First Insight into the Prevalence of Coxiella burnetii Infection among Veterinary Medicine Students in Bulgaria
Abstract
:1. Introduction
2. Materials and Methods
2.1. Target Population and Sample Collection
2.2. Case Definition
2.3. Serological Tests
2.4. PCR Assay
2.5. Statistical Analysis
2.6. Ethical Considerations
3. Results
3.1. Characterization of the Study Population
3.2. Serology and PCR Analysis
3.3. Molecular Analysis
3.4. Relative Risk Assessment of Q Fever Exposure
4. Discussion
- Experimental animals in veterinary laboratories/farms must be placed in separate rooms;
- Pregnant infected animals (sheep, goats, cows, etc.) should not be used for practical student work;
- Mandatory biosafety procedures must be strictly followed in the microbiological and biomedical laboratories of Faculties of Veterinary Medicine;
- Placentas, aborted fetuses, other birth products and waste must be buried deeply using appropriate personal protective equipment (PPE); also, do not permit the eating of placenta by animals;
- Infectious waste must be sterilized and disposed at a specialized facility;
- All working surfaces must be disinfected against bodily fluids and animal dust;
- Wearing respiratory protective equipment and gloves is essential while handling animals when giving birth or in case of miscarriage.
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Eldin, C.; Melenotte, C.; Mediannikov, O.; Ghigo, E.; Million, M.; Edouard, S.; Mege, J.L.; Maurin, M.; Raoult, D. From Q fever to Coxiella burnetii infection: A paradigm change. Clin. Microbiol. Rev. 2017, 30, 115–190. [Google Scholar] [CrossRef] [PubMed]
- Angelakis, E.; Raoult, D. Q fever. Vet. Microbiol. 2010, 140, 297–309. [Google Scholar] [CrossRef] [PubMed]
- Ullah, Q.; Jamil, T.; Saqib, M.; Iqbal, M.; Neubauer, H. Q fever—A neglected zoonosis. Microorganisms 2022, 10, 1530. [Google Scholar] [CrossRef] [PubMed]
- Hurtado, A.; Zendoia, I.I.; Alonso, E.; Beraza, X.; Bidaurrazaga, J.; Ocabo, B.; Arrazola, I.; Cevidanes, A.; Barandika, J.F.; Garcia-Perez, A.L. A Q fever outbreak among visitors to a natural cave, Bizkaia, Spain, December 2020 to October 2021. Euro Surveill. 2023, 28, 2200824. [Google Scholar] [CrossRef] [PubMed]
- Melenotte, C.; Protopopescu, C.; Million, M.; Edouard, S.; Carrieri, M.P.; Eldin, C.; Angelakis, E.; Djossou, F.; Bardin, N.; Fournier, P.E.; et al. Clinical features and complications of Coxiella burnetii infections from the French national reference center for Q Fever. JAMA Netw. Open. 2018, 1, e181580. [Google Scholar] [CrossRef] [PubMed]
- Winter, F.; Campe, A. Q fever expertise among human and veterinary health professionals in Germany—A stakeholder analysis of knowledge gaps. PLoS ONE 2022, 17, e0264629. [Google Scholar] [CrossRef] [PubMed]
- Negru, A.R.; Popescu, C.; Radulescu, M.; Lobodan, A.; Lapadat, I.; Gliga, S.; Dulama, R.; Cristea, D.; Arama, V. Coxiella burnetii endocarditis–A real threat in the context of Q fever re-emergence. BMC Infect. Dis. 2014, 14 (Suppl. S7), P32. [Google Scholar] [CrossRef]
