Submit or Track your Manuscript LOG-IN

HV_7_4_97_108

 

 

 

Review Article

Lumpy Skin Disease Virus Infection: An Emerging Threat to Cattle Health in Bangladesh

Mohammad Enamul Hoque Kayesh1,2*, Mohammad Tufazzal Hussan3, Md. Abul Hashem2,4, Mohammad Eliyas5 and A.K.M. Mostafa Anower1

1Department of Microbiology and Public Health, Faculty of Animal Science and Veterinary Medicine, Patuakhali Science and Technology University, Barishal-8210, Bangladesh; 2Transboundary Animal Diseases Centre, Joint Faculty of Veterinary Medicine, Kagoshima University, Kagoshima, Japan; 3Department of Anatomy and Histology, Faculty of Animal Science and Veterinary Medicine, Patuakhali Science and Technology University, Barishal-8210, Bangladesh; 4Department of Health, Chattogram City Corporation, Chattogram-4000, Bangladesh; 5Upazila Livestock Office and Veterinary Hospital, Pekua, Cox’s Bazar, Department of Livestock Services, Bangladesh.

Abstract | Lumpy skin disease (LSD) is a highly infectious and economically important transboundary disease of cattle caused by LSD virus (LSDV). LSD is characterized by fever and the appearance of nodular lesions in the skin covering all parts of the body. LSD is currently endemic in many African countries and causing significant economic losses. LSD has recently spread out of Africa into the Middle East region, and still continuing to spread other territories of the world. In September 15, 2019 the first occurrence of LSD outbreak in Bangladesh has been reported to the OIE (World Organization for Animal Health). LSD is a vector-borne disease, and climatic conditions of Bangladesh are favorable for the propagation of vectors, which should influence the rapid transmission of LSD in the cattle population of Bangladesh. Therefore, LSD may appear as a big challenge to cattle health in Bangladesh in the near future. Consequently, it is very important to take strategic plans and immediate control measures for LSD outbreak control and prevention in Bangladesh. In this review article, we will focus on epidemiology and modes of LSDV transmission, and its effective control and preventive measures to reduce or eradicate the LSDV infection from a recently infected country like Bangladesh. In addition, we will highlight on impacts of LSD outbreaks in cattle industry of Bangladesh, and necessity of farmers’ awareness building and telemedicine service during the Coronavirus disease 2019 (COVID-19) outbreaks in controlling LSD.


Received | July 28, 2020; Accepted | August 04, 2020; Published | August 17, 2020

*Correspondence | Mohammad Enamul Hoque Kayesh, Department of Microbiology and Public Health, Faculty of Animal Science and Veterinary Medicine, Patuakhali Science and Technology University, Barishal-8210, Bangladesh; Email: mehkayesh@pstu.ac.bd

DOI | http://dx.doi.org/10.17582/journal.hv/2020/7.4.97.108

Citation | Kayesh, M.E.H., M.T. Hussan, M.A. Hashem, M. Eliyas and A.K.M.M. Anower. 2020. Lumpy skin disease virus infection: An emerging threat to cattle health in Bangladesh. Hosts and Viruses, 7(4): 97-108.

Keywords | Lumpy skin disease, Epidemiology, Transmission, Control, Prevention


Introduction

Lumpy skin disease (LSD), an economically important transboundary disease of cattle, is transmitted by arthropod vectors (Woods, 1988). It was first described as “pseudo-urticaria” in Zambia (formerly Northern Rhodesia) in 1929 (MacDonald, 1931). Later, in the 1940s it was identified as an infectious viral disease caused by lumpy skin disease virus (LSDV) (Von-Backström, 1945). LSD is characterized by nodular lesions development in the skin covering the whole body (Tageldin et al., 2014). LSD may cause systemic effects such as fever, anorexia, dysgalactia and pneumonia, and lesions in the mouth and upper respiratory tract (Davies, 1991a). LSDV, a double stranded DNA virus has a genome of approximately 151 kbp with a central coding region of 156 putative genes (Tulman et al., 2001). Similar to other poxviruses, the central coding region of the LSDV genome is bounded by two identical inverted terminal repeat regions of about 2.4 kbp at both termini (Tulman et al., 2001). LSDV belongs to the genus Capripoxvirus in the family Poxviridae (Tulman et al., 2001). The genus Capripoxvirus comprised of three closely related important animal virus species, such as sheeppox virus (SPV), goatpox virus (GPV), and LSDV, affecting sheep, goats, and cattle, respectively (Babiuk et al., 2008; Kitching, 2003). These viruses cause significant economic damages to the sheep, goat, and cattle industry in Africa and Asia (Fenner, 1996). Sheep pox was originally reported in the first century AD, and goatpox was notified in Southern Europe and Northern Africa in the 1880s (Diallo and Viljoen, 2007), suggesting LSD as an old disease but recently identified, and the true evolutionary history and spread of the Capripoxviruses (CaPVs) still remain to be resolved. Generally, CaPV infections are host-specific, and the geographic distribution patterns of sheeppox, goatpox, and LSD are different (Carn, 1993). All three CaPVs only can produce disease in ruminants, and zoonoses are not reported (Limon et al., 2020). Moreover, LSD has not been observed in sheep and goats even when they are kept in a close contact with infected cattle (Davies, 1991b). Despite the fact the origin of LSD is obscure but until recently it was believed to be a disease confined to Africa, where it is endemic in most countries (Coetzer, 2004). LSD is now considered as a rapidly emerging disease of major consequence, and its recent spreading to many Asian countries becoming a big threat to cattle population (EFSA, 2015, 2018). LSD is listed as a World Organization for Animal Health (OIE)-notifiable disease for rapid spreading and great economic impacts. In 2019, for the first time LSD outbreak was reported in Bangladesh (OIE World Animal Health Information Database, 2019; EFSA, 2020). LSD outbreaks in 2019 caused infections in a large number of cattle populations countrywide, and appearing as an emerging threat to cattle health in Bangladesh. Again, in 2020 the LSD outbreaks are being reported in different areas of the country, where LSD is rapidly spreading in thousands of cattle with at least 50 deaths in the northern and north-eastern districts of Bangladesh (Dhaka Tribune, 2020b). During this global pandemic of COVID-19, Bangladesh is also being badly attacked, as of 6 July 2020, there are 165618 confirmed COVID-9 cases in Bangladesh, including 2096 related deaths (WHO, 2020). Due to the Coronavirus disease 2019 (COVID-19) outbreaks, it is speculated that the smooth veterinary health services are subject to interruption, which may negatively impact the outcome of the LSD (Gortázar and de la Fuente, 2020). Therefore, it is important to ascertain the health service by enhancing telemedicine during this COVID-19 health emergency. The origin and spread of the virus in the cattle of Bangladesh remain to be investigated. Therefore, investigation to detect the origin of the disease and its modes of transmission is paramount to reduce/eradicate its further spread in Bangladesh, as LSD has a high impact on production efficiency and profitability which may result in substantial economic losses to cattle industry of the country. In this study, we aimed to focus on epidemiology and modes of transmission of LSD, as well as measures to be taken for the effective control and prevention of LSD. Furthermore, we will discuss the economic impacts of LSD on the cattle farming in Bangladesh. In addition, we will discuss the importance of active surveillance and early detection of the LSD to limit the re-emergence and future spread of LSD, the neglected tropical disease of cattle.

