© 2015 Calvo-Cano et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.  The attached file is the published version of the article

A Berry

Agustín Franco

Antonia Calvo-Cano

BB Obeng

BL Webster

D Wichmann

David Rollinson

H Moné

JE Azar

Joaquim Gascon

Josefina Pardos

L Cnops

Lieselotte Cnops

Lisette van Lieshout

M. E. Valls

Malcolm K. Jones

MB Taberner

ML Casella

T Huyse

Tine Huyse

VR Southgate

PLoS Neglected Tropical Diseases

English

PubMed

© 2015 Calvo-Cano et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.  The attached file is the published version of the article.NHM Repositor

Calvo-Cano, A

Cnops, L

Huyse, T

van Lieshout, L

Pardos, J

Valls, ME

Franco, A

Rollinson, D

Gascon, J

Natural History Museum Repository

SYMPOSIUMA Case of Urogenital Human Schistosomiasisfrom a Non-endemic AreaAntonia Calvo-Cano1*, Lieselotte Cnops2, Tine Huyse2,3, Lisette van Lieshout4,Josefina Pardos5, M. E. Valls5, Agustín Franco6, David Rollinson7, Joaquim Gascon11 ISGlobal, Barcelona Center of International Health Research (CRESIB), Hospital Clínic-Universitat deBarcelona, Barcelona, Spain, 2 Department of Clinical Sciences, Institute of Tropical Medicine, Antwerp,Belgium, 3 Department of Biology, Royal Museum for Central Africa, Tervuren, Belgium, 4 Department ofParasitology, Centre of Infectious Diseases, Leiden University Medical Centre, Leiden, The Netherlands,5 Microbiology Department, Hospital Clínic, Barcelona, Spain, 6 Urology Department, Diagnostic Unit,Hospital Clínic, Barcelona, Spain, 7 Department of Life Sciences, Natural History Museum, London, UnitedKingdom* acalvocano@gmail.comIntroductionSchistosomiasis is a parasitic disease reported in 78 countries, with an additional recent out-break in Corsica [1,2]. Generally, Schistosoma haematobium causes urogenital problems,whereas S.mansoni, S. japonicum, S.mekongi, S. guineensis, and S. intercalatum generate intes-tinal symptoms. Occasionally, ectopic tissue tropisms [3] and infections by parasites resultingfrom hybridization occur [4,5]. Geographical distribution and transmission of Schistosomaspecies depend on the presence of suitable intermediate snail hosts to complete the life cycle.Here we report on an unusual case of urogenital schistosomiasis in a Dominican adult male,living in Spain, with no history of visiting a known endemic area.Case PresentationIn September 2013, a 45-year-old man presented at the outpatient clinic with intermittent dys-uria, back pain, and haematuria. He reported a history of discontinuous haematuria sincechildhood and periodic dysuria and painful ejaculation in the last ten years. During this lastdecade, a urologic study was performed and indicated renal colic due to lithiasis. Born in theDominican Republic, he often took baths in the Macasía River until 1984. One of his brothersdied of renal failure, but he was unaware of cases of haematuria in the community. He hadresided in Spain since September 2006. The only visits abroad were to Portugal in 2009 and tohis homeland in 2010 and 2012. He had no history of sexually transmitted diseases, allergies, orchronic treatments. On examination, he had no urethral discharge or palpable inguinal adeno-pathies; abdomen and digital rectal examinations were normal. A urine sample, urethral smear,and blood sample were analyzed. A single dose of azithromycin (1 g, orally) was administeredfor empirical treatment of infectious urethritis without clinical improvement. Haematuria wasconfirmed (4–10 erythrocytes/μL), and tests for HIV, Treponema pallidum,Mycobacteria (uri-nary culture), Chlamydia trachomatis (PCR), and Neisseria gonorrheae (urethral smear) werenegative. Blood count, coagulation, and biochemistry parameters were normal. A serologic test(Bilharziose Fumouze, indirect hemagglutination assays [IHA]) was positive (titer 1/80). Twoout of three urine samples each showed a single viable schistosome egg of 164 and 155 μmlong, respectively, with a terminal spine (Fig 1) typical of the S. haematobium group. Egg detec-tion was negative in feces and semen. An abdominal ultrasound was normal, but cystoscopyPLOS Neglected Tropical Diseases | DOI:10.1371/journal.pntd.0004053 November 5, 2015 1 / 4a11111OPEN ACCESSCitation: Calvo-Cano A, Cnops L, Huyse T, vanLieshout L, Pardos J, Valls ME, et al. (2015) A Caseof Urogenital Human Schistosomiasis from a Non-endemic Area. PLoS Negl Trop Dis 9(11): e0004053.doi:10.1371/journal.pntd.0004053Editor: Malcolm K. Jones, University of Queensland,AUSTRALIAPublished: November 5, 2015Copyright: © 2015 Calvo-Cano et al. This is an openaccess article distributed under the terms of theCreative Commons Attribution License, which permitsunrestricted use, distribution, and reproduction in anymedium, provided the original author and source arecredited.Funding: The authors received no specific fundingfor this work.Competing Interests: The authors have declaredthat no competing interests exist.revealed two exophytic lesions in the fundus of approximately 2 mm, whose biopsy did notshow direct or indirect signs of the presence of Schistosoma eggs. Computed scanner (CT) uro-graphy excluded any other cause of haematuria. There was no evidence of calcification in thebladder. Real-time PCR was performed in two European reference laboratories on DNAextracts of two different urine collections. DNA was extracted with the MagNa Pure LC2.0(Roche) using the Total Nucleic Acid Isolation High Performance Kit (Roche). The urine sam-ples were positive with PCR targeting the S. haematobium complex-specific Dra1 sequence [6]and the Schistosoma genus-specific fragment of the internal transcribed spacer (ITS) [7]. Nosignal was obtained in feces and serum with the Dra1 PCR. The signal in urine was too weak toidentify the causing species with an additional species-specific PCR [8], probably due to lowDNA load. Feces, serum, and urine were negative with the S.mansoni-specific Sm1-7 real-timePCR [9]. Praziquantel was administered at 40 mg/kg/d for two days, with a complete recoveryof urinary symptoms and no evidence of schistosome eggs in urine after 14 months