Abstract
Q fever is a zoonotic disease caused by the obligate intracellular pathogen Coxiella burnetii, for which domestic ruminants are the primary source of infection in humans. Herein, we investigated the presence of C. burnetii in humans, sheep, and goats in the semi-arid region of northeastern Brazil. The presence of anti-C. burnetii antibodies was surveyed using indirect immunofluorescence assay, and detection of C. burnetii DNA was performed by polymerase chain reaction (PCR). Anti-C. burnetii antibodies were detected in 60% of farms, 4.8% of goats, 1.5% of sheep, and 4.5% of human samples. PCR was positive in 18.9% of blood samples, 7.7% of milk samples, and 7.7% of vaginal mucus samples. A DNA sequence of a C. burnetii DNA sample extracted from the goat vaginal mucus showed 99.2–99.4% nucleotide identity with other strains previously reported in Brazil. These results indicate that C. burnetii is present in the surveyed area, where it poses a risk to both public and animal health. These findings indicate an urgent need for educative actions to protect population, as well as better training of veterinarians to detect and report Q fever.
Similar content being viewed by others
References
Bauer AE, Hubbard KRA, Johnson AJ, Messick JB, Weng HY, Pogranichniy RM (2016) A cross sectional study evaluating the prevalence of Coxiella burnetii, potential risk factors for infection, and agreement between diagnostic methods in goats in Indiana. Prev Vet Med 126:131–137. https://doi.org/10.1016/j.prevetmed.2016.01.026
Abdel-Moein KA, Hamza DA (2018) Rat as an overlooked reservoir for Coxiella burnetii: a public health implication. Comp Immunol Microbiol Infect Dis 61:30–33. https://doi.org/10.1016/j.cimid.2018.11.002
Angelakis E, Raoult D (2010) Q fever. Vet Microbiol 140:297–309. https://doi.org/10.1016/j.vetmic.2009.07.016
Eldin C, Mélenotte C, Mediannikov O, Ghigo E, Million M, Edouard S, Mege JL, Maurin M, Raoult D (2017) From Q fever to Coxiella burnetii infection: a paradigm change. Clin Microbiol Rev 30:115–190. https://doi.org/10.1128/CMR.00045-16
Guatteo R, Beaudeau F, Berri M, Rodolakis A, Joly A, Seegers H (2006) Shedding routes of Coxiella burnetii in dairy cows: implications for detection and control. Vet Res 37:827–833. https://doi.org/10.1051/vetres:2006038
Todkill D, Fowler T, Hawker JI (2018) Estimating the incubation period of acute Q fever, a systematic review. Epidemiol Infect 146:665–672. https://doi.org/10.1017/S095026881700303X
Gale P, Kelly L, Mearns R, Duggan J, Snary EL (2015) Q fever through consumption of unpasteurised milk and milk products – A risk profile and exposure assessment. J Appl Microbiol 118:1083–1095. https://doi.org/10.1111/jam.12778
Astobiza I, Barral M, Ruiz-Fons F, Barandika JF, Gerrikagoitia X, Hurtado A, García-Pérez AL (2011) Molecular investigation of the occurrence of Coxiella burnetii in wildlife and ticks in an endemic area. Vet Microbiol 147:190–194. https://doi.org/10.1016/j.vetmic.2010.05.046
Cooper A, Stephens J, Ketheesan N, Govan B (2013) Detection of Coxiella burnetii DNA in wildlife and ticks in Northern Queensland, Australia. Vector Borne Zoonotic Dis 13:12–16. https://doi.org/10.1089/vbz.2011.0853
