Amadou Garba

Amina A. Hamidou

Bonnie L. Webster

David Rollinson

Elsa Léger

Huyse

Joanne P. Webster

King

Moné

Rollinson

Steinmann

Taylor

Tom Pennance

Vercruysse

Webster

Emerging Infectious Diseases

English

PubMed

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Introgressed Animal Schistosomes Schistosoma curassoni and S. bovis Naturally Infecting Humans

Leger, E

Garba, A

Hamidou, A A

Webster, B L

Pennance, T

Rollinson, D

Webster, J P

RVC Research Online

Using MEGA 7.0 software (http://www.megasoftware.net) with the maximum-likelihood algorithm and a boot-strap of 1,000 replicates, we constructed a phylogenetic tree (online Technical Appendix Figure). All 8 sequences clustered within subtype 4d of HEV. The sequences were similar to each other (95.5%–99.8% similarity in nucleotide sequence) and similar to sequences reported for other cattle (83.3%–85.3%; online Technical Appendix Figure). More-over, these sequences shared 96.1%–96.6% similarity with a human HEV strain (GenBank accession no. KC163335) from the Yantai Prefecture in 2012 and 95.7%–97.9% similarity with a swine strain (GenBank accession no. KF176351) isolated in Shandong Province the same year.Our data strongly indicate that HEV infection occurs in yellow cattle and that they could also play a role as a reservoir of HEV. Because these animals serve mainly as a source of food, consumption of undercooked meat from yellow cattle, similar to pork, might also contribute to the transmission of HEV to humans. Additionally, we also de-tected HEV RNA in 8 of 70 sheep (online Technical Ap-pendix Table 2). Eight sequences from yellow cattle had 95.1%–99.8% nt homology with 8 sheep-derived HEV strains, possibly because mixed raising of domestic live-stock is popular in this region. Our finding of high sequence similarity between yellow cattle, sheep, swine, and human populations suggests a complicated interspecies transmis-sion of HEV occurred in this province. Further studies are required to evaluate the contribution of the yellow cattle reservoir to human HEV infection.AcknowledgmentsWe thank our colleagues at the China CDC at the prefectural and county level for sample collection in this study. This study was supported by a grant from Taishan Scholar  Program of Shandong Province (No. ts201511105) and a grant from the Shandong Medical Health Science and Technology Development Program (2015ws0042).References  1. Kamar N, Bendall R, Legrand-Abravanel F, Xia NS, Ijaz S,  Izopet J, et al. Hepatitis E. Lancet. 2012;379:2477–88.  http://dx.doi.org/10.1016/S0140-6736(11)61849-7  2. Pérez-Gracia MT, García M, Suay B, Mateos-Lindemann ML.  Current knowledge on hepatitis E. J Clin Transl Hepatol. 2015;3:117–26. http://dx.doi.org/10.14218/JCTH.2015.00009  3. Xu F, Pan Y, Baloch AR, Tian L, Wang M, Na W, et al. Hepatitis E virus genotype 4 in yak, northwestern China. Emerg Infect Dis. 2014;20:2182–4. http://dx.doi.org/10.3201/eid2012.131599  4. Huang F, Li Y, Yu W, Jing S, Wang J, Long F, et al. Excretion of infectious hepatitis E virus into milk in cows imposes high risks of zoonosis. Hepatology. 2016;64:350–9. http://dx.doi.org/10.1002/hep.28668  5. Hu GD, Ma X. Detection and sequences analysis of bovine  hepatitis E virus RNA in Xinjiang autonomous region [in Chinese]. Bing Du Xue Bao. 2010;26:27–32.  6. Li K, Zhang Y, Mao Y, Cornforth D, Dong P, Wang R, et al.  Effect of very fast chilling and aging time on ultra-structure and meat quality characteristics of Chinese yellow cattle M. longissimus lumborum. Meat Sci. 2012;92:795–804. http://dx.doi.org/10.1016/j.meatsci.2012.07.003  7. Wang YC, Zhang HY, Xia NS, Peng G, Lan HY, Zhuang H, et al. Prevalence, isolation, and partial sequence analysis of hepatitis E virus from domestic animals in China. J Med Virol. 2002;67:516–21. http://dx.doi.org/10.1002/jmv.10131  8. Geng Y, Wang C, Zhao C, Yu X, Harrison TJ, Tian K, et al. Serological prevalence of hepatitis E virus in domestic animals and diversity of genotype 4 hepatitis E virus in China. Vector Borne Zoonotic Dis. 2010;10:765–70. http://dx.doi.org/10.1089/vbz.2009.0168  9. Li F, Meng JH, Dong C, Dai X, Yang YG, Zhou ZX. Design and application of a set of universal PCR primers for genotyping of hepatitis E virus [in Chinese]. Bing Du Xue Bao. 2009;25:9–16.10. Smith DB, Simmonds P, Izopet J, Oliveira-Filho EF, Ulrich RG, Johne R, et al. Proposed reference sequences for hepatitis E virus subtypes. J Gen Virol. 