Abstract
Pigeon farming for meat has developed into an important economic industry in most countries, especially in China. Trichomoniasis, caused by the protozoan parasite Trichomonas gallinae, is a worldwide disease in pigeons. However, studies of the prevalence and distribution of T. gallinae lineages in domestic pigeons in southern China are limited. In this study, a total of 636 pigeon throat swabs samples from four regions in Guangdong Province were screened for T. gallinae by in vitro culture assays and microscopy. The results revealed an overall prevalence of T. gallinae infection in southern China of 26.6% (169/636). There were significant differences in the infection rate of T. gallinae between the four regions (χ2 = 117.948, df = 4, P = 0.000), with up to 44.6% in the Pearl River Delta region. The infection rate of young pigeons was as high as 70.8%. The rDNA sequences (18S rRNA/ITS1-5.8S rRNA-ITS2) of 153 positive samples were amplified and sequenced. Results identified 58.2% (89/153) overall as ITS-A (18S-VI) (also known as ITS-OBT-Tg-1) and 41.8% (64/153) as ITS-B (18S-IV) (also known as ITS-OBT-Tg-2). Thus, ITS-A (18S-VI) was the dominant T. gallinae genotype in southern China, especially in young pigeon (97.0%, 32/33). In conclusion, a high prevalence of T. gallinae infection in domestic pigeons was identified in southern China, particularly in the Pearl River Delta region. The ITS-A (18S-VI) was the dominant genotype highly pathogenic, which may weaken the immune system of pigeons, and cause a negative impact on the development of the pigeon industry in China.
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Data availability
The nucleotide sequence generated in the present study has been deposited in GenBank (https://www.ncbi.nlm.nih.gov/) under accession number ON303479 and ON303472. The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Adinehbeigi K, Ebrahimi M, Soltani Eini M, et al. (2018) Prevalence of Haemoproteus columbae (Apicomplexa: Haemoproteidae) and Trichomonas gallinae (Metamonada: Trichomonadidae) infections among pigeons (Columba livia) in West Azerbaijan Province, Iran. Arch Razi Inst 73:147–152. https://doi.org/10.22092/ari.2018.116619
Albeshr MF, Alrefaei AF (2020) Isolation and characterization of novel Trichomonas gallinae ribotypes infecting domestic and wild birds in Riyadh, Saudi Arabia. Avian Dis 64:130–134. https://doi.org/10.1637/0005-2086-64.2.130
Alkharigy FA, El Naas AS, El Maghrbi AA (2018) Survey of parasites in domestic pigeons (Columba livia) in tripoli, Libya. Open Vet J 8:360–366. https://doi.org/10.4314/ovj.v8i4.2
Alrefaei AF (2020) Molecular detection and genetic characterization of Trichomonas gallinae in falcons in Saudi Arabia. PLoS ONE 15:e0241411–e0241411. https://doi.org/10.1371/journal.pone.0241411
Alrefaei AF, Gerhold RW, Nader JL et al (2019) Improved subtyping affords better discrimination of Trichomonas gallinae strains and suggests hybrid lineages. Infect Genet Evol 73:234–241. https://doi.org/10.1016/j.meegid.2019.05.007
Alrefaei AF, Low R, Hall N et al (2019) Multilocus analysis resolves the european finch epidemic Strain of Trichomonas gallinae and suggests introgression from divergent Trichomonads. Genome Biol Evol 11:2391–2402. https://doi.org/10.1093/gbe/evz164
Anderson NL, Grahn RA, Van Hoosear K et al (2009) Studies of trichomonad protozoa in free ranging songbirds: prevalence of Trichomonas gallinae in house finches (Carpodacus mexicanus) and corvids and a novel trichomonad in mockingbirds (Mimus polyglottos). Vet Parasitol 161:178–186. https://doi.org/10.1016/j.vetpar.2009.01.023
Arfin S, Sayeed MA, Sultana S et al (2019) Prevalence of Trichomonas gallinae infection in Pigeon of Jessore District, Bangladesh. J Adv Vet Anim Res 6:549–552. https://doi.org/10.5455/javar.2019.f381
Ben QS, Lv MN, He X et al (2017) PCR identification and phylogenetic analysis of Trichomonas gallinae from domestic pigeons in Guangzhou, China. Korean J Parasitol 55:333–336. https://doi.org/10.3347/kjp.2017.55.3.333