of follow-up.Case DiscussionThis report of urogenital schistosomiasis in an adult without bathing history in knownendemic areas for S. haematobium is intriguing. Syndromic diagnosis is clear: positive serology,microscopic identification of terminal-spined eggs in two urine samples, and confirmation bytwo different PCR tests on two urine samples, together with the clinical picture and response totreatment. Etiological diagnosis is also clear: the causative agent of this case is not S.mansonibecause of (1) the characteristic egg morphologies and (2) the positive PCR reaction for S. hae-matobium complex, and not for S.mansoni. Within the species of the S. haematobium com-plex, only S. haematobium or its hybrids with S. bovis, S. intercalatum, or S. curassoni can eliciturogenital disease [4,10]. The former is described in Africa, the Arabian Peninsula, andrecently in Corsica [1], and hybrids have been reported in Cameroon and Senegal. DespiteFig 1. Morphology of the schistosome egg detected in a urine sample from the case report. Scale bar100 μm.doi:10.1371/journal.pntd.0004053.g001PLOS Neglected Tropical Diseases | DOI:10.1371/journal.pntd.0004053 November 5, 2015 2 / 4performing additional PCR tests, we were not able to confirm the species identification,although egg shape suggested the possibility of an S. bovis–S. haematobium hybrid [5].Chronic symptoms since childhood make the Dominican Republic the most likely locationfor acquiring the infection. The patient was living until 1984 in Las Matas de Farfán, San Juande la Maguana Province. The main economic activities of this village are agriculture and cattlefarming. Although there is no record of S. bovis transmission nor Bulinus introduction in thearea, some environmental factors might have facilitated autochthonous transmission of thisspecies. From 1880, Lebanese migrants entered the Dominican Republic through the Haitianborder, and have been established until today in San Juan de la Maguana. Lebanon was one ofthe countries with known transmission of S. haematobium [11]. In the 1970s and 1980s manydams were built in this province of the Dominican Republic, with irrigation of culture fields.This increase in freshwater habitats may have supported the introduction of a compatible snailhost, giving rise to some limited transmission.However, if schistosomiasis was acquired by the patient 30 years ago, there are severalinconclusive factors: delay on diagnosis, the absence of other cases in the community exceptpossibly his brother, discontinuation of symptoms, and lack of structural lesions associatedwith prolonged egg laying. There are old records of Bulinus in the south of Portugal and Pla-norbarius metidjensis in Spain that can transmit S. bovis [12]. The patient denied swimming inrivers or lakes in Portugal, but reported bathing in freshwater in Ciudad Real province in 2009.We interviewed three accompanying travelers who also bathed, but they have no symptoms.ConclusionIn summary, this is an unusual case report of schistosomiasis, both for its urinary tropism andits geographical origin. It is intriguing that other cases of urogenital schistosomiasis have notbeen recorded in the Dominican Republic nor in Spain. There is a need to establish whetherthere is a low prevalence of infection in associated communities and to screen freshwater habi-tats for compatible snail hosts.Ethics StatementWritten informed consent was given by the patient to publish clinical data.Key Learning Points• Despite many control efforts, schistosomiasis continues to be a threat to public health.Since the distribution of suitable vectors exceeds that of schistosomiasis, there arepotential new transmission foci in many parts of the world.• Clinicians should consider a diagnosis of urogenital schistosomiasis even whenpatients have not travelled to known endemic areas.• Field surveys are needed to assess infection in associated communities and to screenfreshwater habitats for compatible snail vectors.PLOS Neglected Tropical Diseases | DOI:10.1371/journal.pntd.0004053 November 5, 2015 3 / 4References1. Berry A, Moné H, Iriart X, Mouahid G, Aboo O, Boissier J, et al. Schistosomiasis Haematobium, Cor-sica, France. 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A Schistosoma haematobiumspecific real-time PCRfor diagnosis of urogenital schistosomiasis in serum samples of international travelers and migrants.PLoS Negl Trop Dis. 2013; 7(8):e2413. doi: 10.1371/journal.pntd.0002413 PMID: 240097916. Obeng BB, Aryeetey YA, de Dood CJ, Amoah AS, Larbi IA, Deelder AM, et al. Application of a circulat-ing-cathodic-antigen (CCA) strip test and real-time PCR, in comparison with microscopy, for the detec-tion of Schistosoma haematobium in urine samples from Ghana. Ann Trop Med Parasitol. 2008 Oct;102(7):625–33. doi: 10.1179/136485908X337490 PMID: 188176037. Webster BL, Rollinson D, Stothard JR, Huyse T. Rapid diagnostic multiplex PCR (RD-PCR) to discrimi-nate Schistosoma haematobium and S. bovis. J Helminthol. 2010 Mar; 84(1):107–14. doi: 10.1017/S0022149X09990447 PMID: 196463078. Wichmann D, Panning M, Quack T, Kramme S, Burchard G-D, Grevelding C, et al. Diagnosing schisto-somiasis by detection of cell-free parasite DNA in human plasma. PLoS Negl Trop Dis. 2009; 3(4):e422. doi: 10.1371/journal.pntd.0000422 PMID: 193812859. Webster BL, Diaw OT, Seye MM, Webster JP, Rollinson D. Introgressive hybridization of Schistosomahaematobium group species in Senegal: species barrier break down between ruminant and humanschistosomes. PLoS Negl Trop Dis. 2013; 7(4):e2110. doi: 10.1371/journal.pntd.0002110 PMID:2359351310. Azar JE, Zurayk HC. Present status of schistosomiasis in Lebanon. J Méd Liban Leban Med J. 1972;25(3):167–76.11. Taberner MB, Dionisio JLH. Freshwater Molluscs of Huelva Province (SW Spain). Iberus. 2004;22:19–31.12. Moné H, Mouahid G, Morand S. The distribution of Schistosoma bovis Sonsino, 1876 in relation to inter-mediate host mollusc-parasite relationships. Adv Parasitol. 1999; 44:99–138. PMID: 10563396PLOS Neglected Tropical Diseases | DOI:10.1371/journal.pntd.0004053 November 5, 2015 4 / 4