2016;97:537–42. http://dx.doi.org/10.1099/jgv.0.000393Address for correspondence: Aiqiang Xu, Shandong Center for Disease Control and Prevention, 16992, Jingshi Road, Jinan, 250014, China; email: aqxuepi@163.comIntrogressed Animal  Schistosomes Schistosoma curassoni and S. bovis  Naturally Infecting HumansElsa Léger, Amadou Garba, Amina A. Hamidou, Bonnie L. Webster, Tom Pennance,  David Rollinson, Joanne P. WebsterAuthor affiliations: Royal Veterinary College, University of London, London, UK (E. Léger, T. Pennance, J.P. Webster); RISEAL Niger, Niamey, Niger (A. Garba, A.A. Hamidou); Natural History Museum, London (B.L. Webster, D. Rollinson)DOI: http://dx.doi.org/10.3201/eid2212.160644To the Editor: Schistosomiasis, a disease caused by infection with parasitic worms (schistosomes), is a ne-glected tropical disease across many parts of the world. Numbers of infected livestock are unknown, but >250 million persons are infected; the greatest number of cases are in sub-Saharan Africa (1). Schistosome eggs are ex-creted through urine or feces, depending on the species, and hatch into miracidia upon contact with freshwater. Larvae are transmitted to the mammalian host indirectly through a molluscan intermediate host. Goals to eliminate schistosomiasis by 2020 in select countries in Africa have 2212 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 22, No. 12, December 2016LETTERSbeen proposed by the World Health Organization (http://www.who.int/neglected_diseases/NTD_RoadMap_2012_Fullversion.pdf) and a coalition of partners combating ne-glected tropical diseases (2).Selective pressures imposed by natural phenomena and human activities affect the dynamics and distribution of schistosomiasis. For example, ongoing changes in ag-ricultural practices in some regions are creating new water bodies shared by humans and domestic livestock. These anthropogenic changes increase opportunities for mix-ing of and subsequent exposure to different Schistosoma species, especially those that infect humans and livestock. Such mixing could increase the potential for novel zoonotic hybrid parasites to emerge and become established (3,4).Since the 1940s, researchers have suspected that natu-ral hybridization within and between human and animal schistosome species occurs in definitive and intermediate hosts. In western Africa, hybrids, predominantly between S. haematobium (human schistosome) and S. bovis or S. cu-rassoni (livestock schistosomes), have been isolated from children and snails (5,6). Hybrids between these livestock-only Schistosoma species have also been reported in cattle and sheep but not in other hosts (7). As demonstrated in the field and under experimental laboratory conditions, neither S. bovis nor S. curassoni, as single species, can fully de-velop in humans or nonhuman primates (8,9).We report evidence of a child in Niger who was infected by livestock-specific schistosomes through the hybridiza-tion and introgression of S. bovis with S. curassoni. Sam-ples were collected from a 10-year-old girl in Kokourou, Tillaberi region, Niger (14°20′61.50′′N, 0°91′94.0′′E), as part of longitudinal monitoring and evaluation of national disease control interventions in the area. Tillaberi has an ongoing high prevalence and infection intensity of schis-tosomiasis, despite more than a decade of high-coverage mass treatment with praziquantel.Schistosoma eggs were recovered from the child’s urine. Miracidia that hatched from the eggs were stored on a Whatman FTA card (Sigma-Aldrich, St. Louis, MO, USA), providing the opportunity to perform noninvasive molecular characterization on schistosome larvae without any necessi-ty for laboratory passage. Multilocus analyses of mitochon-drial and nuclear DNA regions (6) on all 42 larvae collected from the child identified 2 individual miracidia with a live-stock S. bovis × S. curassoni hybrid profile with no genetic signal from human-specific S. haematobium. Although no species-specific markers exist for determining parental lin-eages, internal transcribed spacer (ITS), a powerful marker for detecting introgression, has been used successfully to detect hybridization events across the Schistosoma genus. A partial mitochondrial cox1 sequence for miracidia was iden-tical to that for S. bovis, and the nuclear ITS and partial 18S rDNA sequences were identified as S. curassoni. One miracidium from the child had a pure S. haema-tobium profile, 13 had S. bovis (cox1) × S. haematobium (ITS) profiles, and 5 had S. bovis (cox1) × S. haematobium × S. curassoni (ITS) profiles, suggesting the potential for repeated interactions and cross-pairings among these 3 spe-cies. No