Seroprevalence of Coxiella burnetii in an Indigenous Population from the Sierra Nevada De Santa Marta, Colombia

Regina Oakley Swiss Tropical and Public Health Institute, Allschwil, Switzerland;
University of Basel, Basel, Switzerland;

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Anou Dreyfus Swiss Tropical and Public Health Institute, Allschwil, Switzerland;
University of Basel, Basel, Switzerland;
Vetsuisse Faculty, University of Zürich, Zurich, Switzerland;
Institut Pasteur, Antananarivo, Madagascar;

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Gustavo Concha Organización Wiwa Yugumaiun Bunkuanarua Tairona, Valledupar, Colombia;

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Sven Poppert Swiss Tropical and Public Health Institute, Allschwil, Switzerland;

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Michèle Plag Swiss Tropical and Public Health Institute, Allschwil, Switzerland;

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Celine Meile Swiss Tropical and Public Health Institute, Allschwil, Switzerland;
Rothen Medizinische Laboratorien AG, Basel, Switzerland;

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Stephen Graves Australian Rickettsial Reference Laboratory, Geelong, Victoria, Australia;

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Daniel H. Paris Swiss Tropical and Public Health Institute, Allschwil, Switzerland;
University of Basel, Basel, Switzerland;

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Simone Kann medmissio Institute for Global Health, Würzburg, Germany

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ABSTRACT.

Coxiella burnetii is an underreported zoonotic pathogen in many rural regions globally. We investigated C. burnetii exposure in a remote indigenous tribe residing in the Sierra Nevada de Santa Marta, Colombia. The high seroprevalence of 35% (95% CI, 27–43%) demonstrates the need for One Health studies to identify risk factors, clinical impact, and potential medical, veterinary, and environmental interventions.

Coxiella burnetii, the causative agent of Q fever, presents acutely with flu-like symptoms, often including pneumonia and acute hepatitis, and cannot be readily distinguished from other etiologies, both bacterial and viral.1 Q fever fatigue syndrome is a complication associated with a state of prolonged fatigue (> 6 months), with musculoskeletal and other symptoms in about 20% of patients.2

Chronic Q fever occurs in 1% to 5% of patients after acute infection and can result in endocarditis, chronic vascular infections, osteomyelitis, chronic pulmonary infections, and chronic hepatitis.1 Patients with valvular heart disease, a vascular graft, or an arterial aneurysm or who are pregnant or immunocompromised are at higher risk of developing chronic Q fever.1

Coxiella burnetii is an obligate intracellular bacterium reported as having a global distribution, except in New Zealand.1 Human infection is associated with animal contact, particularly with livestock, and with living in rural areas. Ruminants (cattle, sheep, and goats) represent the main reservoir that infect humans, but C. burnetii has also been detected in other domestic mammals, wildlife, marine mammals, birds, and reptiles and in over 40 tick species, the latter being the likely primary reservoir.1

The Wiwa are an indigenous tribe residing in the Sierra Nevada de Santa Marta, Colombia, with limited contact with the outside world or medical services. A high proportion of zoonotic diseases was expected in this population because they live in close contact with livestock and slaughter animals, use traditional agricultural methods (top dressing), and have simple houses (clay huts, palm roofs, unsealed floors), poor sanitation, limited access to clean drinking water (rivers, unprotected wells), and low socioeconomic status.3 This study aimed to determine the seroprevalence of C. burnetii in Wiwa communities in Colombia.

This cross-sectional study included a subset of 150 Wiwa participants from a research program on Chagas disease and emerging infectious diseases (including tick-borne diseases).3 The sample size for C. burnetii seroprevalence determination was calculated using epitools.4 Considering a precision of 0.05, a confidence of 0.95, and an estimated C. burnetii seroprevalence of 10% (based on studies in healthy individuals), it was calculated that a sample size of 139 participants was required.5,6

Participants were aged 2 to 80 years, with a median (interquartile range [IQR]) age of 13 years (7–34 years), with 50% being female. Written informed consent was obtained from participants (legal guardians for children), or a witnessed thumbprint was obtained for illiterate participants. Serum samples were randomly selected and stratified by village: Tezhumake (n = 46) of the Department of Cesar, and Ashintuwa (n = 30), Cherua (n = 31), and Seminke (n = 43) of the Department of La Guajira.

