Exposure of South African Abattoir Workers to Coxiella burnetii
Abstract
:1. Introduction
2. Materials and Methods
3. Results
3.1. Participating Abattoir Workers
3.2. Coxiella burnetii Seroprevalence Estimates
3.3. Correlates of C. burnetii Seropositivity
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Raoult, D.; Marrie, T.; Mege, J. Natural History and Pathophysiology of Q Fever. Lancet Infect. Dis. 2005, 5, 219–226. [Google Scholar] [CrossRef]
- Eldin, C.; Mélenotte, 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] [Green Version]
- Schneeberger, P.M.; Wintenberger, C.; van der Hoek, W.; Stahl, J.P. Q Fever in the Netherlands 2007–2010: What We Learned from the Largest Outbreak Ever. Méd. Mal. Infect. 2014, 44, 339–353. [Google Scholar] [CrossRef] [PubMed]
- Cutler, S.J.; Bouzid, M.; Cutler, R.R. Q Fever. J. Infect. 2007, 54, 313–318. [Google Scholar] [CrossRef] [PubMed]
- Porter, S.R.; Czaplicki, G.; Mainil, J.; Guattéo, R.; Saegerman, C. Q Fever: Current State of Knowledge and Perspectives of Research of a Neglected Zoonosis. Int. J. Microbiol. 2011, 2011, 1–22. [Google Scholar] [CrossRef] [PubMed]
- Maurin, M.; Raoult, D. Q Fever. Clin. Microbiol. Rev. 1999, 12, 518–553. [Google Scholar] [CrossRef] [Green Version]
- Wielders, C.C.H.; Teunis, P.F.M.; Hermans, M.H.A.; van der Hoek, W.; Schneeberger, P.M. Kinetics of Antibody Response to Coxiella burnetii Infection (Q Fever): Estimation of the Seroresponse Onset from Antibody Levels. Epidemics 2015, 13, 37–43. [Google Scholar] [CrossRef] [Green Version]
- Wielders, C.C.H.; Boerman, A.W.; Schimmer, B.; van den Brom, R.; Notermans, D.W.; van der Hoek, W.; Schneeberger, P.M. Persistent High IgG Phase I Antibody Levels against Coxiella burnetii among Veterinarians Compared to Patients Previously Diagnosed with Acute Q Fever after Three Years of Follow-Up. PLoS ONE 2015, 10, e0116937. [Google Scholar] [CrossRef]
- Vanderburg, S.; Rubach, M.P.; Halliday, J.E.B.; Cleaveland, S.; Reddy, E.A.; Crump, J.A. Epidemiology of Coxiella burnetii Infection in Africa: A One Health Systematic Review. PLoS Negl. Trop. Dis. 2014, 8, e2787. [Google Scholar] [CrossRef]
- Frean, J.; Blumberg, L. Tick Bite Fever and Q Fever: A South African Perspective. S. Afr. Med. J. 2007, 97, 1198–1202. [Google Scholar]
- Salifu, S.P.; Bukari, A.R.A.; Frangoulidis, D.; Wheelhouse, N. Current Perspectives on the Transmission of Q Fever: Highlighting the Need for a Systematic Molecular Approach for a Neglected Disease in Africa. Acta Trop. 2019, 193, 99–105. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kelly, P.J.; Metthewman, L.A.; Mason, P.R.; Raoult, D. Q Fever in Zimbabwe: A Review of the Disease and the Results of a Serosurvey of Humans, Cattle, Goats and Dogs. SA Med. J. 1993, 83, 21–25. [Google Scholar]
- Gear, J.H.S.; Wolstenholme, B.; Cort, A. Q Fever: Serological Evidence of the Occurrence of a Case in South Africa. SA Med. J. 1950, 24, 409–411. [Google Scholar]
- Ranking, D.L. Q Fever: Serological Evidence of the Occurrence of Another Case in South Africa. SA Med. J. 1950, 24, 1006–1007. [Google Scholar]
