Lack of Bovine leukemia virus transmission during natural breeding of cattle

Abstract

Bovine leukosis is a chronic lymphoproliferative disorder that leads to significant economic losses in the beef and dairy industries. The major route of virus transmission is believed to be iatrogenic through the transfer of blood containing infected lymphocytes. In addition, BLV proviral DNA has been identified in nasal secretions, saliva, milk, colostrum, semen and smegma; however, natural transmission of BLV through these secretions has not been clearly demonstrated. The use of bulls for natural breeding has been identified as a risk factor in BLV infected dairy herds . However, the risk of BLV-infected bulls transmitting the virus is unknown. The objective of this study was to evaluate the potential for BLV transmission during natural breeding between a BLV-infected bull and uninfected heifers. Forty healthy, BLV seronegative, and proviral-negative beef heifers were randomly assigned to one of two groups: control heifers (n = 20) exposed to a BLV seronegative and proviral negative bull and challenged heifers (n = 20) exposed to a BLV seropositive and proviral-positive bull. Each group was housed with the bull for a period of 38 days in a 5-acre pasture to replicate the housing of commercial beef cattle during the breeding season. Blood samples were collected from heifers at −60, −30 and 0 days prior to breeding and day 30, 60 and 90 after the breeding period ended. Blood samples were tested for BLV antibodies by ELISA and BLV proviral DNA by CoCoMo-qPCR. New infection was not detected by ELISA or CoCoMo-qPCR in any of the challenge or control heifers at any time point during the study. Based on these results, BLV infected bulls that are healthy and aleukemic may not be a significant risk of BLV transmission during a defined breeding season.

Introduction

Bovine leukosis is a chronic lymphoproliferative disorder in cattle caused by the deltaretrovirus, bovine leukemia virus (BLV). Most BLV infected animals remain asymptomatic and act as carriers of the virus; 30–40% of infected cattle have a persistent lymphocytosis, while less than 5% progress to lymphosarcoma, the fatal, clinical form of BLV infection [1,2]. Surveys indicate that lymphoma accounts for 13.5% of beef cattle condemnations at US slaughter plants [3,4]. Economic losses associated with BLV in the dairy industry in the U.S estimated at $285 million [5]. To prevent further economic losses and animal welfare concerns due to BLV, the identification of primary routes of BLV transmission within and among herds is crucial to optimize management decisions.

The most common means of BLV spread is horizontal transmission by direct contact with biological fluid contaminated with BLV infected lymphocytes [1]. Virus transmission can happen through iatrogenic procedures that transfer blood between cattle [6,7]. Also, proviral DNA has been identified in nasal secretions [8], saliva [8], semen [9] and smegma [10] however, natural transmission through these secretions has not been clearly demonstrated. Transmission via milk and biting flies has been well documented [11,12].

Our research group has identified the use of breeding bulls in dairy herds as a risk factor for BLV infection at the herd level [13]. As part of an ongoing integrated study of chronic diseases in bulls, we collected blood from 121 beef bulls (>2 years old) from 38 beef farms in Michigan. Amongst sampled bulls, 45% (55/122) were BLV seropositive and 5.5% had detectable BLV proviral DNA in smegma [10]. Natural service is still used in approximately half of dairy operations across the US [14] and is the most commonly used breeding method (approximately 90%) in beef cattle herds in the U.S [15]. The high rate of BLV infection in beef bulls and their frequent use for natural breeding combine to create a considerable risk of BLV transmission during natural breeding via smegma, semen or from blood transfer from trauma to the penis, vulva and vagina. The objective of this study was to evaluate the potential for BLV transmission during natural breeding between a BLV-infected bull and uninfected heifers.

Section snippets

Animals

Forty 12-month-old Angus crossbred heifers were selected from a larger group of purchased heifers. To be selected, the heifers needed to be clinically healthy, seronegative for BLV, negative for BLV provirus by Coordination of Common Motifs-Quantitative polymerase chain reaction (CoCoMo –qPCR) (Riken Genesis CO,Tokyo, Japan) and determined to be cycling and not pregnant during examination of the uterus and ovaries by transrectal ultrasonography. Two bulls were acquired for this study. The first

Results

Characteristics and BLV diagnostics and of the bulls prior to and during the study are shown in Table 1. In the BLV challenge group, estrus activity was observed in 100% of the heifers and all were mounted by the BLV positive bull at least once during the study. Pregnancy percentage for the BLV challenge group was 85% (17/20). Among the 17 pregnant heifers, 70.5% (n = 12/17) became pregnant in the first two weeks of the breeding period (Fig. 1). In the control group, estrus activity was

Discussion

To our knowledge, this is the first study evaluating the possibility of BLV transmission though natural breeding in cattle. In this study, we were unable to detect any BLV transmission from a BLV-infected bull to BLV-negative heifers during a 38-day breeding period. Although BLV provirus was found in the smegma and blood of the BLV positive bull and there was direct contact during copulation with all the heifers at least once (as determined by observation and pregnancy status), no evidence of

Acknowledgements

This research was supported by The Michigan Alliance for Animal Agriculture and the Michigan State University College of Veterinary Medicine Edward and Roberta Sterner Endowed Research Fund. The authors thank our collaborators, AntelBio, Northstar Cooperative, Lansing, MI and the team members at the MSU Beef Cattle Teaching and Research Center. We also thank Jacqueline Maeroff, Hannah Barnard and Diamond Garrett for their assistance in heat detection.

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© 2018 Published by Elsevier Inc.