Spatial and temporal distribution of contagious bovine pleuro-pneumonia in Uganda (1956-2011)

Spatial and temporal distribution of contagious bovine pleuro-pneumonia in Uganda (1956-2011)

Marvin Apollo Ssemadaali^1,2, Samuel Majalija^1,&, Robert Mwebe³, Susan Olet⁴, Margaret Loy Khaitsa⁵

¹College of Veterinary Medicine, Animal Resources and Biosecurity, Makerere University, Kampala, Uganda, ²Department of Microbiological Sciences, North Dakota State University, PO Box 6050 Fargo, ND 58108-6050, USA, ³National Animal Diseases Diagnostic and Epidemiology Centre, Ministry of Agriculture, Animal Resources and Fisheries, Entebbe, Uganda, ⁴Department of Statistics, North Dakota State University, Dept. 2770, PO Box 6050 Fargo, ND 58108-6050, USA, ⁵Department of Pathobiology and Population Medicine, College of Veterinary Medicine, Mississippi State University, P.O. Box 6100, MS 39762, USA

^&Corresponding author
Samuel Majalija, College of Veterinary Medicine, Animal Resources and Biosecurity, Makerere University, Kampala, Uganda

Introduction    

Contagious bovine pleuro-pneumonia (CBPP) is a trans-boundary bovine respiratory disease caused by a bacterium, Mycoplasma mycoides subsp. mycoides small colony (MmmSC). CBPP is listed among the notifiable diseases that have to be reported to the World Organization for Animal Health (OIE) [1,2]. CBPP is an endemic cattle disease in a large area of Sub-Saharan Africa, including Uganda. It is also one of the most economically serious diseases of cattle in Uganda, affecting production through mortality and reduced productivity, and losses per annum estimated to be €3.7 million [3]. The disease can spread rapidly and transmission in cattle is mainly through inhalation of contaminated droplets from or contact with infected cattle. Transmission of CBPP occurs from direct, close, repeated contacts between diseased and healthy animals at water holes, dip tanks, markets, and communal grazing areas [4,5]. In recent years, CBPP has emerged from areas where it has been persisting in endemic form to reinvade others from which it had previously been eradicated. This increased incidence of the disease is mainly due to the illegal trans-boundary animal movement and trade [4,6]. Control and eradication of CBPP is therefore important as a way to salvage the losses and increase the incomes of livestock owners. The current policy advocated by The African Union-Interafrican Bureau for Animal Resource (AU-IBAR) for the control of CBPP includes: collection of epidemiological data and information; to determine and detect foci of infection; effective control of animal movements from and towards these foci; mass vaccination of cattle regularly for at least five consecutive years; and repeat vaccination of the same cattle each year [7,8]. The objectives of this study were to describe the temporal and spatial distribution of CBPP in Uganda (1956-2011), and determine possible factors associated with its occurrence.

Methods     

This was a retrospective case series conducted through a review of data on CPBB collected and archived by Ministry of Agriculture, Animal Industry and Fisheries (MAAIF) between 1956 and 2011. Annual reports and laboratory registry books were used for tallying suspected and confirmed cases of CBPP that occurred between 1956 and 2011 in Uganda. The collected data were entered into Microsoft Excel spreadsheets, and later transferred to SPSS software for analysis.

Results     

Number of samples received from different regions

The MAAIF received 849,337 suspected cases of CBPP between 1956 and 2011. The samples were collected from different regions of the country during the study period (1956-2011), and totals are shown in Table 1. A total of 6,410 positive samples were detected from the different regions, the majority (2896) were obtained from Karamoja, followed by Western Uganda (1506), Northern Uganda (1018), Central Uganda (879), and only 11 were from Eastern Uganda (Table 1).

Positivity rates of CBPP

Out of 849,337 screened samples for CBPP, a total of 6410 (0.76%) tested positive, 7022 (0.82%) had missing results, and the majority, 835,905 (98.42%) tested negative for CBPP. The positivity rate of CBPP was calculated based on a total of 842,315 samples that were tested and had results. Therefore, the overall positivity rate of CBPP from 1956-2011 was 0.76%. Based on regions, the highest positivity rate CBPP was recorded in Western Uganda (16.2%), followed by Northern Uganda (3.1%), and lowest in Karamoja (0.4%) (Figure 1).