Bobrek K, Urbanowicz J, Chorbiński P et al (2017) Molecular analysis of Trichomonas gallinae in racing pigeons from Upper Silesia, Poland. Pol J Vet Sci 20:185–187. https://doi.org/10.1515/pjvs-2017-0023
Borges FP, De Brum VP, Wiltuschnig RCM et al (2008) Characterization of nucleoside triphosphate diphosphohydrolase activity in Trichomonas gallinae and the influence of penicillin and streptomycin in extracellular nucleotide hydrolysis. FEMS Microbiol Lett 283:189–195. https://doi.org/10.1111/j.1574-6968.2008.01172.x
Borji H, Razmi GH, Movassaghi AH et al (2011) Prevalence and pathological lesion of Trichomonas gallinae in pigeons of Iran. J Vet Parasitol 25:103–106. https://doi.org/10.1007/s12639-011-0047-2
Bunbury N, Jones CG, Greenwood AG et al (2008) Epidemiology and conservation implications of Trichomonas gallinae infection in the endangered Mauritian pink pigeon. Biol Conserv 141:153–161. https://doi.org/10.1016/j.biocon.2007.09.008
Cepicka I, Hampl V, Kulda J (2010) Critical taxonomic revision of parabasalids with description of one new genus and three new species. Protist 161:400–433. https://doi.org/10.1016/j.protis.2009.11.005
Chaudhry M, Rashid HB, Angot A et al (2018) Risk factors for Avian Influenza H9 infection of chickens in live bird retail stalls of lahore district, Pakistan 2009–2010. Sci Rep 8:5634. https://doi.org/10.1038/s41598-018-23895-1
Chi JF, Lawson B, Durrant C et al (2013) The finch epidemic strain of Trichomonas gallinae is predominant in British non-passerines. Parasitology 140:1234–1245. https://doi.org/10.1017/S0031182013000930
Chou S, Hadano S, Kojima A et al (2021) Genetic characterization of Trichomonas gallinae (Rivolta, 1878) in companion birds in Japan and the genotypical relationship in the Asia region. J Microbiol Immunol Infect S1684–1182(21):00137–00147. https://doi.org/10.1016/j.jmii.2021.05.010
Dudek BM, Kochert MN, Barnes JG et al (2018) Prevalence and risk factors of Trichomonas gallinae and Trichomonosis in golden eagle (Aquila chrysaetos) nestlings in western north America. J Wildl Dis 54:755–764. https://doi.org/10.7589/2017-11-271
El-Khatam AO, AbouLaila MR, Ibrahim M et al (2016) Trichomonas gallinae: prevalence and molecular characterization from pigeons in Minoufiya governorate. Egypt Exp Parasitol 170:161–167. https://doi.org/10.1016/j.exppara.2016.09.016
Fadhil LT, Faraj AA, AL-Amery AM (2020) Trichomonas gallinae identification and histopathological study in pigeon (Columba livia domestica) in Baghdad city, Iraq. Iraqi J Vet Med 44:57–63. https://doi.org/10.30539/ijvm.v44i(e0).1022
Feng SY, Chang H, Li FH et al (2018) Prevalence and molecular characterization of Trichomonas gallinae from domestic pigeons in Beijing, China. Infect Genet Evol 65:369–372. https://doi.org/10.1016/j.meegid.2018.08.021
Grabensteiner E, Bilic I, Kolbe T, Hess M (2010) Molecular analysis of clonal trichomonad isolates indicate the existence of heterogenic species present in different birds and within the same host. Vet Parasitol 172:53–64. https://doi.org/10.1016/j.vetpar.2010.04.015
Jiang X, Sun J, Wang F et al (2016) Prevalence of Trichomonas spp. in domestic pigeons in Shandong Province, China, and genotyping by restriction fragment length polymorphism. Vet J 211:88–93. https://doi.org/10.1016/j.tvjl.2015.10.029
Lalitha S (2000) Primer Premier 5. Biotech Softw Internet Rep 1:270–272. https://doi.org/10.1089/152791600459894
Lawson B, Cunningham AA, Chantrey J et al (2011) A clonal strain of Trichomonas gallinae is the aetiologic agent of an emerging avian epidemic disease. Infect Genet Evol 11:1638–1645. https://doi.org/10.1016/j.meegid.2011.06.007
Martínez-Herrero MC, Sansano-Maestre J, Azami-Conesa I et al (2021) Sequence subtyping of Trichomonas gallinae from Bonelli’s eagle (Aquila fasciata) during four years (2014–2017) reveals that MLS type is associated with lesions. Avian Pathol 50:339–349. https://doi.org/10.1080/03079457.2021.1940099