Epidemiology

Cattle are the natural hosts for LSDV (Tuppurainen et al., 2015; Şevik et al., 2016). Asian water buffaloes can also be naturally infected with LSDV (El-Nahas et al., 2011). LSDV is highly host-restricted, while SPV and GPV can cause infection in both sheep and goat (Limon et al., 2020). Although LSDV‐specific antibodies have been reported in some wild ruminants like eland, blue wildebeest, giraffe, greater kudu and impala, but their role in the LSD epidemiology is not well documented (Barnard, 1997). The incubation period for LSD in natural infections is about 1-4 weeks (Coetzer, 2004). The morbidity rate can greatly vary, ranging from 3 to 85% (Thomas and Maré, 1945). Although mortality rate of LSD is usually low (1 to 3%), but in some cases it may reach 40% (Babiuk et al., 2008; Coetzer, 2004). LSDV has a lower mortality rate compared to SPV and GPV infection (Limon et al., 2020). A recent study reported no significant variations were found in prevalence of LSD in cattle regarding age and sex (Elhaig et al., 2017), whereas the disease severity considerably varies depending on the breed of cattle (Davies, 1991a). Crossbred cattle are more susceptible to LSDV infection compared to zebu cattle (Gari et al., 2011; Kiplagat et al., 2020). Also, disease severity in young animals and cows in the peak of lactation is more pronounced causing severe loss to production (Al-Salihi, 2014). Since 2012, the disease has been spreading outside the African continent with outbreaks in many Middle East countries such as Israel, Jordan and Lebanon in 2012-2013, and continued spreading into and through Turkey in 2013, and it is now endemic (EFSA, 2015, 2018). In 2014, LSD outbreak was reported in Azerbaijan (Zeynalova et al., 2016). In 2015, LSDV spread to Greece, the Caucasus and Russia. In 2016, the virus further spread east into the Balkan region, north towards Moscow, and west into Kazakhstan (Sprygin et al., 2018a; Tasioudi et al., 2016). According to the OIE, LSD outbreak has also been notified in many other countries, including Kuwait (1991), Lebanon (1993), Yemen (1995), United Arab Emirates (2000), Bahrain (2003), Israel (2006-2007), and Oman (2010) (Shimshony and Economides, 2006). LSD was first reported in Bangladesh in September, 2019, but the outbreak was started in July, 2019 and confirmed in August, 2019 (Figure 1) (OIE World Animal Health Information Database, 2019). In 2019, LSD was also reported in China and India for the first time (EFSA, 2020). The overall prevalence of 2019 LSD outbreak in cattle of Bangladesh was 2.19%, and the highest prevalence was 8.26%, observed in Chattogram (Table 1) (Food Security Cluster. Situation Report: Lumpy Skin Disease in Bangladesh, 2019). The lowest prevalence (0.01%) was observed in the cattle of Sylhet and Mymensingh division, Bangladesh (Table 1), which may indicate the influence of geographic distribution on LSD outbreak due to vectors prevalence involved in LSDV transmission. The seasonal pattern influencing LSD outbreaks is an important factor from epidemiological point of view to consider, indicating its relationships with vector prevalence (EFSA, 2019). In Bangladesh during monsoon season (May–August) the vector activity is increased and that will influence the outbreaks of LSD. In 2020, the outbreaks of LSD are ongoing which causing thousands of new infections with 1-2% mortality (Dhaka Tribune, 2020b). During no or minimal vector activity where LSDV resides is not well characterized (Tuppurainen et al., 2017a). Although there is no report indicating a carrier state for LSDV infected animals (Tuppurainen et al., 2017a), but a recent study in an experimental infection demonstrated the presence of live LSDV in lymph nodes and testicles of clinically and sub-clinically infected animals, suggestive for the reservoirs of live LSDV (Kononov et al., 2019).

 

Table 1: Prevalence of LSD in cattle population in different divisions of Bangladesh (Food Security Cluster. Situation Report: Lumpy Skin Disease in Bangladesh, 2019).

Division

Cattle population

LSD cases

Prevalence (%)

95% CI

P value

Dhaka

3906043

17300

0.44

0.43-0.45

P<0.0001

Chattogram

3145717

259765

8.26

8.23-8.29

Rajshahi

4276463

13854

0.32

0.31-0.33

Khulna

3610506

235633

6.53

6.5-6.56

Sylhet

1572944

182

0.01

0.01-0.01

Barisal

1770563

22232

1.26

1.24-1.28

Rangpur

4608034

4256

0.09

0.09-0.09

Mymensingh

2437626

306

0.01

0.01-0.01

95% CI: 95%-confidence interval.

