Rat trade and leptospirosis: Molecular epidemiology of Leptospira species in rats exported from Cambodia to Vietnam.
Leptospira
Cambodia
Vietnam
leptospirosis
molecular epidemiology
rat
Journal
Transboundary and emerging diseases
ISSN: 1865-1682
Titre abrégé: Transbound Emerg Dis
Pays: Germany
ID NLM: 101319538
Informations de publication
Date de publication:
May 2022
May 2022
Historique:
revised:
09
03
2021
received:
13
01
2021
accepted:
15
03
2021
pubmed:
19
3
2021
medline:
7
5
2022
entrez:
18
3
2021
Statut:
ppublish
Résumé
Rats are an important maintenance host of Leptospira spp., the causative agents of leptospirosis, a zoonotic disease with worldwide distribution. Rats are traded as food in the Mekong Delta, where Cambodia exports tons of rats to Vietnam. Handling wild rats is a potential health risk, but the information on Leptospira spp. carried by rats traded in the region remains limited. In this study, we investigated the carriage of Leptospira spp. in rats exported from Cambodia to Vietnam using bacterial culture, nested PCR and DNA sequencing. Isolates were then assessed using serological analysis and whole-genome sequencing (WGS), and Leptospira DNA detected in rat kidney tissues was also analysed by multilocus sequence typing (MLST). Seventy-two rats (2 Bandicota indica, 57 Rattus argentiventer, 11 R. losea, 1 R. norvegicus and 1 R. rattus) were subjected to bacterial culture, and three L. borgpetersenii serogroup Javanica isolates were obtained from R. argentiventer (5.3%). WGS revealed that although Cambodian isolates were genetically related to L. borgpetersenii serogroup Javanica strains widely distributed in East and South-East Asian countries, they formed a different cluster from other strains. In addition to the three L. borgpetersenii sequences, the flaB sequence of L. interrogans was detected in 18 R. argentiventer and 7 R. losea kidney tissue samples (38.9%) using nested PCR followed by DNA sequencing. The L. interrogans flaB-positive samples were further analysed by MLST, revealing that seven housekeeping genes (glmU, pntA, sucA, tpiA, pfkB, mreA and caiB) contained novel sequences with distinct lineages from other sequence types. This study revealed a high prevalence of Leptospira spp. among rats exported from Cambodia to Vietnam, indicating a potential risk to people engaging in rat trade and demonstrating that a fastidious L. interrogans strain circulates among Cambodian rats.
Banques de données
GENBANK
['CP026671.1', 'CP026672.1']
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1641-1648Subventions
Organisme : The Japan Agency for Medical Research and Development (AMED)
ID : JP19fk0108049
Organisme : The Japan Agency for Medical Research and Development (AMED)
ID : JP20fk0108139
Organisme : The Japan Society for the Promotion of Science (JSPS)
ID : JPJSBP12099923
Informations de copyright
© 2021 Wiley-VCH GmbH.
Références
Alston, J. M., & Broom, J. C. (1958). Leptospirosis in man and animals. E. & S. Livingstone.
