First molecular evidence of bovine hemoplasmas in houseflies (Musca domestica).
Candidatus mycoplasma haemobos
Mycoplasma wenyonii
Bovine hemoplasma
Houseflies
Transmission route
Journal
BMC veterinary research
ISSN: 1746-6148
Titre abrégé: BMC Vet Res
Pays: England
ID NLM: 101249759
Informations de publication
Date de publication:
30 Oct 2024
30 Oct 2024
Historique:
received:
05
08
2024
accepted:
21
10
2024
medline:
31
10
2024
pubmed:
31
10
2024
entrez:
31
10
2024
Statut:
epublish
Résumé
Hemoplasma infections in cattle are caused by Mycoplasma wenyonii and Candidatus Mycoplasma haemobos and induce asymptomatic or chronic infections but occasionally lead to life-threatening hemolytic anemia. Despite the global distribution of bovine hemoplasmas, information regarding their transmission vectors and prevalence is still lacking in the Republic of Korea. Therefore, this study aims to investigate the infection rate of bovine hemoplasma in cattle and houseflies and to assess the risk factors associated with hemoplasma infection in cattle. Overall, 376 blood samples were collected from Korean indigenous cattle (male, 10-13 months old), along with 2,690 houseflies (Musca domestica) from the same farm where the cattle were raised. PCR assays targeting the 16S rRNA gene were performed to detect hemoplasmas, and positive samples were sequenced. The infection rate of bovine hemoplasmas was 50.8% (191/376) in cattle and 7.4% in pooled houseflies. Among cattle, 18.6% (70/376) and 20.0% (75/376) tested positive for M. wenyonii and Candidatus M. haemobos, respectively. Conversely, in houseflies, Candidatus M. haemobos was more frequently detected (5.9%) than M. wenyonii (0.7%). Co-infection was 12.2% (46/376) in cattle and 0.7% in flies. Furthermore, hemoplasma infection was significantly associated with the grazing experience of their dams. Cattle born to cows with grazing experience exhibited a higher risk for M. wenyonii infection (odds ratio [OR] = 1.62; 95% confidence interval [CI]: 1.03-2.55; P = 0.045), whereas these cattle had a lower risk for Candidatus M. haemobos infection (OR = 0.32, 95% CI: 0.19-0.74; P = 0.000) than animals born to cows without grazing experience. The sequences obtained from houseflies were confirmed as Candidatus M. haemobos, which displayed high similarity (98.2-100%) to those from cattle obtained in this study. To our knowledge, this study represents the first report of bovine hemoplasmas identified in houseflies. This molecular evidence suggests that houseflies may be possible vectors for Candidatus M. haemobos.
Sections du résumé
BACKGROUND
BACKGROUND
Hemoplasma infections in cattle are caused by Mycoplasma wenyonii and Candidatus Mycoplasma haemobos and induce asymptomatic or chronic infections but occasionally lead to life-threatening hemolytic anemia. Despite the global distribution of bovine hemoplasmas, information regarding their transmission vectors and prevalence is still lacking in the Republic of Korea. Therefore, this study aims to investigate the infection rate of bovine hemoplasma in cattle and houseflies and to assess the risk factors associated with hemoplasma infection in cattle.
METHODS
METHODS
Overall, 376 blood samples were collected from Korean indigenous cattle (male, 10-13 months old), along with 2,690 houseflies (Musca domestica) from the same farm where the cattle were raised. PCR assays targeting the 16S rRNA gene were performed to detect hemoplasmas, and positive samples were sequenced.
RESULTS
RESULTS
The infection rate of bovine hemoplasmas was 50.8% (191/376) in cattle and 7.4% in pooled houseflies. Among cattle, 18.6% (70/376) and 20.0% (75/376) tested positive for M. wenyonii and Candidatus M. haemobos, respectively. Conversely, in houseflies, Candidatus M. haemobos was more frequently detected (5.9%) than M. wenyonii (0.7%). Co-infection was 12.2% (46/376) in cattle and 0.7% in flies. Furthermore, hemoplasma infection was significantly associated with the grazing experience of their dams. Cattle born to cows with grazing experience exhibited a higher risk for M. wenyonii infection (odds ratio [OR] = 1.62; 95% confidence interval [CI]: 1.03-2.55; P = 0.045), whereas these cattle had a lower risk for Candidatus M. haemobos infection (OR = 0.32, 95% CI: 0.19-0.74; P = 0.000) than animals born to cows without grazing experience. The sequences obtained from houseflies were confirmed as Candidatus M. haemobos, which displayed high similarity (98.2-100%) to those from cattle obtained in this study.
