Molecular identification and genetic diversity of zoonotic hookworm infections in domestic dogs from northeastern, Thailand.

Animal Genetic diversity Hookworm Infectious Molecular identification Zoonotic

Journal

Parasitology research
ISSN: 1432-1955
Titre abrégé: Parasitol Res
Pays: Germany
ID NLM: 8703571

Informations de publication

Date de publication:
29 Jan 2024
Historique:
received: 09 08 2023
accepted: 18 01 2024
medline: 29 1 2024
pubmed: 29 1 2024
entrez: 29 1 2024
Statut: epublish

Résumé

Hookworm infections remain a significant public health concern in tropical and subtropical regions, including Thailand. This study investigated the species and genetic diversity of hookworm infections in domestic dogs from northeastern Thailand. The molecular analysis focused on amplifying and sequencing specific regions of ribosomal RNA genes (ITS1-5.8S-ITS2 region) and the mitochondrial cytochrome c oxidase subunit 1 (cox1) gene in hookworm larvae recovered from 21 domestic dog stool samples. Among 21 larvae (one larva per infected dog) analyzed, 14 had sequences identical to Ancylostoma caninum, and 7 showed sequences almost identical to Ancylostoma ceylanicum. Phylogenetic analysis of cox1 sequences placed A. caninum and A. ceylanicum in separate clades. The median-joining network of A. caninum cox1 sequences from Thailand showed high haplotype diversity and belonged to the same cluster as sequences from Australia while forming separate clusters from those of A. caninum samples from the USA. The available published A. ceylanicum cox1 sequences (n = 33), in combination with seven sequences in the present study, represented 15 haplotypes distributed among three clusters. Interestingly, A. ceylanicum sequences from dogs and humans shared the same haplotypes. These findings are crucial for recognizing the potential for zoonotic transmission, highlighting the necessity for targeted control measures, and increasing awareness among pet owners and healthcare professionals to mitigate the risk of hookworm transmission to humans.

Identifiants

pubmed: 38285129
doi: 10.1007/s00436-024-08134-z
pii: 10.1007/s00436-024-08134-z
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

115

Subventions

Organisme : Thailand Science Research and Innovation (TSRI)
ID : 6506035/2565

Informations de copyright

© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.