Annual positivity rates of CBPP (1956-2011)

Three main phases of CBPP outbreaks in the country were observed. During phase 1, between 1956 and 1974, the highest positivity rate (17.8%) was recorded in 1959, with other peaks in 1969 (4.3%), 1964 (2.2%), 1963 (1.2%), and in 1965 and 1971 (0.8%), among others (Figure 2a). Notably, from 1975 to 1990, fewer samples (1124) were submitted; and of these, only 5 were tested (4 positive); for the other 1119 samples, the results could not be determined. Between 1991 and 2011, the highest positivity rate was reported in 1996 (84.2%), followed by 1993 (50.3%), and in 2010 (39.8%) (Figure 2b). However, CBPP positivity rate of between 4.2% and 25.1% was recorded in most of the remaining years, with the exception of 1991 and 1999 (Figure 2b).

Average monthly positivity rates of CBPP (1970-2011)

The month of November had the highest positive samples (39.50%) recorded, while the lowest (3.10%) were in March (Figure 3). A gradual increase was observed from March (3.10%) to June (20%), and this was followed by a four month decrease to 4.8% in October (Figure 3). The data used here only included 1970 through 2011; as monthly records for the previous years (1956 to 1969) could not be obtained.

Regional positivity rates of CBPP in Uganda in three phases

During the first phase (1956-1974), CBPP was reported in the three regions of Karamoja, (0.5%), Northern (0.3%) and Central region (0.2%) as shown in Figure 4. In phase two (1975-1990), CPBB was only recorded in Northern (3.0%) and Western Uganda (0.5%), and no cases were recorded from other regions (Figure 4). In phase three (1991-2011), CBPP was recorded in all four regions of Uganda, with higher prevalence compared to phase 1 and phase 2. The highest positivity rate (21.9%) was recorded in Karamoja region, followed by Western region (14.1%), then Northern region (10.8%), and lowest in Eastern Uganda (2.1%) (Figure 4). Also, there was a general increase in CBPP positivity rates in all the regions over the years, as shown in Figure 4.

Discussion     

This study aimed to describe the temporal and spatial distribution of CBPP in Uganda from 1956 through 2011, and to determine factors that could be associated with its occurrence. Results indicated that the disease was widespread in the country during the study period, particularly between 1956-1974 and 1991-2011. Uganda has been listed as one of the CBPP endemic countries [9], and the disease is continuing to cause economic and productivity losses [3]. During the first phase (1956-1974), CBPP was mainly confined to three regions; Karamoja, Northern, and Central Uganda. There were no reported cases from the Eastern and Western Uganda regions. Karamoja region reported the highest positivity rate of CBPP, possibly because of the nomadic pastoral way of life that involves a lot of cattle movement. Also, Karamoja is the region where CBPP was first reported in the country, and the region has remained endemic with the disease. The uncontrolled movement of animals in search of water and pasture is the main risk factor for the spread of CBPP in the region [6,10]. Therefore, this region is prone to higher infections because animals move across the Uganda borders into Kenya and Southern Sudan, where animals could have also acquired infection. In 1959, Karamoja region experienced an outbreak of CBPP, a possible explanation for the high CBPP positivity rate observed in 1959, as recorded in this study. Between 1964 and 1966, CBPP outbreaks in Karamoja region were due to cattle introduced from Sudan [11-13]. This led to establishment of quarantine and diagnostic stations in Uganda, along cattle routes to control CBPP in trade animals as they were being transported within the country. Also, in order to contain the disease, the government of Uganda undertook several control measures including: massive testing of animals, massive vaccination campaigns, and control of cattle movement [4]. Since the disease is still endemic in this region, these vaccination campaigns have continued to be carried out, especially in the Karamoja, region due to the high number of affected animals [14].

In the second phase (1975-1990), there were generally very few animals tested in the country, especially in Karamoja region due to political instability. During this time, there could have been a breakdown in the previously established CBPP control measures. This led to unchecked illegal cattle movement and ineffective vaccination campaigns, hence the spread of CBPP to the neighboring regions (Acholi region). In addition, the fact that Western Uganda recorded the second highest rate of CBPP infections (0.5%) during this period was not surprising. Following the insurgency and armed conflict in the Karamoja sub-region of Teso, animals were smuggled, and transported to markets and farms in Western Uganda, thereby introducing CBPP infection to Western Uganda. Also, between 1977 and 1988, CBPP diagnosis in animals was mainly based on post-mortem reports, and no serological techniques were used as in the first phase. This could also be attributed to lack of reagents and technical staff in the diagnostic center to process the samples due to the political insurgency in the country.

