Prevalence and epidemiological features of bovine viral diarrhoea virus infection in Lithuania

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Prevalence and epidemiological features of bovine viral diarrhoea virus infection in Lithuania
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  Veterinary Microbiology 99 (2004) 51–57 Prevalence and epidemiological features of bovineviral diarrhoea virus infection in Lithuania Violeta Mockeli¯unien ˙ e a , ∗ , Algirdas Šalomskas a ,Raimundas Mockeli¯unas a , Saulius Petkeviˇcius a , b a  Lithuanian Veterinary Academy Veterinary Institute, Instituto 2, 56115 Kaišiadorys, Lithuania b  Danish Centre for Experimental Parasitology, The Royal Veterinary and Agricultural University, Dyrl æ egevej, DK-1870 Frederiksberg C, Copenhagen, Denmark  Received 22 April 2003; received in revised form 7 November 2003; accepted 22 November 2003 Abstract Theobjectivesofthepresentworkweretoestimatethelevelofbovineviraldiarrhoeavirus(BVDV)infectionincattleherdsatthe different Lithuanian districts and to determine factors influencing the course of BVDV infection. The studies were exploredin 147 intensive dairy cattle breeding herds from 27 different Lithuanian regions in 1997–2001. BVDV infection was diagnosedin all investigated regions. The existing variations in the structure of cattle population determined different distribution patternsof BVDV infection. The number of seropositive animals ranged from 11.9 to 100%. It must be pointed out that 29.9% of theherds were not infected with BVDV and in 32.7% of the herds from 70 to 100% of cattle were seropositive to BVDV. A positivecorrelation between the number of seropositive cattle, and the size of herds and age of animals was determined. Sex of animalhad no influence on the prevalence of BVDV. It was estimated that the annual incidence risk of infection with BVDV decreaseswith the animal age.© 2004 Elsevier B.V. All rights reserved. Keywords:  Bovine viral diarrhoea virus; Cattle-viruses; Epidemiology 1. Introduction The bovine viral diarrhoea virus (BVDV) infec-tion is a major problem worldwide affecting differentspecies of ruminants (Pringle, 1999). Studies from1994 to 1995 (Šalomskas et al., 1998) showed awidespread distribution of BVDV and there have beenno investigations performed during recent years, butother respiratory, enteric and reproductive disorders ∗ Corresponding author. Tel.:  + 370-346-60687;fax:  + 370-346-60697.  E-mail address: (V. Mockeli¯unien ˙e ). that could be associated with BVDV are frequent(Sedereviˇcius and Bertašius, 1993). Bovine viral di-arrhoea virus belongs to the  Pestivirus  genus in the Flaviviridae  family (Wengler et al., 1995; Pringle,1999). Based on the effect in bovine cell culture twobiotypes of the virus, non-cytopathogenic (ncp) andcytopathogenic (cp), can be distinguished (Meyersand Thiel, 1996). An examination of the epidemi-ology and pathogenesis of disease have proved thatmost of the pathological changes caused by BVDVare associated with the ncp virus. This biotype, whichis most frequently isolated during investigations ischaracterised by a vertical virus transmission and is 0378-1135/$ – see front matter © 2004 Elsevier B.V. All rights reserved.doi:10.1016/j.vetmic.2003.11.008  52  V. Mockeli¯ unien ˙e  et al. / Veterinary Microbiology 99 (2004) 51–57  responsible for a permanent BVDV circulation in thecattle population (Brownlie, 1991; Booth et al., 1995). The significant economic impact inflicted due to pro-ductive and reproductive losses: by a reduced milkyield, reduced conception rate, abortion, foetus mum-mification, congenital malformations, weak calvesand increased animal mortality. The estimates of eco-nomic losses due to BVDV infection vary dependingon the immune status of the cattle population and thepathogenicity of the virus strains (Houe, 1999). Theinvestigations on spread of BVDV, its manifestationand distribution depend not only on the propertiesof the agent, ways of transmission or immune statusof the animal, but can also be associated with de-mographic risk factors. The existing differences inthe structure of cattle population in Lithuania maycause different distribution patterns of BVDV infec-tion. The objectives of our study were to determinethe prevalence of BVDV infection in Lithuania andthe possible influence of different risk factors, suchas animal density in herds, animal age and sex of the animals. Further, it was the objective to estimateincidence risk of infection in different age groups. 