- Sulyok, K.M.; Kreizinger, Z.; Hornstra, H.M.; Pearson, T.; Szigeti, A.; Dan, A.; Balla, E.; Keim, P.S.; Gyuranecz, M. Genotyping of Coxiella burnetii from domestic ruminants and human in Hungary: Indication of various genotypes. BMC Vet. Res. 2014, 10, 107. [Google Scholar] [CrossRef] [PubMed]
- Genova-Kalou, P.; Vladimirova, N.; Stoitsova, S.; Krumova, S.; Kurchatova, A.; Kantardjiev, T. Q fever in Bulgaria: Laboratory and epidemiological findings on human cases and outbreaks, 2011 to 2017. Euro Surveill. 2019, 24, 1900119. [Google Scholar] [CrossRef] [PubMed]
- Guatteo, R.; Seegers, H.; Taurel, A.F.; Joly, A.; Beaudeau, F. Prevalence of Coxiella burnetii infection in domestic ruminants: A critical review. Vet. Microbiol. 2011, 149, 1–16. [Google Scholar] [CrossRef] [PubMed]
- Rodolakis, A. Q fever, state of art: Epidemiology, diagnosis and prophylaxis. Small Rumin. Res. 2006, 62, 121–124. [Google Scholar] [CrossRef]
- Abdel-Moein, K.A.; Zaher, H.M. Parturient cat as a potential reservoir for Coxiella burnetii: A hidden threat to pet owners. Vector Borne Zoonotic Dis. 2021, 21, 264–268. [Google Scholar] [CrossRef] [PubMed]
- Agerholm, J.S. Coxiella burnetii associated reproductive disorders in domestic animals—A critical review. Acta Vet. Scand. 2013, 55, 13. [Google Scholar] [CrossRef] [PubMed]
- Parker, N.R.; Barralet, J.H.; Bell, A.M. Q fever. Lancet 2006, 367, 679–688. [Google Scholar] [CrossRef] [PubMed]
- Marrie, T.J. Coxiella burnetii (Q fever) pneumonia. Clin. Infect. Dis. 1995, 21 (Suppl. S3), S253–S264. [Google Scholar] [CrossRef] [PubMed]
- Maurin, M.; Raoult, D. Q fever. Clin. Microbiol. Rev. 1999, 12, 518–553. [Google Scholar] [CrossRef] [PubMed]
- Fenollar, F.; Fournier, P.E.; Carrieri, M.P.; Habib, G.; Messana, T.; Raoult, D. Risks factors and prevention of Q fever endocarditis. Clin. Infect. Dis. 2001, 33, 312–316. [Google Scholar] [CrossRef] [PubMed]
- Bernit, E.; Pouget, J.; Janbon, F.; Dutronc, H.; Martinez, P.; Brouqui, P.; Raoult, D. Neurological involvement in acute Q fever: A report of 29 cases and review of the literature. Arch. Intern. Med. 2002, 162, 693–700. [Google Scholar] [CrossRef] [PubMed]
- Mori, M.; Mertens, K.; Cutler, S.J.; Santos, A.S. Critical aspects for detection of Coxiella burnetii. Vector Borne Zoonotic Dis. 2017, 17, 33–41. [Google Scholar] [CrossRef] [PubMed]
- Meekelenkamp, J.C.; Schneeberger, P.M.; Wever, P.C.; Leenders, A.C. Comparison of ELISA and indirect immunofluorescent antibody assay detecting Coxiella burnetii IgM phase II for the diagnosis of acute Q fever. Eur. J. Clin. Microbiol. Infect. Dis. 2012, 31, 1267–1270. [Google Scholar] [CrossRef] [PubMed]
- Mertens, K.; Gerlach, C.; Neubauer, H.; Henning, K. Q fever–An update. Curr. Clin. Microbiol. Rep. 2017, 4, 61–70. [Google Scholar] [CrossRef]
- Lepidi, H.; Houpikian, P.; Liang, Z.; Raoult, D. Cardiac valves in patients with Q fever endocarditis: Microbiological, molecular, and histologic studies. J. Infect. Dis. 2003, 187, 1097–1106. [Google Scholar] [CrossRef] [PubMed]