Références

Blouin MS (2002) Molecular prospecting for cryptic species of nematodes: mitochondrial DNA versus internal transcribed spacer. Int J Parasitol 32:527–531. https://doi.org/10.1016/s0020-7519(01)00357-5
doi: 10.1016/s0020-7519(01)00357-5 pubmed: 11943225
Bowman DD, Montgomery SP, Zajac AM, Eberhard ML, Kazacos KR (2010) Hookworms of dogs and cats as agents of cutaneous larva migrans. Trends Parasitol 26:162–167. https://doi.org/10.1016/j.pt.2010.01.005
doi: 10.1016/j.pt.2010.01.005 pubmed: 20189454
Bui KL, Nguyen TH, Duong HD, Nguyen VL, Nguyen TN, Le LA, Cong HM, Tran KT, Le DV, Nagayasu E, Nonaka N, Yoshida A (2021) Ancylostoma ceylanicum infections in humans in Vietnam. Parasitol Int 84:102405. https://doi.org/10.1016/j.parint.2021.102405
doi: 10.1016/j.parint.2021.102405 pubmed: 34139361
Conlan JV, Khamlome B, Vongxay K, Elliot A, Pallant L, Sripa B, Blacksell SD, Fenwick S, Thompson RC (2012) Soil-transmitted helminthiasis in Laos: a community-wide cross-sectional study of humans and dogs in a mass drug administration environment. Am J Trop Med Hyg 86:624–634. https://doi.org/10.4269/ajtmh.2012.11-0413
doi: 10.4269/ajtmh.2012.11-0413 pubmed: 22492147 pmcid: 3403769
Croese J, Loukas A, Opdebeeck J, Fairley S, Prociv P (1994) Human enteric infection with canine hookworms. Ann Intern Med 120:369–374. https://doi.org/10.7326/0003-4819-120-5-199403010-00003
doi: 10.7326/0003-4819-120-5-199403010-00003 pubmed: 8304653
e Silva LM, Miranda RR, Santos HA, Rabelo EM (2006) Differential diagnosis of dog hookworms based on PCR-RFLP from the ITS region of their rDNA. Vet Parasitol 140(373):377. https://doi.org/10.1016/j.vetpar.2006.04.012
doi: 10.1016/j.vetpar.2006.04.012
Garcia L, Bruckner D (2001) Diagnostic medical parasitology. American Society for Microbiology, Washington, DC
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Hasegawa H, Sato H, Fujita S, Nguema PP, Nobusue K, Miyagi K, Kooriyama T, Takenoshita Y, Noda S, Sato A, Morimoto A, Ikeda Y, Nishida T (2010) Molecular identification of the causative agent of human strongyloidiasis acquired in Tanzania: dispersal and diversity of Strongyloides spp. and their hosts. Parasitol Int 59:407–413. https://doi.org/10.1016/j.parint.2010.05.007
doi: 10.1016/j.parint.2010.05.007 pubmed: 20621633
Hossain M, Bhuiyan JU (2016) Hookworm infection: a neglected tropical disease of mankind. J Inf Mol Biol 4:24–43. https://doi.org/10.14737/journal.jimb/2016/4.2.24.43
doi: 10.14737/journal.jimb/2016/4.2.24.43
Hotez PJ, Brindley PJ, Bethony JM, King CH, Pearce EJ, Jacobson J (2008) Helminth infections: the great neglected tropical diseases. J Clin Invest 118:1311–1321. https://doi.org/10.1172/JCI34261
doi: 10.1172/JCI34261 pubmed: 18382743 pmcid: 2276811
Hu M, Chilton NB, Gasser RB (2004) The mitochondrial genomics of parasitic nematodes of socio-economic importance: recent progress, and implications for population genetics and systematics. Adv Parasitol 56:133–212. https://doi.org/10.1016/s0065-308x(03)56003-1
doi: 10.1016/s0065-308x(03)56003-1 pubmed: 14710997
Inpankaew T, Schär F, Dalsgaard A, Khieu V, Chimnoi W, Chhoun C, Sok D, Marti H, Muth S, Odermatt P, Traub RJ (2014) High prevalence of Ancylostoma ceylanicum hookworm infections in humans, Cambodia, 2012. Emerg Infect Dis 20:976–982. https://doi.org/10.3201/eid2006.131770
doi: 10.3201/eid2006.131770 pubmed: 24865815 pmcid: 4036766
Jimenez Castro PD, Howell SB, Schaefer JJ, Avramenko RW, Gilleard JS, Kaplan RM (2019) Multiple drug resistance in the canine hookworm Ancylostoma caninum: an emerging threat? Parasit Vectors 12(1):576. https://doi.org/10.1186/s13071-019-3828-6
doi: 10.1186/s13071-019-3828-6 pubmed: 31818311 pmcid: 6902405
