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Coxiella burnetii abortion in a dairy farm selling artisanal cheese directly to consumers and review of Q fever as a bovine abortifacient in South America and a human milk-borne disease

  • Veterinary Microbiology - Review
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Abstract

Coxiella burnetii is a highly transmissible intracellular bacterium with a low infective dose that causes Q fever (coxiellosis), a notifiable zoonotic disease distributed worldwide. Livestock are the main source of C. burnetii transmission to humans, which occurs mostly through the aerogenous route. Although C. burnetii is a major abortifacient in small ruminants, it is less frequently diagnosed in aborting cattle. We report a case of C. burnetii abortion in a lactating Holstein cow from a dairy farm producing and selling artisanal cheese directly to consumers in Uruguay, and review the literature on coxiellosis as a bovine abortifacient in South America and as a milk-borne disease. The aborted cow had severe necrotizing placentitis with abundant intratrophoblastic and intralesional C. burnetii confirmed by immunohistochemistry and PCR. After primo-infection in cattle, C. burnetii remains latent in the lymph nodes and mammary glands, with milk being a significant and persistent excretion route. Viable C. burnetii has been found in unpasteurized milk and cheeses after several months of maturing. The risk of coxiellosis after the consumption of unpasteurized dairy products, including cheese, is not negligible. This report raises awareness on bovine coxiellosis as a potential food safety problem in on-farm raw cheese manufacturing and sales. The scant publications on abortive coxiellosis in cattle in South America suggest that the condition has probably gone underreported in all countries of this subcontinent except for Uruguay. Therefore, we also discuss the diagnostic criteria for laboratory-based confirmation of C. burnetii abortion in ruminants as a guideline for veterinary diagnosticians.

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References

  1. Arricau-Bouvery N, Rodolakis A (2005) Is Q fever an emerging or re-emerging zoonosis? Vet Res 36:327–349. https://doi.org/10.1051/vetres:2005010

    Article  CAS  PubMed  Google Scholar 

  2. OIE (2020) World Organization for Animal Health. OIE-Listed diseases, infections and infestations in force in 2020. https://www.oie.int/en/animal-health-in-the-world/oie-listed-diseases-2021/. Accessed 9 January 2021

  3. Grace D, Mutua F, Ochungo P, Kruska R, Jones K, Brierley L, Lapar L, Said M, Herrero M, Phuc PM, Thao NB, Akuku I, Ogutu F (2012) Mapping of poverty and likely zoonoses hotspots. Zoonoses Project 4. Report to the UK Department for International Development. Nairobi, Kenya: ILRI

  4. Roest HIJ, Tilburg JJHC, Van der Hoek W, Vellema P, Van Zijderveld FG, Klaassen CHW, Raoult D (2011) The Q fever epidemic in The Netherlands: history, onset, response and reflection. Epidemiol Infect 139(1):1–12. https://doi.org/10.1017/S0950268810002268

    Article  CAS  PubMed  Google Scholar 

  5. Bielawska-Drózd A, Cieslik P, Mirski T, Bartoszcze M, Knap JP, Gawel J, Zakowska D (2013) Q fever-selected issues. Ann Agr Environ Med 20(2):222–232

    Google Scholar 

  6. Bildfell RJ, Thomson GW, Haines DM, McEwen BJ, Smart N (2000) Coxiella burnetii infection is associated with placentitis in cases of bovine abortion. J Vet Diagn Invest 12(5):419–425. https://doi.org/10.1177/104063870001200505

    Article  CAS  PubMed  Google Scholar 

  7. Clothier K, Anderson M (2016) Evaluation of bovine abortion cases and tissue suitability for identification of infectious agents in California diagnostic laboratory cases from 2007 to 2012. Theriogenology 85(5):933–938. https://doi.org/10.1016/j.theriogenology.2015.11.001

    Article  CAS  PubMed  Google Scholar 

  8. Macías-Rioseco M, Riet-Correa F, Miller MM, Sondgeroth K, Fraga M, Silveira C, Uzal F, Giannitti F (2019) Bovine abortion caused by Coxiella burnetii: report of a cluster of cases in Uruguay and review of the literature. J Vet Diagn Invest 31:634–639. https://doi.org/10.1177/1040638719856394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Agerholm JS (2013) Coxiella burnetii associated reproductive disorders in domestic animals–a critical review. Acta Vet Scand 55:13. https://doi.org/10.1186/1751-0147-55-13