2. Materials and methods 2.1. Sampling of animals The blood sera samples for this study were selectedamong samples submitted to the virological laborato-ries at Lithuanian Veterinary Academy Veterinary In-stitute and Lithuanian National Veterinary Laboratoryduring 1997–2001. All samples had been submittedby practicing veterinarians from 147 differently sizedcattle herds either due to clinical signs or due to gen-eral interest in the occurrence of BVDV infection inthe herd. The large herds consisted of cattle breed-ing companies whereas the small herds was familyfarms. The 147 herds came from 27 Lithuanian re-gions. In addition, the cattle blood samples came fromfrom Lithuanian Artificial Insemination (AI) Centersamong the breeding bulls sperm donors. A total of 4098 blood sera samples obtained from animals of different age and sex were investigated. Of this sam-ples 3295 came from the large herds, 503 came fromsmall herds and additionally 300 samples came fromAI Centers. 2.2. Herd size InLithuania,approximately70%ofmilkcomefromfarms with ≤ 5 cows, and 25% from farms with >100cows. The rest part (5%) of milk come from herdswith 5–100 animals. This explain why there in thisstudy were no herds with a size from 15 to 50 animals.To study the influence of herd size on the distributionof BVDV infection, the animals were grouped intosmall (3–15 animals) and large (>50 animals) herds.The group of small herds contained 503 animals, thegroup of large herds, 3295 animals. 2.3. Animal age The possible influence of animal age on distributionofBVDVwasdeterminedbygroupingthecattle(1935animals) into the following age groups: 0–1, 2–4, 4–6,6–12 months and 1–2, 2–3, 3–4, 4–5, 5–6, 6–7, >7years. 2.4. Animal sex For investigation of the number of antibody carri-ers depending on sex 1402 animals were divided intotwo groups: cows ( n = 1178) and bulls ( n = 224), re-spectively. Each group was divided into subgroups of different age categories: aged 2–4, 4–6 and >6 years. 2.5. Testing of sera The distribution of BVDV infection was evaluatedby the number of seropositive animals. There areno animals vaccinated against BVDV in Lithuania.The commercial enzyme linked immunosorbent as-say (ELISA) kits from IDEXX (Sweden) and fromInstitute Pourquer (France) was used for serologicaltests. 2.6. Ethical consideration The experiments were approved by the LithuanianAnimal Ethical Committee (State News, 1997, vol.108). Meetings were held with the agricultural andlaboratory technicians to explain the purpose of thestudyandwhatwasrequiredfromthepersonshandlingthe cattle.  V. Mockeli¯ unien ˙e  et al. / Veterinary Microbiology 99 (2004) 51–57   53 2.7. Statistical analysis Differences in prevalence between large and smallherds were tested for each year by chi-square test.Also differences in prevalence between bulls andcows were tested by chi-square test (Proc Freq;SAS, 1999).The logarithmic probability of annual incidence riskof BVDV infection was calculated from age-specificprevalence of antibody carriers using the formula de-scribed by Lilienfeld and Lilienfeld (1980): P  y  = 1 − ( 1 − IR ) y where  P y  is the proportion of the population who havebecome infected by age  y  (i.e. the prevalence of an-tibody carriers); IR the probability of becoming in-fected in 1 year (annual incidence risk);  y  is age inyears and  ( 1 − IR ) y the probability of not having be-come infected by age  y  (Houe and Meyling, 1991). The calculations of incidence was based on differentage groups of animals. 