The studies were performed in accordance with the principles of the Declaration of Helsinki and were approved by the Ethics Committee of the Tropical Health Foundation Santa Marta, Colombia (Acta Number 032018). Ethical approval and authorization to perform the study were also granted by the Governors of the Wiwa and Kogius communities with permission to enter their territory.

Serological testing was performed at the Swiss Tropical and Public Health Institute, Basel, Switzerland. The serum samples were tested with an immunofluorescence assay (IFA) for IgG phase I/II and IgM phase I/II (Fuller Laboratories, Fullerton, CA). Two independent readers scored the IFA slides. Antibody titers of ≥ 1:16 were considered positive.7 The manufacturers report the IFA assay to be both 100% sensitive and specific.

Data were recorded in Microsoft Excel (Microsoft Corp., Redmond, WA), and statistical analysis was performed using Stata/IC 16.1 (StataCorp, College Station, TX). Overall seropositivity, based on a composite endpoint, was 35% (n = 52; 95% CI, 27–43%), with IgG phase I and II seropositivities both at 21% (n = 31; 95% CI, 15–28%) and IgM phase I and II seropositivities at 15% (n = 22; 95% CI, 10–21%) and 17% (n = 25; 95% CI, 11–24%), respectively.

Univariable analysis was performed with IFA seropositivity as the outcome, with the explanatory variables sex, village, and age (Table 1). People living in Siminke were significantly (P value ≤ 0.05) less likely to be seropositive overall (odds ratio [OR] = 0.15; 95% CI, 0.04–0.48, P value = 0.001). Age was positively associated with overall seropositivity, with participants aged between 12 and 44 years (OR = 4.00; 95% CI, 1.77–8.87, P = 0.001) and ≥ 45 years (OR = 5.25; 95% CI, 1.73–15.95, P = 0.003) having increased odds of being seropositive compared with those aged between 0 and 11 years. Seropositivity for the individual antibodies also showed a statistically significant association with age. Participants aged between 12 and 44 years had increased odds of being seropositive for IgG phase I (OR = 5.18; 95% CI, 1.82–14.79, P = 0.002), IgG phase II (OR = 3.68; 95% CI, 1.36–9.95, P = 0.010), and IgM phase II (OR = 4.17; 95% CI, 1.30–13.36, P = 0.016). Similarly, participants aged > 44 years had increased odds of being seropositive for IgG phase I (OR = 4.14; 95% CI, 1.05–16.31, P = 0.042), IgG phase II (OR = 4.38; 95% CI, 1.22–15.80, P = 0.024), IgM phase I (OR = 6.81; 95% CI, 1.68–27.62, P = 0.007), and IgM phase II (OR = 6.81; 95% CI, 1.68–27.62, P = 0.007).

Table 1

Summary of associations between the explanatory variables and C. burnetii seropositivity in Wiwa people*