    Article  PubMed  PubMed Central  Google Scholar 

  10. Groten T, Kuenzer K, Moog U, Hermann B, Maier K, Boden K (2020) Who is at risk of occupational Q fever: new insights from a multi-profession cross-sectional study. BMJ Open 10(2). https://bmjopen.bmj.com/content/10/2/e030088

  11. van der Hoek W, Hogema BM, Dijkstra F, Rietveld A, Wijkmans CJ, Schneeberger PM, Zaaijer HL (2012) Relation between Q fever notifications and Coxiella burnetii infections during the 2009 outbreak in The Netherlands. Eurosurveillance 17(3):20058. https://doi.org/10.2807/ese.17.03.20058-en

    Article  PubMed  Google Scholar 

  12. Maurin M, Raoult D (1999) Q fever. Clin Microbiol Rev 12(4):518–553

    Article  CAS  Google Scholar 

  13. Somma-Moreira RE, Caffarena RM, Somma S, Pérez G, Monteiro M (1987) Analysis of Q fever in Uruguay. Rev Infect Dis 9(2):386–387. https://doi.org/10.1093/clinids/9.2.386

    Article  CAS  PubMed  Google Scholar 

  14. Eldin C, Mahamat A, Demar M, Abboud P, Djossou F, Raoult D (2014) Q fever in French Guiana. Am J Trop Med Hyg 91(4):771–776. https://doi.org/10.4269/ajtmh.14-0282

    Article  PubMed  PubMed Central  Google Scholar 

  15. Mares-Guia MAM, Rozental T, Guterres A, dos Santos FM, Botticini RDG, Terra AKC, Marraschi S, Bochner R, Lemos ER (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(5):1090–1094. https://doi.org/10.4269/ajtmh.15-0575

    Article  PubMed  PubMed Central  Google Scholar 

  16. de Lemos ERS, Rozental T, Siqueira BN, Júnior AAP, Joaquim TE, da Silva RG, de Andrade C, Alvarez A, Ferreira da Cunha M, Borghi DP (2018) Q Fever in military firefighters during cadet training in Brazil. Am J Trop Med Hyg 99(2):303–305. https://doi.org/10.4269/ajtmh.17-0979

    Article  PubMed  PubMed Central  Google Scholar 

  17. Echeverría G, Reyna-Bello A, Minda-Aluisa E, Celi-Erazo M, Olmedo L, García HA, García-Bereguiain MA, de Waard JH (2019) Serological evidence of Coxiella burnetii infection in cattle and farm workers: is Q fever an underreported zoonotic disease in Ecuador? Infect Drug Resist 12:701. https://doi.org/10.2147/IDR.S195940

    Article  PubMed  PubMed Central  Google Scholar 

  18. Tapia T, Stenos J, Flores R, Duery O, Iglesias R, Olivares MF, Gallegos D, Rosas C, Wood H, Acevedo J, Araya P, Graves S, Hormazabal JC (2020) Evidence of Q fever and rickettsial disease in Chile. Trop Med Infect Dis 5(2):99. https://doi.org/10.3390/tropicalmed5020099

    Article  PubMed Central  Google Scholar 

  19. Hernández S, Lyford-Pike V, Alvarez ME, Tomasina F (2007) Q fever outbreak in an experimental wildlife breeding station in Uruguay. J Trop Path 36(2):129–140. https://doi.org/10.5216/rpt.v36i2.1801

    Article  Google Scholar 

  20. Mares-Guia MAMDM, Rozental T, Guterres A, Gomes R, Almeida DND, Moreira NS, Dias-Barreira J, Rodrigues-Favacho A, Lopes-Santana A, Lemos ERSD (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(2):231–234. https://doi.org/10.1590/0037-8682-0076-2013

    Article  PubMed  Google Scholar 

  21. Tigertt WD, Benenson AS, Gochenour WS (1961) Airborne Q fever. Bacteriol Rev 25(3):285–293

    Article  CAS  Google Scholar 

  22. Guatteo R, Beaudeau F, Joly A, Seegers H (2007) Coxiella burnetii shedding by dairy cows. Vet Res 38:849–860. https://doi.org/10.1051/vetres:2007038