 

 

Modes of transmission of LSDV

The transmission modes of LSDV between animals and from herd to herd are incompletely understood. Direct transmission of LSDV between animals may occur but its relative importance compared to vector transmission yet to confirm. Several studies suggest that LSDV can be mechanically transmitted by different blood-feeding vectors (Sprygin et al., 2019). LSDV is mainly transmitted by arthropod vectors like biting flies, ticks such as Rhipicephalus appendiculatus, Rhipicephalus decoloratus and Amblyomma hebraeum, and mosquitoes (Aedes aegypti) (Chihota et al., 2001; Lubinga et al., 2014). The virus can be transmitted through contaminated mouth parts of vectors without real replication of the virus inside arthropod cells or tissues (Sprygin et al., 2019). Chihota et al. (2001) demonstrated the mechanical transmission of LSDV in the mosquito Aedes aegypti, which is prevalent in Bangladesh (Paul et al., 2018), and may act as mechanical vector for LSDV transmission. Tuppurainen et al. showed the association of male Rhipicephalus appendiculatus ticks in LSDV transmission (Tuppurainen et al., 2013). Kamal et al. (1996) reported the prevalence of Rhipicephalus appendiculatus ticks in 65.45% cattle of Chittagong hilly area in Bangladesh, and it is noteworthy to mention that the first outbreak of LSDV infection was reported in Chittagong area of Bangladesh (OIE World Animal Health Information Database, 2019). Stomoxys calcitrans (Stable fly) was reported as the most important vector for LSDV transmission during LSD outbreaks in Israel (Yeruham et al., 1995; Kahana-Sutin et al., 2017). A recent study demonstrated Stomoxys calcitrans as the most efficient vector for LSDV transmission, where Aedes aegypti was found as an efficient vector, but Culicoides nubeculosus, Anopheles stephensi, and Culex quinquefasciatus were inefficient for LSDV transmission (Gubbins, 2019). Sohier et al. (2019) showed that both Stomoxys calcitrans and Haematopota spp. can support mechanical transmission of LSDV. Chihota et al. (2003) reported the failure of LSDV transmission by Culicoides nubeculosus. In a recent study, Sprygin et al. (2018b) demonstrated that the common housefly (Musca domestica) could be involved in the LSD transmission. Although further work is required to confirm the role of M. domestica in the transmission of LSDV (Sprygin et al., 2018b), but it is speculated that houseflies may play an important role in the seasonal transmission of LSD in Bangladesh.

The sharing of feed or water troughs contaminated by discharges from infected animals may act as an indirect route of LSDV transmission (Ali et al., 2012). LSDV can be transmitted by intrauterine transmission (Rouby and Aboulsoud, 2016), as well as from mother to calf through skin lesions on the mother’s udder and teats or through contaminated milk (Tuppurainen et al., 2017b). Prevalence of arthropod vectors may vary between regions due to variations in climate, season, temperature, humidity and vegetation, therefore, vectors in different areas are required to be investigated for the involvement in LSDV transmission depending on their abundance and feeding behaviour. Indirect vector transmission is predominant at small distances, but movement of infected animals may play the vital role in long-distance spreading of the disease (Sprygin et al., 2019; Saegerman et al., 2018). Extremes of weather and natural disasters may influence the spreading of vector-borne infectious disease, suggesting an association of climate change with these events (Jones et al., 2008). A recent study indicated that precipitation and temperature are positively associated with the risks for LSDV, while negatively affected by wind (Machado et al., 2019). Therefore, understanding the cause of a disease emergence is very critical to its prevention.

 

 

Pathogenesis

A schematic representation of LSD pathogenesis has been indicated in Figure 2. Briefly, LSD is a systemic disease of cattle, characterized by fever, followed by the development of nodular lesions in the skin that can cover the entire body (Tuppurainen et al., 2017b; Constable et al., 2017). Then virus spread to the secondary sites of replication, primarily by monocytes. LSDV has a tropism of keratinocytes, and it causes hyperplasia and ballooning degeneration of keratinocytes (Coetzer, 2004). Then, there is the formation of epidermal microvesicles, and inflammatory cells enter into dermis. Finally, epidermal microvesicles coalesce into large vesicles, and ulceration develops (Mulatu and Feyisa, 2018).

The economic impacts of LSD in the world and Bangladesh

LSD is one of the economically significant diseases causing severe production loss. The impacts of disease are usually easy to identify but difficult to quantify. When the disease outbreaks are broad a long-term effect on livestock leads to the great impacts on the economy of the country. The cost of animal disease depends on the losses related to animal illness, death, reduced production and losses in trade and other revenues (Rushton, 2009). LSD renders decreased milk and beef production, loss of draft power, mortality, increased treatment and vaccination costs, embargo on trades, and thus LSD may affect overall economy of the farmers as well as of the country (Gari et al., 2011). LSD also has socio-economic impacts (Tuppurainen and Oura, 2012). The economic impact of the disease relates to the prolonged convalescence, and in this respect, LSD is similar to another transboundary disease of cloven-hoofed animals, foot-and-mouth disease. The OIE categorizes LSD as a notifiable disease because of the major economic impact caused by the outbreak. LSD occurrence in dairy herd causes sharp decrease in the milk production. In addition, LSD occurrence results loss of weight gain, increased abortion rates, and damage to hides (Tuppurainen et al., 2012). A recent study in Ethiopia showed LSD as an economically devastating viral disease causing financial problems in livestock industries due to significant milk production loss, infertility, abortion, trade embargo and sometimes death (Gumbe, 2018). Another recent study demonstrated how LSD can cause significant economic losses, and it was found that the economic losses were related to death of the LSDV-infected animals, selling of the infected animals at low price, slaughtering of the animals, treatment cost, and production loss of milk and meat (Limon et al., 2020).

The livestock sector in Bangladesh is an integral component of agriculture, which accounts for 1.54% of total gross domestic product (GDP) in Bangladesh (Livestock Economy at a Glance, 2018). Cattle are one of the main components of the livestock sector in Bangladesh. LSD may substantially impact on the livelihoods of small-scale farmers and poor rural communities, which make up the majority of cattle owners in Bangladesh. The cost for providing supportive treatment for 2-3 months during the recovery period from LSD is unrealistic for many of these low-income farmers (Food Security Cluster. Situation Report: Lumpy Skin Disease in Bangladesh, 2019).

Control and prevention of LSD

So far, there is no effective antiviral against LSDV infection. Different approaches are in use for the prevention and control of LSD outbreaks. Using a single approach, it is difficult to effectively control and prevent LSDV infection. Therefore, multiple approaches are required for control and prevention of the LSDV infection, including restricted movements, screening, quarantine, and disinfection of the infected animals, control of vectors, vaccinations and treatment of affected animals to prevent secondary bacterial infections (Tuppurainen et al., 2017b).