3. Results The prevalence of BVDV is shown in Table 1.Seropositive animals were found in 70% of herdswhich have been investigated (Table 2). In the smallherds (3–15 animals), the average number of in-fected animals (30.6% of positive) was statisticallysignificantly lower compared to the large herds (>50animals) (62.4% of positive) ( P <  0 . 0001). In 4 outof 5 years a similar tendency was seen. When large Table 1Seroprevalence of BVDV in 147 herds of Lithuanian cattle popu-lation 1997–2001Year Number of animalsNumber of animalsPositive Negative Doubtful n  %  n  %  n  %1997 1638 1080 65.9 513 31.3 45 2.81998 716 487 68.0 185 25.9 44 6.11999 413 169 40.9 211 51.1 33 8.02000 433 187 43.2 245 56.6 1 0.22001 598 288 48.2 296 49.5 14 2.3Total 3798 2211 58.2 1450 38.2 137 3.6Table 2Percentage distribution of cattle seropositive to BVDV in 147Lithuanian herdsPercentage distribution inthe cattle herdsNumber of herds n  %0 44 29.91–30 23 15.631–69 32 21.870–100 48 32.7Total 147 100 herds were compared to small herds, the infectionlevel was from 1.8- to 2.7-fold higher in large herds(Table 3).The results from our study demonstrated that thenumber of seropositive animals increases with age(Fig. 1). The lowest number of seropositive animalswas determined in the age groups 2–4 and 6–12months (27.8–28.4%, respectively). In the third andconsecutive years of life the number of seroposi-tive animals increased reaching the peak in group of animals aged 6–7 and >7 years (70.1 and 77% of seropositive animals, respectively). The animal agewas in direct correlation with the number of seropos-itive animals.Animal’s sex (Fig. 2) was investigated as a com-plementary factor, which can have influence on preva-lence of BVDV infection. In the animals aged 2–4years 63.5% of bulls were seropositive and 57.6% of cows were seropositive. There was no significant dif-ference in prevalence between groups of sex ( P > 0 . 5). However, despite the tendency that in cows aged4–6 and >6 years the number of seropositive animalswas higher compared to the bulls in corresponding agegroups, but the difference was not statistically signif-icant ( P >  0 . 5).The annual incidence risk of BVDV infection de-termined according to specific distribution of antibodycarriers ( P y ) depending on the animal age in bothgroups of animals (bulls and cows) was comparable(Table 4). It was typical for the both groups of cowsand bulls that the younger (aged 1–4 years) animalswere subject to a greater risk of infection. The annualincidence risk of BVDV infection among them was0.28–0.36, whereas among the older animals groupsthe annual incidence risk decreased to 0.13–0.18.  54  V. Mockeli¯ unien ˙e  et al. / Veterinary Microbiology 99 (2004) 51–57  Table 3The influence of cattle herd size on the seroprevalence of BVDV infection among 147 herdsYear Large herds Small herdsSerologically tested ( n ) Antibody positive cattle Serologically tested ( n ) Antibody positive cattle n  %  n  %1997 1581 1066 67.4 ∗ 57 14 24.6 ∗ 1998 543 414 76.2 ∗ 173 73 42.2 ∗ 1999 365 150 41.1 48 19 39.62000 294 158 53.7 ∗ 139 29 20.9 ∗ 2001 512 269 52.5 ∗ 86 19 22.1 ∗ Total 3295 2057 62.4 ∗ 503 154 30.6 ∗∗ P <  0 . 0001.Fig. 1. Distribution of seropositive animals in different age groups.Table 4Annual incidence risk of infection with BVDV as calculated from the age-specific prevalence of antibody carriersAge (years) Bulls from 6 AI Centers Cattle from breeding farms (large herds)Totalanimals, n Antibodypositive, n Prevalenceof antibodycarriers,  P y Annualincidencerisk, IRTotalanimals, n Antibodypositive, n Prevalenceof antibodycarriers,  P y Annualincidencerisk, IR1–2 76 30 0.40 0.29 444 216 0.49 0.362–3 41 24 0.59 0.30 260 154 0.59 0.303–4 44 30 0.68 0.28 257 144 0.56 0.214–5 26 13 0.58 0.18 186 99 0.53 0.155–6 22 16 0.73 0.21 125 77 0.62 0.166–7 32 23 0.72 0.18 107 75 0.70 0.17>7 59 40 0.68 0.13 243 187 0.77 0.15Total 300 176 0.59 – 1622 952 0.59 –“Bulls from 6 AI Centers” it is bulls whose age was exactly known. “Cattle from breeding farms” it is cows, heifers, calves with noted age.  