- Gear, J.H.S.; Wolstenholme, B.; Miller, B.; Sher, B.; Schneider, J. Q Fever in South Africa. In Medicine in a Tropical Environment; A.A. Balkema: Cape Town, South Africa, 1977; pp. 471–478. [Google Scholar]
- Schutte, A.P.; Kurz, J.; Barnard, B.J.H.; Roux, D.J. Q Fever in Cattle and Sheep in Southern Africa: A Preliminary Report. Onderstepoort J. Vet. Res. 1976, 43, 129–132. [Google Scholar]
- Gummow, B.; Poerstamper, N.; Herr, S. The Incidence of Coxiella burnetii Antibodies in Cattle in the Transvaal. Onderstepoort J. Vet. Res. 1987, 54, 569–571. [Google Scholar]
- Simpson, G.J.G.; Quan, V.; Frean, J.; Knobel, D.L.; Rossouw, J.; Weyer, J.; Marcotty, T.; Godfroid, J.; Blumberg, L.H. Prevalence of Selected Zoonotic Diseases and Risk Factors at a Human-Wildlife-Livestock Interface in Mpumalanga Province, South Africa. Vector Borne Zoonotic Dis. 2018, 18, 303–310. [Google Scholar] [CrossRef]
- Derrick, E.H. The Epidemiology of Q Fever. J. Hyg. 1944, 43, 357–361. [Google Scholar] [CrossRef]
- Gidding, H.F.; Wallace, C.; Lawrence, G.L.; McIntyre, P.B. Australia’s National Q Fever Vaccination Program. Vaccine 2009, 27, 2037–2041. [Google Scholar] [CrossRef]
- O’Neill, T.J.; Sargeant, J.M.; Poljak, Z. The Effectiveness of Coxiella burnetii Vaccines in Occupationally Exposed Populations: A Systematic Review and Meta-Analysis. Zoonoses Public Health 2014, 61, 81–96. [Google Scholar] [CrossRef]
- 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] [Green Version]
- Massey, P.D.; Irwin, M.; Durrheim, D.N. Enhanced Q Fever Risk Exposure Surveillance May Permit Better Informed Vaccination Policy. CDI 2009, 33, 41–45. [Google Scholar] [PubMed]
- Schonell, M.E.; Brotherston, J.G.; Burnett, R.C.S.; Campbell, J.; Coghlan, J.D.; Moffat, M.A.J.; Norval, J.; Sutherland, J.A.W. Occupational Infections in the Edinburgh Abattoir. Br. Med. J. 1966, 2, 148–150. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Riemann, H.P.; Brant, P.C.; Behymer, D.E.; Franti, C.E. Toxoplasma Gondii and Coxiella Burnetii Antibodies among Brazilian Slaughterhouse Employees. Am. J. Epidemiol. 1975, 102, 386–393. [Google Scholar] [CrossRef] [PubMed]
- Esmaeili, S.; Naddaf, S.R.; Pourhossein, B.; Hashemi Shahraki, A.; Bagheri Amiri, F.; Gouya, M.M.; Mostafavi, E. Seroprevalence of Brucellosis, Leptospirosis, and Q Fever among Butchers and Slaughterhouse Workers in South-Eastern Iran. PLoS ONE 2016, 11, e0144953. [Google Scholar] [CrossRef] [Green Version]
- Chu, H.; Yoo, S.J.; Hwang, K.J.; Lim, H.S.; Lee, K.; Park, M.Y. Seroreactivity to Q Fever among Slaughterhouse Workers in South Korea. J. Prev. Med. Public Health 2017, 50, 195–200. [Google Scholar] [CrossRef]
- Park, J.H.; Hwang, S.; Acharya, D.; Lee, S.; Hwang, K.; Yoo, S.J.; Lee, K. Seroreactivity and Risk Factors Associated with Coxiella burnetii Infection among Cattle Slaughterhouse Workers in South Korea. Int. J. Environ. Res. Public Health 2018, 15, 2264. [Google Scholar] [CrossRef] [Green Version]