Jiraanankul V, Aphijirawat W, Mungthin M, Khositnithikul R, Rangsin R, Traub RJ, Piyaraj P, Naaglor T, Taamasri P, Leelayoova S (2011) Incidence and risk factors of hookworm infection in a rural community of central Thailand. Am J Trop Med Hyg 84:594–598. https://doi.org/10.4269/ajtmh.2011.10-0189
doi: 10.4269/ajtmh.2011.10-0189 pubmed: 21460016 pmcid: 3062455
Jung BK, Lee JY, Chang T, Song H, Chai JY (2020) Rare case of enteric Ancylostoma caninum hookworm infection, South Korea. Emerg Infect Dis 26:181–183. https://doi.org/10.3201/eid2601.191335
doi: 10.3201/eid2601.191335 pubmed: 31855538 pmcid: 6924899
Kalkofen UP (1987) Hookworms of dogs and cats. Vet Clin North Am Small Anim Pract 17:1341–1354. https://doi.org/10.1016/s0195-5616(87)50005-5
doi: 10.1016/s0195-5616(87)50005-5 pubmed: 3328392
Kladkempetch D, Tangtrongsup S, Tiwananthagorn S (2020) Ancylostoma ceylanicum: The neglected zoonotic parasite of community dogs in Thailand and its genetic diversity among Asian countries. Animals (basel) 10:2154. https://doi.org/10.3390/ani10112154
doi: 10.3390/ani10112154 pubmed: 33228101
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
doi: 10.1093/molbev/msy096 pubmed: 29722887 pmcid: 5967553
Lamb J, Napier M, Mukaratirwa S (2012) PCR-based identification reveals unique Southern African internal transcribed spacer (ITS) haplotypes of hookworms (Ancylostoma) of dogs from the Durban metropole, South Africa. Afr J Biotechnol 11:2099–2106. https://doi.org/10.5897/AJB11.3065
doi: 10.5897/AJB11.3065
Landmann JK, Prociv P (2003) Experimental human infection with the dog hookworm, Ancylostoma caninum. Med J Aust 178:69–71. https://doi.org/10.5694/j.1326-5377.2003.tb05222.x
doi: 10.5694/j.1326-5377.2003.tb05222.x pubmed: 12526725
Leigh JW, Bryant D (2015) PopART v1.7: full-feature software for haplotype network construction. Methods Ecol Evol 6:1110–1116. https://doi.org/10.1111/2041-210X.12410
doi: 10.1111/2041-210X.12410
Liu Y, Zheng G, Alsarakibi M, Zhang X, Hu W, Lu P, Lin L, Tan L, Luo Q, Li G (2013) Molecular identification of Ancylostoma caninum isolated from cats in southern China based on complete ITS sequence. Biomed Res Int 2013:868050. https://doi.org/10.1155/2013/868050
doi: 10.1155/2013/868050 pubmed: 24175305 pmcid: 3794661
Liu Y, Zheng G, Alsarakibi M, Zhang X, Hu W, Lin L, Tan L, Luo Q, Lu P, Li G (2014) The zoonotic risk of Ancylostoma ceylanicum isolated from stray dogs and cats in Guangzhou. South China Biomed Res Int 2014:208759. https://doi.org/10.1155/2014/208759
doi: 10.1155/2014/208759 pubmed: 24877068
Liu YJ, Zheng GC, Zhang P, Alsarakibi M, Zhang XH, Li YW, Liu T, Ren SN, Chen ZX, Liu YL, Li SJ, Li GQ (2015) Molecular identification of hookworms in stray and shelter dogs from Guangzhou city, China using ITS sequences. J Helminthol 89:196–202. https://doi.org/10.1017/S0022149X13000783
doi: 10.1017/S0022149X13000783 pubmed: 24280028
Mahdy MA, Lim YA, Ngui R, Siti Fatimah MR, Choy SH, Yap NJ, Al-Mekhlafi HM, Ibrahim J, Surin J (2012) Prevalence and zoonotic potential of canine hookworms in Malaysia. Parasit Vectors 5:88. https://doi.org/10.1186/1756-3305-5-88
doi: 10.1186/1756-3305-5-88 pubmed: 22564445 pmcid: 3461414
Merino-Tejedor A, Nejsum P, Mkupasi EM, Johansen MV, Olsen A (2019) Molecular identification of zoonotic hookworm species in dog faeces from Tanzania. J Helminthol 93:313–318. https://doi.org/10.1017/S0022149X18000263
doi: 10.1017/S0022149X18000263 pubmed: 29606160
Ngcamphalala PI, Lamb J, Mukaratirwa S (2019) Molecular identification of hookworm isolates from stray dogs, humans and selected wildlife from South Africa. J Helminthol 94:e39. https://doi.org/10.1017/S0022149X19000130
doi: 10.1017/S0022149X19000130 pubmed: 30789121
