Seroprevalence of melioidosis in animals and environmental factors influencing presence of Burkholderia pseudomallei in small ruminant farms in peninsular Malaysia

Melioidosis results in chronic debilities that reduce productivity and causes condemnation of carcasses of affected animals. There have been anecdotal reports of increase in the disease in animals in Malaysia in recent times. However, there are limited scientific information on the distribution and risk factors of the disease in animal populations as well as the factors in the environments of endemic areas that influence presence of the disease agent. A study was carried out to determine the distribution, risk factors and environmental factors that may influence the presence of the disease agent in small ruminant farms in Peninsular Malaysia. Dataset on the continuous surveillance of melioidosis in animals and another on rainfall and wind speed were both obtained for a period of 10 years. The data were summarized according to animal species, state, year and month of occurrence and relationships between disease prevalence and rainfall and wind speed were examined. The overall seroprevalence between the year 2000 and 2009 was 6.20% (95% CI; 6.02-6.37). The seroprevalence according to animal species showed that buffalo had the highest prevalence (28.18%, 95% CI; 19.04-39.54), followed by sheep (16.55%, 95% CI; 16.03 – 17.09), cattle (7.42%, 95% CI; 5.61-9.75), deer (6.45%, 95% CI; 4.50-9.17), pigs (5.88%, 95% CI; 1.05–26.98), rabbits (3.90%, 95% CI 2.90-4.90) and goats (2.19%, 95% CI; % 2.06-2.37). In terms of year of the study, the prevalence varied from 3.14% (95% CI; 2.84-3.46) in 2008 to 11.79% (95%CI; 10.6-13.09) in 2003. The prevalence for the year 2004 (7.46%, 95% CI; 6.73-8.26) was observed to be significantly higher while those for the years 2008 (3.14%, 95% CI; 2.84-3.46) and 2009 (3.64%, 95% CI; 3.27-4.04) were significantly lower when compared to the prevalence for the year 2000 (6.11%, 95% CI; 5.24-7.11). Correlation analysis showed a moderate, positive and statistically significant correlation between melioidosis prevalence and rainfall (r =0.58, 95% CI; 0.12-0.87, p=0.047) during the period under review. The apparently low seroprevalence among pigs (5.88%) and goats (2.19%) may partly be due to intensive farm management systems in which animals had less contact with contaminated soil and water while the relatively high seroprevalence in buffaloes may partly be due to the extensive management system in which animals are at higher risk of exposure to the disease agent. The higher prevalence in 2000-2004 may be due to increased importations of animals and unfavorable weather conditions during this period. The study however observed that serosurveillance and data recording were not carried out consistently across states, year and animal or livestock species. To investigate the farm level risk factors of melioidosis seropositivity, questionnaires were administered to the identified melioidosis negative and positive farms from four selected states (Pahang, Perak, Negeri Sembilan and Selangor). The characteristics and putative exposure to risk factors were compared between case and the control farms using Chi-square test and logistic regression analysis. In the logistic regression model, melioidosis–positive farms were significantly more likely to have; had bush clearing around farms (odds ratio [OR]; 6.61, 95% confidence interval [CI]; 1.12- 38.84, p<0.037), B. pseudomallei present in the farm soil (OR; 6.23, 95% CI; 1.03- 37.68, p<0.046), other species raised on farm (OR; 7.96, 95% CI; 1.14-55.99, p<0.037) and flooding or waterlogging condition (OR;11.95, 95% CI;1.39-102.6, p=0.024) compared to negative farms. Farms that treated the soil with lime (OR; 0.028, 95% CI; 0.003-0.29, p=0.003) were protected from the infection. Bush clearing may increase the risk of exposure to B. pseudomallei because it involves dispersal of large amount of dust into the atmosphere, brings up agents located at lower levels to the surface thereby increasing the risk of infection. Flood and or waterlogging and presence of agent in farm soil may increase the risk of contact between agent in soil and water with resident animals in the farm. To investigate the physicochemical properties of soil and water that may influence occurrence of the agent in the farm environment, soil and water samples collected from small ruminant farms in the four states and cultured for B. pseudomallei. For the soil properties, comparisons of the B. pseudomallei-positive and negative soil samples using logistic regression model found that, when compared with B. pseudomallei negative soil samples, a positive sample was found to be significantly (p<0.05) more likely to have higher iron contents (OR; 1.009, 95% CI; 1.001-1.018, p=0.034), higher water contents (OR; 1.28, 95% CI; 1.052-1.546, p=0.013) and higher clay contents (OR; 1.54, 95% CI; 1.153-2.062, p=0.004). The significantly higher iron, water and clay contents of the B. pseudomallei-positive soil is consistent with the understanding that iron regulates expression of respiratory enzymes, soil water is essential for soil ecology and agent’s biological processes and clay has excellent water and nutrient retention capabilities due to its surface area and chemical activity which favor survival of the agent in soil. Investigation of the water properties found that, when compared with B. pseudomallei negative water samples, positive water samples were found to be significantly (p<0.05) more likely to have higher chemical oxygen demand (COD) (OR; 1.002, 95% CI; 1.000-1.004, p=0.031) and higher pH value (OR; 12.69, 95% CI; 2.67-60.34, p=0.001). This suggested that higher COD and higher water pH supported the survival of the agent in water samples. In conclusion, melioidosis is widely distributed in Peninsular Malaysia and affects all livestock species regardless of the size, species, population size and breed. The disease occurrence was associated with several factors such as events/activities around farm such bush clearing, water logging/flooding and presence of other species of animal in the farm. The farm soil iron, water and clay content as well chemical oxygen demand and pH of farm water supplies were the factors that influence the presence of B. pseudomallei in farm environments. This information may be of benefits when planning for control strategies against exposure to B. pseudomallei from soil or water source.

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