Vaccines and vaccination

Despite some limitations such as adverse reactions, longer waiting period after last outbreak to achieve disease free status, limited clinical surveillance for the disease in subpopulation, etc., vaccination has been proved as best tool for quick and effective control of LSD, as it reduces the total number of susceptible animals within the population, and prevent entry and spread of the disease (EFSA, 2019). Moreover, vaccination is easier to implement than other approaches such as vector control and stamping out of the affected cattle or unaffected cattle in the affected herds. Also, vaccination protects the animals from the clinical manifestation of the disease and thus direct and indirect economic losses are prevented. Notably, different countries have shown the success in controlling LSD outbreak by vaccination campaign. For example, vaccination campaign of cattle population in Balkan region with LSD homologous vaccine strain reduced the outbreaks from 7483 cases in 2016 to 385 cases in 2017, and in 2018 there was no reports of outbreaks, confirming the effectiveness of LSD homologous vaccine strain (EFSA, 2019). Genomic analysis revealed the closeness of the CaPVs, where 98% sequence similarity exists between all three species (Tulman et al., 2002; Gershon and Black, 1988; Black et al., 1986), and Capripoxviruses cannot be distinguished serologically from each other (Carn, 1993). Due to the antigenic homology these viruses can provide cross-protection (Capstick and Coackley, 1961). Therefore, it might be possible to use a single vaccine strain to protect cattle, sheep and goats (Kitching, 2003). Despite effectivity of a heterogenous vaccine sometimes recurrence of disease after vaccination becomes a limitation to its use. An incomplete protection has been reported in cattle vaccinated with SPV vaccines against LSD (Brenner et al., 2009; Ayelet et al., 2013). Notably, in Turkey, despite continued vaccination with heterologous vaccines since 2014 still there is LSD outbreak reports, indicating an insufficient protection of heterologous vaccine (EFSA, 2019, 2020). In addition, Abdallah et al. (2018) reported the infection of LSDV in cattle previously vaccinated with Romanian SPPV vaccine, which requires further evaluation of vaccine efficacy under field conditions. Moreover, in an efficacy study, Kenyan sheep pox virus strain vaccine (KS1 O-180) showed poor efficacy in protecting cattle populations against LSD infection under field conditions (Molla et al., 2017). However, a recent study demonstrated that Goatpox virus (G20-LKV) vaccine strain elicits a strong protective response and showed full protection in cattle against LSD (Zhugunissov et al., 2020).

In another field study in Israel, Ben-Gera et al. showed that Neethling vaccines provide good protection in cattle, and is superior to attenuated SPV vaccine in preventing LSD morbidity (Ben-Gera et al., 2015). In 2019, no LSD outbreak was reported in South‐Eastern Europe, where a mass vaccination programme with homologous LSD vaccine was conducted (EFSA, 2020). There are different vaccines for LSD, including LSDV Neethling vaccine, Kenyan sheep and goat pox (KSGP) O-180 strain vaccines and Gorgan goat pox vaccine, with different trade names. Therefore, selection of a right vaccine candidate against LSD is crucial for its effective control and prevention. According to Officials of DLS-Bangladesh, a heterogenous goatpox vaccine was administered to 34,000 heads of cattle in Chattogram, Bangladesh, and the vaccine was found to be effective against LSD (Dhaka Tribune, 2020). Until recently, there is no LSDV vaccine developed in Bangladesh for vaccinating cattle against LSD (personal communication). An effective homogenous LSDV vaccine is essential for successful control and elimination of the LSD (EFSA, 2020). In particular, achieving the highest vaccination coverage in the shortest period of time is cornerstone to rapidly control of LSD outbreaks, along with good clinical surveillance for immediate notification of suspected clinical cases that should be confirmed in the laboratory to differentiate LSD field virus from the vaccine strain. Also, any country lifting its vaccination program is expected to demonstrate that it is disease-free by setting up a surveillance scheme along the lines indicated by the OIE. Although stamping out strategy is implemented in some countries as an efficient method despite high cost for preventing the spread of an infectious disease like LSD, but this strategy seems to be not that much feasible in the context of the economy of Bangladesh, as the majority of cattle farmers in this country are poor or very poor. In case of stamping out policy implementation the affected farmers should be sufficiently compensated.

Vector control

Vector-borne transmission of LSD is a big threat towards LSD control and prevention. An effective vector control or vector elimination program is crucial to limit the transmission of LSDV. Information on how long the insect vectors remain infective for LSDV transmission and the capability of spreading the disease is important to control LSD. It is important to detect which insect acts as a major vector for LSDV transmission in a certain geographic region. Also, better LSD control and prevention strategies are important for the prevention of the re-emergence of disease in an area where outbreak already occurred. Effective vector control is imperative as it is thought that it will reduce the impact of the disease in endemic areas and also inhibit further spread of the disease into new areas. Design and implementation of effective and economically viable vector control plans are important to make the vector control program successful and to reduce the expense of the vector control program. It has been evident that LSD is endemic in many countries in Africa and has never been eradicated once it has entered a new region, indicating effective vector control is crucial for the prevention of the re-emergence of the disease. In Bangladesh the climatic conditions are favorable for vectors propagation, which may make difficult of the successful vector control program and thus LSD control. So the possibility of resurge of infection in the coming years cannot be ruled out. Notably, in Russia the first LSD outbreak was reported in 2015, but most devastating year for Russia was 2016 (Kononov et al., 2017). The risk in farms with outdoor access is six times higher than in farms where animals are kept indoors, independent of vaccination status, possibly because of higher exposure to vectors bite (EFSA, 2018). A proper epidemiological investigation to assess the risk factors associated with the ever first LSD outbreaks in Bangladesh is needed to develop a context-appropriate intervention for preventing infections and limiting the spread of LSDV in cattle population.

Awareness building

Considering the consequence of LSD outbreaks in cattle industry in Bangladesh, DLS-Bangladesh should take different steps to tackle the spread of the disease, including active monitoring and surveillance of the cattle farms, holding of the awareness increasing events for the farmers, cattle traders, and personnel related to cattle industry, and technicians, strategic plans about vaccinations, etc. Furthermore, to reduce the LSD spread implementation of all the possible approaches should be ascertained, including restricted or total banned of cattle movement in affected areas, awareness building of the farmers, instructions on separation of the affected cattle and avoidance of communal grazing, and frequent treatment of cattle with insect repellents to minimize the risk of vector transmission of the disease. Furthermore, the farmers should be introduced about the telemedicine veterinary services, which is very important particularly to reduce the LSD spread and avoid fatal outcome of LSD during this COVID-19 health emergency.