Pacheco RC, Echaide IE, Alves RN, Beletti ME, Nava S, Labruna MB (2013) Coxiella burnetii in ticks, Argentina. Emerg Infect Dis 19:344–346. https://doi.org/10.3201/eid1902.120362
Miller HK, Priestley RA, Kersh GJ (2021) Q fever: a troubling disease and a challenging diagnosis. Clin Microbiol Newsl 43:109–118. https://doi.org/10.1016/j.clinmicnews.2021.06.003
Nusinovici S, Frössling J, Widgren S, Beaudeau F, Lindberg A (2015) Q fever infection in dairy cattle herds: increased risk with high wind speed and low precipitation. Epidemiol Infect 143:3316–3326. https://doi.org/10.1017/S0950268814003926
Instituto Brasileiro de Geografia e Estatística (2019) SIDRA – Sistema de recuperação automática. https://sidra.ibge.gov.br/pesquisa/ppm/quadros/brasil/2019. Accessed 21 Dec 2023
Castro RLP, Brito DRB, Ribeiro MC, Costa JVD, Pires Filho PCS (2022) Caracterização de pequenas criações de caprinos e ovinos da Ilha De São Luís. Rev Sítio Novo 6:30–41. https://doi.org/10.47236/2594-7036.2022.v6.i1.30-41p
Ministério da Agricultura Pecuária e Abastecimento (2013) Instrução Normativa N° 50. https://www.in.gov.br/materia/-/asset_publisher/Kujrw0TZC2Mb/content/id/31061237/do1-2013-09-25-instrucao-normativa-n-50-de-24-de-setembro-de-2013-31061233. Accessed 21 Dec 2023
Ministério da Saúde (2014) Portaria N° 1 271de 6 de junho de 2014. https://bvsms.saude.gov.br/bvs/saudelegis/gm/2014/prt1271_06_06_2014.html. Accessed 21 Dec 2023
Souza EAR, Castro EMS, Oliveira GMB, Azevedo SS, Peixoto RM, Labruna MB, Horta MC (2018) Serological diagnosis and risk factors for Coxiella burnetii in goats and sheep in a semi-arid region of Northeastern Brazil. Rev Bras Parasitol Vet 27:514–520. https://doi.org/10.1590/S1984-296120180086
Instituto Brasileiro de Geografia e Estatística (2021) Panorama e pesquisa – Município Petrolina. https://cidades.ibge.gov.br/brasil/pe/petrolina/panorama. Accessed 21 Dec 2023
Reeves WK, Loftis AD, Sanders F, Spinks MD, Wills W, Denison AM, Dasch GA (2006) Borrelia, Coxiella and Rickettsia in Carios capensis (Acari: Argasidae) from a brown pelican (Pelecanus occidentalis) rookery in South Carolina, USA. Exp Appl Acarol 39:321–329. https://doi.org/10.1007/s10493-006-9012-7
Guimarães MF, Araujo AC, Freire DP, Machado DMR, Martins NNVM, Moraes-Filho J, Horta MC (2017) Investigação sorológica De Rickettsia rickettsii E Coxiella burnetii em caprinos e ovinos no entorno do Parque Nacional Da Serra das Confusões, Piauí. Pesq Vet Bras 37:555–560. https://doi.org/10.1590/S0100-736X2017000600004
Mares-Guia MAMM, Rozental T, Guterres A, Ferreira MS, Botticini RG, Terra AKC, Marraschi S, Bochner R, Lemos ERS (2016) Molecular identification of Q fever in patients with a suspected diagnosis of dengue in Brazil in 2013–2014. Am J Trop Med Hyg 94:1090–1094. https://doi.org/10.4269/ajtmh.15-0575
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98
Tamura K, Stecher G, Kumar S (2021) MEGA 11: Molecular Evolutionary Genetics Analysis. Version 11. Mol Biol Evol 38:3022–3027. https://doi.org/10.1093/molbev/msab120
Hosmer DW, Lemeshow S (2000) Applied Logistic Regression. Second Edition. New York: John Wiley & Sons. https://doi.org/10.1002/0471722146
