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Prevalence and occupational exposure to zoonotic diseases in high-risk populations in the Free State Province, South Africa

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Cornelius G. van der Westhuizen, Felicity Jane Burt, Nina van Heerden, Willie van Zyl, Tonia Anthonissen, Jolly Musoke

Zoonotic diseases cause billions of human cases globally, yet they can look like ordinary infections and remain underdiagnosed. This study follows the risk across both sides of the animal-human interface: cattle and the people who work with them.

Abstract

Introduction: Zoonotic diseases are responsible for 2.5 billion human cases globally and approximately 2.7 million deaths annually. Surveillance of animal handlers and livestock for zoonotic pathogens contributes to understanding the true disease burden and risk factors within a community. This study investigated the prevalence of selected zoonoses in cattle, farm workers and occupational exposure to endemic zoonotic diseases and their associated risk factors. Methods: Sputum samples from farmworkers were screened for Mycobacterium bovis. Blood specimens from farmworkers and archived sera were tested for serological evidence of Brucella sp., hantaviruses, and Leptospira sp. Communal and commercial cattle herds were tested for bovine tuberculosis and brucellosis. Results: Mycobacterium bovis was not isolated from human samples. A total of 327 human sera were screened, and 35/327 (10.7%) were Brucella sp. IgG positive, 17/327 (5.2%) Leptospira sp. IgM positive, and 38/327 (11.6%) hantavirus IgG positive (95% CI). A higher proportion of Brucella sp. IgG-positive samples were detected among veterinarians (value of p = 0.0006). Additionally, two cattle from a commercial dairy farm were bovine tuberculosis (bTB) positive using the bTB skin test and confirmatory interferon-gamma assay. A higher percentage of confirmed brucellosis-positive animals were from communal herds (8.7%) compared to commercial herds (1.1%). Discussion: These findings highlight the brucellosis and M. bovis prevalence in commercial and communal herds, the zoonotic disease risk in commercial and subsistence farming in developing countries, and the occupational and rural exposure risk to zoonotic pathogens.

Transcript

Zoonotic diseases cause billions of human cases globally, yet they can look like ordinary infections and remain underdiagnosed. This study follows the risk across both sides of the animal-human interface: cattle and the people who work with them. Zoonotic diseases are responsible for 2.5 billion human cases globally and approximately 2.7 million deaths annually.

Surveillance of animal handlers and livestock for zoonotic pathogens contributes to understanding the true disease burden and risk factors within a community. This study investigated the prevalence of selected zoonoses in cattle, farm workers and occupational exposure to endemic zoonotic diseases and their associated risk factors.

Zoonotic pathogen surveillance studies at the animal-human interface and among populations at occupational risk with direct animal exposure or exposure due to residing in rural conditions are crucial for identifying circulating pathogens with public health implications. These zoonoses clinically present with symptoms generally shared with a range of other common infectious diseases, including malaria and typhoid fever, leading to difficulties in diagnosis and underestimating the true burden of these diseases.

The study aimed to investigate the prevalence and associated risk factors of M. bovis and Brucella sp. in cattle and farmworkers from two farming communities: communal or backyard subsistence farming and large-scale commercial farming.

The study also aimed to document occupational and environmental exposure to Brucella sp., Leptospira sp., and hantaviruses across the Free State province, South Africa. A prospective, cross-sectional study was conducted using two populations, including workers with occupational exposure to animals and cattle.

The study was conducted between November 2019 and March 2020. All selected farms had cattle scheduled for routine bTB and BB screening as part of the DALRRD Free State province surveillance program. Farmworkers on the chosen farms were screened for Mycobacterium tuberculosis complex and Brucella IgG antibodies and asked to complete a questionnaire.

Figure one maps the study sites across the Fezile Dabi district in South Africa’s Free State province, spanning the Moqhaka, Ngwathe, Metsimaholo, and Mafube municipal regions. Its key distinguishes dairy farms, beef farms, and the Maokeng community kraal, showing how the sampling locations were distributed geographically.

This matters because the authors selected commercial dairy and beef farms, plus the community kraal, for routine screening of cattle for bTB and brucellosis. The bTB and BB study comprised two sample groups, A and B. In group A, 26 on-site prospective sputum and serum samples were collected from farmworkers in the Maokeng community kraal, commercial dairy farm B, and commercial beef farm C.