Active surveillance and early detection

To limit the spread of LSDV infection, active surveillance and early detection are very important. Particularly, active monitoring and surveillance is highly essential as many farmers are not aware of LSDV infection and its impacts on animal health. Many farmers also lack of knowledge of transmission patterns of LSD. Furthermore, there are some farmers those are even not aware of this cattle disease in Bangladesh. Both active and passive monitoring and surveillance should be enforced for limiting the spread of the infection, and effective vector control program and adopting vaccination strategy may finally remove LSDV infection from Bangladesh and restore the LSD-free status in the country. Also, free-ranging herds that are not monitored daily outbreaks may remain undetected for weeks, may help in further spreading. Active surveillance is very much essential for early detection of the disease (EFSA, 2020). If vaccinations are done, post-vaccination monitoring and evaluation of vaccination program is also important. The outbreaks in India (EFSA, 2020) represent a threat for the neighboring Bangladesh, which can be at risk of new incursion. Due to religious value in India maybe no stamping out policy will be implemented, so the affected cattle may remain as the source for further infection. Therefore, a continued active monitoring will be necessary for controlling LSDV infection in Bangladesh.

Early detection of the disease is paramount in limiting the spread of any disease, particularly LSD. Any lacking in laboratory capacity may compromise the early detection of LSD, which may facilitate the spreading of the disease. Therefore, an improved laboratory facilities towards early detection of LSDV infection is also required. It is also of importance to establish the reference laboratory for LSDV detection and molecular characterization, and monitoring of the affected animals/herds. Moreover, continuous monitoring and surveillance are important for screening and early detection of LSD. Moreover, the majority of the small-scale cattle farmers in Bangladesh lack knowledge of LSDV infection, therefore, it is also necessary to train the farmers. Prophylactic vaccination of the entire cattle population may control and prevent the outbreaks, if vaccination is done well in advance in at-risk areas. In economic context, slaughtering of all LSDV-infected and in-contact animals is not feasible in majority of the cattle rearing farmers in Bangladesh, which may further complicate the control and eradication of LSDV, because of the transmission of the virus via arthropod vectors from asymptomatic viraemic animals (Tuppurainen et al., 2017b). The knowledge in the context of cattle rearing practices, vaccination approaches, managing sick/dead animals should be made available to the farmers, which will help toward control and prevention of the disease. Moreover, molecular epidemiologic study is necessary to detect the isolates and origin of the isolates causing LSD outbreaks in the cattle population of Bangladesh, which is also needed for proper control planning and its implementation.

 

Conclusion

LSD is economically important due to its significant effects on the livelihoods of small-scale farmers. LSD may be considered as an emerging animal disease of substantial importance as climatic changes favoring arthropod vectors propagation that involved in LSDV transmission. Once LSD has occurred in a country virtually it is impossible to eradicate. An effective vaccination campaign is required to greatly reduce the morbidity and economic effects of an epizootic. It is important to set a nationwide control plan for early detection by active surveillance to take immediate action if any outbreak/infection is reported. Moreover, it is important to investigate and detect the risk factors for LSD in the context of Bangladesh. The information on LSDV local isolates and their phylogenetic analysis is of importance to understand LSDV molecular epidemiology and to develop vaccine with local isolates for effective control and prevention of the disease.

 

Acknowledgements

The authors would like to thank Prof. Dr. Kyoko Tsukiyama-Kohara, Kagoshima University, Japan for her logistic support. The authors are also grateful to Dr. Sayeh Ezzikouri, Institut Pasteur du Maroc, Morocco for his help in data analysis.

 

Authors Contribution

All authors contributed equally to this study.

Conflict of interest

The authors have declared no conflict of interest.

 

References

Abdallah, F.M., H.M. El-Damaty and G.F. Kotb. 2018. Sporadic cases of lumpy skin disease among cattle in Sharkia province, Egypt: Genetic characterization of lumpy skin disease virus isolates and pathological findings. Vet. World. 11: 1150–1158. https://doi.org/10.14202/vetworld.2018.1150-1158

Ali, H., A.A. Ali, M.S. Atta and A. Cepica.2012. Common, emerging, vector-borne and infrequent abortogenic virus infections of cattle. Transbound, Emerg. Dis. 59: 11–12. https://doi.org/10.1111/j.1865-1682.2011.01240.x

Al-Salihi, K., 2014. Lumpy skin disease: Review of literature. Mirror Res. Vet. Sci. Anim., (MRVSA) 3: 6–23.

Ayelet, G., Y. Abate, T. Sisay, H. Nigussie, E. Gelaye, S. Jemberie and K. Asmare. 2013. Lumpy skin disease: preliminary vaccine efficacy assessment and overview on outbreak impact in dairy cattle at Debre Zeit, central Ethiopia. Antivir. Res. 98: 261–265. https://doi.org/10.1016/j.antiviral.2013.02.008

Babiuk, S., T. Bowden, D. Boyle, D. Wallace and R. Kitching. 2008. Capripoxviruses: an emerging worldwide threat to sheep, goats and cattle. Transbound. Emerg. Dis., 55: 263–272. https://doi.org/10.1111/j.1865-1682.2008.01043.x

Barnard, B.J.H., 1997. Antibodies against some viruses of domestic animals in South African wild animals. Onderstepoort J. Vet. Res., 64: 95–110.

Ben-Gera, J., E. Klement, E. Khinich, Y. Stram and N.Y. Shpigel. 2015. Comparison of the efficacy of Neethling lumpy skin disease virus and x10RM65 sheep-pox live attenuated vaccines for the prevention of lumpy skin disease - The results of a randomized controlled field study. Vaccine. 33: 4837–4842. https://doi.org/10.1016/j.vaccine.2015.07.071

Black, D.N., J.M. Hammond and R.P. Kitching. 1986. Genomic relationship between capripoxviruses. Virus Res. 5: 277–292. https://doi.org/10.1016/0168-1702(86)90024-9

Brenner, J., M. Bellaiche, E. Gross, D, Elad, Z. Oved, M. Haimovitz, A. Wasserman, O. Friedgut, Y. Stram, V.Y. Bumbarov and H. Yadin. 2009. Appearance of skin lesions in cattle populations vaccinated against lumpy skin disease: statutory challenge. Vaccine. 27: 1500–1503. https://doi.org/10.1016/j.vaccine.2009.01.020