- Htwe, K.K.; Yoshida, T.; Hayashi, S.; Miyake, T.; Amano, K.; Morita, C.; Yamaguchi, T.; Fukushi, H.; Hirai, K. Prevalence of Antibodies to Coxiella burnetii in Japan. J. Clin. Microbiol. 1993, 31, 722–723. [Google Scholar] [CrossRef] [Green Version]
- Esmaeili, S.; Bagheri Amiri, F.; Mokhayeri, H.; Kayedi, M.H.; Maurin, M.; Rohani, M.; Mostafavi, E. Seroepidemiological Study of Q Fever, Brucellosis and Tularemia in Butchers and Slaughterhouses Workers in Lorestan, Western of Iran. Comp. Immunol. Microbiol. Infect. Dis. 2019, 66, 101322. [Google Scholar] [CrossRef]
- Woldeyohannes, S.M.; Gilks, C.F.; Baker, P.; Perkins, N.R.; Reid, S.A. Seroprevalance of Coxiella burnetii among Abattoir and Slaughterhouse Workers: A Meta-Analysis. One Health 2018, 6, 23–28. [Google Scholar] [CrossRef]
- Wolter, K. Introduction to Variance Estimation. In Statistics for Social and Behavioral Sciences; Springer: New York, NY, USA, 2007. [Google Scholar]
- Rogan, W.J.; Gladen, B. Estimating prevalence from the results of a screening test. Am. J. Epidemiol. 1978, 107, 71–76. [Google Scholar] [CrossRef] [PubMed]
- Archer, K.J.; Lemeshow, S. Goodness-of-Fit Test for a Logistic Regression Model Fitted Using Survey Sample Data. Stata J. 2006, 6, 97–105. [Google Scholar] [CrossRef] [Green Version]
- Wilson, L.E.; Couper, S.; Prempeh, H.; Young, D.; Pollock, K.G.J.; Stewart, W.C.; Browning, L.M.; Donaghy, M. Investigation of a Q Fever Outbreak in a Scottish Co-Located Slaughterhouse and Cutting Plant: Scottish Outbreak of Q Fever. Zoonoses Public Health 2010, 57, 493–498. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Carrieri, M.; Tissot-Dupont, H.; Rey, D.; Brousse, P.; Renard, H.; Obadia, Y.; Raoult, D. Investigation of a Slaughterhouse-Related Outbreak of Q Fever in the French Alps. Eur. J. Clin. Microbiol. Infect. Dis. 2002, 21, 17–21. [Google Scholar] [CrossRef]
- Lord, H.; Fletcher-Lartey, S.; Weerasinghe, G.; Chandra, M.; Egana, N.; Schembri, N.; Conaty, S. A Q Fever Cluster among Workers at an Abattoir in South-Western Sydney, Australia, 2015. WPSAR 2016, 7, 21–27. [Google Scholar] [CrossRef] [Green Version]
- Marrie, T.J.; Fraser, J. Prevalence of Antibodies to Coxiella burnetii among Veterinarians and Slaughterhouse Workers in Nova Scotia. Can. Vet. J. 1985, 26, 181–184. [Google Scholar]
- Esmaeili, S.; Pourhossein, B.; Gouya, M.M.; Amiri, F.B.; Mostafavi, E. Seroepidemiological Survey of Q Fever and Brucellosis in Kurdistan Province, Western Iran. Vector Borne Zoonotic Dis. 2014, 14, 41–45. [Google Scholar] [CrossRef] [Green Version]
- Mostafavi, E.; Molaeipoor, L.; Esmaeili, S.; Ghasemi, A.; Kamalizad, M.; Yousefi Behzadi, M.; Naserifar, R.; Rohani, M.; Hashemi Shahraki, A. Seroprevalence of Q Fever among High-Risk Occupations in the Ilam Province, the West of Iran. PLoS ONE 2019, 14, e0211781. [Google Scholar] [CrossRef]
- De Rooij, M.M.T.; Borlée, F.; Smit, L.A.M.; de Bruin, A.; Janse, I.; Heederik, D.J.J.; Wouters, I.M. Detection of Coxiella burnetii in Ambient Air after a Large Q Fever Outbreak. PLoS ONE 2016, 11, e0151281. [Google Scholar] [CrossRef] [Green Version]
