Introduction
Bovine respiratory disease (BRD) is the leading cause of death in beef calves 3 weeks of age to weaning, costing cow–calf producers approximately $165 million annually (Wang et al., Reference Wang, Schneider, Hubbard and Smith2018). The disease is even more common and more costly after weaning and is the leading cause of morbidity and mortality in beef feeding and finishing systems (Griffin, Reference Griffin1998; Miles, Reference Miles2009). The disease syndrome is complex and surprisingly difficult to accurately diagnose. The incidence of BRD has not waned despite the widespread use of improved vaccines and antimicrobials (Miles, Reference Miles2009). The anatomy and physiology of the bovine lung may make cattle inherently susceptible to BRD (Veit and Farrell, Reference Veit and Farrell1978). However, many other factors contribute to its occurrence.
Causal thinking
Part of the challenge in controlling BRD is the confusing array of factors that sometimes seem to explain the disease, but sometimes do not. This lack of consistent effect of putative risk factors confounds our understanding of actions that might prevent the BRD from occurring. The concepts of component and sufficient causes help explain this phenomenon. Risk factors are causal factors because they contribute to the causal pathway of disease. Risk factors may include factors related to the disease-causing agents (e.g. pathogens or toxins), the ability of the host to resist the effects of the agents, or management and other environmental factors that may affect host and agent interactions. Key determinants are those causal factors which are under management control. In disease causal theory, each factor that contributes to the development of disease is a component cause (Rothman, Reference Rothman1976). Clinical signs of disease are expressed when various component causes add up to complete a sufficient cause. Each outbreak of respiratory disease is the result of the completion of a sufficient cause, which might have also included components of viral and bacterial pathogens, a certain state of immunity, or other component causes of respiratory disease in cattle that we fail to understand. Disease is expressed when a sufficient cause is completed. This is why some known component causes of BRD may be observed even though the disease is not expressed. It may appear to the livestock owner that the component cause that completed a sufficient cause was the sole reason for the disease. For example, a sudden change in weather may precede an outbreak of BRD because it completed the sufficient cause, but viral, bacterial, and immunity factors were unrecognized component causes. Removing one component cause (now the key determinant) means that the sufficient cause is not completed and thus disease is not observed.
Systems thinking
Thinking about the system of production may provide some additional insight into the factors that cause BRD. The science of system dynamics helps us understand how actions and decisions far removed from the immediate problem could be a cause of the problem. Disease events that we observe, such as the occurrence of BRD, usually have relationships with risk factors which are commonly the subject of epidemiologic research and the primary subject of this paper. However, it is important to understand that underlying systems produce those relationships and, ultimately, the occurrence of disease (Fig. 1) (Meadows and Wright, Reference Meadows and Wright2008). A better understanding of how the system may lead to disease outcomes may further our understanding of why BRD occurs and what we can do to mitigate it. For example, a large regional drought might cause cow–calf producers to decide to wean calves early, seek feedlot pens to house cows, or to depopulate their herds – all of which may have effects on feedlot management and health. Small cow–calf producers may decide not to dehorn, castrate, vaccinate, or deworm calves on the farm because they lack facilities or fail to recognize an economic signal to do so. Decisions made months ago at a farm, possibly hundreds of miles away, may result in increased morbidity and mortality in the feedlot (Duff and Galyean, Reference Duff and Galyean2007). Those decisions do not always reflect sub-par husbandry. For example, pneumonia in calves prior to weaning is a systems problem paradoxically associated with highly managed herds (Woolums et al., Reference Woolums, Berghaus, Smith, White, Engelken, Irsik, Matlick, Jones, Ellis, Smith, Mason and Waggoner2013; Woolums et al., Reference Woolums, Berghaus, Smith, White, Engelken, Irsik, Matlick, Jones and Smith2014).
Fig. 1. The iceberg structure of system dynamics. The disease events we observe have relationships with other causal factors that are often studied by epidemiologists and other animal health researchers, but the systems that produce those relationships and the ultimate events require further understanding.
The epidemiology of BRD
Traditionally, disease control programs have focused on agent–host interactions with some consideration of environmental factors. However, political, social, economic, and cultural factors also contribute to disease ecology as it affects the movement of people, animals, and animal products.
The failure of disease control programs, whether at a local, regional, or global level, frequently results from failure to consider or understand the system comprising the disease's ecology, including the decisions made by people responding to factors within the system (e.g. economic factors).