- Sahu, R.; Rawool, D.B.; Vinod, V.K.; Malik, S.V.S.; Barbuddhe, S.B. Current approaches for the detection of Coxiella burnetii infection in humans and animals. J. Microbiol. Methods 2020, 179, 106087. [Google Scholar] [CrossRef] [PubMed]
- Anderson, A.; Bijlmer, H.; Fournier, P.E.; Graves, S.; Hartzell, J.; Kersh, G.J.; Limonard, G.; Marrie, T.J.; Massung, R.F.; McQuiston, J.H.; et al. Diagnosis and management of Q fever–United States, 2013: Recommendations from CDC and the Q fever working group. MMWR Recomm. Rep. 2013, 62, 1–30, Erratum in MMWR Recomm. Rep. 2013, 62, 730. [Google Scholar] [PubMed]
- Dupuis, G.; Peter, O.; Peacock, M.; Burgdorfer, W.; Haller, E. Immunoglobulin responses in acute Q fever. J. Clin. Microbiol. 1985, 22, 484–487. [Google Scholar] [CrossRef] [PubMed]
- Sukocheva, O.A.; Marmion, B.P.; Storm, P.A.; Lockhart, M.; Turra, M.; Graves, S. Long-term persistence after acute Q fever of non-infective Coxiella burnetii cell components, including antigens. QJM 2010, 103, 847–863. [Google Scholar] [CrossRef] [PubMed]
- Raoult, D.; Marrie, T.; Mege, J. Natural history and pathophysiology of Q fever. Lancet Infect. Dis. 2005, 5, 219–226. [Google Scholar] [CrossRef] [PubMed]
- McQuiston, J.H.; Childs, J.E. Q fever in humans and animals in the United States. Vector Borne Zoonotic Dis. 2002, 2, 179–191. [Google Scholar] [CrossRef] [PubMed]
- Groten, T.; Kuenzer, K.; Moog, U.; Hermann, B.; Maier, K.; Boden, K. Who is at risk of occupational Q fever: New insights from a multi-profession cross-sectional study. BMJ Open 2020, 10, e030088. [Google Scholar] [CrossRef] [PubMed]
- Whitney, E.A.; Massung, R.F.; Candee, A.J.; Ailes, E.C.; Myers, L.M.; Patterson, N.E.; Berkelman, R.L. Seroepidemiologic and occupational risk survey for Coxiella burnetii antibodies among US veterinarians. Clin. Infect. Dis. 2009, 48, 550–557. [Google Scholar] [CrossRef] [PubMed]
- Palkhade, R.; Mishra, S.; Barbuddhe, S. Occupation-related biological health hazards and infection control practices among Indian veterinarians. Vet. Med. Int. 2022, 2022, 2503399. [Google Scholar] [CrossRef] [PubMed]
- Conan, A.; Gallagher, C.A.; Erskine, N.; Howland, M.; Smith-Anthony, M.; Marchi, S.; Magouras, I.; Muller, A.; Becker, A.A.M.J. Is there a higher risk of exposure to Coxiella burnetii for pre-clinical veterinary students? One Health 2023, 16, 100485. [Google Scholar] [CrossRef] [PubMed]
- Riemann, H.P.; Brant, P.C.; Franti, C.E.; Reis, R.; Buchanan, A.M.; Stormont, C.; Behymer, D.E. Antibodies to Toxoplasma gondii and Coxiella burnetii among students and other personnel in veterinary colleges in California and Brazil. Am. J. Epidemiol. 1974, 100, 197–208. [Google Scholar] [CrossRef] [PubMed]
- Dorko, E.; Kalinova, Z.; Pilipcinec, E. Seroprevalence of Coxiella burnetii antibodies among students of the Faculty of Medicine in Kosice (Slovakia). Folia Microbiol. (Praha) 2008, 53, 563–568. [Google Scholar] [CrossRef] [PubMed]
- de Lange, M.M.A.; van der Hoek, W.; Schneeberger, P.M.; Swart, A.; Heederik, D.J.J.; Schimmer, B.; Wouters, I.M. High Coxiella burnetii seroconversion rate in veterinary students, the Netherlands, 2006–2010. Emerg. Infect. Dis. 2020, 26, 3086–3088. [Google Scholar] [CrossRef] [PubMed]