CONCLUSIONS
CONCLUSIONS
To our knowledge, this study represents the first report of bovine hemoplasmas identified in houseflies. This molecular evidence suggests that houseflies may be possible vectors for Candidatus M. haemobos.
Identifiants
pubmed: 39478614
doi: 10.1186/s12917-024-04343-x
pii: 10.1186/s12917-024-04343-x
doi:
Substances chimiques
RNA, Ribosomal, 16S
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
497Subventions
Organisme : National Research Foundation of Korea
ID : NRF-2021R1A2C1011579
Informations de copyright
© 2024. The Author(s).
Références
Messick JB. Hemotrophic mycoplasmas (hemoplasmas): a review and new insights into pathogenic potential. Vet Clin Pathol. 2004;33:2–13. https://doi.org/10.1111/j.1939-165x.2004.tb00342.x .
doi: 10.1111/j.1939-165x.2004.tb00342.x
pubmed: 15048620
Maggi RG, Mascarelli PE, Balakrishnan N, Rohde CM, Kelly CM, Ramaiah L, et al. Candidatus Mycoplasma haemomacaque and Bartonella quintana bacteremia in cynomolgus monkeys. J Clin Microbiol. 2013;51:1408–11. https://doi.org/10.1128/JCM.03019-12 .
doi: 10.1128/JCM.03019-12
pubmed: 23408694
pmcid: 3647913
Hofmann-Lehmann R, Meli ML, Dreher UM, Gonczi E, Deplazes P, Braun U, et al. Concurrent infections with vector-borne pathogens associated with fatal hemolytic anemia in a cattle herd in Switzerland. J Clin Microbiol. 2004;42:3775–80. https://doi.org/10.1128/JCM.42.8.3775-3780.2004 .
doi: 10.1128/JCM.42.8.3775-3780.2004
pubmed: 15297529
pmcid: 497630
Tagawa M, Matsumoto K, Inokuma H. Molecular detection of Mycoplasma wenyonii and ‘Candidatus Mycoplasma haemobos’ in cattle in Hokkaido. Japan Vet Microbiol. 2008;132:177–80. https://doi.org/10.1016/j.vetmic.2008.05.006 .
doi: 10.1016/j.vetmic.2008.05.006
pubmed: 18571343
Smith JA, Thrall MA, Smith JL, Salman MD, Ching SV, Collins JK. Eperythrozoon wenyonii infection in dairy cattle. J Am Vet Med Assoc. 1990;196:1244–50. https://doi.org/10.2460/javma.1990.196.08.1244 .
doi: 10.2460/javma.1990.196.08.1244
pubmed: 2332369
Hoelzle K, Winkler M, Kramer MM, Wittenbrink MM, Dieckmann SM, Hoelzle LE. Detection of Candidatus Mycoplasma haemobos in cattle with anaemia. Vet J. 2011;187:408–10. https://doi.org/10.1016/j.tvjl.2010.01.016 .
doi: 10.1016/j.tvjl.2010.01.016
pubmed: 20188610
Baggenstos R, Wenzinger B, Meli ML, Hofmann-Lehmann R, Knubben-Schweizer G. Haemoplasma infection in a dairy cow. Tierarztl Prax Ausg G Grosstiere Nutztiere. 2012;40:397–400. https://doi.org/10.5167/uzh-69252 .
doi: 10.5167/uzh-69252
pubmed: 23242150
Erol U, Sahin OF, Altay K. Molecular prevalence of bovine hemoplasmosis in Turkey with first detection of Mycoplasma wenyonii and Candidatus Mycoplasma haemobos in cattle and water buffalo. Vet Res Commun. 2023;47:207–15. https://doi.org/10.1007/s11259-022-09943-2 .