Ng-Nguyen D, Hii SF, Nguyen VA, Van Nguyen T, Van Nguyen D, Traub RJ (2015) Re-evaluation of the species of hookworms infecting dogs in Central Vietnam. Parasit Vectors 8:401. https://doi.org/10.1186/s13071-015-1015-y
doi: 10.1186/s13071-015-1015-y pubmed: 26216353 pmcid: 4517506
Ngui R, Lim YA, Traub R, Mahmud R, Mistam MS (2012) Epidemiological and genetic data supporting the transmission of Ancylostoma ceylanicum among human and domestic animals. PLoS Negl Trop Dis 6:e1522. https://doi.org/10.1371/journal.pntd.0001522
doi: 10.1371/journal.pntd.0001522 pubmed: 22347515 pmcid: 3274503
Ngui R, Mahdy MA, Chua KH, Traub R, Lim YA (2013) Genetic characterization of the partial mitochondrial cytochrome oxidase c subunit I (cox 1) gene of the zoonotic parasitic nematode, Ancylostoma ceylanicum from humans, dogs and cats. Acta Trop 128:154–157. https://doi.org/10.1016/j.actatropica.2013.06.003
doi: 10.1016/j.actatropica.2013.06.003 pubmed: 23774318
Oliveira-Arbex AP, David EB, Oliveira-Sequeira TC, Katagiri S, Coradi ST, Guimarães S (2017) Molecular identification of Ancylostoma species from dogs and an assessment of zoonotic risk in low-income households, São Paulo State, Brazil. J Helminthol 91:14–19. https://doi.org/10.1017/S0022149X15001145
doi: 10.1017/S0022149X15001145 pubmed: 26752269
Palmer CS, Traub RJ, Robertson ID, Hobbs RP, Elliot A, While L, Rees R, Thompson RC (2007) The veterinary and public health significance of hookworm in dogs and cats in Australia and the status of A. ceylanicum. Vet Parasitol 145:304–313. https://doi.org/10.1016/j.vetpar.2006.12.018
doi: 10.1016/j.vetpar.2006.12.018 pubmed: 17276602
Phoosangwalthong P, Kamyingkird K, Kengradomkij C, Chimnoi W, Odermatt P, Inpankaew T (2023) Molecular detection and genetic characterization of zoonotic hookworm in semi-domesticated cats residing in monasteries in Bangkok. Thailand Trop Med Infect Dis 8:122. https://doi.org/10.3390/tropicalmed8020122
doi: 10.3390/tropicalmed8020122 pubmed: 36828538
Phosuk I, Intapan PM, Thanchomnang T, Sanpool O, Janwan P, Laummaunwai P, Aamnart W, Morakote N, Maleewong W (2013) Molecular detection of Ancylostoma duodenale, Ancylostoma ceylanicum, and Necator americanus in humans in northeastern and southern Thailand. Korean J Parasitol 51:747–749. https://doi.org/10.3347/kjp.2013.51.6.747
doi: 10.3347/kjp.2013.51.6.747 pubmed: 24516284 pmcid: 3916468
Prociv P, Croese J (1990) Human eosinophilic enteritis caused by dog hookworm Ancylostoma caninum. Lancet 335:1299–1302. https://doi.org/10.1016/0140-6736(90)91186-e
doi: 10.1016/0140-6736(90)91186-e pubmed: 1971376
Prociv P, Croese J (1996) Human enteric infection with Ancylostoma caninum: hookworms reappraised in the light of a “new” zoonosis. Acta Trop 62:23–44. https://doi.org/10.1016/s0001-706x(96)00016-2
doi: 10.1016/s0001-706x(96)00016-2 pubmed: 8971276
Pumidonming W, Salman D, Gronsang D, Abdelbaset AE, Sangkaeo K, Kawazu SI, Igarashi M (2017) Prevalence of gastrointestinal helminth parasites of zoonotic significance in dogs and cats in lower Northern Thailand. J Vet Med Sci 78:1779–1784. https://doi.org/10.1292/jvms.16-0293
doi: 10.1292/jvms.16-0293 pubmed: 27570099
Romstad A, Gasser RB, Nansen P, Polderman AM, Chilton NB (1998) Necator americanus (Nematoda: Ancylostomatidae) from Africa and Malaysia have different ITS-2 rDNA sequences. Int J Parasitol 28:611–615. https://doi.org/10.1016/s0020-7519(97)00213-0
doi: 10.1016/s0020-7519(97)00213-0 pubmed: 9602384
Šlapeta J, Dowd SE, Alanazi AD, Westman ME, Brown GK (2015) Differences in the faecal microbiome of non-diarrhoeic clinically healthy dogs and cats associated with Giardia duodenalis infection: impact of hookworms and coccidia. Int J Parasitol 45:585–594. https://doi.org/10.1016/j.ijpara.2015.04.001