- de Rooij, M.M.; Schimmer, B.; Versteeg, B.; Schneeberger, P.; Berends, B.R.; Heederik, D.; van der Hoek, W.; Wouters, I.M. Risk factors of Coxiella burnetii (Q fever) seropositivity in veterinary medicine students. PLoS ONE 2012, 7, e32108. [Google Scholar] [CrossRef] [PubMed]
- Khalili, M.; Qorbani, A.; Sharifi, H.; Golchin, M. Prevalence and risk factor of Q fever among veterinary students in Iran. Trop. Biomed. 2015, 32, 704–709. [Google Scholar] [PubMed]
- Valencia, M.C.; Rodriguez, C.O.; Punet, O.G.; de Blas Giral, I. Q fever seroprevalence and associated risk factors among students from the Veterinary School of Zaragoza, Spain. Eur. J. Epidemiol. 2000, 16, 469–476. [Google Scholar] [CrossRef] [PubMed]
- Gutierrez-Bautista, J.F.; Tarrino, M.; Gonzalez, A.; Olivares Duran, M.J.; Cobo, F.; Reguera, J.A.; Rodriguez-Granger, J.; Sampedro, A. Comparison of an enzyme linked-immunosorbent assay and a chemiluminescent immunoassay with an immunofluorescence assay for detection of phase II IgM and IgG antibodies to Coxiella burnetii. Microorganisms 2024, 12, 552. [Google Scholar] [CrossRef] [PubMed]
- Hoover, T.A.; Vodkin, M.H.; Williams, J.C. A Coxiella burnetii repeated DNA element resembling a bacterial insertion sequence. J. Bacteriol. 1992, 174, 5540–5548. [Google Scholar] [CrossRef] [PubMed]
- Berri, M.; Laroucau, K.; Rodolakis, A. The detection of Coxiella burnetii from ovine genital swabs, milk and fecal samples by the use of a single touchdown polymerase chain reaction. Vet. Microbiol. 2000, 72, 285–293. [Google Scholar] [CrossRef] [PubMed]
- Khalili, M.; Naderi, H.R.; Salehnia, N.; Abiri, Z. Detection of Coxiella burnetii in acute undifferentiated febrile illnesses (AUFIs) in Iran. Trop. Doct. 2016, 46, 221–224. [Google Scholar] [CrossRef] [PubMed]
- Lobato, L.; Bethony, J.M.; Pereira, F.B.; Grahek, S.L.; Diemert, D.; Gazzinelli, M.F. Impact of gender on the decision to participate in a clinical trial: A cross-sectional study. BMC Public Health 2014, 14, 1156. [Google Scholar] [CrossRef] [PubMed]
- Ergonul, O.; Zeller, H.; Kilic, S.; Kutlu, S.; Kutlu, M.; Cavusoglu, S.; Esen, B.; Dokuzoguz, B. Zoonotic infections among veterinarians in Turkey: Crimean-Congo hemorrhagic fever and beyond. Int. J. Infect. Dis. 2006, 10, 465–469. [Google Scholar] [CrossRef] [PubMed]
- Bernard, H.; Brockmann, S.O.; Kleinkauf, N.; Klinc, C.; Wagner-Wiening, C.; Stark, K.; Jansen, A. High seroprevalence of Coxiella burnetii antibodies in veterinarians associated with cattle obstetrics, Bavaria, 2009. Vector Borne Zoonotic Dis. 2012, 12, 552–557. [Google Scholar] [CrossRef] [PubMed]
- Van den Brom, R.; Schimmer, B.; Schneeberger, P.M.; Swart, W.A.; van der Hoek, W.; Vellema, P. Seroepidemiological survey for Coxiella burnetii antibodies and associated risk factors in Dutch livestock veterinarians. PLoS ONE 2013, 8, e54021. [Google Scholar] [CrossRef] [PubMed]