    Article  PubMed  Google Scholar 

  23. Barandika JF, Alvarez-Alonso R, Jado I, Hurtado A, García-Pérez AL (2019) Viable Coxiella burnetii in hard cheeses made with unpasteurized milk. Int J Food Microbiol 303:42–45. https://doi.org/10.1016/j.ijfoodmicro.2019.05.010

    Article  CAS  PubMed  Google Scholar 

  24. Krumbiegel ER, Wisniewski HJ (1970) II. Consumption of infected raw milk by human volunteers. Arch Environ Health: An Int J 21(1):63–65. https://pubmed.ncbi.nlm.nih.gov/5467889/

  25. Miller HK, Priestley RA, Kersh GJ (2020) Transmission of Coxiella burnetii by ingestion in mice. Epidemiol Infect 148:e21. https://doi.org/10.1017/S0950268820000059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Giannitti F, Anderson M, Miller M, Rowe J, Sverlow K, Vasquez M, Cantón G (2016) Chlamydia pecorum: fetal and placental lesions in sporadic caprine abortion. J Vet Diagn Invest 28(2):184–189. https://doi.org/10.1177/1040638715625729

    Article  CAS  PubMed  Google Scholar 

  27. Berri M, Rekiki A, Boumedine KS, Rodolakis A (2009) Simultaneous differential detection of Chlamydophila abortus, Chlamydophila pecorum and Coxiella burnetii from aborted ruminant’s clinical samples using multiplex PCR. BMC Microbiol 9(1):1–8. https://doi.org/10.1186/1471-2180-9-130

    Article  CAS  Google Scholar 

  28. Terzolo HR, Paolicchi A, Morelra AR, Homse A (1991) Skirrow agil for simultaneous isolation of Brucella and Campylobacter species. Vet Rec 129:531–532

    CAS  PubMed  Google Scholar 

  29. Zarantonelli L, Suanes A, Meny P et al (2018) Isolation of pathogenic Leptospira strains from naturally infected cattle in Uruguay reveals high serovar diversity, and uncovers a relevant risk for human leptospirosis. PLoS Negl Trop Dis 12(9):e0006694. https://doi.org/10.1371/journal.pntd.0006694

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Campero CM, Moore DP, Odeón AC, Cipolla AL, Odriozola E (2003) Aetiology of bovine abortion in Argentina. Vet Res Commun 27(5):359–369. https://doi.org/10.1023/a:1024754003432

    Article  CAS  PubMed  Google Scholar 

  31. Morrell E (2010) Caracterización diagnóstica de las causas infecciosas del aborto bovino. Dissertation, Universidad Nacional de La Plata. http://sedici.unlp.edu.ar/bitstream/handle/10915/1588/Documento_completo_en_baja_resoluci%C3%B3n.pdf?sequence=25&isAllowed=y

  32. Antoniassi NA, Juffo GD, Santos AS, Pescador CA, Corbellini LG, Driemeier D (2013) Causas de aborto bovino diagnosticadas no Setor de Patologia Veterinária da UFRGS de 2003 a 2011. Pesqui Vet Bras 33(2):155–160. https://doi.org/10.1590/S0100-736X2013000200004

    Article  Google Scholar 

  33. Corbellini LG, Pescador CA, Frantz F, Wunder E, Steffen D, Smith DR, Driemeier D (2006) Diagnostic survey of bovine abortion with special reference to Neospora caninum infection: importance, repeated abortion and concurrent infection in aborted fetuses in Southern Brazil. Vet J 172(1):114–120. https://doi.org/10.1016/j.tvjl.2005.03.006

    Article  PubMed  Google Scholar 

  34. Muskens J, Wouda W, von Bannisseht-Wijsmuller T, Van Maanen C (2012) Prevalence of Coxiella burnetii infections in aborted fetuses and stillborn calves. Vet Rec 170(10):260–260. https://doi.org/10.1136/vr.100378

    Article  CAS  PubMed  Google Scholar 

  35. Anderson ML (2007) Infectious causes of bovine abortion during mid-to late-gestation. Theriogenology 68(3):474–486. https://doi.org/10.1016/j.theriogenology.2007.04.001