Anderson A, Bijlmer H, Fournier PE, Graves S, Hartzell J, Kersh GJ, Limonard G, Marrie TJ, Massung RF, McQuiston JH, Nicholson WL, Paddock CD, Sexton DJ (2013) Diagnosis and management of Q fever - United States, 2013: Recommendations from CDC and the Q fever working group. MMWR Recomm Rep 62:1–30. https://www.cdc.gov/mmwr/preview/mmwrhtml/rr6203a1.htm. Accessed 21 Dec 2023
The Center for Food Security and Public Health (2017) Q fever. https://www.cfsph.iastate.edu/Factsheets/pdfs/q_fever.pdf. Accessed 21 Dec 2023
Rodolakis A, Berri M, Héchard C, Caudron C, Souriau A, Bodier CC, Blanchard B, Camuset P, Devillechaise P, Natorp JC, Vadet JP, Arricau-Bouvery N (2007) Comparison of Coxiella burnetii shedding in milk of dairy bovine, caprine, and ovine herds. J Dairy Sci 90:5352–5360. https://doi.org/10.3168/jds.2006-815
Instituto Brasileiro de Geografia e Estatística (2017) Censo agropecuário. https://cidades.ibge.gov.br/brasil/pe/petrolina/pesquisa/24/76693. Accessed 21 Dec 2023
Aragão BB, Trajano SC, Silva JG, Oliveira JMB, Santos AS, Melo RPB, Peixoto RM, Mota RA (2020) Avaliação Da contaminação Por Staphylococcus aureus em queijo coalho artesanal elaborado com leite de cabra produzido no estado de Pernambuco. Arq Bras Med Vet Zootec 72:615–622. https://doi.org/10.1590/1678-4162-10723
de Mioni SR, Ribeiro MSR, Peres BLD, Teixeira MG, Pelícia WSR, Motta VC, Labruna RG, Ribeiro MB, Sidi-Boumedine MG, Megid K J (2019) Real-time quantitative PCR-based detection of Coxiella burnetii in unpasteurized cow’s milk sold for human consumption. Zoonoses Public Health 66:695–700. https://doi.org/10.1111/zph.12609
Mares-Guia MAMM, Rozental T, Guterres A, Gomes R, Almeida DN, Moreira NS, Barreira JD, Favacho AR, Santana AL, Lemos ERS (2014) Molecular identification of the agent of Q fever – Coxiella burnetii – in domestic animals in state of Rio De Janeiro, Brazil. Rev Soc Bras Med Trop 47:231–234. https://doi.org/10.1590/0037-8682-0076-2013
Centers for Disease Control and Prevention (2019) Q fever. https://www.cdc.gov/qfever/healthcare-providers/index.html. Accessed 21 Dec 2023
Mioni MSR, Sidi-Boumedine K, Dalanezi FM, Joaquim SF, Denadai S, Teixeira WSR, Labruna MB, Megid J (2020b) New genotypes of Coxiella burnetii circulating in Brazil and Argentina. Pathogens 9:30. https://doi.org/10.3390/pathogens9010030
Santos GB, Gomes IMMG, Silveira JAG, Pires LCSR, Azevedo SS, Antonelli AC, Ribeiro MFB, Horta MC (2017) Tristeza Parasitária em bovinos do semiárido pernambucano. Pesq Vet Bras 37:1–7. https://doi.org/10.1590/S0100-736X2017000100001
Duron O, Sidi-Boumedine K, Rousset E, Moutailler S, Jourdain E (2015) The importance of Ticks in Q Fever transmission: what has (and has not. Been Demonstrated? Trends Parasitol 31:536–552. https://doi.org/10.1016/j.pt.2015.06.014
Coelho MCSC, Souza VC, Coelho MIS, Cunha MPD, Medina FT (2011) Aspectos sanitários de rebanhos caprinos e ovinos criados em assentamentos no município de Petrolina-PE. Rev Semiárido Visu 1:32–40. https://doi.org/10.31416/rsdv.v1i1.207
Alves AR, Vilela MS, Andrade MVM, Pinto LS, Lima DB, Lima LLL (2017) Caracterização do sistema de produção caprino e ovino na região Sul do Estado do Maranhão, Brasil. Vet Zootec 24:515–524. https://doi.org/10.35172/rvz.2017.v24.287
