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Paper Efficacy of vaccination against lumpy skin disease in Jordanian cattle S. M. Abutarbush The objective of this study was to assess the value and efficacy of vaccination against a natural outbreak of lumpy skin disease (LSD). Epidemiological data were collected from 101 vaccinated and unvaccinated farms in Jordan. In the unvaccinated holdings, the overall morbidity rate was 42.6 per cent, mortality rate 10.2 per cent and case fatality rate 23.9 per cent. Decreased feed intake, decreased milk production and fever were seen in 100 per cent, 76.9 per cent and 92.3 per cent of the cattle farms, respectively. The percentage reduction in milk production ranged from 0 to 100 per cent (mean=38.5 per cent, SE±9.6 per cent). The total loss/animal in the farm ranged from £27 to £2210 (mean=486, SE±162). In the vaccinated holdings, the overall morbidity rate was 4.7 per cent, mortality rate 1 per cent and case fatality rate 22.9 per cent. Decreased feed intake, decreased milk production and fever were seen in 23.8 per cent, 21.4 per cent and 23.8 per cent of the cattle farms, respectively. Percentage of decrease in milk production ranged from 0 to 100 per cent (mean=6 per cent, SE±1.8 per cent). The total loss/animal in the farm ranged from 0 to £2210 (mean=78, SE±29). Vaccination against LSD remains a viable method of control. Although it does not provide complete protection against the disease, it appears to reduce morbidity and mortality rates, production loss and treatment cost.

Introduction

Lumpy skin disease (LSD) is a serious, rapidly spreading, emerging disease of cattle. It is a vector borne disease caused by lumpy skin disease virus (LSDV). The virus belongs to the genus Capripoxvirus within the subfamily Chordopoxvirinae of the family Poxviridae. The disease has been reported in different countries of the Middle East, and now appears to be spreading to new territories such as Turkey and Iraq, which were thought to be free of the disease (OIE 2013, ProMEDMail 2013). LSD is becoming a more imminent threat to Europe, Asia and the rest of the world (Davies 1991, Tuppurainen and Oura 2012, Abutarbush and others 2013). LSD can be associated with mild or severe illness. It causes fever, generalised skin nodules and enlarged lymph nodes. Skin nodules are usually firmly circumscribed and affect all parts of the body, including the mucous membranes. In most clinically affected cases, the ‘inverted conical zone’ of necrosis and so-called ‘sitfast’ lesions are usually seen and considered characteristic. Clinical signs, histopathology lesions, virus isolation and PCR can all be used to diagnose LSD. Antibody ELISAs have been used in the past with limited success (Davies 1991, Tuppurainen and Oura 2012). Members of the capripox virus family are known to provide cross protection. Live attenuated sheep pox, goat pox and LSDV

Veterinary Record (2014) S. M. Abutarbush, BVSc, MVetSc, Diplomate ABVP, Diplomate ACVIM, Department of Veterinary Clinical Sciences, Faculty of Veterinary Medicine, Jordan University of Science and Technology, Irbid 22110, Jordan Veterinary Medicine Department, College of Food and Agriculture, United Arab Emirates University, Al Ain, UAE

doi: 10.1136/vr.102271 E-mail for correspondence: [email protected] Reprints will not be available from the authors Provenance: Not commissioned; externally peer reviewed Accepted June 16, 2014

vaccines can all be used to protect cattle against LSD infection (Kitching 1983). However, published reports about the field efficacy of the vaccines used in LSD prevention are scarce in the l­ iterature and their efficacy has been questioned (Brenner and ­others 2009, Ayelet and others 2013). There are two main published peerreviewed studies that investigated the efficacy of field vaccines (Brenner and others 2009, Ayelet and others 2013). In the first study (Brenner and others 2009), 11.1 per cent of the vaccinated cattle developed skin lesions after natural exposure to the disease. However, the number of affected cattle with clinical disease was five times higher compared with the unvaccinated cattle. In the second study (Ayelet and others 2013), the authors concluded that Kenyan sheep pox vaccine strain used to protect cattle from LSDV infection did not confer good protection against LSDV infection. In this study 22.9 per cent of animals were clinically affected while 2.31 per cent died of the disease. The aim of this study was to assess the efficacy of field vaccination against a natural outbreak of LSD in Jordan.

Materials and methods Study overview

LSD outbreak was reported in the governorate of Irbid in northern Jordan. After a vaccination campaign was started, the outbreak began to come to an end in the affected governorate. At that time, different cattle holdings were visited in various regions of the affected governorate. Unaffected and affected, vaccinated and unvaccinated farms were visited. Epidemiological data were collected about the study animals, farms, and course of the disease.