doi: 10.1007/s11259-022-09943-2
pubmed: 35624402
Neimark H, Johansson KE, Rikihisa Y, Tully JG. Proposal to transfer some members of the genera Haemobartonella and Eperythrozoon to the genus Mycoplasma with descriptions of ‘Candidatus Mycoplasma haemofelis’, ‘Candidatus Mycoplasma haemomuris’, ‘Candidatus Mycoplasma haemosuis’ and ‘Candidatus Mycoplasma wenyonii’. Int J Syst Evol Microbiol. 2001;51:891–9. https://doi.org/10.1099/00207713-51-3-891 .
doi: 10.1099/00207713-51-3-891
pubmed: 11411711
Murugesan AC, Kumaragurubaran K, Gunasekaran K, Murugasamy SA, Arunachalam S, Annamalai R, et al. Molecular detection of hemoplasma in animals in Tamil Nadu, India and hemoplasma genome analysis. Vet Res Commun. 2024;48:955–68. https://doi.org/10.1007/s11259-023-10263-2 .
doi: 10.1007/s11259-023-10263-2
pubmed: 38032521
Thongmeesee K, Chonglomkrod B, Srisakdi C, Saributr M, Suksai P, Kamkong P, et al. Molecular detection of Mycoplasma wenyonii and its closely related hemotropic Mycoplasma sp. in blood-sucking flies from a buffalo farm in Chachoengsao province, Thailand. Acta Trop. 2022;235:106647. https://doi.org/10.1016/j.actatropica.2022.106647 .
doi: 10.1016/j.actatropica.2022.106647
pubmed: 35961407
Kim Y, Kim H, Choi JH, Cho HC, Ji MJ, Park YJ, et al. Preliminary report of Mycoplasma Wenoynii and Candidatus Mycoplasma haemobos infection in Korean native cattle. BMC Vet Res. 2024;20:121. https://doi.org/10.1186/s12917-024-03976-2 .
doi: 10.1186/s12917-024-03976-2
pubmed: 38532391
pmcid: 10964582
Diaz-Sanchez AA, Corona-Gonzalez B, Meli ML, Alvarez DO, Canizares EV, Rodriguez OF, et al. First molecular evidence of bovine hemoplasma species (Mycoplasma spp.) in water buffalo and dairy cattle herds in Cuba. Parasit Vectors. 2019;12:78. https://doi.org/10.1186/s13071-019-3325-y .
doi: 10.1186/s13071-019-3325-y
pubmed: 30732656
pmcid: 6367761
Niethammer FM, Ade J, Hoelzle LE, Schade B. Hemotrophic mycoplasma in Simmental cattle in Bavaria: prevalence, blood parameters, and transplacental transmission of ‘Candidatus Mycoplasma haemobos’ and Mycoplasma wenyonii. Acta Vet Scand. 2018;60:74. https://doi.org/10.1186/s13028-018-0428-y .
doi: 10.1186/s13028-018-0428-y
pubmed: 30445976
pmcid: 6240245
Kamani J, Shand M, Shekaro A, Laminu B, Toyin O, Abasiama MS, et al. Mycoplasma wenyonii and Candidatus Mycoplasma Haemobos in pastoralists cattle in Nigeria. Acta Parasitol. 2023;68:430–8. https://doi.org/10.1007/s11686-023-00683-0 .
doi: 10.1007/s11686-023-00683-0
pubmed: 37170044
Schambow RA, Poulsen K, Bolin S, Krahn D, Norby B, Sockett D, et al. Apparent prevalence of Mycoplasma wenyonii, Candidatus Mycoplasma haemobos, and bovine leukemia virus in Wisconsin and Michigan dairy cattle herds. JDS Commun. 2021;2:261–6. https://doi.org/10.3168/jdsc.2020-0033 .
doi: 10.3168/jdsc.2020-0033
Hornok S, Micsutka A, Meli ML, Lutz H, Hofmann-Lehmann R. Molecular investigation of transplacental and vector-borne transmission of bovine haemoplasmas. Vet Microbiol. 2011;152:411–4. https://doi.org/10.1016/j.vetmic.2011.04.031 .
doi: 10.1016/j.vetmic.2011.04.031
pubmed: 21605950
Sasaoka F, Suzuki J, Hirata T, Ichijo T, Furuhama K, Harasawa R, et al. Vertical transmission of Mycoplasma wenyonii in cattle, supported by analysis of the ribonuclease P RNA gene - short communication. Acta Vet Hung. 2015;63:271–4. https://doi.org/10.1556/004.2015.025 .