- Fenga, C.; Gangemi, S.; De Luca, A.; Calimeri, S.; Lo Giudice, D.; Pugliese, M.; Licitra, F.; Alibrandi, A.; Costa, C. Seroprevalence and occupational risk survey for Coxiella burnetii among exposed workers in Sicily, Southern Italy. Int. J. Occup. Med. Environ. Health 2015, 28, 901–907. [Google Scholar] [CrossRef] [PubMed]
- Verso, M.G.; Vesco, G.; Villari, S.; Galluzzo, P.; Gargano, V.; Matranga, D.; De Marchis, P.; Picciotto, D. Analysis of seroprevalence against Coxiella burnetii in a sample of farm workers in Western Sicily. Ann. Agric. Environ. Med. 2016, 23, 71–74. [Google Scholar] [CrossRef] [PubMed]
- Dal Pozzo, F.; Martinelle, L.; Leonard, P.; Renaville, B.; Renaville, R.; Thys, C.; Smeets, F.; Czaplicki, G.; Van Esbroeck, M.; Saegerman, C. Q fever serological survey and associated risk factors in veterinarians, Southern Belgium, 2013. Transbound. Emerg. Dis. 2017, 64, 959–966. [Google Scholar] [CrossRef] [PubMed]
- Tiscione, E.; Ademollo, B.; Donato, R.; Roller, S.; Signorini, L.F. Prevalence of antibodies against Coxiella burnetii in 2 geographical zones of Tuscany Article in Italian. Ann. Ig. 1989, 1, 1133–1143. [Google Scholar] [PubMed]
- Pascual Velasco, F.; Otero Ferrio, I.; Borobio Enciso, M.V. Prevalence of antibodies against Coxiella burnetii in a healthy population in Lanzarote (Canary Islands) Article in Spanish. An. Med. Interna 1991, 8, 233–234. [Google Scholar] [PubMed]
- McCaughey, C.; McKenna, J.; McKenna, C.; Coyle, P.V.; O’Neill, H.J.; Wyatt, D.E.; Smyth, B.; Murray, L.J. Human seroprevalence to Coxiella burnetii (Q fever) in Northern Ireland. Zoonoses Public Health 2008, 55, 189–194. [Google Scholar] [CrossRef] [PubMed]
- Brandwagt, D.A.; Herremans, T.; Schneeberger, P.M.; Hackert, V.H.; Hoebe, C.J.; Paget, J.; van Der Hoek, W. Waning population immunity prior to a large Q fever epidemic in the South of the Netherlands. Epidemiol. Infect. 2016, 144, 2866–2872. [Google Scholar] [CrossRef] [PubMed]
- Weitzel, T.; Lopez, J.; Acosta-Jamett, G.; Edouard, S.; Parola, P.; Abarca, K. Absence of convincing evidence of Coxiella burnetii infection in Chile: A cross-sectional serosurvey among healthy adults in four different regions. BMC Infect. Dis. 2016, 16, 541. [Google Scholar] [CrossRef] [PubMed]
- Neare, K.; Janson, M.; Hutt, P.; Lassen, B.; Viltrop, A. Coxiella burnetii antibody prevalence and risk factors of infection in the human population of Estonia. Microorganisms 2019, 7, 629. [Google Scholar] [CrossRef] [PubMed]
- Jaubert, J.; Naze, F.; Camuset, G.; Larrieu, S.; Pascalis, H.; Guernier, V.; Naty, N.; Bertolotti, A.; Manaquin, R.; Mboussou, Y.; et al. Seroprevalence of Coxiella burnetii (Q fever) exposure in humans on Reunion Island. Open Forum Infect. Dis. 2019, 6, ofz227. [Google Scholar] [CrossRef] [PubMed]
- Kersh, G.J.; Fitzpatrick, K.; Pletnikoff, K.; Brubaker, M.; Bruce, M.; Parkinson, A. Prevalence of serum antibodies to Coxiella burnetii in Alaska native persons from the Pribilof Islands. Zoonoses Public Health 2020, 67, 89–92. [Google Scholar] [CrossRef] [PubMed]
- Dragan, A.L.; Voth, D.E. Coxiella burnetii: International pathogen of mystery. Microbes Infect. 2020, 22, 100–110. [Google Scholar] [CrossRef] [PubMed]