During the third phase (1990 to 2011), an increase in CBPP positivity rates was recorded in all the regions of the country, possibly due to the political stability experienced at that time. This time period was characterized by free trade policies in the country, and that possibly favored movement of cattle for trade and search of better profits by farmers. A study of CBPP in Southern Africa region [6] confirmed that CBPP spread along the trade routes as pastoralists moved long distances in search for better markets. In addition, the high CBPP positivity rate could be attributed to the collapse of quarantine stations in the country; most quarantine stations were destroyed during the period of political instability in the country (1974 to late 1980s). Therefore, illegal cattle movements went unchecked leading to spread of the disease. The high CBPP positivity rate reported in Karamoja (21.9%) in the third phase could mainly be due to political insurgences in the region. There was a breakdown in the CBPP control systems during this time leading to an increase in prevalence. In addition, the observed high CBPP positivity rate in Northern Uganda (10.8%), during the third phase, could be attributed to the many government and non-government organization programs for re-stocking of livestock in the region, following the cessation of the insurgency. A majority of the animals could have been acquired from Western Uganda. It is common practice for animals used for re-stocking to be acquired from cattle slaughter markets. These animals could be exposed to infections and could have been a source of infection. In addition, animals from some regions are not quarantined before being transported to other regions. This is because the previously designated quarantine stations along the cattle routes were not functional. In 1996, CBPP outbreaks were reported in Western Uganda [15], contributing to the high CBPP positivity rate observed in this region.

The overall positivity rate of CBPP was highest in Western Uganda (16.2%) and lowest in Karamoja region (0.4%), possibly due to the difference in diagnostic techniques used in the two regions. Most of the samples from the Karamoja region (over 90%) were collected during the first phase, when CFT and SAT techniques (which are less sensitive) were being used; yet, these techniques are less accurate in CBPP diagnosis compared to the new techniques, like cELISA and improved CFT (which are more sensitive). Therefore, the high CBPP reported in Western region could be due to the high sensitivity and specificity of the new techniques used in the third phase (1991-2011). The higher number of CBPP positive samples reported during November, could be attributed to the long dry season (June to August), where most pastoralists move with their animals in search for pastures, hence leading to new infections that are later detected in November. The nomadic lifestyle of some cattle keeping communities, especially Karamajong, involves moving from one place to another in search of water and pastures. A study conducted in Zambia did in fact report that nomadic pastoralists in Southern and Western provinces contribute to the spread of CBPP [10].

Conclusion     

The temporal distribution of CBPP occurrence in Uganda during the study period varied significantly during three distinct time periods (1956-1974, 1975-1990, and 1990-2011) due to various possible factors including: political instability, a disruption in CBPP control measures, lack of livestock movement control; change in diagnostic tests; and implementation of free trade government policies in the country. The breakdown in livestock movement control consequently could have led to the spread of CBPP from the endemic region of Karamoja to the rest of the country. Due to the transboundary nature of this disease, and its documented economic impact, there is a need for the Uganda government to strengthen regional control programs and surveillance systems, including; sensitization of cattle farmers about the benefits of vaccination of their animals, so that they fully participate in the CBPP control programs. Re-establishment of quarantine stations to monitor cattle movement and development of a new vaccine with long lasting immunity and less post-vaccinal reactions would be highly beneficial.

Competing interests     

The authors declare no competing interests.

Authors´ contributions     

Drs. Marvin A. Ssemadaali, Samuel Majalija, Robert Mwebe, and Prof. Margaret Khaitsa were involved in research conceptualization, study design, and manuscript preparation; Drs. Marvin Ssemadaali and Robert Mwebe did data collection and summarizing; Drs. Marvin Ssemadaali and Susan Olet did the data analysis. All authors reviewed the manuscript. All authors have read and agreed to the final version of this manuscript.

Acknowledgments     

The authors would like to thank the US Agency for International Development (USAID) for funding this research through the project “Capacity building in Integrated Management of Trans-boundary Animal Diseases and Zoononses (CIMTRADZ)”. We would also like to thank Dr. Ademun Rose and Mr. Sekitto James, from the Entebbe Epidemiological and Diagnostic Unit and NaLIRRI-Tororo (MAAIF), respectively, for their efforts in accessing the archived data.

Table and figures     

Table 1: number (percentage) of samples collected from different regions and those that tested positive

Figure 1: prevalence of contagious bovine pleuro-pneumonia by region (1956-2011)

Figure 2: annual prevalence of contagious bovine pleuro-pneumonia in Uganda (1956-2011)

Figure 3: average monthly prevalence from 1970-2011

Figure 4: regional contagious bovine pleuro-pneumonia prevalence for the three phases

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