Description of the study area

The study was done in Irbid governorate which is located in the far north of Jordan, bordering the West Bank (Palestinian authority), Israel and Syria, and consists of nine districts. Vaccinated farms were considered at risk since the disease was reported across the affected governorate. September 27, 2014 | Veterinary Record

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Paper Farm visits and data collection

45.0%

Field vaccine testing

There were two main vaccines used by farmers. The first one, which was used extensively, was a sheep pox vaccine strain RM 65, Jovivac, produced by a local vaccine manufacturer, Jordan Bioindustries Centre (JOVAC). The second, which was used in a limited number of cases, was not labelled and was of unknown origin. Both vaccines were submitted to the Pirbright Institute, UK for molecular characterisation and further testing of the field vaccines.

40.0% 35.0% 30.0% Percentage (%)

Different cattle farms were visited in the various regions of Irbid ­governorate (affected/unaffected, vaccinated/unvaccinated). A questionnaire was filled out for each farm and information was gathered about infection (yes/no), vaccination (yes/no), date of vaccination, date of first clinical signs of the disease seen, total number of cattle in the premises, number of cattle affected, the number of cattle which died due to the disease, distribution of the skin lesion (body, udder and teat), presence of fever (yes/no), decrease feed intake (yes/no), abortion (yes/no), and decreased milk production (yes/no), approximate percentage of decreased milk production (if present), duration of illness, and the approximate cost of treatment until the time of data collection in Jordanian Dinar, which was converted to British pounds (£).

25.0% 20.0% 15.0% 10.0% 5.0% 0.0% Morbidity Rate

Not Vaccinated Farms

Microsoft Excel 2007 was used to record and organise the collected, cleaned and coded data. Data were analysed using descriptive statistical analysis software (SPSS software V.17, SPSS Inc, Chicago, Illinois, USA).

TABLE 1: Epidemiological data collected after using vaccination in a lumpy skin disease outbreak in Jordan Parameter

Non-vaccinated

Vaccinated

Vaccinated after infection

Number of holdings Total number of cattle Number of cattle in each holding Morbidity rate

13

84

4

108

1014

36

1–30 animals (mean=8, SE±2) 20–100% (mean=63.8%, SE±9.1%) 0–100% (mean=31.8%, SE±7.6%) 0–100% (mean=24.6%, SE±10.1%) 0–100% (mean=38.5%, SE±9.6%)

1–85 (mean=12, SE±2) 0–100% (mean=9.5%, SE±2.4%) 0–100% (mean=2.4%, SE±1.3%) 0–100% (mean=4.8%, SE±2%) 0–100% (mean=6%, SE±1.8%)

3–18 animals (mean=9, SE±3.7) 10–30% (mean=22.5%, SE±4.7%) 0–30% (mean=7.5%, SE±7.5%) 0–100% (mean=25%, SE±25%) 0–50% (mean=18.8%, SE±11%)

0–25% (mean=1.9%, SE±1.9%) 3–80 (mean=39, SE±6.8)

0–50% (mean=1.4%, SE±0.7%) 0–76 (mean=7.8 day, SE±1.8) 0–2210 (mean=78, SE±29)

0–30% (mean=12.5%, SE±6.2%) 14–66 (mean=31, SE±12)

Mortality rate Case fatality rate Percentage of decrease in milk production ranged from Abortion rate Duration of illness (days) The total cost of treatment and losses per animal in the holding (£)

27–2210 (mean=486, SE±162)

Veterinary Record | September 27, 2014

25–737 (mean=310, SE±146)

Vaccinated Farms Vaccinated Farms After Infection

FIG 1: The overall percentage of morbidity/mortality/case fatality in cattle on the vaccinated/non-vaccinated and vaccinated after infection farms against lumpy skin disease

intake, decreased milk production and fever, as well as abortion rate of the three different animal groups (unvaccinated, vaccinated, and vaccinated after appearance of clinical signs) are compared in Fig 2. Lesions on the body, udder and teats were present in 100 per cent, 76.9 per cent and 69.2 per cent of the unvaccinated cattle farms, respectively. In the vaccinated holdings, lesions on the body, udder and teats were present in 26.1 per cent, 10.7 per cent and 9.5 per cent of the cattle farms, respectively. The time between vaccination and appearance of clinical signs in these farms ranged from 1 to 57 days 100% 90% Percentage of Farms (%)

