the screening of human schistosomiasis in immigrants and refugees from African countries: An approach with Latent Class Analysis.

Authors:  Anna Beltrame; Massimo Guerriero; Andrea Angheben; Federico Gobbi; Ana Requena-Mendez; Lorenzo Zammarchi; Fabio Formenti; Francesca Perandin; Dora Buonfrate; Zeno Bisoffi
Journal:  PLoS Negl Trop Dis       Date:  2017-06-05

Review 6.  Clinical Spectrum of Schistosomiasis: An Update.

Authors:  Cristina Carbonell; Beatriz Rodríguez-Alonso; Amparo López-Bernús; Hugo Almeida; Inmaculada Galindo-Pérez; Virginia Velasco-Tirado; Miguel Marcos; Javier Pardo-Lledías; Moncef Belhassen-García
Journal:  J Clin Med       Date:  2021-11-25       Impact factor: 4.241

7.  Persistence of schistosomal transmission linked to the Cavu river in southern Corsica since 2013.

Authors:  Lauriane Ramalli; Stephen Mulero; Harold Noël; Jean-Dominique Chiappini; Josselin Vincent; Hélène Barré-Cardi; Philippe Malfait; Guillaume Normand; Florian Busato; Vincent Gendrin; Jean-François Allienne; Judith Fillaux; Jérôme Boissier; Antoine Berry
Journal:  Euro Surveill       Date:  2018-01

Review 8.  Schistosomiasis: Still a Cause of Significant Morbidity and Mortality.

Authors:  Mohamud A Verjee
Journal:  Res Rep Trop Med       Date:  2019-12-31
  8 in total

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