Long-term changes in the spatial distribution of lumpy skin disease hotspots in Zimbabwe Samuel Swiswa, Mhosisi Masocha, Davies M. Pfukenyi, Solomon Dhliwayo & Silvester M. Chikerema Tropical Animal Health and Production ISSN 0049-4747 Trop Anim Health Prod DOI 10.1007/s11250-016-1180-9
1 23
Your article is protected by copyright and all rights are held exclusively by Springer Science +Business Media Dordrecht. This e-offprint is for personal use only and shall not be selfarchived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”.
1 23
Author's personal copy Trop Anim Health Prod DOI 10.1007/s11250-016-1180-9
REGULAR ARTICLES
Long-term changes in the spatial distribution of lumpy skin disease hotspots in Zimbabwe Samuel Swiswa 1,3 & Mhosisi Masocha 2 & Davies M. Pfukenyi 1 & Solomon Dhliwayo 1 & Silvester M. Chikerema 1
Received: 15 March 2016 / Accepted: 17 October 2016 # Springer Science+Business Media Dordrecht 2016
Abstract Outbreaks of lumpy skin disease (LSD) are reported almost every year in Zimbabwe but not much is known regarding whether the pattern of the disease is changing in response to major socio-economic programmes such as the land reform launched in 2000. In this paper, geo-referenced data of LSD cases was used to detect and map significant LSD hotspots over a 20-year period (1995–2014). The hotspots were then overlaid on top of a land tenure map to explore whether hotspots have spread or persist in some land tenure types. The main results are that LSD outbreaks are on the rise and the disease is spreading throughout the country with areas formerly large-scale commercial farms now experiencing more outbreaks. These results suggest that regular vaccination should be now recommended in most districts in the country. Keywords Lumpy skin disease . Land tenure . Hotspot
Introduction Lumpy skin disease (LSD) is caused by a virus belonging to the family Poxviridae and shares the genus Capripoxvirus with sheep pox (type member) and goat pox viruses. LSD is one of the most economically significant transboundary, * Silvester M. Chikerema
[email protected] 1
Department of Clinical Veterinary Studies, University of Zimbabwe, Box MP 167, Mount Pleasant, Harare, Zimbabwe
2
Department of Geography and Environmental Science, University of Zimbabwe, Box MP 167, Mount Pleasant, Harare, Zimbabwe
3
Department of Livestock and Veterinary Services, 18 Borrowdale Road, Harare, Zimbabwe
emerging viral diseases of cattle. The disease was recognised as a high impact, rapidly spreading epidemic disease by the World Organisation for Animal Health (OIE). Recently, several outbreaks have been reported in some European and Middle Eastern countries (Abutarbush et al. 2015; Alkhamis and VanderWaal 2016; Tasioudi et al. 2016). Major consequences of the disease are sterility and infertility in both sexes, loss of draught power, abortion, reduction in milk yield and permanent hide damage (OIE 2010). Movement restrictions imposed on animals when the disease occurs also lead to loss of market opportunities. Different types of biting and blood-feeding arthropods, including mosquitoes and flies (Chihota et al. 2001, 2003), are likely responsible for the mechanical spread of the LSD virus, with direct and indirect contact playing a minor role in the transmission of the virus. Female Aedes aegypti mosquitoes have been shown to transmit LSD virus (LSDV) from infected to susceptible cattle for 2–6 days post-feeding on experimentally infected animals (Chihota et al. 2001). However, attempts to transmit LSDV between experimentally infected and susceptible cattle by Stomoxys calcitrans failed (Chihota et al. 2003), as did the transmission of LSDV by two species of mosquito (Anopheles stephensi and Culex quinquefasciatus) and the biting midge (Culicoides nubeculosus) (Chihota et al. 2003). LSD may occur in different ecological and climatic zones and has the potential to extend its boundaries (Davies 1991). However, warm and humid agro-climatic zones have been considered a favourable environment for the occurrence of large populations of biting flies (Tuppurainen and Oura 2012), which may aid the transmission of the LSD virus. Introduction of new animals into a herd, together with the sharing of grazing areas and watering points, also increase the risk of LSD, in the herd (Getachew et al. 2010). Legal or illegal movements of cattle, trade activities and non-vectorial transmission such as illegal transport of
Author's personal copy Trop Anim Health Prod