Bankevich, A., Nurk, S., Antipov, D., Gurevich, A. A., Dvorkin, M., Kulikov, A. S., Lesin, V. M., Nikolenko, S. I., Pham, S., Prjibelski, A. D., Pyshkin, A. V., Sirotkin, A. V., Vyahhi, N., Tesler, G., Alekseyev, M. A., & Pevzner, P. A. (2012). SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing. Journal of Computational Biology, 19, 455-477. https://doi.org/10.1089/cmb.2012.0021
Berlioz-Arthaud, A., Guillard, B., Goarant, C., & Hem, S. (2010). Surveillance active de la leptospirose humaine en milieu hospitalier au Cambodge. Bulletin De La Société De Pathologie Exotique, 103, 111-118. https://doi.org/10.1007/s13149-010-0043-2
Bharti, A. R., Nally, J. E., Ricaldi, J. N., Matthias, M. A., Diaz, M. M., Lovett, M. A., Levett, P. N., Gilman, R. H., Willig, M. R., Gotuzzo, E., Vinetz, J. M., & Peru-United States Leptospirosis Consortium (2003). Leptospirosis: A zoonotic disease of global importance. Lancet Infectious Diseases, 12, 757-771. https://doi.org/10.1016/s1473-3099(03)00830-2
Boey, K., Shiokawa, K., & Rajeev, S. (2019). Leptospira infection in rats: A literature review of global prevalence and distribution. PLoS Neglected Tropical Diseases, 13, e0007499. https://doi.org/10.1371/journal.pntd.0007499
Boonsilp, S., Thaipadungpanit, J., Amornchai, P., Wuthiekanun, V., Bailey, M. S., Holden, M. T. G., Zhang, C., Jiang, X., Koizumi, N., Taylor, K., Galloway, R., Hoffmaster, A. R., Craig, S., Smythe, L. D., Hartskeerl, R. A., Day, N. P., Chantratita, N., Feil, E. J., Aanensen, D. M., … Peacock, S. J. (2013). A single multilocus sequence typing (MLST) scheme for seven pathogenic Leptospira species. PLoS Neglected Tropical Diseases, 7, e1954. https://doi.org/10.1371/journal.pntd.0001954
Cerqueira, G. M., & Picardeau, M. (2009). A century of Leptospira strain typing. Infection, Genetics and Evolution, 9, 760-768. https://doi.org/10.1016/j.meegid.2009.06.009
Cosson, J.-F., Picardeau, M., Mielcarek, M., Tatard, C., Chaval, Y., Suputtamongkol, Y., Buchy, P., Jittapalapong, S., Herbreteau, V., & Morand, S. (2014). Epidemiology of Leptospira transmitted by rodents in Southeast Asia. PLoS Neglected Tropical Diseases, 8, e2902. https://doi.org/10.1371/journal.pntd.0002902
Costa, F., Hagan, J. E., Calcagno, J., Kane, M., Torgerson, P., Martinez-Silveira, M. S., Stein, C., Abela-Ridder, B., & Ko, A. I. (2015). Global morbidity and mortality of leptospirosis: A systematic review. PLoS Neglected Tropical Diseases, 9, e0003898. https://doi.org/10.1371/journal.pntd.0003898
Croucher, N. J., Page, A. J., Connor, T. R., Delaney, A. J., Keane, J. A., Bentley, S. D., Parkhill, J., & Harris, S. R. (2015). Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Research, 43, e15. https://doi.org/10.1093/nar/gku1196
Cuong, N. V., Carrique-Mas, J., Be, H. V., An, N. N., Tue, N. T., Anh, N. L., Anh, P. H., Phuc, N. T., Baker, S., Voutilainen, L., Jääskeläinen, A., Huhtamo, E., Utriainen, M., Sironen, T., Vaheri, A., Henttonen, H., Vapalahti, O., Chaval, Y., Morand, S., & Bryant, J. E. (2015). Rodents and risk in the Mekong Delta of Vietnam: Seroprevalence of selected zoonotic viruses in rodents and humans. Vector-Borne and Zoonotic Diseases, 15, 65-72. https://doi.org/10.1089/vbz.2014.1603
Doyle, K. (2014). Cambodian rat meat: A growing export market. Retrieved from https://www.bbc.com/news/world-asia-28863315
Ellis, W. A., Montgomery, J., & Cassells, J. A. (1985). Dihydrostreptomycin treatment of bovine carriers of Leptospira interrogans serovar hardjo. Research in Veterinary Science, 39, 292-295. https://doi.org/10.1016/S0034-5288(18)31716-8
Faine, S., Adler, B., Bolin, C., & Perolat, P. (1999). Leptospira and leptospirosis, (2nd edn). MediSci.