doi: 10.1016/j.ijpara.2015.04.001 pubmed: 25934152
Štrkolcová G, Mravcová K, Mucha R, Mulinge E, Schreiberová A (2022) Occurrence of hookworm and the first molecular and morphometric identification of Uncinaria stenocephala in dogs in Central Europe. Acta Parasitol 67:764–772. https://doi.org/10.1007/s11686-021-00509-x
doi: 10.1007/s11686-021-00509-x pubmed: 35067865
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526. https://doi.org/10.1093/oxfordjournals.molbev.a040023
doi: 10.1093/oxfordjournals.molbev.a040023 pubmed: 8336541
Traub RJ (2013) Ancylostoma ceylanicum, a re-emerging but neglected parasitic zoonosis. Int J Parasitol 43:1009–1015. https://doi.org/10.1016/j.ijpara.2013.07.006
doi: 10.1016/j.ijpara.2013.07.006 pubmed: 23968813
Traub RJ, Robertson ID, Irwin P, Mencke N, Thompson RC (2004) Application of a species- specific PCR-RFLP to identify Ancylostoma eggs directly from canine faeces. Vet Parasitol 123:245–255. https://doi.org/10.1016/j.vetpar.2004.05.026
doi: 10.1016/j.vetpar.2004.05.026 pubmed: 15325050
Traub RJ, Hobbs RP, Adams PJ, Behnke JM, Harris PD, Thompson RC (2007) A case of mistaken identity–reappraisal of the species of canid and felid hookworms (Ancylostoma) present in Australia and India. Parasitology 134:113–119. https://doi.org/10.1017/S0031182006001211
doi: 10.1017/S0031182006001211 pubmed: 16987431
Traub RJ, Inpankaew T, Sutthikornchai C, Sukthana Y, Thompson RC (2008) PCR-based coprodiagnostic tools reveal dogs as reservoirs of zoonotic ancylostomiasis caused by Ancylostoma ceylanicum in temple communities in Bangkok. Vet Parasitol 155:67–73. https://doi.org/10.1016/j.vetpar.2008.05.001
doi: 10.1016/j.vetpar.2008.05.001 pubmed: 18556131
Traversa D (2012) Pet roundworms and hookworms: a continuing need for global worming. Parasit Vectors 5:91. https://doi.org/10.1186/1756-3305-5-91
doi: 10.1186/1756-3305-5-91 pubmed: 22574783 pmcid: 3418564
Traversa D, Frangipane di Regalbono A, Di Cesare A, La Torre F, Drake J, Pietrobelli M (2014) Environmental contamination by canine geohelminths. Parasit Vectors 7:67. https://doi.org/10.1186/1756-3305-7-67
doi: 10.1186/1756-3305-7-67 pubmed: 24524656 pmcid: 3929561
Wang MW, Yan XX, Hang JX, Shi XL, Fu YQ, Zhang P, Yang F, Pan WD, Li GQ (2019) Molecular differentiation of three canine and feline hookworms in South China through HRM analysis. J Helminthol 93:159–165. https://doi.org/10.1017/S0022149X18000068
doi: 10.1017/S0022149X18000068 pubmed: 29400266
Wongwigkan J, Inpankaew T (2020) Semi-domesticated dogs as a potential reservoir for zoonotic hookworms in Bangkok, Thailand. Vet World 13:909–915. https://doi.org/10.14202/vetworld.2020.909-915
doi: 10.14202/vetworld.2020.909-915 pubmed: 32636587 pmcid: 7311867
Xu FF, Niu YF, Chen WQ, Liu SS, Li JR, Jiang P, Wang ZQ, Cui J, Zhang X (2021) Hookworm infection in central China: morphological and molecular diagnosis. Parasit Vectors 14:537. https://doi.org/10.1186/s13071-021-05035-3
doi: 10.1186/s13071-021-05035-3 pubmed: 34649597 pmcid: 8518228
Yoshikawa M, Ouji Y, Hirai N et al (2018) Ancylostoma ceylanicum, novel etiological agent for traveler’s diarrhea-report of four Japanese patients who returned from Southeast Asia and Papua New Guinea. Trop Med Health 46:6. https://doi.org/10.1186/s41182-018-0087-8
doi: 10.1186/s41182-018-0087-8 pubmed: 29563849 pmcid: 5848582
Zibaei M, Nosrati MRC, Shadnoosh F, Houshmand E, Karami MF, Rafsanjani MK, Majidiani H, Ghaffarifar F, Cortes HCE, Dalvand S, Badri M (2020) Insights into hookworm prevalence in Asia: a systematic review and meta-analysis. Trans R Soc Trop Med Hyg 114:141–154. https://doi.org/10.1093/trstmh/trz115
doi: 10.1093/trstmh/trz115 pubmed: 31917423