animal products like hides and skins may play a role in LSD introduction (Tasioudi et al. 2016). Although in Zimbabwe the LSD outbreaks are reported almost every year (average of 309 cases per year), there has been little work to describe the distributional patterns of the disease (Marange 2008, unpublished data). Changes in land ownership after the land reform programme launched in 2000 have resulted in cattle movement from communal areas into the previous commercial farms. The actual total number of cattle moved during this land reform is not known but is likely to be in excess of 500,000 assuming each of the 300,000 households that benefited from the land reform on average owned two heads of cattle (Scoones and Wolmer 2007). This implies that the land reform changed cattle distribution in the country. In addition, breakdown in fencing that demarcated the commercial farms from communal areas also resulted in further mixing of cattle from different herds, thus potentially resulting in the introduction of diseases in areas that may have been free of diseases. The new farm owners may also have lacked adequate knowledge, resources and skills to undertake seasonal vaccinations, dipping and other measures recommended for the control of the disease. Spatial clustering statistics are generally used to identify if the spatial distribution of observed phenomena significantly differs from an expectation of the distribution of those phenomena under complete spatial randomness (Barro et al. 2015). When it is applied to a disease, clustering can be defined as an excess of reported cases in time, space or both space and time (hotspots), or areas with fewer than expected cases (coldspots) (Jacquez et al. 1996). The Gi* statistic of Getis and Ord (Getis and Ord 1992; Ord and Getis 1995), a distance-based statistic, is one of the commonly used local statistics in spatial epidemiology. Barro et al. (2015) and Kracalik et al. (2012) used the Gi* statistic to identify hotspots of human anthrax transmission in Georgia and to analyse the spatial patterns of livestock anthrax in Kazakhstan, respectively. The epidemiological concept of a hotspot as it is applied to LSD in this study is an excess of reported LSD cases in both space and time than would be expected to occur by chance (Jacquez et al. 1996; Barro et al. 2015). To this end, the current study focused on using the Gi* statistic to identify changes in the distribution of LSD hotspots in the context of the land reform programme in Zimbabwe.
Methods Data collection Geo-referenced data of LSD cases occurring in various localities in Zimbabwe were obtained from the Central Epidemiology Unit in the Division of Veterinary Field Services. LSD is notifiable in Zimbabwe; hence, every case
must be reported to the veterinary authority. The data set consisted of the dip tank georeference, number of outbreaks and cases per outbreak. All outbreaks occurring in an area serviced by the same dip tank have the same georeference number, except for the large-scale commercial farms, which have individual dip tanks. Symptomatic disease identification of cases is done using the appearance of cutaneous nodules/ lesions in the body and the enlargement of superficial lymph nodes by experienced veterinary extension workers and animal health inspectors in the various districts, and confirmed by district veterinary officers. No laboratory confirmation of the disease was done. The data covered the period 1 January 1995 to 31 December 2014. Spatial analysis of LSD cases and hotspots The spatial distribution of LSD cases between 1995 and 2014 was mapped in four 5-year periods: 1995–1999, 2000–2004, 2005–2009 and 2010–2014. The mapping was done using ArcGIS software v. 10.1. Significant LSD hotspots during the time periods were determined and mapped as well; hotspots were determined as areas where clustering of cases was greater than would occur by chance. Hotspot analysis was conducted using the Getis-Ord Gi* tool in ArcGIS v. 10.1. The output for this tool is a Gi* statistic in the form of a Z score, which indicates where number of cases with either high or low value cluster spatially. A statistically significant hotspot has a Z score greater than +1.96 (Mitchell 2005). The spatial distribution of LSD, based on pre-land reform land tenure type, was also evaluated. The three classes of land tenure evaluated in this study were communal areas (CA), large-scale commercial farming areas (LSCFA) and smallscale commercial farming areas (SSCFA). The land tenure classes were derived from the published land classification map of Zimbabwe (Department of the Surveyor General 1979). The test for proportions was used to test for differences in the proportions of hotspots between the different land tenure systems over the four periods. The P values were adjusted in R software using the Benjamini and Yekutieli (‘BY’) method (Benjamini and Yekutieli 2001).