    Article  PubMed  Google Scholar 

  36. Jensen TK, Montgomery DL, Jaeger PT, Lindhardt T, Agerholm JS, BIlle-Hansen V, Boye M (2007) Application of fluorescent in situ hybridisation for demonstration of Coxiella burnetii in placentas from ruminant abortions. APMIS 115(4):347–353. https://doi.org/10.1111/j.1600-0463.2007.apm_591.x

    Article  CAS  PubMed  Google Scholar 

  37. Rabaza A, Fraga M, Corbellini LG, Turner KM, Riet-Correa F, Eisler MC (2020) Molecular prevalence of Coxiella burnetii in bulk-tank milk from bovine dairy herds: systematic review and meta-analysis. One Health 12:100208. https://doi.org/10.1016/j.onehlt.2020.100208

    Article  PubMed  PubMed Central  Google Scholar 

  38. McQuiston JH, Childs JE, Thompson HA (2002) Q fever. J Am Vet Med A 221(6):796–799

    Article  Google Scholar 

  39. Rahal M, Tahir D, Eldin C, Bitam I, Raoult D, Parola P (2018) Genotyping of Coxiella burnetii detected in placental tissues from aborted dairy cattle in the north of Algeria. Comp Immunol Microbiol Infect Dis 57:50–54. https://doi.org/10.1016/j.cimid.2018.06.001

    Article  CAS  PubMed  Google Scholar 

  40. Frickmann H, Zautner AE, Moter A, Kikhney J, Hagen RM, Stender H, Poppert S (2017) Fluorescence in situ hybridization (FISH) in the microbiological diagnostic routine laboratory: a review. Crit Rev Microbiol 43(3):263–293. https://doi.org/10.3109/1040841X.2016.1169990

    Article  CAS  PubMed  Google Scholar 

  41. Aistleitner K, Jeske R, Wölfel R, Wießner A, Kikhney J, Moter A, Stoecker K (2018) Detection of Coxiella burnetii in heart valve sections by fluorescence in situ hybridization. J Med Microbiol 67(4):537–542. https://doi.org/10.1099/jmm.0.000704

    Article  CAS  PubMed  Google Scholar 

  42. Macías-Rioseco M, Silveira C, Fraga M, Casaux L, Cabrera A, Francia ME, Robello C, Zarantonelli L, Suanes A, Colina R, Buschiazzo A, Giannitti F, Riet-Correa F (2020) Causes of abortion in dairy cows in Uruguay. Pesqui Vet Bras 40(5):325–332. https://doi.org/10.1590/1678-5150-pvb-6550

    Article  Google Scholar 

  43. Easton C (2006) Estudio patológico de las principales causas infecciosas en el aborto bovino en Uruguay: identificación de la acción de agentes infecciosos vinculados con el aborto bovino. Dissertation, Universidad de la República

  44. Meyer L (2013) Estudio descriptivo de las principales causas de aborto bovino, diagnosticadas entre los años 1991 y 2010 en el Instituto de Patología Animal de la Universidad Austral de Chile. Dissertation, Universidad Austral de Chile

  45. de Souza Ribeiro Mioni M (2018) Sorologia e detecção molecular de Coxiella burnetii em bovinos no estado de São Paulo, Brasil. Dissertation, Universidade Estadual Paulista

  46. Changoluisa D, Rivera-Olivero IA, Echeverria G, Garcia-Bereguiain MA, De Waard JH (2019) Serology for Neosporosis, Q fever and Brucellosis to assess the cause of abortion in two dairy cattle herds in Ecuador. BMC Vet Res 15(1):1–5. https://doi.org/10.1186/s12917-019-1924-7

    Article  Google Scholar 

  47. Eldin C, Melenotte 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(1):115–190. https://doi.org/10.1128/CMR.00045-16

    Article  PubMed  Google Scholar 

  48. 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

    Article  CAS  PubMed  Google Scholar 

  49. Oyston PCF, Davies C (2011) Q fever: the neglected biothreat agent. J Med Microbiol 60(1):9–21. https://doi.org/10.1099/jmm.0.024778-0

    Article  CAS  PubMed  Google Scholar 

  50. Zubkova RI (1957) Survival of Rickettsia burnetii in milk and milk products. J Microbiol Epidemiol Immunobiol 28(9/10):1259–1263