- Borawski, K.; Dunaj, J.; Pancewicz, S.; Krol, M.; Czupryna, P.; Moniuszko-Malinowska, A. Coxiella burnetii and Q fever—A review. Przegl. Epidemiol. 2020, 74, 43–48. [Google Scholar] [CrossRef] [PubMed]
- Abeykoon, A.M.H.; Clark, N.J.; Soares Magalhaes, R.J.; Vincent, G.A.; Stevenson, M.A.; Firestone, S.M.; Wiethoelter, A.K. Coxiella burnetii in the environment: A systematic review and critical appraisal of sampling methods. Zoonoses Public Health 2021, 68, 165–181. [Google Scholar] [CrossRef] [PubMed]
- Zendoia, I.I.; Barandika, J.F.; Hurtado, A.; Lopez, C.M.; Alonso, E.; Beraza, X.; Ocabo, B.; Garcia-Perez, A.L. Analysis of environmental dust in goat and sheep farms to assess Coxiella burnetii infection in a Q fever endemic area: Geographical distribution, relationship with human cases and genotypes. Zoonoses Public Health 2021, 68, 666–676. [Google Scholar] [CrossRef] [PubMed]
- Van den Brom, R.; van Engelen, E.; Roest, H.I.; van der Hoek, W.; Vellema, P. Coxiella burnetii infections in sheep or goats: An opinionated review. Vet. Microbiol. 2015, 181, 119–129. [Google Scholar] [CrossRef] [PubMed]
- Robi, D.T.; Demissie, W.; Temteme, S. Coxiellosis in livestock: Epidemiology, public health significance, and prevalence of Coxiella burnetii infection in Ethiopia. Vet. Med. 2023, 14, 145–158. [Google Scholar] [CrossRef] [PubMed]
- Espana, P.P.; Uranga, A.; Cilloniz, C.; Torres, A. Q fever (Coxiella burnetii). Semin. Respir. Crit. Care Med. 2020, 41, 509–521. [Google Scholar] [CrossRef] [PubMed]
- Gale, P.; Kelly, L.; Mearns, R.; Duggan, J.; Snary, E.L. Q fever through consumption of unpasteurised milk and milk products—A risk profile and exposure assessment. J. Appl. Microbiol. 2015, 118, 1083–1095. [Google Scholar] [CrossRef] [PubMed]
- Basanisi, M.G.; La Bella, G.; Nobili, G.; Raele, D.A.; Cafiero, M.A.; Coppola, R.; Damato, A.M.; Fraccalvieri, R.; Sottili, R.; La Salandra, G. Detection of Coxiella burnetii DNA in sheep and goat milk and dairy products by droplet digital PCR in South Italy. Int. J. Food Microbiol. 2022, 366, 109583. [Google Scholar] [CrossRef] [PubMed]
- Yessinou, R.E.; Katja, M.S.; Heinrich, N.; Farougou, S. Prevalence of Coxiella-infections in ticks—Review and meta-analysis. Ticks Tick Borne Dis. 2022, 13, 101926. [Google Scholar] [CrossRef] [PubMed]
- Muhammad, K.A.; Gadzama, U.N.; Onyiche, T.E. Distribution and prevalence of Coxiella burnetii in animals, humans, and ticks in Nigeria: A systematic review. Infect. Dis. Rep. 2023, 15, 576–588. [Google Scholar] [CrossRef] [PubMed]
- Roest, H.I.; Bossers, A.; van Zijderveld, F.G.; Rebel, J.M. Clinical microbiology of Coxiella burnetii and relevant aspects for the diagnosis and control of the zoonotic disease Q fever. Vet. Q. 2013, 33, 148–160. [Google Scholar] [CrossRef] [PubMed]
- Melenotte, C.; Million, M.; Raoult, D. New insights in Coxiella burnetii infection: Diagnosis and therapeutic update. Expert Rev. Anti Infect. Ther. 2020, 18, 75–86. [Google Scholar] [CrossRef] [PubMed]