Results Spatial distribution of LSD cases and spatial shifts of LSD hotspots Figure 1a–d shows changes in the distribution of LSD from 1995 to 2014. There were fewer cases of the disease reported in the first period, with number cases almost doubling after each consecutive 5-year period. There was also a gradual increase in the spatial spread of the cases over the study period. Most of the cases were reported in the communal areas. In the
Author's personal copy Trop Anim Health Prod
Fig. 1 Spatial distribution of LSD cases for the periods 1995–1999 (a); 2000–2004 (b); 2005–2009 (c) and 2010–2014 (d)
first period (1995–1999), there were few significant hotspots (ten) located mostly in the communal land in the northern, southern and south-eastern parts of the country (Fig. 2a). During the period 2000–2014, the number of significant hotspots increased from 115 in the second 5-year period to 187 in the last 5-year period (Fig. 2a–d). At the same time, the geographic distribution of hotspots expanded to other regions including the western areas of the country. During the third period (2005–2009), significant disease hotspots persisted in the southern, northern and western areas of the country with new hotspots appearing in the central areas, especially in large-scale commercial farmland. Table 1 compares proportions of hotspots between different major land tenure systems for each 5-year period. It can be observed that communal land tenure system consistently had the highest proportion of significant LSD hotspots compared to other land tenure systems. Table 1 also shows that during the successive 5-year periods, the proportion of LSD hotspots increased in areas formerly large-scale commercial farmland.
Discussion Geo-referenced data on LSD cases routinely collected over a period of 20 years was used to demonstrate the spatial spread
Note: solid white lines represent administrative district boundaries
Fig. 2 Significant LSD hotspots for the periods 1995–1999 (a); 2000– 2004 (b); 2005–2009 (c) and 2010–2014 (d). Note: solid white lines represent administrative district boundaries
of the disease and to identify LSD hotspots. In many developing countries, there is lack of geo-referenced animal disease data. The present paper illustrates the benefits of collecting long-term livestock data that is geo-referenced. It also shows the value of a disease surveillance system based on a relatively simple system of the clinical recognition of a disease by trained animal health workers as means of collecting relevant data. Implementation of such a surveillance system that incorporates geo-referencing of animal disease data will markedly assist in understanding factors involved in the spatial spread of Table 1 Proportions of hotspots in different land tenure systems over the study period Period
CA
LSCFA
SSFA
Total
1995–1999 2000–2004 2005–2009 2010–2014
0.6a 0.66a 0.61a 0.44a
0.1b 0.22b 0.21b 0.40b
0.3c 0.11c 0.19b 0.16c
10 115 107 187
Note: proportions with different letters of the alphabet in the same row differ significantly at α = 0.05 LSCFA large-scale commercial farming areas, SSCFA small-scale commercial farming areas, CA communal Area
Author's personal copy Trop Anim Health Prod
LSD in most African countries where the disease is known to be endemic. The results show an overall increase in the geographic distribution and number of significant hotspots over the studied period. These changes coincided with the start of the land reform programme in 2000. Both the observed increase in the number of LSD cases and its spread to the rest of the country could be attributed to a complex interplay of socioeconomic and ecological factors, which were not explored in this present study. However, it is likely that these changes are linked to increased cattle movements following the allocation of commercial land to new farmers as was reported for Bovine brucellosis in Zimbabwe recently (Matope et al. 2010). In a study by Gari et al. (2010) in Ethiopia, communal grazing and introduction of new animals to a herd were associated with occurrence of LSD, although, surprisingly, no association was found between cattle movements and LSD prevalence (Tuppurainen and Oura 2012). Another important aspect of the results is that in the postland reform period, LSD hotspots started occurring in districts where they did not occur before. This implies that longdistance movement of