doi: 10.1556/004.2015.025
pubmed: 26551417
Girotto-Soares A, Soares JF, Bogado ALG, de Macedo CAB, Sandeski LM, Garcia JL, et al. Candidatus Mycoplasma haemobos’: transplacental transmission in dairy cows (Bos taurus). Vet Microbiol. 2016;195:22–4. https://doi.org/10.1016/j.vetmic.2016.08.020 .
doi: 10.1016/j.vetmic.2016.08.020
pubmed: 27771066
Shi H, Duan L, Liu F, Hu Y, Shi Z, Chen X, et al. Rhipicephalus (Boophilus) microplus ticks as reservoir and vector of ‘Candidatus Mycoplasma haemobos’ in China. Vet Parasitol. 2019;274:108929. https://doi.org/10.1016/j.vetpar.2019.108929 .
doi: 10.1016/j.vetpar.2019.108929
pubmed: 31568995
Ferrari LDR, Hassan-Kadle AA, Collere FCM, Coradi VS, Ibrahim AM, Osman AM, et al. Hemoplasmas and ticks in cattle from Somalia. Acta Trop. 2022;236:106696. https://doi.org/10.1016/j.actatropica.2022.106696 .
doi: 10.1016/j.actatropica.2022.106696
pubmed: 36189489
Ybanez AP, Ybanez RHD, Armonia RKM, Chico JKE, Ferraren KJV, Tapdasan EP, et al. First molecular detection of Mycoplasma wenyonii and the ectoparasite biodiversity in dairy water buffalo and cattle in Bohol, Philippines. Parasitol Int. 2019;70:77–81. https://doi.org/10.1016/j.parint.2019.02.004 .
doi: 10.1016/j.parint.2019.02.004
pubmed: 30776450
Arendt M, Stadler J, Ritzmann M, Ade J, Hoelzle K, Hoelzle LE. Hemotrophic mycoplasmas-vector transmission in livestock. Microorganisms. 2024;12:7. https://doi.org/10.3390/microorganisms12071278 .
doi: 10.3390/microorganisms12071278
Bertolini AB, Thyssen PJ, Brandao PE, Prado AM, Silva SOD, Mioni MDR, et al. Flies (Insecta, Diptera) collected in the environment of dairy farms as carriers of rotavirus A and betacoronavirus. J Appl Microbiol. 2023;134:lxad020. https://doi.org/10.1093/jambio/lxad020 .
doi: 10.1093/jambio/lxad020
pubmed: 36725209
Issa R. Musca domestica acts as transport vector hosts. Bull Natl Res Cent. 2019;43:73. https://doi.org/10.1186/s42269-019-0111-0 .
doi: 10.1186/s42269-019-0111-0
Hamdan M, Kamalanathan T, Iqbal A, Gnanaprakasam AR, Shajahan S, Alsadeq MH, et al. Kdr kdr mutations and deltamethrin resistance in houseflies in Abu Dhabi, UAE. Parasit Vectors. 2024;17:47. https://doi.org/10.1186/s13071-024-06128-5 .
doi: 10.1186/s13071-024-06128-5
pubmed: 38302967
pmcid: 10832251
Gioia G, Severgnini M, Cremonesi P, Castiglioni B, Freeman J, Sipka A, et al. Genomic characterization of Mycoplasma arginini isolated from a housefly on a dairy farm and comparison with isolates from bovine milk and lung tissue. Microbiol Spectr. 2023;11:e0301022. https://doi.org/10.1128/spectrum.03010-22 .
doi: 10.1128/spectrum.03010-22
pubmed: 37199649
Park SH, Zhang Y, Piao H, Yu DH, Jeong HJ, Yoo GY, et al. Use of cytochrome c oxidase subunit i (COI) nucleotide sequences for identification of the Korean Luciliinae fly species (Diptera: Calliphoridae) in forensic investigations. J Korean Med Sci. 2009;24:1058–63. https://doi.org/10.3346/jkms.2009.24.6.1058 .
doi: 10.3346/jkms.2009.24.6.1058
pubmed: 19949660
pmcid: 2775852
Santos NJR, Brito DRB, Abate HL, Paixao SF, Soares EDS, Vieira T, et al. Hemotropic mycoplasmas infection in water buffaloes (Bubalus bubalis) from Northeastern Brazil. Comp Immunol Microbiol Infect Dis. 2018;56:27–9. https://doi.org/10.1016/j.cimid.2017.12.003 .