Pneumonia in calves prior to weaning
Pneumonia is a leading cause of sickness and death of calves in some cow–calf herds – especially after the first few weeks of life (USDA, 2011). This is perplexing because ranch calves typically live in conditions of little stress and relative isolation. Surveys of beef cattle producers (Woolums et al., Reference Woolums, Berghaus, Smith, White, Engelken, Irsik, Matlick, Jones, Ellis, Smith, Mason and Waggoner2013) and veterinarians (Woolums et al., Reference Woolums, Berghaus, Smith, White, Engelken, Irsik, Matlick, Jones and Smith2014) from the northern plains region and southeastern US indicate that pre-weaning BRD is a problem for approximately one out of five cattle producers. Pre-weaning BRD may affect up to 10% of US beef calves (Hanzlicek et al., Reference Hanzlicek, Renter, White, Wagner, Dargatz, Sanderson, Scott and Larson2013), resulting in the death of 0.6–1.4% of all calves (Dutil et al., Reference Dutil, Fecteau, Bouchard, Dutremblay and Pare1999; Snowder et al., Reference Snowder, Van Vleck, Cundiff and Bennett2005; USDA, 2010). Calves affected with pre-weaning BRD may weigh 17–37 pounds less at weaning, compared to calves not affected (Wittum et al., Reference Wittum, Salman, King, Mortimer, Odde and Morris1994; Snowder et al., Reference Snowder, Van Vleck, Cundiff and Bennett2005).
As with all infectious diseases, the occurrence of BRD is affected by factors of host immunity, presence of specific pathogens, and opportunity for transmission of pathogens between or within herds. Although the bacterial pathogens of pneumonia are commonly found in the upper respiratory tract of cattle, the inciting damage is often due to viral infections that may not be present in all cattle herds all the time. Commonly recognized viral BRD pathogens are bovine herpes virus 1, bovine viral diarrhea virus, and bovine respiratory syncytial virus, but many others, including bovine coronavirus (McNulty et al., Reference McNulty, Bryson, Allan and Logan1984; Kapil and Goyal, Reference Kapil and Goyal1995), are likely to be involved. Pathogen exposure may be necessary but it is not causally sufficient because it is difficult to replicate the clinical presentation of BRD through experimental challenge with bacteria or viruses alone (Taylor et al., Reference Taylor, Fulton, Lehenbauer, Step and Confer2010a).
In confinement systems, the opportunity for pathogen transmission is high because of animal density. But, even in extensive pasture-based systems typical of cow–calf production, the opportunities for pathogen transmission may be high because cattle congregate closely around water sources and feedbunks, in shade, and when bothered by flies. Some management practices such as pasture moves and gathering for sorting also result in high animal density and greater opportunity for pathogen transmission.
Passively acquired maternal immunity is important for protecting young calves against respiratory pathogens. However, maternal antibodies wane with time. Approximately every 16–20 days after ingestion, the serum concentration of maternal antibodies is halved, so that by 96–120 days of age, a calf retains <2% of the antibodies it absorbed from colostrum. The immune system is functional but unprimed at birth, and prior to 5–8 months of age, the immune response of calves is weak, slow, and easy to overcome (Cortese, Reference Cortese2009). Therefore, even in the absence of additional stressors, calves 3–5 months of age may be particularly susceptible to pneumonia. This age-related susceptibility due to loss of maternal immunity may explain sudden outbreaks of pre-weaning BRD in herds with managed breeding seasons. Herd immunity is the protection afforded to susceptible individuals because most of the individuals in the population are immune. In herds with a narrow calving window, calves are similar in age and herd immunity is lost over a short span of time as the majority of calves approach 90–120 days of age. However, the optimum vaccination protocol to prevent BRD in calves of this age remains an important subject of investigation. Weaning, commingling groups, and exposure to severe weather can be powerful stressors that further reduce a calf's ability to resist disease.