Auteurs

Rutchanee Rodpai (R)

Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen, 40002, Thailand.
Mekong Health Science Research Institute, Khon Kaen University, Khon Kaen, 40002, Thailand.

Oranuch Sanpool (O)

Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen, 40002, Thailand.
Mekong Health Science Research Institute, Khon Kaen University, Khon Kaen, 40002, Thailand.

Lakkhana Sadaow (L)

Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen, 40002, Thailand.
Mekong Health Science Research Institute, Khon Kaen University, Khon Kaen, 40002, Thailand.

Patcharaporn Boonroumkaew (P)

Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen, 40002, Thailand.
Mekong Health Science Research Institute, Khon Kaen University, Khon Kaen, 40002, Thailand.

Pewpan M Intapan (PM)

Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen, 40002, Thailand.
Mekong Health Science Research Institute, Khon Kaen University, Khon Kaen, 40002, Thailand.

Wanchai Maleewong (W)

Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen, 40002, Thailand.
Mekong Health Science Research Institute, Khon Kaen University, Khon Kaen, 40002, Thailand.

Manachai Yingklang (M)

Faculty of Public Health, Burapha University, Chonburi, 20131, Thailand.

Penchom Janwan (P)

Department of Medical Technology, School of Allied Health Sciences, Walailak University, Nakhon Si Thammarat, 80160, Thailand.

Kotchaphon Vaisusuk (K)

Department of Veterinary Technology and Veterinary Nursing, Faculty of Agricultural Technology, Rajabhat Maha Sarakham University, Maha Sarakham, 44000, Thailand.

Wasupon Chatan (W)

Faculty of Veterinary Sciences, Mahasarakham University, Maha Sarakham, 44000, Thailand.

Supawadee Piratae (S)

Faculty of Veterinary Sciences, Mahasarakham University, Maha Sarakham, 44000, Thailand.

Tongjit Thanchomnang (T)

Faculty of Medicine, Mahasarakham University, Maha Sarakham, 44000, Thailand. tongjit.t@msu.ac.th.

Classifications MeSH