A convenience sampling method was used. All participants above 18 years old were approached and enrolled if they agreed to participate in the current study. Specimen collection could not be achieved on farms A and D due to COVID-19 travel restrictions.

Because the distributions were skewed, descriptive statistics included frequencies and percentages for categorical variables, and medians and quartiles for numerical variables. Associations between categorical variables and laboratory outcomes were assessed using chi-squared or Fisher’s exact test when data were sparse.

Differences between laboratory outcome groups regarding numerical variables were assessed using Mann–Whitney tests. All statistical analyses were performed by the University of the Free State Department of Biostatistics using SAS Version 9.4. A total of 321 cattle were screened for bTB using SIST and CIST, and bTB results were available for 301 of the 321 cattle, or 93.8 percent.

The Maokeng community kraal had the least number of animals that returned for bTB results, with 51 of 71 animals returning. Based on the SIST results, 3 of 51 cattle, or 5.9 percent, were suspect reactors in the Maokeng community, and 4 of 33, or 12.1 percent, were suspect reactors in farm A.

No positive bTB results with a value of twenty or more were detected. A total of 1,862 cattle were available for Brucella sp. testing using the RBT, although three haemolysed samples were not included. A total of 52 of 1,859 cattle, or 2.8 percent, had a positive RBT result and were subjected to confirmatory testing using the CFT.

Of those 52 results, 19, or 36.5 percent, were confirmed CFT positive, 6, or 11.5 percent, were suspect, and 27, or 51.9 percent, were negative. Look across the rows, and the community entry stands out: Maokeng reports eight RBT-positive reactions, with six CFT-positive results, while both dairy farms report zero RBT-positive reactions.

Among the beef farms, Farm D shows the largest counts in the RBT-positive and CFT-positive columns, with Farm C reporting fewer in each. A total of 327 human serum samples were screened for IgG antibodies against Brucella sp.

and hantaviruses, and IgM antibodies against Leptospira sp. For each assay, the results were normalized by calculating the ratio for each sample to that of the cut-off control, according to manufacturers’ instructions. Ratio values calculated for each sample in all three assays were plotted in Figures 3A to 3C.

In panel A, most blue sample points cluster well below the two red cut-off lines, with a smaller set extending above them. Panels B and C show a similar concentration below their red thresholds, but each also contains scattered higher-ratio points, including a few prominent outliers.

P-value analysis of the Brucella IgG positive results showed that age, veterinary work, and laboratory work were all significant risk factors. The p-value for age was 0.0008, for veterinary work it was 0.0006, and for laboratory work it was 0.031.

Illness after exposure to animal tissue or blood was statistically significant to Brucella IgG seropositivity, with a p-value of 0.029. Based on the available data and confirmatory interferon-gamma assay and skin tests, the cattle bTB prevalence detected in this study was 0.7 percent, or two animals, all originating from commercial dairy farm B.

These findings were lower than reports from other sub-Saharan countries: 6.2 percent in Algeria, 7.4 percent in Sudan, and approximately 27 percent in Ethiopia. The results demonstrate the potentially effective control schemes in lowering bTB transmission in the study site.

In South Africa, the bTB eradication and control scheme was implemented in 1969, following the test-and-slaughter approach. That approach led to a substantial decrease in bTB in cattle within the commercial sector, from a prevalence of 11.8 percent in 1971 to 0.39 percent in 1995.

In the Farm B column, the comparative skin test records eight positive and eight suspect results, alongside one hundred ten negative results. By contrast, Farm A’s comparative test lists zero positive and zero suspect results, with thirty-three negative results; the single-test rows also show three suspects in Maokeng and four in Farm A.

South Africa has a large proportion of the human population dependent on animals for their livelihood, whether as a source of food, trade, companionship, or services. The importance of a One Health approach to zoonotic pathogens should be encouraged.

More emphasis should be placed on populations at higher risk of contracting zoonotic infections regarding epidemiological investigations. The study found evidence of several zoonotic exposures in farmworkers and cattle, with occupational factors linked to Brucella IgG positivity and confirmed bovine tuberculosis in two dairy cattle.

That makes coordinated One Health surveillance especially important.

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