Investigation of acute clinical and chronic anaplasmosis on breeding soundness in beef bulls

Abstract

The causative agent of bovine anaplasmosis, Anaplasma marginale, costs the U.S. cattle industry an estimated $300 million per year. Natural service breeding by bulls is common in U.S. beef cow-calf operations. Anemia and fever associated with clinical anaplasmosis may reduce bull breeding soundness and affect testicular tissue beyond resolution of clinical disease. Cattle that recover from acute clinical anaplasmosis transition to a chronic disease state and serve as transmission reservoirs of A. marginale. The impact of chronic A. marginale infection on reproductive performance parameters in carrier bulls is unknown. The impact of anaplasmosis on bull breeding soundness was investigated among bulls with clinical anaplasmosis (Objective 1) and among bulls with chronic anaplasmosis (Objective 2). In Objective 1, breeding soundness examination (BSE) outcomes and clinical changes were evaluated in beef bulls over the course of clinical anaplasmosis and after recovery. In Objective 2, the prevalence of chronic A. marginale infection in bulls from eastern Kansas was investigated and breeding soundness parameters and overall satisfactory breeding potential rates were compared between A. marginale infected and uninfected bulls. To investigate the effect of clinical anaplasmosis on bull breeding soundness, six healthy, Anaplasma-negative, mature, Angus bulls of satisfactory breeding status were included. Fresh blood from an A. marginale-infected donor cow was used to challenge three bulls, the other three remaining as unchallenged controls. All bulls were observed for disease progression and soundness of breeding. Fever, anemia via packed cell volume (PCV), pallor, and icterus were monitored weekly. Progression of anaplasmosis was evaluated via quantitative PCR and percent parasitized erythrocytes (PPE). Seroconversion was monitored by cELISA. Injectable oxytetracycline was given to bulls with a PCV <15% or a temperature >105°F. Weekly BSEs using electroejaculation were performed on all bulls for 16 weeks. Breeding soundness parameters included sperm morphology and motility, external and internal genitalia exam, and physical exam. All A. marginale-challenged bulls were PCR-positive, seropositive, and showed clinical signs by 3-, 17-, and 24-days post-challenge, respectively. Common clinical signs of acute anaplasmosis included weight loss, pallor, icterus and fever (≥104.3°F). Acute anemia was observed in all challenged bulls with PCV nadirs ≤18% and peak PPEs ≥50%. Reduced breeding soundness outcomes were observed starting at the onset of clinical signs and continued for weeks beyond resolution of clinical anaplasmosis. Bulls in the control group remained negative for A. marginale by PCR and cELISA, and never developed dramatic reductions in breeding soundness outcomes. To investigate the impact of chronic A. marginale infection on bull breeding soundness, 537 Eastern Kansas, client-owned beef bulls undergoing a routine breeding soundness examination (BSE) were enrolled. Complete BSEs were performed by recruited local veterinarians according to the Society for Theriogenology Manual for BSE of Bulls, 2nd edition. Breeding soundness examination parameters included sperm morphology and motility, palpation of external genitalia and internal accessory sex glands, and overall physical soundness. Blood samples were collected for packed cell volume determination and analysis of A. marginale infection status via quantitative PCR and cELISA. Logistic and linear regression methods were used to evaluate factors associated with A. marginale infection status and BSE parameters. Prevalence of chronic A. marginale was 45.7% (245/537) among the sampled eastern Kansas bulls. Of the bulls with unsatisfactory BSE results, 53.6% were chronically-infected with A. marginale. Common reasons for unsatisfactory BSE results were poor sperm motility or increased abnormal sperm morphology. Collectively, results from this program of work suggest acute anaplasmosis is a driver of reduced breeding soundness in beef bulls and prevalence of A. marginale infection among bulls tested is common and similar to eastern Kansas cow infection rates. Bulls that undergo acute disease can recover from or have prolonged evidence of reduced breeding soundness. Many bulls with chronic A. marginale infection retain overall satisfactory breeding potential. Outcomes from this research expanded information on the pathogenesis of anaplasmosis in bulls, regional prevalence, and the reproductive and production consequences of bulls exposed to A. marginale. Further research pursuits should include additional data collection on the A. marginale prevalence status of bulls and females in other areas of the U.S. and a larger clinical trial investigating the effects on testicular tissue in bulls during and after clinical anaplasmosis using advanced diagnostics and imaging. Studies investigating the inter-observer agreement of veterinarians performing BSEs on a specific subset of bulls are also warranted.