Explanatory variables Univariate analysis Multivariate analysis
Pos n/total N (%) OR 95% CI P value OR 95% CI P value
IgG phase I
 Sex (f) 17/75 (22.7) 1.23 0.58–2.82 0.546 NA
 Village
  Tezuhmake 9/46 (19.6) Ref Ref
  Cherua 12/30 (40.0) 2.74 0.98–7.69 0.055 2.97 1.02–8.67 0.047
  Ashintukwa 10/31 (32.3) 1.96 0.69–5.58 0.209 2.72 0.89–8.34 0.079
  Siminke 0/43 (0.0) Omitted Omitted
 Age (years)
  0–11 5/63 (7.9) Ref Ref
  12–44 21/68 (30.9) 5.18 1.82–14.79 0.002 4.77 1.53–14.84 0.007
  ≥ 45 5/19 (26.3) 4.14 1.05–16.31 0.042 3.49 0.81–15.05 0.094
IgG phase II
 Sex (f) 17/75 (22.7) 1.28 0.58–2.82 0.546 NA
 Village
  Tezuhmake 10/46 (21.7) Ref Ref
  Cherua 11/30 (36.7) 2.08 0.75–5.79 0.159 2.21 0.77–6.29 0.139
  Ashintukwa 10/31 (32.3) 1.71 0.61–4.79 0.304 2.20 0.75–6.50 0.152
  Siminke 0/43 (0.0) Omitted Omitted
 Age (years)
  0–11 6/63 (9.5) Ref Ref
  12–44 19/68 (27.9) 3.68 1.36–9.95 0.010 3.13 1.07–9.16 0.037
  ≥ 45 6/19 (31.6) 4.38 1.22–15.80 0.024 3.58 0.91–14.16 0.069
IgM phase I
 Sex (f) 15/75 (20.0) 2.43 0.93–6.36 0.071 2.76 1.01–7.53 0.047
 Village
  Tezuhmake 8/46 (17.4) Ref NA
  Cherua 3/30 (10.0) 0.53 0.13–2.17 0.376
  Ashintukwa 7/31 (22.6) 1.39 0.44–4.31 0.574
  Siminke 4/43 (9.3) 0.49 0.14–1.75 0.271
 Age (years)
  0–11 4/63 (6.3) Ref Ref
  12–44 12/68 (17.6) 3.16 0.96–10.38 0.058 3.22 0.97–10.71 0.056
  ≥ 45 6/19 (31.6) 6.81 1.68–27.62 0.007 7.93 1.88–33.45 0.005
IgM phase II
 Sex (f) 17/75 (22.7) 2.45 0.99–6.10 0.053 2.76 1.07–7.14 0.036
 Village
  Tezuhmake 9/46 (19.6) Ref NA
  Cherua 4/30 (13.3) 0.63 0.18–2.28 0.483
  Ashintukwa 8/31 (25.8) 1.43 0.48–4.23 0.518
  Siminke 4/43 (9.3) 0.42 0.12–1.49 0.179
 Age (years)
  0–11 4/63 (6.3) Ref Ref
  12–44 15/68 (22.1) 4.17 1.30–13.36 0.016 4.30 1.33–13.96 0.015
  ≥ 45 6/19 (31.6) 6.81 1.68–27.62 0.007 7.93 1.89–33.40 0.005
Overall
 Sex (f) 28/75 (37.3) 1.27 0.65–2.48 0.493 NA
 Village
  Tezuhmake 19/46 (41.3) Ref Ref
  Cherua 13/30 (43.3) 1.09 0.43–2.76 0.861 1.13 0.43–2.98 0.805
  Ashintukwa 16/31 (51.6) 1.52 0.61–3.79 0.374 2.11 0.78–5.71 0.141
  Siminke 4/43 (9.3) 0.15 0.04–0.48 0.001 0.20 0.06–0.67 0.010
 Age (years)
  0–11 11/63 (17.5) Ref Ref
  12–44 31/68 (45.6) 4.00 1.77–8.87 0.001 3.75 1.55–9.04 0.003
  ≥ 45 10/19 (52.6) 5.25 1.73–15.95 0.003 4.67 1.42–15.41 0.011

f = female; NA = not applicable; Pos = positive; Ref = reference.

Univariable logistic regression analysis was performed for the association between explanatory variables (sex, village of residence, and age) and the following outcomes: C. burnetii seropositivity in IgG phase I and IgG phase II and overall C. burnetii seropositivity (for any isotype) in the Wiwa people. A multivariable logistic regression model was used for the association between the explanatory variables (village of residence and age) and the outcomes C. burnetii overall seropositivity, C. burnetii IgG phase I positivity, and C. burnetii IgG phase II positivity and the explanatory variables (village of residence and sex) and the outcomes C. burnetii IgM phase I positivity and C. burnetii IgM phase II positivity. The immunofluorescence assay was considered positive at a titer cutoff of ≥ 1:16. Statistically significant variables (P value ≤ 0.05) are highlighted in bold.