S. curassoni mitochondrial DNA was found in mi-racidia. The molecular data suggest that these hybrids were not first generation, but a result of parental and/or hybrid backcrosses. The data confirm the occurrence of bidirec-tional introgression between Schistosoma species that in-fect livestock and those that infect humans in Niger. Our data also show that hybrid livestock:livestock schistosomes can directly infect humans without combining with a Schis-tosoma species that infects humans. Hybridization of parasites is an emerging public health concern at the interface of infectious disease biology and evolution (3). Our results raise several critical questions regarding the evolution, epidemiology, health effects, and ultimate control of schistosomiasis. Hybrid schistosomes, and, in particular, hybridized livestock:livestock schisto-somes infecting humans, could potentially extend interme-diate and definitive host ranges; confer altered infectivity, virulence, and drug efficacy; or even potentially replace existing single species (3,4). Hybrid vigor has been ob-served experimentally for schistosomes, and similar evi-dence is gathering from experiments with other parasites. Our results strongly indicate that hybrid livestock:livestock schistosomes can infect a human definitive host, even when neither of its single parental livestock species appears com-patible. Such novel livestock schistosome hybrids infecting humans could be predicted to spread to wherever suitable intermediate snail hosts are endemic, as has recently been reported for zoonotic Schistosoma hybrids in Corsica (10).It is imperative to identify and understand the trans-mission dynamics of introgressed Schistosoma species combinations. The detection of multiple introgressed hy-brids with mixed ancestry in a single child suggests that Schistosoma species may be adapting to recent anthropo-genic changes. If novel zoonotic hybrid species are playing a role in maintaining and exacerbating schistosome trans-mission, illness caused by infection, or both, treatments for humans and livestock may have to be adjusted accordingly within a One Health framework (4).AcknowledgmentsWe thank Aidan Emery, Fiona Allan, and Muriel Rabone for  accessing our parasite samples archived within the Schistosome  Collections at the Natural History Museum, London, UK.This research was funded by a combined Biotechnology and  Biological Sciences Research Council, Medical Research  Council, Economic and Social Research Council, Natural  Environment Research Council, Defence Science and Technology Laboratory, and Department for International Development   Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 22, No. 12, December 2016 2213LETTERSZoonoses and Emerging Livestock Systems (ZELS) research grant, no. BB/L018985/1.The data used in this study were collected as part of the monitoring  and evaluation processes of the Schistosomiasis Control Initiative programs taking place in Niger. Sequences were obtained using the DNA sequencing facilities in the Natural History Museum. Ethical approval for this research was granted by the Niger  Ministry of Health Ethical Review Board and by the Imperial  College Research Ethics Committee (ICREC_8_2_2, EC no. 03.36, R&D no. 241 03/SB/003E) in combination with ongoing Schistosomiasis Control Initiative activities. All infected children in the study were provided treatment with 40 mg/kg praziquantel.References  1. Steinmann P, Keiser J, Bos R, Tanner M, Utzinger J. Schistosomiasis  and water resources development: systematic review, meta- analysis, and estimates of people at risk. Lancet Infect Dis. 2006;6:411–25 http://dx.doi.org/10.1016/S1473-3099(06)70521-7  2. Uniting to Combat Neglected Tropical Diseases. London  declaration on neglected tropical diseases [cited 2016 Jan 22]. http://unitingtocombatntds.org/resource/london-declaration  3. King KC, Stelkens RB, Webster JP, Smith DF, Brockhurst MA. Hybridization in parasites: consequences for adaptive evolution, pathogenesis, and public health in a changing world. PLoS Pathog. 2015;11:e1005098 http://dx.doi.org/10.1371/journal.ppat.1005098  4. Webster JP, Gower CM, Knowles SC, Molyneux DH, Fenton A. One Health—an ecological and evolutionary framework for  tackling neglected zoonotic diseases. Evol Appl. 2016;9:313–33   http://dx.doi.org/10.1111/eva.12341  5. Huyse T, Webster BL, Geldof S, Stothard JR, Diaw OT, Polman K, et al. Bidirectional introgressive hybridization between a cattle  and human schistosome species. PLoS Pathog. 