infected stock could have played an important role in the spread of the disease as hypothesised in other studies (Tasioudi et al. 2016). In other countries such as Egypt, Ethiopia, Israel, Turkey, Jordan, Azerbaijan, Lebanon, Palestine, Iran and Iraq, LSD outbreaks were also linked to legal as well as illegal movement of infected animals (Getachew et al. 2010; Magori-Cohen et al. 2012; EFSA 2015). Hence, the increased uncontrolled livestock movements in the country during the land reform starting in 2000 probably explain the spatial increase and spread of LSD. However, it is possible that the number of hotspots could have increased due to a shift in the distribution of cattle following the land reform programme. The policy changes on land tenure cannot be ruled out as one of the factors underlying the increase and spread of LSD cases in the country. Hence, the study illustrates the importance of assessing the impacts (both negative and positive) of policy changes on relevant sectors (e.g., animal health and production) before a large-scale implementation. The spread of LSD in the Middle East region is reported to be due to a large-scale importation of cattle, uncontrolled cattle movements, communal grazing and nomadism (Tuppurainen and Oura 2012). The persistence of a high number of significant LSD hotspots in the communal land tenure is due to open access resource management regime in which herds share grazing and watering points. This, in turn, increases chances of disease transmission. It is also noteworthy that the post-land reform programme coincided with a major economic decline experienced from 2000 to 2008 (AEDI 2009), which disrupted regular dipping and vaccination programmes that were in place before, particularly in communal lands. In the large-scale commercial farmland, the observed increase in the number and
spread of LSD hotspots likely mirrors the combined effects of partitioning of large-scale commercial farms into smaller units, destruction of existing veterinary fences, as well as the introduction of mixed herds from communal lands resulting in increased mixing of herds. However, the relative importance of each of these drivers warrants further investigation. While the results of the geographic analysis of the distribution of LSD hotspots indicate that the disease is spreading throughout the country and more hotspots are occurring after the land reform period compared to before, caution is needed when interpreting the results as increased effort by veterinary officers may have resulted in more cases being captured in the post-land reform period. Further, although LSD is a reportable disease in Zimbabwe, not all cases are reported; hence, there is possibility of some bias in the data collected. It is also possible that the bias may have changed with time as more veterinary officers became aware of the significance of the disease. Nevertheless, the present results hold given that the number of unreported cases is likely to be low. LSD was classified as a listed disease in 1995, which coincides with the start of the studied period. Thus, veterinary officers are obliged to report its occurrence to the veterinary authority during the study period (Chikerema et al. 2012).
Conclusion In this paper, we detected lumpy skin disease hotspots and investigated whether the location of these hotspots is shifting over a 20-year period in Zimbabwe. The influence of land tenure was also examined. The main conclusions that can be drawn are that LSD outbreaks are on the rise and the disease is spreading throughout the country with areas of the former large-scale commercial farms now experiencing more outbreaks than was the case before the land reform. These results imply that regular vaccination should now be recommended in most districts of the country. The analysis employed here to detect hotspots is simple and may be replicated in other countries to investigate changes in disease patterns in relation to the major socio-economic changes. Compliance with ethical standards Conflict of interest The authors declare that they have no conflict of interest.
References Abutarbush, S.M., Ababneh, S.M., Al Zoubi, I.G., Al Sheyab, O.M., Al Zoubi, O.M., Alekish, M.O. Al Gharabat, R.J., 2015. Lumpy Skin Disease in Jordan: Disease Emergence, Clinical Signs, Complications and Preliminary-associated Economic. Transboundary and Emerging Diseases, 62, 549-554.