A total of 1158 dairy cattle on 101 dairy cattle holdings were surveyed. The cattle on 84 of the farms were vaccinated, the cattle on 13 farms were unvaccinated and the cattle on a further four farms were vaccinated after the appearance of clinical signs. Table 1 shows information about the farms, vaccination status and associated clinical problems reported in each case. The overall morbidity, mortality and case fatality rates of the three different animal groups (unvaccinated, vaccinated, and vaccinated after appearance of clinical signs) are compared in Fig 1. Percentage of decreased feed

Case Fatality Rate

Parameter

Data management and analysis

Results

Mortality Rate

80% 70% 60% 50% 40% 30% 20% 10% 0% Decreased Feed Intake

Decreased Milk Production

Fever

Abortion

Paramenter Not Vaccinated Farms Vaccinated Farms Vaccinated Farms After Infection

FIG 2: Percentage of vaccinated and unvaccinated farms showing decreased feed intake, decreased milk production and fever against lumpy skin disease

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Paper (mean=16, SE±2.8). In the four farms which were vaccinated after the appearance of the clinical disease in individual cattle, lesions on the body, udder and teats were present in 75 per cent, 50 per cent and 50 per cent of the cattle farms, respectively. The time between appearance of clinical signs and vaccination in these farms ranged from 5 to 20 days (mean=12.5, SE±3.2). Molecular characterisation of the two vaccines, which was carried out at the Pirbright Institute, confirmed the identity of the sheep pox vaccine strain RM 65 (Jovivac). Furthermore the unlabelled vaccine was confirmed to be LSDV vaccine. It was unknown exactly which farms used the unlabelled or RM 65 vaccine; however, it appeared that most cattle received the sheep pox vaccine strain RM 65. The origin of the unlabelled vaccine was not revealed.

Discussion

The results of the present study indicate that field vaccination provides a high degree of protection, although not complete. The overall morbidity rate was almost 10 times higher in the unvaccinated cattle group compared with the vaccinated cattle group. In addition, some animals showed clinical signs as early as 1 day after vaccination and such cases should not be counted as a vaccination failure. The mortality rate in the vaccinated group in this study was 4.7 per cent, which is very close to that reported before (6.6 per cent) in a similar vaccinated dairy population (Brenner and others 2009). In that study, sheep pox RM 65 strain was used and the morbidity rate was much higher in feedlot animals. This was related to probable technical and management difficulties in vaccination associated with beef cattle production practice (Brenner and others 2009). However, a much higher morbidity rate (22.9 per cent) was reported after cattle which were vaccinated with Kenyan sheep pox vaccine strain were exposed to natural infection of LSD (Ayelet and others 2013). Vaccination failure and breakdown in some animals, or incomplete protection of the herd after vaccination, as seen in the present study, has several causes. Some are general and may be encountered in any disease vaccination campaign, while others are specific to the disease process and associated circumstances. General causes include administering the vaccine while animals are incubating the disease, failing to vaccinate all animals in a herd, administering incorrect doses, inappropriate storage of the vaccine, and vaccine inactivation due to mishandling and exposure to direct sunlight and high environmental temperatures. In addition, interference between maternally derived antibodies and vaccine-induced immunity is another cause of vaccine failure in calves less than six months old (Carn 1993, Hunter and Wallace 2001, Kitching 2003, Tuppurainen and Oura 2012). Furthermore, in Jordan, the number of available vaccines was not enough initially to satisfy the high demand at the time, to the extent that the vaccine was sold on the black market at a much higher price. In addition, some people took advantage of the situation and were selling fractions of the dose as a full dose. This highlights the problems that can arise when local veterinary authorities do not carry out sufficient control and monitoring measures relating to infectious disease. A final reason for apparent vaccine breakdown is that pseudo-LSD and fly bites and hypersensitivity were often mistaken as an LSD infection (Brenner and others 2009). Decreased feed intake, decreased milk production and fever were almost five times more frequently observed in unvaccinated cattle compared with the vaccinated cattle group. Those changes in the parameters were likely related to the severity of infection which appears to be milder in vaccinated cattle. Considering the mean values, the percentage of decrease in milk production in unvaccinated cattle was more than six times higher compared with the vaccinated group. In addition, duration of illness was five times longer in unvaccinated cattle compared with the vaccinated ones. Vaccination appeared to