- Husin, N.A.; AbuBakar, S.; Khoo, J.J. Current tools for the diagnosis and detection of spotted fever group Rickettsia. Acta Trop. 2021, 218, 105887. [Google Scholar] [CrossRef] [PubMed]
- Ross, C.; Morrow, P.S. Q fever: An issue in occupational health & safety? An overview of the methods of control and the effects of Coxiella burnetii on the human host. J. R. Soc. Health 1994, 114, 151–152. [Google Scholar] [CrossRef] [PubMed]
- Egberink, H.; Addie, D.; Belak, S.; Boucraut-Baralon, C.; Frymus, T.; Gruffydd-Jones, T.; Hartmann, K.; Hosie, M.J.; Lloret, A.; Lutz, H.; et al. Coxiellosis/Q fever in cats: ABCD guidelines on prevention and management. J. Feline Med. Surg. 2013, 15, 573–575. [Google Scholar] [CrossRef] [PubMed]
- Aitken, I.D. Clinical aspects and prevention of Q fever in animals. Eur. J. Epidemiol. 1989, 5, 420–424. [Google Scholar] [CrossRef] [PubMed]
City | Sex | IgM (−) | IgM (−) | IgM (+) | IgM (+) | IgM (+) | IgM (+) |
---|---|---|---|---|---|---|---|
IgG (−) | IgG (+) | IgG (−) | IgG (−) | IgG (+) | IgG (+) | ||
PCR (−) | PCR (−) | PCR (−) | PCR (+) | PCR (−) | PCR (+) | ||
Sofia | Males | 16 | 5 | - | - | - | - |
Females | 31 | 1 | 2 | 1 | 2 | 3 | |
Stara Zagora | Males | 19 | 15 | - | 1 | 2 | 1 |
Females | 64 | 7 | 8 | 4 | 2 | 1 |
Variables | Total, n | Exposed, n (%) | Unexposed, n (%) | Chi Square Statistics (df) | p-Value | Relative Risk (%) |
---|---|---|---|---|---|---|
Pooled Sex | ||||||
Males | 59 | 24 (40.6) | 35 (59.4) | 2.22 (1) | <0.05 | 41 |
Females | 126 | 31 (24.6) | 95 (75.4) | 25 | ||
Pooled Location | ||||||
Sofia | 61 | 14 (23.0) | 47 (77.0) | 4.00 (1) | <0.05 | 23 |
Stara Zagora | 124 | 41 (33.1) | 83 (66.9) | 33 | ||
Males | ||||||
Sofia | 21 | 5 (23.8) | 16 (76.2) | 3.89 (1) | <0.05 | 24 |
Stara Zagora | 38 | 19 (50.0) | 19 (50.0) | 50 | ||
Females | ||||||
Sofia | 40 | 9 (22.5) | 31 (77.5) | 0.14 (1) | >0.1 | 23 |
Stara Zagora | 86 | 22 (25.6) | 64 (74.4) | 26 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Genova-Kalou, P.; Hodzhev, Y.; Tsachev, I.; Pepovich, R.; Panaiotov, S.; Dobrinov, V.; Krumova, S.; Boneva-Marutsova, B.; Chakarova, B.; Todorova, K.; et al. First Insight into the Prevalence of Coxiella burnetii Infection among Veterinary Medicine Students in Bulgaria. Infect. Dis. Rep. 2024, 16, 794-805. https://doi.org/10.3390/idr16050061
Genova-Kalou P, Hodzhev Y, Tsachev I, Pepovich R, Panaiotov S, Dobrinov V, Krumova S, Boneva-Marutsova B, Chakarova B, Todorova K, et al. First Insight into the Prevalence of Coxiella burnetii Infection among Veterinary Medicine Students in Bulgaria. Infectious Disease Reports. 2024; 16(5):794-805. https://doi.org/10.3390/idr16050061
Chicago/Turabian StyleGenova-Kalou, Petia, Yordan Hodzhev, Ilia Tsachev, Roman Pepovich, Stefan Panaiotov, Veselin Dobrinov, Stefka Krumova, Betina Boneva-Marutsova, Borislava Chakarova, Keytlin Todorova, and et al. 2024. "First Insight into the Prevalence of Coxiella burnetii Infection among Veterinary Medicine Students in Bulgaria" Infectious Disease Reports 16, no. 5: 794-805. https://doi.org/10.3390/idr16050061