Overall = participants that tested positive for at least one of the four antibodies included.

For the outcomes of IgG phase I and II and overall seropositivity, the model of best fit for the multivariable analysis included “village” and “age” (likelihood ratio test), whereas the model of best fit for IgM phase I and II included “sex” and “age” (Table 1). Lower odds of overall seropositivity (OR = 0.20; 95% CI, 0.06–0.67, P = 0.010) were still seen for participants living in Siminke, whereas those living in Cherua had increased odds of being seropositive for IgG phase I (OR = 2.97; 95% CI, 1.02–8.67, P = 0.047). Age was again positively associated with seropositivity, with the age group of 12 to 44 years having increased odds for IgG phase I (OR = 4.77; 95% CI, 1.53–14.84, P = 0.007), IgG phase II (OR = 3.13; 95% CI 1.07–9.16, P = 0.037), IgM phase II (OR = 4.30; 95% CI, 1.33–13.96, P = 0.015), and overall seropositivity (OR = 4.00; 95% CI, 1.77–8.87, P = 0.001). Increased odds were also observed for the ≥ 45-year age group for IgM phase I (OR = 7.93; 95% CI, 1.88–33.45, P = 0.005), IgM phase II (OR = 7.93; 95% CI, 1.88–33.45, P = 0.005), and overall seropositivity (OR = 4.67; 95% CI, 1.42–15.41, P = 0.011). Women had increased odds of being seropositive for IgM phase I (OR = 2.76; 95% CI, 1.01–7.53, P = 0.047) and phase II (OR = 2.76; 95% CI, 1.07–7.14, P = 0.036).

Our study is the first to report C. burnetii exposure in the Wiwa population, providing evidence of an underappreciated risk of Q fever in these remote communities. Further, current transmission of C. burnetii is indicated by the detection of IgM antibodies. Q fever is not a reportable disease in Colombia and is likely to be underreported nationally.8 Because Q fever was first reported in Colombia in the 1970s, only limited studies focusing on livestock and people with occupational exposure are available.812 These studies found that 25.9% of farmers and 19.5% of their cattle were positive for C. burnetii DNA, and additional serological studies reported exposure in farmers of 31.9%, in slaughterhouse workers of 54%, and in cattle from 27.1% to 60%.1012 One study in small ruminants reported C. burnetii DNA in 6% of sheep’s milk and 0.6% of vaginal swabs from goats.9 Risk factors associated with seropositivity to C. burnetii identified in other studies in Colombian farming communities included tick bites, working with cattle, consuming raw milk products, livestock slaughtering, and keeping hens.12

Previous C. burnetii cases reported from Colombia were linked to endocarditis and pneumonia, which may be fatal for remote communities with limited access to health care.13,14 Approximately 1% to 5% of acute cases develop chronic disease, from which the 35% seroprevalence in our study population (n = 150) can be extrapolated to mean as many as 17 chronic Q fever cases per 1,000 indigenous people in this region.1

The study had the following limitations. No clinical or risk factor data linked to C. burnetii transmission were available for these samples, so the study does not indicate how often seroconversion was associated with actual illness rather than asymptomatic seroconversion, often seen with C. burnetii exposure. The sample size calculation was based on an anticipated seroprevalence of 10%, but we found a much higher seroprevalence. Although this may limit the interpretation of the logistic regression analysis, for the seroprevalence estimate, we calculated the 95% CI (27–43). Our conclusions would be unaffected by a true estimate at either the lower or upper limit of this range.