Gruber, K. (2016). Rodent meat - a sustainable way to feed the world? EMBO Reports, 17, 630-633. https://doi.org/10.15252/embr.201642306
Guglielmini, J., Bourhy, P., Schiettekatte, O., Zinini, F., Brisse, S., & Picardeau, M. (2019). Genus-wide Leptospira core genome multilocus sequence typing for strain taxonomy and global surveillance. PLoS Neglected Tropical Diseases, 13, e0007374. https://doi.org/10.1371/journal.pntd.0007374
Hem, S., Ly, S., Votsi, I., Vogt, F., Asgari, N., Buchy, P., Heng, S., Picardeau, M., Sok, T., Ly, S., Huy, R., Guillard, B., Cauchemez, S., & Tarantola, A. (2016). Estimating the burden of leptospirosis among febrile subjects aged below 20 years in Kampong Cham communities, Cambodia, 2007-2009. PLoS One, 11, e0151555. https://doi.org/10.1371/journal.pone.0151555
Hornsby, R. L., Alt, D. A., & Nally, J. E. (2020). Isolation and propagation of leptospires at 37°C directly from the mammalian host. Scientific Reports, 10, 9620. https://doi.org/10.1038/s41598-020-66526-4
Huong, N. Q., Nga, N. T. T., Long, N. V., Luu, B. D., Latinne, A., Pruvot, M., Phuong, N. T., Quang, L. T. V., Hung, V. V., Lan, N. T., Hoa, N. T., Minh, P. Q., Diep, N. T., Tung, N., Ky, V. D., Roberton, S. I., Thuy, H. B., Nguyen Long, N. V., Gilbert, M., … Olson, S. H. (2020). Coronavirus testing indicates transmission risk increases along wildlife supply chains for human consumption in Vietnam, 2013-2014. PLoS One, 15, e0237129. https://doi.org/10.1371/journal.pone.0237129
Ivanova, S., Herbreteau, V., Blasdell, K., Chaval, Y., Buchy, P., Guillard, B., & Morand, S. (2012). Leptospira and rodents in Cambodia: Environmental determinants of infection. American Journal of Tropical Medicine and Hygiene, 86, 1032-1038. https://doi.org/10.4269/ajtmh.2012.11-0349
Kasper, M. R., Blair, P. J., Touch, S., Sokhal, B., Yasuda, C. Y., Williams, M., Richards, A. L., Burgess, T. H., Wierzba, T. F., & Putnam, S. D. (2012). Infectious etiologies of acute febrile illness among patients seeking health care in south-central Cambodia. American Journal of Tropical Medicine and Hygiene, 86, 246-253. https://doi.org/10.4269/ajtmh.2012.11-0409
Khiem, N., Cuong, L., & Chien, H. (2003). Market study of meat from field rats in the Mekong Delta. In G. Singleton, L. Hinds, C. Krebs, & D. Spratt (Eds.), Rats, mice and people: Rodent biology and management (pp. 543-547). Australian Centre for International Agricultural Research.