Capstick, P.B. and W. Coackley. 1961. Protection of cattle against lumpy skin disease: I.-trials with a vaccine against Neethling type infection. Res. Vet. Sci., 2: 362–368. https://doi.org/10.1016/S0034-5288(18)34940-3

Carn, V.M., 1993. Control of capripoxvirus infections. Vaccine. 11: 1275–1279. https://doi.org/10.1016/0264-410X(93)90094-E

Chihota, C.M., L.F. Rennie, R.P. Kitching and P.S. Mellor. 2001. Mechanical transmission of lumpy skin disease virus by Aedes aegypti (Diptera: Culicidae). Epidemiol. Infect., 126: 317–321. https://doi.org/10.1017/S0950268801005179

Chihota, C.M., L.F. Rennie, R.P. Kitching and P.S. Mellor. 2003. Attempted mechanical transmission of lumpy skin disease virus by biting insects. Med. Vet. Entomol., 17: 294–300. https://doi.org/10.1046/j.1365-2915.2003.00445.x

Coetzer, J.A.W., 2004. Lumpy skin disease. In: Infectious diseases of livestock (Eds. J.A.W. Coetzer, R.C. Tustin). 2nd ed., vol. 2, Oxford University Press, Cape Town, pp. 1268–1276.

Constable, P.D., K.W. Hinchcliff, S.H.Done and W. Grundberg. 2017. Veterinary Medicine: A Textbook of the Diseases of Cattle, Horses, Sheep, Pigs, and Goats. 11th edn. Elsevier, UK. pp. 1591.

Davies, F.G., 1991a. Lumpy skin disease, an African capripox virus disease of cattle. Br. Vet. J., 147: 489–503. https://doi.org/10.1016/0007-1935(91)90019-J

Davies, F.G., 1991b. Lumpy skin disease of cattle: A growing problem in Africa and the Near East. World Anim. Rev., 68: 37–42.

Dhaka Tribune. January 11, 2020a. Vaccination to curb LSD epidemic of cattle. https://www.dhakatribune.com/bangladesh/nation/2020/01/11/vaccination-to-curb-lsd-epidemic-of-cattle.

Dhaka Tribune. June 24, 2020b. LSD disease returns: Loss of cattle in rapid contagion worries farmers ahead of Eid. https://www.dhakatribune.com/bangladesh/nation/2020/06/24/lsd-disease-resurfaces-loss-of-cattle-in-rapid-contagion-worry-farmers-ahead-eid.

Diallo, A. and G.J. Viljoen. 2007. Poxviruses: Genus capripoxvirus. Edited by Mercer AA, Axel Schmidt A, Weber O, Springer. pp. 167–181. https://doi.org/10.1007/978-3-7643-7557-7_8

EFSA (European Food Safety Authority) 2018. Scientific report on lumpy skin disease II. Data collection and analysis. EFSA J., 16: e05176. https://doi.org/10.2903/j.efsa.2018.5176

EFSA (European Food Safety Authority), P. Calistri, K. DeClercq, S. Gubbins, E. Klement, A. Stegeman, J.C. Abrahantes, D. Marojevic, S.E. Antoniou and A. Broglia. 2020. Lumpy skin disease epidemiological report IV: Data collection and analysis. EFSA J., 18: e06010. https://doi.org/10.2903/j.efsa.2020.6010

EFSA (European Food Safety Authority), P. Calistri, K. DeClercq, S. Gubbins, E. Klement, A. Stegeman, J. Cortinas-Abrahantes, S.E. Antoniou, A. Broglia and A. Gogin. 2019. Scientific report on lumpy skin disease: III. Data collection and analysis. EFSA J., 17: e05638. https://doi.org/10.2903/j.efsa.2019.5638

EFSA A.H.A.W., 2015. Panel (EFSA Panel on Animal Health and Welfare). Scientific opinion on lumpy skin disease. EFSA J. 13: 3986. https://doi.org/10.2903/j.efsa.2015.3986

Elhaig, M.M., A. Selim and M. Mahmoud. 2017. Lumpy skin disease in cattle: Frequency of occurrence in a dairy farm and a preliminary assessment of its possible impact on Egyptian buffaloes. Onderstepoort. J. Vet. Res., 84: e1–e6. https://doi.org/10.4102/ojvr.v84i1.1393

El-Nahas, E.M., A.S. El-Habbaa, G.F. El-Bagoury and M.E.I. Radwan. 2011. Isolation and identification of lumpy skin disease virus from naturally infected buffaloes at Kaluobia. Egypt. Glob. Vet., 7: 234–237.

Fenner, F., 1996. Poxviruses. In: Fields B.N., Knipe, D.M., Howley, P.M., editors. Fields virology. Philadelphia, Pa: Lippincott-Raven. pp. 2673–2702.

Food Security Cluster. Situation Report: Lumpy Skin Disease in Bangladesh. 2019. https://fscluster.org/sites/default/files/documents/sitrep_lsd_20191210.pdf.

Gari, G., B.P. onnet, F. Roger and A. Waret-Szkuta 2011. Epidemiological aspects and financial impact of lumpy skin disease in Ethiopia. Prev. Vet. Med., 102: 274–283. https://doi.org/10.1016/j.prevetmed.2011.07.003

Gershon, P.D. and D.N. Black 1988. A comparison of the genomes of capripoxvirus isolates of sheep, goats, and cattle. Virology. 164: 341–349. https://doi.org/10.1016/0042-6822(88)90547-8

Gortázar. C. and J. de la Fuente 2020. COVID-19 is likely to impact animal health. Prev. Vet. Med., 180: 105030. https://doi.org/10.1016/j.prevetmed.2020.105030

Gubbins, S., 2019. Using the basic reproduction number to assess the risk of transmission of lumpy skin disease virus by biting insects. Transbound. Emerg. Dis., 66: 1873–1883. https://doi.org/10.1111/tbed.13216

Gumbe, A.A.F., 2018. Review on lumpy skin disease and its economic impacts in Ethiopia. J. Dairy Vet. Anim. Res., 7: 39–46. https://doi.org/10.15406/jdvar.2018.07.00187

Jones, K.E., N.G. Patel, M.A. Levy, A. Storeygard, D. Balk, J.L. Gittleman and P. Daszak. 2008. Global trends in emerging infectious diseases. Nature. 451: 990–993. https://doi.org/10.1038/nature06536