Here we have presented the first evidence of C. burnetii exposure in the Wiwa people living in the Sierra Nevada de Santa Marta. Comprehensive One Health and fever studies are warranted to identify and characterize C. burnetii in humans, livestock, and ticks located in this region. Determining the true clinical significance and transmission routes of C. burnetii is essential to best guide public health policies on targeted interventions to improve the health of these remote communities.

REFERENCES

  • 1.

    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: 115190.

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  • 2.

    Morroy G , Keijmel SP , Delsing CE , Bleijenberg G , Langendam M , Timen A , Bleeker-Rovers CP , 2016. Fatigue following acute Q-fever: a systematic literature review. PLoS One 11: e0155884.

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  • 3.

    Dreyfus A et al., 2022. Comparison of the Serion IgM ELISA and microscopic agglutination test for diagnosis of Leptospira spp. infections in sera from different geographical origins and estimation of Leptospira seroprevalence in the Wiwa indigenous population from Colombia. PLoS Negl Trop Dis 16: e0009876.

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    Sergeant ESG , 2018. Epitools Epidemiological Calculators. Available at: http://epitools.ausvet.com.au. Accessed February 7, 2022.

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    Costa PSGd , 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: 853859.

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    Tshokey T , Stenos J , Durrheim DN , Eastwood K , Nguyen C , Graves SR , 2017. Seroprevalence of rickettsial infections and Q fever in Bhutan. PLoS Negl Trop Dis 11: e0006107.

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    Noden BH , Tshavuka FI , van der Colf BE , Chipare I , Wilkinson R , 2014. Exposure and risk factors to Coxiella burnetii, spotted fever group and typhus group rickettsiae, and Bartonella henselae among volunteer blood donors in Namibia. PLoS One 9: e108674.

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    Mattar S , Contreras V , González M , Camargo F , Álvarez J , Oteo JA , 2014. Coxiella burnetii infection in a patient from a rural area of Monteria, Colombia. Rev Salud Publica (Bogota) 16: 958961.

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    Contreras V , Gonzalez M , Alvarez J , Mattar S , 2018. Coxiella burnetii infection in sheep and goats: a public risk health, Colombia. Infectio 22: 173177.

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    Cabrera Orrego R , Ríos-Osorio LA , Keynan Y , Rueda ZV , Gutiérrez LA , 2020. Molecular detection of Coxiella burnetii in livestock farmers and cattle from Magdalena Medio in Antioquia, Colombia. PLoS One 15: e0234360.

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    de Ruiz HL , 1977. Q fever in Colombia, S.A. A serological survey of human and bovine populations. Zentralbl Veterinarmed B 24: 287292.

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    Eraso-Cadena MP , Molina-Guzmán LP , Cardona X , Cardona-Arias JA , Ríos-Osorio LA , Gutierrez-Builes LA , 2018. Serological evidence of exposure to some zoonotic microorganisms in cattle and humans with occupational exposure to livestock in Antioquia, Colombia. Cad Saude Publica 34: e00193617.

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    Betancur CA , Múnera AG , 2012. Endocarditis por Coxiella burnetii: fiebre Q. Acta Med Colomb 37: 3133.

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    Meza-Cardona JC , Rosso-Suàrez F , 2012. Neumonía por Coxiella burnetii: presentación de un caso y revisión de la literatura. CES Medicina 26: 201207.

Author Notes

Financial support: This project was funded by Else Kröner-Fresenius-Stiftung (grant number 2019_HA163) and the Stanley Thomas Johnson Foundation (grant number 1053-KF).