    Google Scholar 

  51. Sting R, Molz K, Philipp W, Bothe F, Runge M, Ganter M (2013) Quantitative real-time PCR and phase specific serology are mutually supportive in Q fever diagnostics in goats. Vet Microbiol 167(3–4):600–608. https://doi.org/10.1016/j.vetmic.2013.09.015

    Article  CAS  PubMed  Google Scholar 

  52. Kim SG, Kim EH, Lafferty CJ, Dubovi E (2005) Coxiella burnetii in bulk tank milk samples United States. Emerg Infect Dis 11(4):619. https://doi.org/10.3201/eid1104.041036

    Article  PubMed  PubMed Central  Google Scholar 

  53. Piñero A, Barandika JF, Hurtado A, García-Pérez AL (2014) Evaluation of Coxiella burnetii status in dairy cattle herds with bulk-tank milk positive by ELISA and PCR. Transbound Emerg Dis 61(2):163–168. https://doi.org/10.1111/tbed.12013

    Article  CAS  PubMed  Google Scholar 

  54. Enright JB, Sadler WW, Thomas RC (1957) Pasteurization of milk containing the organism of Q fever. Am J Public Health Nations Health 47(6):695–700. https://doi.org/10.2105/ajph.47.6.695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Benson WW, Brock DW, Mather J (1963) Serologic analysis of a penitentiary group using raw milk from a Q fever infected herd. Public Health Rep 78(8):707. https://doi.org/10.2307/4591908

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Fishbein DB, Raoult D (1992) A cluster of Coxiella burnetii infections associated with exposure to vaccinated goats and their unpasteurized dairy products. Am J Trop Med Hyg 47:35–40. https://doi.org/10.4269/ajtmh.1992.47.35

    Article  CAS  PubMed  Google Scholar 

  57. Hatchette TF, Hudson RC, Schlech WF, Campbell NA, Hatchette JE, Ratnam S, Raoult D, Donovan C, Marrie TJ (2001) Goat-associated Q fever: a new disease in Newfoundland. Emerg Infect Dis 7:413–419. https://doi.org/10.3201/eid0703.017308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Maltezou HC, Constantopoulou I, Kallergi C, Vlahou V, Georgakopoulos D, Kafetzis DA, Raoult D (2004) Q fever in children in Greece. Am J Trop Med Hyg 70:540–544. https://doi.org/10.4269/ajtmh.2004.70.540

    Article  PubMed  Google Scholar 

  59. Signs KA, Stobierski MG (2011) Gandhi TN (2012) Q fever cluster among raw milk drinkers in Michigan. Clin Infect Dis 55(10):1387–1389. https://doi.org/10.1093/cid/cis690

    Article  Google Scholar 

  60. Brown GL, Colwell DC, Hooper WL (1968) An outbreak of Q fever in Staffordshire. Epidemiol Infect 66(4):649–655. https://doi.org/10.1017/S0022172400028382

    Article  CAS  Google Scholar 

  61. Eldin C, Angelakis E, Renvoisé A, Raoult D (2013) Coxiella burnetii DNA, but not viable bacteria, in dairy products in France. Am J Trop Med Hyg 88:765–769. https://doi.org/10.4269/ajtmh.12-0212

    Article  PubMed  PubMed Central  Google Scholar 

  62. Pearson T, Hornstra HM, Hilsabeck R et al (2014) High prevalence and two dominant host-specific genotypes of Coxiella burnetii in US milk. BMC Microbiol 14(1):1–9. https://doi.org/10.1186/1471-2180-14-41

    Article  CAS  Google Scholar 

  63. Rozental T, De Faria L, Forneas D, Guterrres A, Ribeiro JB, Aráujo FR, Lemos ERS, Silva MR (2020) First molecular detection of Coxiella burnetii in Brazilian artisanal cheese: a neglected food safety hazard in ready-to-eat raw-milk product. Braz J Infect Dis 24:208–212. https://doi.org/10.1016/j.bjid.2020.05.003

    Article  PubMed  Google Scholar 

  64. Loftis AD, Priestley RA, Massung RF (2010) Detection of Coxiella burnetii in commercially available raw milk from the United States. Foodborne Pathog Dis 7(12):1453–1456. https://doi.org/10.1089/fpd.2010.0579