Kahana-Sutin, E., E. Klement, I. Lensky and Y. Gottlieb. 2017. High relative abundance of the stable fly Stomoxys calcitrans is associated with lumpy skin disease outbreaks in Israeli dairy farms. Med. Vet. Entomol., 31: 150–160. https://doi.org/10.1111/mve.12217

Kamal, A., K. Uddin, M. Islam and M. Mondal 1996. Prevalence of economically important ticks in cattle and goat at Chittagong Hilly areas of Bangladesh. Asian-Austral. J. Anim. Sci., 9: 567–570. https://doi.org/10.5713/ajas.1996.567

Kiplagat, S.K., P.M. Kitala, J.O. Onono, P.M. Beard and N.A. Lyons. 2020. Risk Factors for Outbreaks of Lumpy Skin Disease and the Economic Impact in Cattle Farms of Nakuru County, Kenya. Front Vet. Sci. 7: 259. https://doi.org/10.3389/fvets.2020.00259

Kitching, R., 2003. Vaccines for lumpy skin disease, sheep pox and goat pox. Dev. Biol., 114: 161–167.

Kononov, A., O. Byadovskaya, S. Kononova, R. Yashin, N. Zinyakov, V. Mischenko, N. Perevozchikova and A. Sprygin. 2017. Detection of vaccine-like strains of lumpy skin disease virus in outbreaks in Russia in 2017. Arch. Virol. 164:1575–1585. https://doi.org/10.1007/s00705-019-04229-6

Kononov, A., P. Prutnikov, I. Shumilova, S. Kononova, A. Nesterov, O. Byadovskaya, Y. Pestova, V. Diev and A. Sprygin. 2019. Determination of lumpy skin disease virus in bovine meat and offal products following experimental infection. Transbound. Emerg. Dis., 66: 1332–1340. https://doi.org/10.1111/tbed.13158

Limon, G., A.A. Gamawa, A.I. Ahmed, N.A. Lyons and P.M. Beard. 2020. Epidemiological characteristics and economic impact of lumpy skin disease, sheeppox and goatpox among subsistence farmers in northeast Nigeria. Front. Vet. Sci., 7: 8. https://doi.org/10.3389/fvets.2020.00008

Livestock Economy at a Glance, 2018. Available at: http://dls.portal.gov.bd/sites/default/files/files/dls.portal.gov.bd/page/ee5f4621_fa3a_40ac_8bd9_898fb8ee4700/Livestock%20Economy%20at%20a%20glance%20%20%282017-2018%29.pdf.

Lubinga, J.C., S.J. Clift, E.S. Tuppurainen, W.H. Stoltsz, S. Babiuk, J.A. Coetzer and E.H. Venter. 2014. Demonstration of lumpy skin disease virus infection in Amblyomma hebraeum and Rhipicephalus appendiculatus ticks using immunohistochemistry. Ticks Tick Borne Dis. 5: 113–120. https://doi.org/10.1016/j.ttbdis.2013.09.010

MacDonald, R.A.S., 1931. Pseudo-Urticaria of cattle. Northern rhodesian department of health annual report. pp. 20–21.

Machado, G., F. Korennoy, J. Alvarez, C. Picasso-Risso, A. Perez and K. Vander-Waal. 2019. Mapping changes in the spatiotemporal distribution of lumpy skin disease virus. Transbound. Emerg. Dis., 66: 2045–2057. https://doi.org/10.1111/tbed.13253

Molla, W., K. Frankena, G. Gari and M.C.M. de Jong. 2017. Field study on the use of vaccination to control the occurrence of lumpy skin disease in Ethiopian cattle. Prev. Vet. Med., 147: 34–41. https://doi.org/10.1016/j.prevetmed.2017.08.019

Mulatu, E. and A. Feyisa. 2018. Review: Lumpy Skin Disease. J. Vet. Sci. Technol., 9: 535. https://doi.org/10.4172/2157-7579.1000535

OIE World Animal Health Information Database [WAHID]. 2019. OIE World Animal Health Information Database. Available at: https://www.oie.int/wahis_2/public/wahid.php/Reviewreport/Review?page_refer=MapFullEventReport&reportid=31742.

Paul, K.K., P. Dhar-Chowdhury, C.E. Haque, H.M. Al-Amin, D.R. Goswami, M.A.H. Kafi, M.A. Drebot, L.R. Lindsay, G.U. Ahsan and, W.A. Brooks. 2018. Risk factors for the presence of dengue vector mosquitoes, and determinants of their prevalence and larval site selection in Dhaka, Bangladesh. PLoS One. 13: e0199457. https://doi.org/10.1371/journal.pone.0199457

Rouby, S. and E. Aboulsoud. 2016. Evidence of intrauterine transmission of lumpy skin disease virus. Vet. J., 209: 193–195. https://doi.org/10.1016/j.tvjl.2015.11.010

Rushton, J., 2009. The economics of animal health and production. CABI, Oxfordshire, UK. pp. 73–197.

Saegerman, C., S. Bertagnoli, G. Meyer, J.P. Ganière, P. Caufour, K. De Clercq, P. Jacquiet, G. Fournié, C. Hautefeuille, F. Etore and J. Casal. 2018. Risk of introduction of lumpy skin disease in France by the import of vectors in animal trucks. PLoS One. 13: e0198506. https://doi.org/10.1371/journal.pone.0198506

Şevik, M., O. Avci, M. Doğan and Ö.B. İnce. 2016. Serum biochemistry of lumpy skin disease virus-infected cattle. Biomed. Res. Int., 2016: 6. https://doi.org/10.1155/2016/6257984

Shimshony, A. and Economides. 2006. Disease prevention and preparedness for animal health emergencies in the Middle East. Rev. Sci. Tech., 25: 253–269. https://doi.org/10.20506/rst.25.1.1667

Sohier, C., A. Haegeman, L. Mostin, I. De Leeuw, W. Van Campe, A. De Vleeschauwer, E.S.M. Tuppurainen, T. van den Berg, N. De Regge and K. De Clercq 2019. Experimental evidence of mechanical lumpy skin disease virus transmission by Stomoxys calcitrans biting flies and Haematopota spp. horseflies. Sci. Rep., 9: 20076. https://doi.org/10.1038/s41598-019-56605-6