Koboldt, D. C., Zhang, Q., Larson, D. E., Shen, D., McLellan, M. D., Lin, L., Miller, C. A., Mardis, E. R., Ding, L., & Wilson, R. K. (2012). VarScan 2: Somatic mutation and copy number alteration discovery in cancer by exome sequencing. Genome Research, 22(3), 568-576. https://doi.org/10.1101/gr.129684.111
Koizumi, N., Izumiya, H., Mu, J. J., Arent, Z., Okano, S., Nakajima, C., Suzuki, Y., Mizutani Muto, M., Tanikawa, T., Taylor, K. R., Komatsu, N., Yoshimatsu, K., Ha, H. T. T., & Ohnishi, M. (2015). Multiple-locus variable-number tandem repeat analysis of Leptospira interrogans and Leptospira borgpetersenii isolated from small feral and wild mammals in East Asia. Infection, Genetics and Evolution, 36, 434-440. https://doi.org/10.1016/j.meegid.2015.08.013
Koizumi, N., Miura, K., Sanai, Y., Takemura, T., Trang, U. T. H., Thanh, L. T., Hirayama, K., Hasebe, F., Hang, N. L. K., Phuong, H. V. M., Cam, N. N., Tuan, K. M., Mai, L. T. Q., Ha, H. T. T., & Ohnishi, M. (2019). Molecular epidemiology of Leptospira interrogans in Rattus norvegicus in Hanoi, Vietnam. Acta Tropica, 194, 204-208. https://doi.org/10.1016/j.actatropica.2019.02.008
Koizumi, N., Mizutani Muto, M., Akachi, S., Okano, S., Yamamoto, S., Horikawa, K., Harada, S., Funatsumaru, S., & Ohnishi, M. (2013). Molecular and serological investigation of Leptospira and leptospirosis in dogs in Japan. Journal of Medical Microbiology, 62, 630-636. https://doi.org/10.1099/jmm.0.050039-0
Koizumi, N., Muto, M., Tanikawa, T., Mizutani, H., Sohmura, Y., Hayashi, E., Akao, N., Hoshino, M., Kawabata, H., & Watanabe, H. (2009). Human leptospirosis cases and prevalence of rats harboring Leptospira interrogans in urban areas of Tokyo, Japan. Journal of Medical Microbiology, 58, 1227-1230. https://doi.org/10.1099/jmm.0.011528-0
Koizumi, N., Wada, T., Morita, M., Mu, J.-J., & Ohnishi, M. (2020). Comparative genomic analysis of Leptospira borgpetersenii serogroup Javanica isolated from Rattus species in Southern Japan, Philippines, and Taiwan. Infection, Genetics and Evolution, 85, 104447. https://doi.org/10.1016/j.meegid.2020.104447
Kudo, Y., Vansith, K., Rin, E., Uchida, K., Kodama, S., Fukui, T., Masuda, S., & Masuzawa, T. (2018). Molecular epidemiological survey of Leptospira infection of wild rodents in the urban settlement of Cambodia. Vector-Borne and Zoonotic Diseases, 18, 144-1150. https://doi.org/10.1089/vbz.2017.2198
Kurtz, S., Phillippy, A., Delcher, A. L., Smoot, M., Shumway, M., Antonescu, C., & Salzberg, S. L. (2004). Versatile and open software for comparing large genomes. Genome Biology, 5, 12. https://doi.org/10.1186/gb-2004-5-2-r12
Levett, P. N. (2001). Leptospirosis. Clinical Microbiology Reviews, 14, 296-326. https://doi.org/10.1128/CMR.14.2.296-326.2001
Li, H. (2011). A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics, 27, 2987-2993. https://doi.org/10.1093/bioinformatics/btr509
Li, H., & Durbin, R. (2010). Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics, 26, 589-595. https://doi.org/10.1093/bioinformatics/btp698
Loan, H. K., Van Cuong, N., Takhampunya, R., Kiet, B. T., Campbell, J., Them, L. N., Bryant, J. E., Tippayachai, B., Van Hoang, N., Morand, S., Hien, V. B., & Carrique-Mas, J. J. (2015). How important are rats as vectors of leptospirosis in the Mekong Delta of Vietnam? Vector-Borne and Zoonotic Diseases, 15, 56-64. https://doi.org/10.1089/vbz.2014.1613
Meerburg, B. G., Singleton, G. R., & Kijlstra, A. (2009). Rodent-borne diseases and their risks for public health. Critical Reviews in Microbiology, 35, 221-270. https://doi.org/10.1080/10408410902989837
Mueller, T. C., Siv, S., Khim, N., Kim, S., Fleischmann, E., Ariey, F., Buchy, P., Guillard, B., González, I. J., Christophel, E.-M., Abdur, R., von Sonnenburg, F., Bell, D., & Menard, D. (2014). Acute undifferentiated febrile illness in rural Cambodia: A 3-year prospective observational study. PLoS One, 9, e95868. https://doi.org/10.1371/journal.pone.0095868
Nguyen, L. T., Schmidt, H. A., Von Haeseler, A., & Minh, B. Q. (2015). IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution, 32, 268-274. https://doi.org/10.1093/molbev/msu300
Rourke, K. O., Costenbader, E., & Packer, C. (2014). A market chain analysis of the cross-border rat trade between Vietnam and Cambodia-Draft Report.