da Costa PSG, Brigatte ME, Greco DB (2005) Antibodies to Rickettsia rickettsii, Rickettsia typhi, Coxiella burnetii, Bartonella henselae, Bartonella quintana, and Ehrlichia chaffeensis among healthy population in Minas Gerais, Brazil. Mem Inst Oswaldo Cruz 100:853–859. https://doi.org/10.1590/S0074-02762005000800006
Costa PSG, Brigatte ME, Greco DB (2006) Questing one Brazilian query: reporting 16 cases of Q fever from Minas Gerais, Brazil. Rev Inst Med Trop Sao Paulo 48:5–9. https://doi.org/10.1590/S0036-46652006000100002
Lamas CC, Rozental T, Bóia MN, Favacho AR, Kirsten AH, da Silva AP, de Lemos ER (2009) Seroprevalence of Coxiella burnetii antibodies in human immunodeficiency virus-positive patients in Jacarepaguá, Rio De Janeiro, Brazil. ESCMID 15:140–141. https://doi.org/10.1111/j.1469-0691.2008.02144.x
Rozental T, Silva ASVD, Oliveira RC, Favacho ARM, Oliveira MLA, Bastos FI, Lemos ERS (2018) Seroprevalence of Bartonella spp., Coxiella burnetii, and Hantavirus among people who inject drugs in Rio de Janeiro, Brazil: A retrospective assessment of a biobank. Rev Inst Med Trop Sao Paulo 60:e31. https://doi.org/10.1590/S1678-9946201860031
Brandão H, Vale LAR, Christovão DA (1953) Investigações sobre a febre Q em São Paulo – I – Estudo sorológico em operários de um frigorífico. Arq Fac Hig Saúde Publ Univ S Paulo 7:127–131. https://doi.org/10.11606/issn.2358-792X.v7i1p127-131
Valle LAR, Brandão H, Christovão DDA, D’Apice M (1955) Investigações sobre a febre Q em São Paulo – II – Estudo em tratadores de gado e em bovinos. Arquivo Da Faculdade De Higiene Saúde E pública Da Universidade De São Paulo. Arq Fac Hig Saúde Pública Univ São Paulo 9:167–180. https://doi.org/10.11606/issn.2358-792X.v9i1-2p167-180
Siciliano RF, Castelli JB, Mansur AJ, Pereira dos Santos F, Colombo S, do Nascimento EM, Paddock CD, Brasil RA, Velho PE, Drummond MR, Grinberg M, Strabelli TM (2015) Bartonella spp. and Coxiella burnetii associated with community-acquired, culture-negative endocarditis, Brazil. Emerg Infect Dis 21:1429–1432. https://doi.org/10.3201/eid2108.140343
Meurer IR, Silva MR, Silva MVF, Duré AIL, Adelino Ter CAVB, Vanelli CP, Guimarães RJPS, Rozental T, Lemos ERS, Corrêa JOA (2021) Seroprevalence estimate and risk factors for Coxiella burnetii infections among humans in a highly urbanised Brazilian state. Trans R Soc Trop Med Hyg 0:1–9. https://doi.org/10.1093/trstmh/trab113
Siciliano RF, Ribeiro HB, Furtado RHM, Castelli JB, Sampaio RO, Santos FCP, Colombo S, Grinberg M, Strabelli TMV (2008) Endocardite Por Coxiella burnetii (febre Q). Doença Rara Ou Pouco Diagnosticada? Relato De Caso. Rev Soc Bras Med Trop 41:409–412. https://doi.org/10.1590/S0037-86822008000400017
de Oliveira JMB, Rozental T, de Lemos ERS, Forneas D, Ortega-Mora LM, Porto WJN, da Fonseca Oliveira AA, Mota RA (2018) Coxiella burnetii in dairy goats with a history of reproductive disorders in Brazil. Acta Trop 183:19–22. https://doi.org/10.1016/j.actatropica.2018.04.010