2009;5:e1000571 http://dx.doi.org/10.1371/journal.ppat.1000571  6. Webster BL, Diaw OT, Seye MM, Webster JP, Rollinson D.  Introgressive hybridization of Schistosoma haematobium group species in Senegal: species barrier break down between ruminant and human schistosomes. PLoS Negl Trop Dis. 2013;7:e2110.  http://dx.doi.org/10.1371/journal.pntd.0002110  7. Rollinson D, Southgate VR, Vercruysse J, Moore PJ. Observations on natural and experimental interactions between Schistosoma  bovis and S. curassoni from West Africa. Acta Trop. 1990;47: 101–14 http://dx.doi.org/10.1016/0001-706X(90)90072-8  8. Taylor MG, Nelson GS, Smith M, Andrews BJ. Comparison of the infectivity and pathogenicity of six species of African schistosomes and their hybrids. 2. Baboons. J Helminthol. 1973;47:455–85  http://dx.doi.org/10.1017/S0022149X00027462  9. Vercruysse J, Southgate VR, Rollinson D. Schistosoma curassoni  Brumpt, 1931 in sheep and goats in Senegal. Journal of Natural  History. 1984;18:969–76 http://dx.doi.org/10.1080/0022293840077085110. Moné H, Holtfreter MC, Allienne JF, Mintsa-Nguéma R,  Ibikounlé M, Boissier J, et al. Introgressive hybridizations of Schistosoma haematobium by Schistosoma bovis at the origin of the first case report of schistosomiasis in Corsica (France, Europe). Parasitol Res. 2015;114:4127–33 http://dx.doi.org/10.1007/s00436-015-4643-4Address for correspondence: Elsa Léger, Department of Pathology and Pathogen Biology, Centre for Emerging, Endemic and Exotic Diseases, Royal Veterinary College, University of London, London AL9 7TA, UK; email: eleger@rvc.ac.ukRickettsia raoultii in  Dermacentor reticulatus Ticks, Chernobyl Exclusion Zone, Ukraine, 2010Grzegorz Karbowiak, Kateryna Slivinska,  Tomasz Chmielewski, Kamila Barszcz, Stanisława Tylewska-Wierzbanowska,  Joanna Werszko, Tomasz Szewczyk,  Piotr WróblewskiAuthor affiliations: W. Stefański Institute of Parasitology,  Polish Academy of Sciences, Warsaw, Poland (G. Karbowiak,  J. Werszko, T. Szewczyk, P. Wróblewski); I.I. Schmalhausen  Institute of Zoology, National Academy of Sciences of Ukraine, Kiev, Ukraine (K. Slivinska); National Institute of Public Health– National Institute of Hygiene, Warsaw (T. Chmielewski,  K. Barszcz, S. Tylewska-Wierzbanowska)DOI: http://dx.doi.org/10.3201/eid2212.160678To the Editor: The Chernobyl Exclusion Zone (CEZ) surrounds the center of the 1986 Chernobyl nuclear power plant disaster. Preliminary study shows predominance of Der-macentor reticulatus ticks in the CEZ; ticks of other species, such as Ixodes ricinus, are surprisingly rare, even in habitats where they should be relatively common (1). A few reports document presence of Ix. trianguliceps ticks (2,3). Preva-lence of pathogens (Anaplasma phagocytophilum, Borrelia burgdorferi s.l., Babesia spp.) in these ticks is higher in the CEZ than in other regions (3,4). One pathogen transmitted by Dermacentor spp. ticks is Rickettsia raoultii, which has been isolated from species of Dermacentor ticks found in Asia (5,6) and since 1999 has also been detected in Europe. In our study, D. reticulatus ticks were collected by use of the flagging method (1) in the CEZ in September 2010. Ticks were collected from areas where they were known to occur, around the former villages of Korohod (51°16′02′′N; 30°01′04′′E) and Cherevach (51°12′44′′N; 30°07′45′′E) and around Chernobyl city (51°17′04′′N; 30°13′25′′E). The habitats investigated included open areas and the remnants of farmlands. A total of 201 D. reticulatus ticks, 87 males and 114 females, were collected and investigated (Table). DNA was extracted by use of the ammonium hydroxide method (7). Isolated DNA was examined for the presence of the Rickettsia sp. citrate synthase gene (gltA) by use of PCR with RpCS.409d and RpCS.1258n primers (8). Positive am-plicons were sequenced, and sequences were edited by using AutoAssembler software (Applied Biosystems, Foster City, CA, USA) and compared with GenBank entries by using blastn version 2.2.13 (http://www.ncbi.nlm.nih.gov/blast/download.shtml). All obtained sequences were submitted to GenBank (accession nos. KX056493 and KX056494).2214 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 22, No. 12, December 2016LETTERS

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Introgressed Animal Schistosomes <i>Schistosoma curassoni</i> and <i>S. bovis</i> Naturally Infecting Humans

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Introgressed Animal Schistosomes Schistosoma curassoni and S. bovis Naturally Infecting Humans

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