Santos, L. A., Adhikarla, H., Yan, X., Wang, Z., Fouts, D. E., Vinetz, J. M., Alcantara, L. C. J., Hartskeerl, R. A., Goris, M. G. A., Picardeau, M., Reis, M. G., Townsend, J. P., Zhao, H., Ko, A. I., & Wunder, E. A. Jr (2018). Genomic comparison among global isolates of L. interrogans serovars Copenhageni and Icterohaemorrhagiae identified natural genetic variation caused by an indel. Frontiers in Cellular and Infection Microbiology, 8, 193. https://doi.org/10.3389/fcimb.2018.00193
Seng, H., Sok, T., Tangkanakul, W., Petkanchanapong, W., Kositanont, U., Sareth, H., Hor, B., & Jiraphongsa, C. (2007). Leptospirosis in Takeo Province, Kingdom of Cambodia, 2003. Journal of the Medical Association of Thailand, 90, 546-551.
Tanizawa, Y., Fujisawa, T., & Nakamura, Y. (2018). DFAST: A flexible prokaryotic genome annotation pipeline for faster genome publication. Bioinformatics, 34, 1037-1039. https://doi.org/10.1093/bioinformatics/btx713
Villanueva, S. Y. A., Ezoe, H., Baterna, R., Yanagihara, Y., Muto, M., Koizumi, N., Fukui, T., Okamoto, Y., Masuzawa, T., Cavinta, L., Gloriani, N., & Yoshida, S. (2010). Serological and molecular studies on Leptospira and leptospirosis among rats in the Philippines. American Journal of Tropical Medicine and Hygiene, 82, 889-898. https://doi.org/10.4269/ajtmh.2010.09-0711
Villanueva, S. Y. A. M., Saito, M., Baterna, R. A., Estrada, C. A. M., Rivera, A. K. B., Dato, M. C., Zamora, P. R. F. C., Segawa, T., Cavinta, L. L., Fukui, T., Masuzawa, T., Yanagihara, Y., Gloriani, N. G., & Yoshida, S.-I. (2014). Leptospira-rat-human relationship in Luzon, Philippines. Microbes and Infection, 16, 902-910. https://doi.org/10.1016/j.micinf.2014.07.001
Vincent, A. T., Schiettekatte, O., Goarant, C., Neela, V. K., Bernet, E., Thibeaux, R., Ismail, N., Mohd Khalid, M. K. N., Amran, F., Masuzawa, T., Nakao, R., Amara Korba, A., Bourhy, P., Veyrier, F. J., & Picardeau, M. (2019). Revisiting the taxonomy and evolution of pathogenicity of the genus Leptospira through the prism of genomics. PLoS Neglected Tropical Diseases, 13, e0007270. https://doi.org/10.1371/journal.pntd.0007270
Weiss, S., Menezes, A., Woods, K., Chanthongthip, A., Dittrich, S., Opoku-Boateng, A., Kimuli, M., & Victoria Chalker, V. (2016). An extended multilocus sequence typing (MLST) scheme for rapid direct typing of Leptospira from clinical samples. PLoS Neglected Tropical Diseases, 10, e0004996. https://doi.org/10.1371/journal.pntd.0004996
Yasuda, S. P., Gamage, C. D., Koizumi, N., Nishio, S., Isozumi, R., Shimizu, K., Koma, T., Amada, T., Suzuki, H., Yoshimatsu, K., & Arikawa, J. (2014). Distinct genetic characteristics of Sri Lankan Rattus and Bandicota (Murinae, Rodentia) inferred from mitochondrial and nuclear markers. Genes & Genetic Systems, 89, 71-80. https://doi.org/10.1266/ggs.89.71