Zanatto DCS, Gatto IRH, Labruna MB, Jusi MMG, Samara SI, Machado RZ, André MR (2019) Coxiella burnetii associated with BVDV (Bovine Viral Diarrhea Virus), BoHV (Bovine herpesvirus), Leptospira spp., Neospora caninum, Toxoplasma gondii and Trypanosoma vivax in reproductive disorders in cattle. Rev Bras Parasitol Vet 28:245–257. https://doi.org/10.1590/S1984-29612019032
Mioni MSR, Costa FB, Ribeiro BLD, Teixeira WSR, Pelicia VC, Labruna MB, Rousset É, Sidi-Boumedine K, Thiéry R, Megid J (2020) Coxiella burnetii in slaughterhouses in Brazil: a public health concern. PLoS ONE 15:e0241246. https://doi.org/10.1371/journal.pone.0241246
Mioni MSR, Henker LC, Teixeira WSR, Lorenzett MP, Labruna MB, Pavarini SP, Driemeier D, Rousset É, Sidi-Boumedine K, Thiéry R, Megid J (2022) Molecular detection of Coxiella burnetii in aborted bovine fetuses in Brazil. Acta Trop 227:106258. https://doi.org/10.1016/j.actatropica.2021.106258
Pereira MF, Mota RA, Peixoto RM, Piatti RM (2013) Estudo De casos de aborto em caprinos e ovinos no estado de Pernambuco, Brasil. Cien Vet Nos Trópicos 16:18–30
Gazzonis AL, Alvarez Garcia G, Zanzani SA, Ortega Mora LM, Invernizzi A, Manfredi MT (2016) Neospora caninum infection in sheep and goats from north-eastern Italy and associated risk factors. Small Rumin Res 140:7–12. https://doi.org/10.1016/j.smallrumres.2016.05.010
Acknowledgements
The authors would like to thank Anna Maria C.F. Evaristo and José E.S. Rocha for their help with field work; Marlene L. S. Peixoto from Secretaria Municipal de Saúde de Petrolina; and the Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco (FACEPE) for providing financial support to Eline A.R. de Souza (IBPG-1014-5.05/17). M.B.L. and M.C.H. are recipients of research fellowships from CNPq (grant numbers 301641/2019-6 and 314019/2021-9, respectively).
Author information
Authors and Affiliations
Contributions
Eline Almeida Rodrigues de Souza: Conceptualization, Methodology, Writing - original draft, Writing - review & editing. Ila Ferreira de Farias: Methodology, Writing - original draft. Tainã Ramos Pesqueira: Methodology, Writing - original draft. Maria Carolina de Azevedo Serpa: Methodology. Thaís Souza Cunha: Methodology. Elenice Andrade de Moraes: Methodology, Writing - review & editing. Paulo Eduardo Brandão: Methodology, Writing - review & editing.
Marcelo Bahia Labruna: Conceptualization, Methodology, Resources, Writing - original draft, Writing - review & editing. Mauricio Claudio Horta: Conceptualization, Methodology, Resources, Writing - original draft, Writing - review & editing.
Corresponding author
Ethics declarations
Competing Interests
All authors declare that they have no known competing financial interests or personal relationships that could have influenced the work reported in this study.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Responsible Editor: David Germano Gonçalves Schwarz
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
de Souza, E.A.R., Farias, I.F., Pesqueira, T.R. et al. Exposure of small ruminants and humans to Coxiella burnetii in the semi-arid region of Northeastern Brazil. Braz J Microbiol (2024). https://doi.org/10.1007/s42770-024-01317-x
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s42770-024-01317-x