V. Mockeli¯ unien ˙e  et al. / Veterinary Microbiology 99 (2004) 51–57   55Fig. 2. Distribution of seropositive animals depending on sex. 4. Discussion Differences of BVDV infection epidemiology indifferent countries and regions can be explained bythe existing structure of cattle population (Houe andMeyling, 1991). This statement was proved by our re-sults obtained in Lithuanian cattle herds. Lithuania isdivided in 10 counties which are divided in 44 re-gions. Our data of investigations include 27 regionsfrom all 10 counties. Naturally, more samples wereinvestigated from regions in which cattle husbandry ismore developed.The investigation of the influence of herd size onBVDVdistributionrevealedthatanimalsinlargeherdsare more likely to be infected than animals in smallherds. Analysis of the effect of the herd size as demo-graphic risk factor on the seroprevalence of BVDV hasrevealed that in the large herds the number of seropos-itive animals was on the average two-fold higher com-pared to the small herds. An infected herd in an areawith large herds has higher impact on the overallprevalence of infection compared with infection of aherd in an area with small herd sizes, because oncea herd infected most animals in the herd will mostlikely become infected sooner or later (Houe et al.,1995). This finding is in agreement with Løken et al.(1991), Alves et al. (1996), Vega et al. (1997) and Valle(2000),whofoundapositivecorrelationbetweenthe prevalence of BVDV and density of cattle popu-lation in the different regions. This tendency was alsoseen for IBR infection in Hungarian cattle, where thenumber of seropositive animals in large herds was sixtimes higher compared to the small herds (Tekes et al.,1999).Analysisoftheinfluenceofanimalageonthepreva-lence of BVDV infection has shown that with age of animals the number of seropositive animals have ten-dency to increase. It should be noted that in the groupaged 4–6 months the number of seropositive animalswas higher than in the group 6–12 months. The causeof this finding could be explained by lower colostralimmunity. Animals of this age are very sensitive to theagents of respiratory diseases, which tend to combineinfections of BVDV, parainfluenza 3, herpes virusesof type 1, respiratory syncytial and other virusescausing respiratory pathologies (Graham et al., 1998;Šalomskas et al., 1998; Saar and Aaver, 1998). Forevaluation of ELISA results, the information aboutthe age of animals is of particular importance, becausecolostral antibodies could complicate the interpreta-tion of serological results in young animals. However,in PI animals maternal antibodies will disappear after3 months, whereas in non-PI animals they will befound until 8 months (Bitsch and Rønsholt, 1995). Forthis reason, seropositive reaction in animals youngerthan 8 months cannot be interpreted as a consequenceof the previous infection. This can explain the factthat in the age group of 6–12 months, the numberof seropositive animals was lower compared to agegroup of 4–6 months. It appears that, in the third andconsecutive years of life the number of seropositiveanimals increases reaching its maximum in the agegroups 5–7 and >7 years .  The increase in antibodyprevalence by increasing age is probably due to thefact that BVDV antibodies in most cases are lifelong.So the older the animal, the higher is the probabilitythat it has been infected during its life.The seroprevalence of BVDV could be affected bythe various risk factors. Therefore, it is important tocalculate the annual incidence risk of this infection onthe basis of a relevant dataset. The values obtainedaccording to specific prevalence of seropositive ani-mals in dairy herds and in Artificial Insemination Cen-ters among the animals of the different age groupswere comparable. Yet, a general trend was determinedthat the younger (aged 1–4 years) animals were sub- ject to a greater risk of infection. Annual incidencerisk was 0.28–0.36, while animals older than 4 yearshave shown two times lower value, 0.13–0.18, respec-tively.OurdatadifferfromthedataobtainedbyDanish
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