Author's personal copy Trop Anim Health Prod AEDI (African Economic Development Institute). 2009. The failing economy of Zimbabwe. (http://www.africaecon.org/index. php/exclusives/read_exclusive/1/2). Alkhamis, M.A. and VanderWaal., 2016. Spatial and Temporal Epidemiology of Lumpy Skin Disease in the Middle East, 20122015, Frontiers in Veterinary Science, doi: 10.3389/fvets.2016.00019 Barro, A.S., Kracalik, I.T., Malania, L., Tsertsvadze, N.L., Manvelyan, J., Imnadze, P. and Blackburn, J.K., 2015. Identifying hotspots of human anthrax transmission using three local clustering techniques, Applied Geography, 60, 29–36. Benjamini, Y. and Yekutieli, D., 2001. The control of the false discovery rate in multiple testing under dependency, The Annals of Statistics, 29, 1165–1188. Chihota, C.M., Rennie, L.F., Kitching, R.P. and Mellor, P.S., 2001. Mechanical transmission of lumpy skin disease virus by Aedes aegypti (Diptera: Culicidae), Epidemiology and Infection, 126, 317–321. Chihota, C.M., Rennie, L.F., Kitching, R.P. and Mellor, P.S., 2003. Attempted mechanical transmission of skin disease virus by biting insects, Medical and Veterinary Entomology, 17, 294–300. Chikerema, S.M., Pfukenyi, D.M., Matope, G. and Bhebhe, E., 2012. Temporal and spatial distribution of cattle anthrax outbreaks in Zimbabwe between 1967 and 2006, Tropical Animal Health and Production, 44, 63–70. Davies, F.G., 1991. Lumpy skin disease: a growing problem in Africa and the Near East, World Animal Review, 68, 37–42. Department of the Surveyor General. 1979. Zimbabwe Land classification, Government Printers, Harare. EFSA (European Food Safety Authority). 2015. Scientific Opinion on Lumpy Skin Disease. European Food Safety Authority Journal, Doi:10.2903/j.efsa.2015.3986. Gari, G., Waret-Szkuta, A., Grosbois, V., Jacquiet, P. and Roger, F., 2010. Risk factors associated with observed clinical lumpy skin disease in Ethiopia, Epidemiology and Infection, 138, 1657–1666. Getachew, G., Waret-Szkuta, A., Grosbois, V. and Jacquite, P. and Roger, F., 2010. Risk factors associated with observed clinical lumpy skin disease in Ethiopia, Epidemiology and Infection, 138(11), 1657-1566.
Getis, A. and Ord, J.K., 1992. The analysis of spatial association by use of distance statistics, Geographical Analysis, 24, 189–196. Jacquez, G., Waller, L., Grimson, R. and Wartenberg, D., 1996. The analysis of disease clusters, Part 1: state of the art, Infection Control and Hospital Epidemiology, 17, 319–327. Kracalik, I.T., Blackburn, J.K., Lukhunova, L., Pazilov, Y., Hugh-Jones, M.E. and Aikimbayev, A., 2012. Analysing the spatial patterns of livestock anthrax in Kazakhstan in relation to environmental factors: a comparison of local (Gi) and morphology cluster statistics, Geospatial Health, 7, 111–126. Magori-Cohen, R., Louzoun, Y., Herziger, Y., Oron, E., Arazi, A., Tuppurainen, E., Shipgel, Y. N. and Klement, E., 2012. Mathematical modeling and evaluation of the different routes of transmission of lumpy skin disease virus, Veterinary Research, 43, 1. Matope, G., Bhebhe, E., Muma, J.B., Lund, A. and Skjerve, E., 2010. Herd-level factors for Brucella seropositivity in cattle reared in smallholder dairy farms of Zimbabwe, Preventive Veterinary Medicine, 94, 213–221. Mitchell, A., 2005. The ESRI Guide to GIS analysis, Volume 2: Spatial measurements and statistics, ESRI Press, Redlands, California. OIE (World Organisation for Animal Health). 2010. OIE Manual of Diagnostic Tests and Vaccines for Terrestrial Animals, Lumpy skin disease, Chapter 2.4.14, pp 768–778. Ord, J. K. and Getis, A., 1995. Local spatial autocorrelation statistics: distributional issues and an application, Geographical Analysis, 27, 286–306. Scoones, I. and Wolmer, W., 2007. Land, landscapes and disease: The case of foot and mouth in southern Zimbabwe, South African Historical Journal, 58, 42–64. Tasioudi, K.E., Antoniou, S.E., Iliadou, P., Sachpatzdis, A., Plevraki, E., Agianniotaki, E.I., Fouki, C., Mangana-Vougiouka, O., Chodrokouki, E. and Dile, C., 2016. Emergence of Lumpy Skin Disease in Greece, 2015, Transboundary and Emerging Diseases, 63, 260–265. Tuppurainen, E.S.M. and Oura, C.A.L., 2012. Review: Lumpy Skin Disease: Am Emerging Threat to Europe, the Middle East and Asia, Transboundary and Emerging Diseases, 59, 40–48.