hasten the farm recovery from the disease. Furthermore the cost of treatment, per animal in the holding, was over six times higher in the unvaccinated cattle compared with the vaccinated ones. All these findings highlight the necessity for using vaccines, even though they do have some side effects and still cannot provide complete protection. In the small number of farms where vaccination was done after the onset of the LSD clinical signs, almost all parameters were better compared with the unvaccinated group, which might suggest that using vaccine after the appearance of clinical signs has some benefits. However, the abortion rate was almost six times higher in the vaccinated group after clinical signs compared with the unvaccinated group. The number of cattle in this category is small and this should be taken into consideration before drawing any conclusions. One limitation of the present study is the fact that there were two vaccines used in the field. It appeared that most cattle in the affected governorate were vaccinated using the sheep pox strain RM 65 vaccine while the other unlabelled vaccine was used in a limited number of cattle, reflecting the lack of control of vaccines and veterinary biological products available to farmers. The results of this study indicate that vaccination against LSD does not provide complete protection, as reported before. However, the use of vaccine in controlling LSD holds a high value and should be used, especially in areas where eradication is just not an applicable or viable method of control.

Acknowledgments

The author would like to thank Dr Eeva Tuppurainen and Mrs Lorraine Frost, Capripoxvirus Reference Laboratory and Drs Katarzyna Bachanek-Bankowska and Nick J. Knowles, Molecular Characterisation and Diagnostics Group, Vesicular Reference Laboratories, The Pirbright Institute, UK, for performing the molecular characterisation of the field vaccines.

References

ABUTARBUSH, S. M., ABABNEH, M. M., AL ZOUBI, I. G., AL SHEYAB, O. M., AL ZOUBI, M. G., ALEKISH, M. O. & AL GHARABAT, R. J. (2013) Lumpy skin disease in Jordan: disease emergence, clinical signs, complications and preliminary-associated ­economic losses. Transboundary and Emerging Diseases. Published Online First: 21 Oct 2013. doi:10.1111/tbed.12177 AYELET, G., ABATE, Y., SISAY, T., NIGUSSIE, H., GELAYE, E., JEMBERIE, S. & ASMARE, K. (2013) Lumpy skin disease: preliminary vaccine efficacy assessment and overview on outbreak impact in dairy cattle at Debre Zeit, central Ethiopia. Antiviral Research 98, 261–265 BRENNER, J., BELLAICHE, M., GROSS, E., ELAD, D., OVED, Z., HAIMOVITZ, M., WASSERMAN, A., FRIEDGUT, O., STRAM, Y., BUMBAROV, V. & YADIN, H. (2009) Appearance of skin lesions in cattle populations vaccinated against lumpy skin disease: statutory challenge. Vaccine 27, 1500–1503 CARN, V. M. (1993) Control of capripoxvirus infections. Vaccine 11, 1275–1279 DAVIES, F. G. (1991) Lumpy skin disease of cattle: a growing problem in Africa and the Near East. World Animal Review 68(3):37–42 HUNTER, P. & WALLACE, D. (2001) Lumpy skin disease in southern Africa: a review of the disease and aspects of control. Journal of the South African Veterinary Association 72, 68–71 KITCHING, P. (1983) Progress towards sheep and goat pox vaccines. Vaccine 1, 4–9 KITCHING, R. P. (2003) Vaccines for lumpy skin disease, sheep pox and goat pox. Vaccines for OIE list A and emerging animal diseases. Proceedings of a Symposium. Ames, IA, USA, September 16–18, 2002. pp 161–167 OIE (2013) Lumpy Skin Disease, Turkey. Immediate Notification Report Number 14106; 9 September. www.oie.int/wahis_2/temp/reports/en_ imm_0000014106_20130917_121547.pdf. Accessed September 17, 2013 ProMED-Mail (2013) PRO/AH/EDR> Lumpy skin disease, bovine – Iraq: susp. RFI. www.promedmail.org/direct.php?id=1831781. Accessed November 7, 2013 TUPPURAINEN, E. S. & OURA, C. A. (2012) Review: lumpy skin disease: an emerging threat to Europe, the Middle East and Asia. Transboundary and Emerging Diseases 59, 40–48

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Efficacy of vaccination against lumpy skin disease in Jordanian cattle S. M. Abutarbush Veterinary Record 2014 175: 302 originally published online July 2, 2014

doi: 10.1136/vr.102271 Updated information and services can be found at: http://veterinaryrecord.bmj.com/content/175/12/302

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Efficacy of vaccination against lumpy skin disease in Jordanian cattle.

The objective of this study was to assess the value and efficacy of vaccination against a natural outbreak of lumpy skin disease (LSD). Epidemiologica...
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