Other factors affecting risk for pre-weaning BRD
Health records representing over 9900 calves from 28 cattle management groups within seven beef cattle ranches were analyzed to test the effect of calf gender and age of the dam (Smith et al., unpublished). We concluded that the sex of calves affects their risk for BRD (males at greater risk than females). Also, of calves affected with BRD, those calves born to 2-year-old dams were more likely to become sick at an earlier age. This is consistent with the knowledge that the male sex of other species has been associated with greater risk for pneumonia (Yamamoto et al., Reference Yamamoto, Saito, Setogawa and Tomioka1991; Gutierrez et al., Reference Gutierrez, Masia, Mirete, Soldan, Rodriguez, Padilla, Hernandez, Royo and Martin-Hidalgo2006). The age of the dam may be a correlate of colostrum absorption. Colostrum ingestion may be delayed for calves born to a young dam because of dystocia or poor mothering skills. Also, the young dam's colostrum may not contain as many antibodies, in quantity and range of protection, as older dams (Odde, Reference Odde1988; Schumann et al., Reference Schumann, Townsend and Naylor1990; Odde, Reference Odde1996).
Pneumonia in calves after weaning
The first several days from the farm of origin to the stocker operation or feedlot can result in the accumulation of stress events that are detrimental to calf health, especially increasing the risk for BRD. Most BRD morbidity occurs in the first 21 days after arrival in the stocker or feedlot operation. By far, the most common illness of stocker calves is BRD (Miles, Reference Miles2009). Other important receiving period diseases are lameness, musculoskeletal injury, diarrhea (e.g. rumen acidosis, Salmonellosis, and coccidiosis), and bloat (Griffin, Reference Griffin1998).
Many small farm operations lack enough natural, human, or capital resources to provide an optimum health program while the calf is on the home farm. For example, the farm may lack facilities, manpower, or knowledge to dehorn, castrate, or vaccinate calves prior to weaning. Weaning often occurs the same day the cattle are marketed from the home farm, resulting in an important abrupt stress event. In addition, the common systems of marketing calves contribute additional stressors to the auction market calf. Calves may not have access to adequate feed or water or may not know how to drink from tanks or consume feed from bunks during transportation to and from the auction market. Calves are likely to be commingled with other calves, and after long distance transportation, may spend several days in an order-buyer facility as other calves are purchased to fill an order. During the phase of marketing, calves may lose rumen fill from not eating, may have shrunk from dehydration, and may be exposed to a variety of enteric and respiratory pathogens. By the time calves have moved through these marketing channels and arrive at the destination feedlot or stocker facility, they may be exhausted, dehydrated, challenged by a variety of social and physical stressors, and incubating a respiratory or enteric infection.
Unfortunately, the marketing system may not reward the small cow–calf farmer for adopting practices that improve immunity and decrease stress. Calves marketed directly from the (typically larger) cow–calf farm to the stocker or feedlot operation may experience some, but often not all, of the stressors of auction market calves; however, because direct marketing is often based on the farmer's reputation, these calves are more likely to have been preconditioned by receiving deworming treatment, vaccination at a prior to weaning, and castration and dehorning at a young age. Calves that are marketed directly, especially those undergoing a pre-conditioning program, may have less morbidity and mortality in the post-weaning phase and are, therefore, often considered calves at low risk for disease. Conversely, commingled, low body condition, freshly weaned calves, transported long distances, and marketed through an auction market are often considered high risk for disease. It is a paradox that some cattle feeders and stocker operators prefer lightweight high-risk calves because they can be purchased for less total dollars and, if they survive, often grow efficiently because of compensatory gains (Ives and Richeson, Reference Ives and Richeson2015).
Attempts to mitigate the risk for BRD in feeding or finishing systems, such as by vaccinating calves at arrival, may not reduce BRD incidence (Taylor et al., Reference Taylor, Fulton, Lehenbauer, Step and Confer2010b) and may sometimes increase BRD incidence, increase mortality, and lower growth performance (Griffin et al., Reference Griffin, Scott, Karisch, Woolums, Blanton, Kaplan, Epperson and Smith2018). Mass medication of calves with injectable antimicrobials at arrival has been the most consistently effective method to reduce BRD incidence (Ives and Richeson, Reference Ives and Richeson2015).
Conclusions
The risk factors for BRD include a complex set of component causes that include bacterial and viral pathogens, level of host immunity, and environmental conditions that favor pathogen transmission and stress-induced susceptibility. During the post-weaning phase, these factors are superimposed on a system of marketing, transportation, and economic opportunity that further increase the risk for BRD.
Acknowledgements
A contribution of the Beef Cattle Population Health and Reproduction Program at Mississippi State University. Supported by the Mikell and Mary Cheek Hall Davis Endowment for Beef Cattle Health.