doi: 10.1016/j.cimid.2017.12.003
pubmed: 29406279
Byamukama B, Tumwebaze MA, Tayebwa DS, Byaruhanga J, Angwe MK, Li J, et al. First molecular detection and characterization of hemotropic Mycoplasma species in cattle and goats from Uganda. Anim (Basel). 2020;10:1624. https://doi.org/10.3390/ani10091624 .
doi: 10.3390/ani10091624
Congli Y, Hong Y, Zhonghai Z, Zhibiao Y, Li C, Jianguo Z, et al. Prevalence of Mycoplasma wenyonii infection on seven dairy farms in Shanghai, China. Thai J Vet Med. 2011;41:179–84. https://doi.org/10.56808/2985-1130.2294 .
doi: 10.56808/2985-1130.2294
Girotto A, Zangirolamo AF, Bogado AL, Souza AS, da Silva GC, Garcia JL, et al. Molecular detection and occurrence of ‘Candidatus Mycoplasma haemobos’ in dairy cattle of Southern Brazil. Rev Bras Parasitol Vet. 2012;21:342–4. https://doi.org/10.1590/S1984-29612012000300034 .
doi: 10.1590/S1984-29612012000300034
pubmed: 23070456
Tagawa M, Ybanez AP, Matsumoto K, Yokoyama N, Inokuma H. Prevalence and risk factor analysis of bovine hemoplasma infection by direct PCR in Eastern Hokkaido, Japan. J Vet Med Sci. 2012;74:1171–6. https://doi.org/10.1292/jvms.12-0118 .
doi: 10.1292/jvms.12-0118
pubmed: 22673725
Song Q, Wang L, Fang R, Khan MK, Zhou Y, Zhao J. Detection of Mycoplasma wenyonii in cattle and transmission vectors by the loop-mediated isothermal amplification (LAMP) assay. Trop Anim Health Prod. 2013;45:247–50. https://doi.org/10.1007/s11250-012-0197-y .
doi: 10.1007/s11250-012-0197-y
pubmed: 22684637
Mohd Hasan LI, Kho KL, Koh FX, Hassan Nizam QN, Tay ST. Molecular evidence of hemoplasmas in Malaysian cattle and ticks. Trop Biomed. 2017;34:668–74.
pubmed: 33592935
Stevanovic O, Jurkovic D, Polkinghorne A, Celes A, Ilic T, Dimitrijevic S, et al. Molecular detection of Babesia divergens and Mycoplasma wenyonii infection in cattle from Bosnia and Herzegovina. Parasitol Res. 2020;119:1423–7. https://doi.org/10.1007/s00436-020-06630-6 .
doi: 10.1007/s00436-020-06630-6
pubmed: 32107621
Espinosa-Gongora C, Dahl J, Elvstrom A, van Wamel WJ, Guardabassi L. Individual predisposition to Staphylococcus aureus colonization in pigs on the basis of quantification, carriage dynamics, and serological profiles. Appl Environ Microbiol. 2015;81:1251–6. https://doi.org/10.1128/AEM.03392-14 .
doi: 10.1128/AEM.03392-14
pubmed: 25501475
pmcid: 4309706
Nazni WA, Luke H, Wan Rozita WM, Abdullah AG, Sa’diyah I, Azahari AH, et al. Determination of the flight range and dispersal of the housefly, Musca domestica (L.) using mark release recapture technique. Trop Biomed. 2005;22:53–61.
pubmed: 16880754
Nayduch D, Neupane S, Pickens V, Purvis T, Olds C. Houseflies are underappreciated yet important reservoirs and vectors of microbial threats to animal and human health. Microorganisms. 2023;11:583. https://doi.org/10.3390/microorganisms11030583 .
doi: 10.3390/microorganisms11030583
pubmed: 36985156
pmcid: 10054770
Alegbeleye OO, Singleton I, Sant’Ana AS. Sources and contamination routes of microbial pathogens to fresh produce during field cultivation: a review. Food Microbiol. 2018;73:177–208. https://doi.org/10.1016/j.fm.2018.01.003 .
doi: 10.1016/j.fm.2018.01.003
pubmed: 29526204
pmcid: 7127387