The Epidemiology of African Swine Fever in "Nonendemic" Regions of Zambia (1989-2015): Implications for Disease Prevention and Control

Abstract

African swine fever (ASF) is a highly contagious and deadly viral hemorrhagic disease of swine. In Zambia, ASF was first reported in 1912 in Eastern Province and is currently believed to be endemic in that province only. Strict quarantine measures implemented at the Luangwa River Bridge, the only surface outlet from Eastern Province, appeared to be successful in restricting the disease. However, in 1989, an outbreak occurred for the first time outside the endemic province. Sporadic outbreaks have since occurred almost throughout the country. These events have brought into acute focus our limited understanding of the epidemiology of ASF in Zambia. Here, we review the epidemiology of the disease in areas considered nonendemic from 1989 to 2015. Comprehensive sequence analysis conducted on genetic data of ASF viruses (ASFVs) detected in domestic pigs revealed that p72 genotypes I, II, VIII and XIV have been involved in causing ASF outbreaks in swine during the study period. With the exception of the 1989 outbreak, we found no concrete evidence of dissemination of ASFVs from Eastern Province to other parts of the country. Our analyses revealed a complex epidemiology of the disease with a possibility of sylvatic cycle involvement. Trade and/or movement of pigs and their products, both within and across international borders, appear to have been the major factor in ASFV dissemination. Since ASFVs with the potential to cause countrywide and possibly regional outbreaks, could emerge from "nonendemic regions", the current ASF control policy in Zambia requires a dramatic shift to ensure a more sustainable pig industry.

Keywords: African swine fever; Asfarviridae; Zambia; domestic pigs; molecular epidemiology; phylogenetic analysis.

Figure 1

Map showing dates of African swine fever (ASF) outbreaks and the spatial distribution of p72 African swine fever virus (ASFV) genotypes identified in “non-endemic” areas in Zambia (1989–2015).

Figure 2

Map of Northwestern Province showing the spread of ASF along livestock trade route during the outbreaks of 2006–2008.

Figure 3

Phylogenetic relationships of nucleotide sequences of p72 gene of ASFVs detected in pigs and soft ticks in Zambia. The analysis was based on 403 bp of the p72 gene. The evolutionary history was inferred using the minimum evolution (ME) method with evolutionary distances being computed using the p-distance method. The ME tree was searched using the close-neighbor-interchange (CNI) algorithm at a search level of 1. The neighbor-joining algorithm was used to generate the initial tree. Numbers at branch nodes indicate bootstrap values ≥50%. The GenBank accession no. of strains included in the analyses are indicated in parenthesis. Virus strains characterized in the present study detected in domestic pigs are shaded in red while those from ticks are shaded in green. Bar, number of substitutions per site.

Figure 4

Phylogenetic relationships of the p54 (a) and p30 (b) genes of ASFVs detected in pigs and soft ticks in Zambia. Analysis was based on 483 bp of the p54 and 528 bp of the p30 genes. The evolutionary history was inferred using the Minimum Evolution method with evolutionary distances being computed using the p-distance method. The ME tree was searched using the close-neighbor-interchange (CNI) algorithm at a search level of 1. The neighbor-joining algorithm was used to generate the initial tree. Numbers at branch nodes indicate bootstrap values ≥50%. The GenBank accession no. of strains included in the analysis are indicated in parenthesis. Virus strains characterized in the present study detected in domestic pigs are shaded in red while those from ticks are shaded in green. Bar, number of substitutions per site.

Figure 4

Phylogenetic relationships of the p54 (a) and p30 (b) genes of ASFVs detected in pigs and soft ticks in Zambia. Analysis was based on 483 bp of the p54 and 528 bp of the p30 genes. The evolutionary history was inferred using the Minimum Evolution method with evolutionary distances being computed using the p-distance method. The ME tree was searched using the close-neighbor-interchange (CNI) algorithm at a search level of 1. The neighbor-joining algorithm was used to generate the initial tree. Numbers at branch nodes indicate bootstrap values ≥50%. The GenBank accession no. of strains included in the analysis are indicated in parenthesis. Virus strains characterized in the present study detected in domestic pigs are shaded in red while those from ticks are shaded in green. Bar, number of substitutions per site.

Figure 5

Multiple sequence alignment of amino acids of the tetrameric tandem repeats of the central variable region (CVR) of ASFVs detected in Zambia. The ASFVs characterized in this study are shown in red and green text for viruses detected in domestic pigs and soft ticks, respectively. The GenBank accession or protein identification no. of strains included in the analyses are indicated in parenthesis while the p72 genotypes are shown after the colon.