Sprygin, A., E. Artyuchova, Y. Babin, P. Prutnikov, E. Kostrova, O. Byadovskaya and A. Kononov. 2018a. Epidemiological characterization of lumpy skin disease outbreaks in Russia in 2016. Transbound. Emerg. Dis., 65: 1514–1521. https://doi.org/10.1111/tbed.12889

Sprygin, A., Y. Pestova, D. Wallace, E. Tuppurainen and A. Kononov. 2019. Transmission of lumpy skin disease virus: A short review. Virus Res., 269: 197637. https://doi.org/10.1016/j.virusres.2019.05.015

Sprygin, A., Y. Pestova, P. Prutnikov and A. Kononov 2018b. Detection of vaccine‐like lumpy skin disease virus in cattle and Musca domestica L. flies in an outbreak of lumpy skin disease in Russia in 2017. Transbound. Emerg. Dis., 65: 1137–1144. https://doi.org/10.1111/tbed.12897

Tageldin, M.H., D.B. Wallace, G.H. Gerdes, J.F. Putterill, R.R. Greyling, M.N. Phosiwa, R.M. Al Busaidy and A.S.I. Ismaaily. 2014. Lumpy skin disease of cattle: an emerging problem in the Sultanate of Oman. Trop. Anim. Health Prod., 46: 241–246. https://doi.org/10.1007/s11250-013-0483-3

Tasioudi, K.E., S.E. Antoniou, P. Iliadou, A. Sachpatzidis, E. Plevraki, E.I. Agianniotaki, C. Fouki, O. Mangana-Vougiouka, E. Chondrokouki, and C. Dile 2016. Emergence of Lumpy Skin Disease in Greece, 2015. Transbound. Emerg. Dis., 63: 260–265. https://doi.org/10.1111/tbed.12497

Thomas, A.D. and C.V.E. Maré. 1945. Knopvelsiekte. J. S. Afr. Vet. Med. Assoc., 16: 36–43.

Tulman, E.R., C.L. Afonso, Z. Lu, L. Zsak, G.F. Kutish and D.L. Rock. 2001. Genome of lumpy skin disease virus. J. Virol., 75: 7122–7130. https://doi.org/10.1128/JVI.75.15.7122-7130.2001

Tulman, E.R., C.L. Alfonso, Z. Lu, L. Zsak, J.H. Sur, N.T. Sandybaev, U.Z. Kerembekova, V.L Zaitsev, G.F. Kutish, and D.L. Rock. 2002. The genomes of sheeppox and goatpox viruses. J. Virol., 76: 6054–6061. https://doi.org/10.1128/JVI.76.12.6054-6061.2002

Tuppurainen, E.S.M., E.H. Venter, J.L. Shisler, G. Gari, G.A. Mekonnen, N. Juleff, N.A. Lyons, K. De Clercq, C. Upton, T.R. Bowden, S. Babiuk and L.A. Babiuk. 2017a. Review: Capripoxvirus diseases: Current status and opportunities for control. Transbound. Emerg. Dis., 64: 729–745. https://doi.org/10.1111/tbed.12444

Tuppurainen, E., T. Alexandrov and D. Beltrán-Alcrudo 2017b. Lumpy skin disease field manual. A manual for veterinarians. FAO Animal Production and Health Manual No. 20. Rome. FAO of the UN. pp. 60.

Tuppurainen, E.S.M. and C.A.L. Oura. 2012. Review: Lumpy skin disease: an emerging threat to Europe, the Middle East and Asia. Transbound. Emerg. Dis., 59: 40–48. https://doi.org/10.1111/j.1865-1682.2011.01242.x

Tuppurainen, E.S.M., E.H. Venter, J.A. Coetzer and L. Bell-Sakyi. 2015. Lumpy skin disease: Attempted propagation in tick cell lines and presence of viral DNA in field ticks collected from naturally-infected cattle. Ticks Tick Borne Dis. 6: 134–140. https://doi.org/10.1016/j.ttbdis.2014.11.002

Tuppurainen, E.S.M., J.C. Lubinga, W.H. Stoltsz, M. Troskie, S.T. Carpenter, J.A.W. Coetzer, E.H. Venter and C.A.L. Oura. 2013. Mechanical transmission of lumpy skin disease virus by Rhipicephalus appendiculatus male ticks. Epidemiol. Infect., 141: 425–430. https://doi.org/10.1017/S0950268812000805

Von-Backström, U., 1945. Ngamiland cattle disease: Preliminary report on a new disease, the aetiological agent being probably of an infectious nature. J. S. Afr. Vet. Med. Assoc., 16: 29–35.

Woods, J.A., 1988. Lumpy skin disease-a review. Trop. Anim. Health Prod., 20: 11–17. https://doi.org/10.1007/BF02239636

World Health Organization. 2020. COVID-19 Bangladesh situation reports: Situation report-19. Available online: https://www.who.int/bangladesh/emergencies/coronavirus-disease-(covid-19)-update/coronavirus-disease-(covid-2019)-bangladesh-situation-reports (accessed on 11 July 2020).

Yeruham, I., O. Nir, Y. Braverman, M. Davidson, H. Grinstein, M. Haymovitch and O. Zamir. 1995. Spread of lumpy skin disease in Israeli dairy herds. Vet. Rec. 137: 91–93. https://doi.org/10.1136/vr.137.4.91

Zeynalova, S., K. Asadov, F. Guliyev, M. Vatani and A.V. liyev. 2016. Epizootology and molecular diagnosis of lumpy skin disease among livestock in Azerbaijan. Front. Microbiol., 7: 1022. https://doi.org/10.3389/fmicb.2016.01022

Zhugunissov, K., Y. Bulatov, M. Orynbayev, L. Kutumbetov, Y. Abduraimov, Y. Shayakhmetov, D. Taranov, Z. Amanova, M. Mambetaliyev, Z. Absatova, M. Azanbekova, B. Khairullin and E. Tuppurainen. 2020. Goatpox Virus (G20-LKV) Vaccine strain elicits a protective response in cattle against lumpy skin disease at challenge with lumpy skin disease virulent field strain in a comparative study. Vet. Microbiol., 245: 108695. https://doi.org/10.1016/j.vetmic.2020.108695

To share on other social networks, click on any share button. What are these?

Hosts and Viruses

December

Vol.10, Pages 1-71

Featuring

Click here for more

Subscribe Today

Receive free updates on new articles, opportunities and benefits


Subscribe Unsubscribe