Marx M, Reiner G, Willems H et al (2017) High prevalence of Trichomonas gallinae in wild columbids across western and southern Europe. Parasit Vectors 10:1–11. https://doi.org/10.1186/s13071-017-2170-0
Mehmood S, Nashiruddullah N, Ahmed JA, et al (2019) Parasitic affections of domesticated pigeons (Columba livia) in Jammu, India. Ann Parasitol 65:53–64. https://doi.org/10.17420/ap6501.182
Niedringhaus KD, Burchfield HJ, Elsmo EJ et al (2019) Trichomonosis due to Trichomonas gallinae infection in barn owls (Tyto alba) and barred owls (Strix varia) from the eastern United States. Vet Parasitol Reg Stud Reports 16:100281. https://doi.org/10.1016/j.vprsr.2019.100281
Saikia M, Bhattacharjee K, Sarmah PC, et al (2021) Prevalence and pathology of Trichomonas gallinae in domestic pigeon (Columba livia domestica) of Assam, India. Indian J Anim Res 55:84–89. https://doi.org/10.18805/IJAR.B-3805
Sansano-Maestre J, Garijo-Toledo MM et al (2009) Prevalence and genotyping of Trichomonas gallinae in pigeons and birds of prey. Avian Pathol 38:201–207. https://doi.org/10.1080/03079450902912135
Santos HM, Tsai CY, Catulin GEM et al (2020) Common bacterial, viral, and parasitic diseases in pigeons (Columba livia): a review of diagnostic and treatment strategies. Vet Microbiol 247:108779. https://doi.org/10.1016/j.vetmic.2020.108779
Santos N, Jambas J, Monteiro A, et al (2019) Trichomonas infection in a community of free-ranging domestic and wild columbiformes and Bonelli’s eagle (Aquila fasciata). Front Vet Sci 6.https://doi.org/10.3389/fvets.2019.00148
Wahhab MA, Abdulrahman NR, Ali SA-K (2017) A study of oropharyngeal parasites infection in doves and domestic pigeons in some villages of Garmian -Iraqi Kurdistan region. Kurdistan J Appl Res 2:15–20. https://doi.org/10.24017/science.2017.1.6
Acknowledgements
We thank Mallory Eckstut, PhD, from Liwen Bianji (Edanz) (www.liwenbianji.cn), for editing the English text of a draft of this manuscript.
Funding
This work was supported by the Key Realm R&D Program of Guangdong Province (2020B0202080004, 2020B0202090004), NSFC grants (31872460), Guangdong Basic and Applied Basic Research Foundation (2021A1515010521, 2021A1515012401, 2020A1515011575, 2019A1515010913, 2021B1515120006), Science and Technology Plan Projects of Guangdong Province (2021B1212050021), Science and technology project of Heyuan (2021008), Science and technology project of Yunfu (2021040202, 2021020604, 2021020607), Science and technology project of Guangzhou (202102080459), Special fund for scientific innovation strategy-construction of high level Academy of Agriculture Science (202110TD, 202122TD, R2020PY-JC001, R2019YJ-YB3010, R2020PY-JG013, R2020QD-048, R2021PY-QY007). Guangdong Provincial special fund for modern Agriculture Industry Technology Innovation teams (2022KJ119). The Project of Collaborative Innovation Center of GDAAS (XTXM202202).
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H.C and L.Y: data collection, writing—original draft, writing—review and editing. Y.Z, Q.Z, Z.Y, N.Q and J.Z: investigation, visualization, writing—review and editing. S.L, J.L, X.L, J.H, S.Y, J.W.L and Z.X: data curation, writing—review and editing. M.S and M.L: conceptualization, data curation, formal analysis, methodology, project administration, supervision, writing—original draft, writing—review and editing. All authors contributed to the article and approved the submitted version.
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Ethical approval for this study was obtained from the animal care and use Committee of the Institute of animal health, Guangdong Academy of Agricultural Sciences. Informed consent was obtained from all individual participants included in the study.
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Cai, H., Liu, Y., Zhu, Y. et al. Prevalence and diversity of Trichomonas gallinae in meat pigeons (Columba livia) in Guangdong Province, People’s Republic of China. Parasitol Res 121, 3183–3191 (2022). https://doi.org/10.1007/s00436-022-07640-2
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DOI: https://doi.org/10.1007/s00436-022-07640-2