A Case of Urogenital Human Schistosomiasis from a Non-endemic Area Antonia

A Schistosoma haematobiumspecific real-time PCR for diagnosis of urogenital schistosomiasis in serum samples of international travelers and migrants. PLoS Negl Trop Dis.

Application of a circulating-cathodic-antigen (CCA) strip test and real-time PCR, in comparison with microscopy, for the detection of Schistosoma haematobium in urine samples from Ghana. Ann Trop Med Parasitol.

Bidirectional Introgressive Hybridization between a Cattle and Human Schistosome Species.

Diagnosing schistosomiasis by detection of cell-free parasite DNA in human plasma. PLoS Negl Trop Dis.

Freshwater Molluscs of Huelva Province (SW Spain). Iberus.

Introgressive hybridization of Schistosoma haematobium group species in Senegal: species barrier break down between ruminant and human schistosomes. PLoS Negl Trop Dis.

Rapid diagnostic multiplex PCR (RD-PCR) to discriminate Schistosoma haematobium

Schistosomiasis at Loum, Cameroun; Schistosoma haematobium, S. intercalatum and their natural hybrid. Z Für Parasitenkd.

Schistosomiasis Haematobium, Corsica, France. Emerg Infect Dis.

Schistosomiasis mansoni of the bladder simulating bladder cancer: a case report. Rev Soc Bras Med Trop.

The distribution of Schistosoma bovis Sonsino, 1876 in relation to intermediate host mollusc-parasite relationships. Adv Parasitol.

Zurayk HC. Present status of schistosomiasis in Lebanon.

A Case of Urogenital Human Schistosomiasis from a Non-endemic Area

Schistosomiasis is a parasitic disease reported in 78 countries, with an additional recent outbreak in Corsica. Generally, Schistosoma haematobium causes urogenital problems, whereas S. mansoni, S. japonicum, S. mekongi, S. guineensis, and S. intercalatum generate intestinal symptoms. Occasionally, ectopic tissue tropisms and infections by parasites resulting from hybridization occur. Geographical distribution and transmission of Schistosoma species depend on the presence of suitable intermediate snail hosts to complete the life cycle. Here we report on an unusual case of urogenital schistosomiasis in a Dominican adult male, living in Spain, with no history of visiting a known endemic area

A Case of Urogenital Human Schistosomiasis from a Non-endemic Area

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