Authors’ addresses: Regina Oakley and Daniel H. Paris, Swiss Tropical and Public Health Institute, Allschwil, Switzerland, and University of Basel, Basel, Switzerland, E-mails: regina.oakley@swisstph.ch and daniel.paris@swisstph.ch. Anou Dreyfus, Vetsuisse Faculty, University of Zürich, Zurich, Switzerland, E-mail: anoudreyfus@outlook.com. Gustavo Concha, Organización Wiwa Yugumaiun Bunkuanarua Tairona, Valledupar, Colombia, E-mail: gustavoconcha16@gmail.com. Sven Poppert and Michèle Plag, Swiss Tropical and Public Health Institute, Allschwil, Switzerland, E-mails: sven@poppert.eu and michele.plag@swisstph.ch. Celine Meile, Rothen Medizinische Laboratorien AG, Basel, Switzerland, E-mail: celine.meile98@gmail.com. Stephen Graves, Australian Rickettsial Reference Laboratory, Geelong, Australia, E-mail: graves.Rickettsia@gmail.com. Simone Kann, medmissio Institute for Global Health, Würzburg, Germany, E-mail: simone_kann@hotmail.com.

Address correspondence to Daniel H. Paris, Swiss Tropical and Public Health Institute, Kreuzstrasse 2, 4123 Allschwil, Switzerland. E-mail: daniel.paris@swisstph.ch
  • 1.

    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: 115190.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2.

    Morroy G , Keijmel SP , Delsing CE , Bleijenberg G , Langendam M , Timen A , Bleeker-Rovers CP , 2016. Fatigue following acute Q-fever: a systematic literature review. PLoS One 11: e0155884.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3.

    Dreyfus A et al., 2022. Comparison of the Serion IgM ELISA and microscopic agglutination test for diagnosis of Leptospira spp. infections in sera from different geographical origins and estimation of Leptospira seroprevalence in the Wiwa indigenous population from Colombia. PLoS Negl Trop Dis 16: e0009876.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    Sergeant ESG , 2018. Epitools Epidemiological Calculators. Available at: http://epitools.ausvet.com.au. Accessed February 7, 2022.

    • PubMed
    • Export Citation
  • 5.

    Costa PSGd , 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: 853859.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    Tshokey T , Stenos J , Durrheim DN , Eastwood K , Nguyen C , Graves SR , 2017. Seroprevalence of rickettsial infections and Q fever in Bhutan. PLoS Negl Trop Dis 11: e0006107.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    Noden BH , Tshavuka FI , van der Colf BE , Chipare I , Wilkinson R , 2014. Exposure and risk factors to Coxiella burnetii, spotted fever group and typhus group rickettsiae, and Bartonella henselae among volunteer blood donors in Namibia. PLoS One 9: e108674.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8.

    Mattar S , Contreras V , González M , Camargo F , Álvarez J , Oteo JA , 2014. Coxiella burnetii infection in a patient from a rural area of Monteria, Colombia. Rev Salud Publica (Bogota) 16: 958961.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Contreras V , Gonzalez M , Alvarez J , Mattar S , 2018. Coxiella burnetii infection in sheep and goats: a public risk health, Colombia. Infectio 22: 173177.

  • 10.

    Cabrera Orrego R , Ríos-Osorio LA , Keynan Y , Rueda ZV , Gutiérrez LA , 2020. Molecular detection of Coxiella burnetii in livestock farmers and cattle from Magdalena Medio in Antioquia, Colombia. PLoS One 15: e0234360.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    de Ruiz HL , 1977. Q fever in Colombia, S.A. A serological survey of human and bovine populations. Zentralbl Veterinarmed B 24: 287292.

  • 12.

    Eraso-Cadena MP , Molina-Guzmán LP , Cardona X , Cardona-Arias JA , Ríos-Osorio LA , Gutierrez-Builes LA , 2018. Serological evidence of exposure to some zoonotic microorganisms in cattle and humans with occupational exposure to livestock in Antioquia, Colombia. Cad Saude Publica 34: e00193617.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Betancur CA , Múnera AG , 2012. Endocarditis por Coxiella burnetii: fiebre Q. Acta Med Colomb 37: 3133.

  • 14.

    Meza-Cardona JC , Rosso-Suàrez F , 2012. Neumonía por Coxiella burnetii: presentación de un caso y revisión de la literatura. CES Medicina 26: 201207.

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