    Article  PubMed  Google Scholar 

  65. Tilburg JJ, Roest HJI, Nabuurs-Franssen MH, Horrevorts AM, Klaassen CH (2012) Genotyping reveals the presence of a predominant genotype of Coxiella burnetii in consumer milk products. J Clin Microbiol 50:2156–2158. https://jcm.asm.org/content/50/6/2156

  66. Cornejo J, Araya P, Ibáñez D, Hormazabal JC, Retamal P, Fresno M, Herve LP, Lapierre L (2020) Identification of Coxiella burnetii in tank raw cow milk: first findings from Chile. Vector-Borne Zoonotic Dis 20(3):228–230. https://doi.org/10.1089/vbz.2019.2535

    Article  PubMed  Google Scholar 

  67. de Souza Ribeiro Mioni M, Ribeiro BLD, Peres MG, Teixeira WSR, Pelícia VC, Motta RG, Labruna MB, Ribeiro MG, Sidi-Boumedine K, Megid J (2019) Real-time quantitative PCR-based detection of Coxiella burnetii in unpasteurized cow’s milk sold for human consumption. Zoonoses Public Health 66(6):695–700. https://doi.org/10.1111/zph.12609

    Article  CAS  PubMed  Google Scholar 

  68. Contreras V, Máttar S, González M, Álvarez J, Oteo JA (2015) Coxiella burnetii in bulk tank milk and antibodies in farm workers at Montería, Colombia. Rev Colomb Cienc Pec 28(2):181–187. https://doi.org/10.17533/udea.rccp.v28n2a07

    Article  Google Scholar 

  69. Jerusalmi C, Camacho M, Mortorio M (2008) Estudio de caso: cluster quesería artesanal en San José y Colonia. Instituto de Competitividad, Universidad Católica del Uruguay. https://ucu.edu.uy/sites/default/files/facultad/fce/i_competitividad/cluster%20queseria.PDF Accessed 2 February 2021

  70. Yoon Y, Lee S, Choi KH (2016) Microbial benefits and risks of raw milk cheese. Food Control 63:201–215. https://doi.org/10.1016/j.foodcont.2015.11.013

    Article  CAS  Google Scholar 

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Acknowledgements

We are grateful to Yisell Perdomo and Cecilia Monesiglio from the “Plataforma de Investigación en Salud Animal” of INIA for their collaboration on the histologic and bacteriologic techniques, respectively. We also thank Karen Sverlow and Juliann Beingesser from CAHFS-UC Davis for technical assistance with the immunohistochemistry. We thank PhD Thomas Chisnall from the Animal and Plant Health Agency (APHA, UK), PhD David Longbottom and PhD Morag Livingstone from Moredun Research Institute (UK) for having kindly provided the positive controls for the duplex PCR. We thank PhD Leticia Zarantonelli from the “Unidad Mixta Pasteur-INIA” (UMPI, Uruguay) for providing the medium for Leptospira spp. culture.

Funding

This work was partially funded by grants FSSA_X_2014_1_105696 of the Uruguayan “Agencia Nacional de Investigación e Innovación” (ANII) and PL_027 N-23398 from the “Instituto Nacional de Investigación Agropecuaria” (INIA). The first author received a graduate scholarship POS_EXT_2015_1_123804 from ANII.

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Ana Rabaza conceptualized the study, conducted laboratory work, wrote the initial manuscript draft, reviewed, edited, and approved the manuscript. Melissa Macías-Rioseco conducted laboratory work, reviewed, edited, and approved the manuscript. Martín Fraga conducted laboratory work, reviewed, edited, and approved the manuscript. Francisco A. Uzal conducted laboratory work, reviewed, edited, and approved the manuscript. Mark C. Eisler reviewed, edited, and approved the manuscript. Franklin Riet-Correa acquired funding, reviewed, edited, and approved the manuscript. Federico Giannitti conceptualized the study, conducted laboratory work, acquired funding, wrote, reviewed, edited, and approved the manuscript.

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Correspondence to Federico Giannitti.

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Rabaza, A., Macías-Rioseco, M., Fraga, M. et al. Coxiella burnetii abortion in a dairy farm selling artisanal cheese directly to consumers and review of Q fever as a bovine abortifacient in South America and a human milk-borne disease. Braz J Microbiol 52, 2511–2520 (2021). https://doi.org/10.1007/s42770-021-00593-1

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