- Sloan-Gardner, T.S.; Massey, P.D.; Hutchinson, P.; Knope, K.; Fearnley, E. Trends and Risk Factors for Human Q Fever in Australia, 1991–2014. Epidemiol. Infect. 2017, 145, 787–795. [Google Scholar] [CrossRef] [Green Version]
- 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] [Green Version]
- Park, J.H.; Chu, H.; Yoo, S.J.; Hwang, K.J.; Lim, H.S. Serologic Survey and Risk Factors for Coxiella burnetii Infection among Dairy Cattle Farmers in Korea. J. Korean Med. Sci. 2018, 33, e245. [Google Scholar] [CrossRef] [PubMed]
- Schimmer, B.; Schotten, N.; van Engelen, E.; Hautvast, J.L.A.; Schneeberger, P.M.; van Duijnhoven, Y.T.H.P. Coxiella burnetii Seroprevalence and Risk for Humans on Dairy Cattle Farms, the Netherlands, 2010–2011. Emerg. Infect. Dis. 2014, 20, 417–425. [Google Scholar] [CrossRef] [PubMed]
- Alonso, E.; Lopez-Etxaniz, I.; Hurtado, A.; Liendo, P.; Urbaneja, F.; Aspiritxaga, I.; Olaizola, J.I.; Piñero, A.; Arrazola, I.; Barandika, J.F.; et al. Q Fever Outbreak among Workers at a Waste-Sorting Plant. PLoS ONE 2015, 10, e0138817. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Characteristic | Total Number | Proportion Seropositive (%) # |
---|---|---|
Sex | ||
Female | 104 | 31/100 (31.0) |
Male | 265 | 77/250 (30.8) |
Education | ||
None | 15 | 4/14 (28.6) |
Primary school | 42 | 11/41 (26.8) |
Secondary school | 294 | 85/278 (30.6) |
Higher education | 18 | 8/17 (47.1) |
Job description | ||
Abattoir cleaner | 15 | 5/15 (33.3) |
Abattoir management | 8 | 2/8 (25.0) |
Abattoir workers | 291 | 85/275 (30.9) |
Other | 55 | 16/52 (30.8) |
Compulsory personal protective equipment | ||
Gloves | 324 | 89/302 (29.5) |
Face mask | 271 | 80/254 (31.5) |
Goggles | 257 | 72/241 (29.9) |
Seroprevalence | 95% Confidence Interval | |
---|---|---|
Apparent estimate | 33% | 28–38% |
True estimate | 30% | 25–35% |
Variable | Total Number | Percent Seropositive | Univariable Analysis | Multivariable Analysis | ||
---|---|---|---|---|---|---|
Unadjusted Odds Ratio (95% CI) | p Value | Adjusted Odds Ratio (95% CI) | p Value | |||
Age | 0.96 (0.93–0.98) | 0.004 | 0.96 (0.94–0.98) | <0.001 | ||
Education | 0.086 * | |||||
Primary school | 41 | 26.8 | 2.13 (0.25–18.11) | |||
Secondary school | 278 | 30.6 | 3.68 (0.70–19.19) | Eliminated | ||
Higher education | 17 | 47.1 | 5.25 (0.68–40.29) | |||
None | 14 | 28.6 | Reference | |||
Abattoir throughput | 0.143 | |||||
High (>40 sheep/day) | 332 | 30.7 | 1.62 (0.83–3.14) | Eliminated | ||
Low | 27 | 25.9 | Reference | |||
Animals sourced for personal consumption | 0.011 | |||||
Yes | 248 | 27.4 | 0.60 (0.41–0.87) | 0.74 (0.51–1.08) | 0.114 | |
No | 111 | 36.9 | Reference | Reference | ||
Animals sourced direct from private farms | 0.115 | |||||
Yes | 316 | 29.7 | 0.62 (0.34–1.14) | Eliminated | ||
No | 43 | 34.9 | Reference | |||
Slaughter pigs | 0.036 | |||||
Yes | 87 | 24.1 | 0.61 (0.39–0.96) | Eliminated | ||
No | 272 | 32.4 | Reference | |||
Slaughter sheep only | 0.136 | |||||
Yes | 53 | 26.4 | 0.71 (0.44–1.13) | Eliminated | ||
No | 306 | 31.0 | Reference | |||
Personnel required to wear a mask | 0.122 | |||||
Yes | 254 | 31.5 | 1.34 (0.92–1.97) | Eliminated | ||
No | 105 | 27.6 | Reference | |||
Previous work experience | 0.101 * | 0.051 * | ||||
Farming | 60 | 28.3 | 1.01 (0.48–2.11) | 0.86 (0.43–1.68) | 0.629 | |
Abattoir/butchery | 94 | 36.2 | 1.86 (0.97–3.58) | 1.89 (1.13–3.17) | 0.019 | |
Other | 195 | 28.7 | Reference | Reference | ||
Daily duration of contact with carcass/meat products | <0.001 * | 0.001 * | ||||
<half day | 33 | 18.2 | 1.41 (0.24–8.09) | 1.72 (0.29–10.30) | 0.530 | |
Whole day | 299 | 33.1 | 3.52 (1.30–9.52) | 4.65 (1.51–14.41) | 0.011 | |
<1 h/day | 17 | 11.8 | Reference | Reference | ||
Schedule | 0.099 | |||||
Full time | 332 | 31.0 | 5.06 (0.71–36.15) | Eliminated | ||
Part time | 13 | 23.1 | Reference | |||
Wearing protective clothing at work | 0.142 | |||||
Regularly/always | 317 | 31.2 | 1.75 (0.81–3.80) | Eliminated | ||
Sometimes/ never | 32 | 25.0 | Reference | |||
Slaughter, evisceration and/or carcass dressing | 0.166 | |||||
Yes | 200 | 32.0 | 1.37 (0.87–2.16) | Eliminated | ||
No | 149 | 28.9 | Reference | |||
Freezing finished products | 0.035 | |||||
Yes | 142 | 27.5 | 0.77 (0.61–0.98) | Eliminated | ||
No | 207 | 32.9 | Reference | |||
Transporting processed material | 0.101 | |||||
Yes | 93 | 25.8 | 0.67 (0.41–1.09) | Eliminated | ||
No | 256 | 32.4 | Reference | |||
Other close animal/product contact | 0.071 | |||||
Yes | 38 | 23.7 | 0.49 (0.23–1.07) | Eliminated | ||
No | 311 | 31.5 | Reference | |||
Treatment for any chronic illness | 0.034 | |||||
Yes | 89 | 22.5 | 0.68 (0.48–0.97) | 0.72 (0.46–1.13) | 0.139 | |
No | 259 | 33.6 | Reference | Reference | ||
Livestock ownership | 0.001 | |||||
Yes | 54 | 14.8 | 0.34 (0.20–0.60) | 0.32 (0.15–0.71) | 0.008 | |
No | 295 | 33.6 | Reference | Reference |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 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
De Boni, L.; Mall, S.; Msimang, V.; de Voux, A.; Rossouw, J.; Frean, J. Exposure of South African Abattoir Workers to Coxiella burnetii. Trop. Med. Infect. Dis. 2022, 7, 28. https://doi.org/10.3390/tropicalmed7020028
De Boni L, Mall S, Msimang V, de Voux A, Rossouw J, Frean J. Exposure of South African Abattoir Workers to Coxiella burnetii. Tropical Medicine and Infectious Disease. 2022; 7(2):28. https://doi.org/10.3390/tropicalmed7020028
Chicago/Turabian StyleDe Boni, Liesl, Sumaya Mall, Veerle Msimang, Alex de Voux, Jennifer Rossouw, and John Frean. 2022. "Exposure of South African Abattoir Workers to Coxiella burnetii" Tropical Medicine and Infectious Disease 7, no. 2: 28. https://doi.org/10.3390/tropicalmed7020028
APA StyleDe Boni, L., Mall, S., Msimang, V., de Voux, A., Rossouw, J., & Frean, J. (2022). Exposure of South African Abattoir Workers to Coxiella burnetii. Tropical Medicine and Infectious Disease, 7(2), 28. https://doi.org/10.3390/tropicalmed7020028