Introduction

Neonatal morbidity and mortality are major causes of economic loss for US beef cattle producers.¹ In 2017, the majority of US beef operations (51.2%) had at least 1 calf that was born alive but died or was lost prior to weaning.² Overall, 2.2% to 3.5% of beef calves born alive die before weaning.^2–4 Based on producer surveys, the most common causes of death in calves < 3 weeks of age are calving-related problems (24.7%), unknown (24.0%), predators (13.8%), weather related (12.5%), digestive diseases (11.9%), and respiratory diseases (8.1%).^2,3 Overall, a high proportion of calves die from unknown reasons, leaving an outcome related knowledge gap for producers. Additionally, while producer driven data are valuable, as many neonatal calf diseases are tentatively diagnosed and treated by producers, determining causes of death based on history and clinical signs alone can be misleading.⁵

A postmortem assessment of pathological findings can provide clarity regarding underlying disease processes. Necropsy data can be useful to confirm disease status of animals especially when morbidities and mortalities are higher than expected, help producers understand outcomes when there is a perceived treatment failure, provide confirmation of a presumptive diagnosis, and potentially identify outcomes that could be controlled through adjusted management strategies.^6,7 A comparison of expected postmortem findings based on clinical signs and administered treatments and actual postmortem findings obtained at necropsy found limited agreement, indicating that necropsies and additional laboratory-based testing should be part of a systematic postmortem examination of causes of death.⁵ That said, in the US, only half of beef cow-calf operations consult with a veterinarian for any reason.⁸ In a Canadian study,⁹ only 9.8% of producers had a veterinarian perform a postmortem examination on ≥ 1 calf in 2010 and 5.2% had veterinarians submit tissues or biological samples to a veterinary diagnostic laboratory.

There are limited numbers of studies that have evaluated beef calf deaths unrelated to birthing or reproductive diseases by use of gross necropsy, histopathology, and laboratory tests. In 1 prospective study that evaluated 203 herds in western Canada, among 558 calves that were > 3 days of age, the most common final diagnoses based on history, field necropsy, and histologic examination were starvation (16%); abomasal ulcer, torsion, and perforation (12%); and enteritis (11%). Although starvation was the most common summary diagnosis, most of the cases had additional lesions, suggesting the calves were compromised by underlying disease.¹⁰

A summary of the common results from postmortem evaluations may prove beneficial to producers and show value in necropsy results. Therefore, the objective of this study was to describe lesions and abnormal test results among neonatal beef calves presented to a veterinary diagnostic laboratory.

Materials and Methods

Results

A total of 1,060 bovine necropsies were performed during the study period. Of these, 95 (8.9%) animals met the inclusion criteria, with a median of 15 cases/y (range, 13 to 19 calves/y). Median calf age was 9 days (range, 2 to 21 days). Median weight was 33.5 kg (range, 11.5 to 58.3 kg). Overall, 51.6% (49/95) of included calves were male, 42.1% (40/95) were female, and 6.3% (6/95) had no sex reported. More calves were submitted for necropsy in the spring (34/95 [35.7%]), followed by the fall (30/95 [31.5%]), winter (21/95 [22.1%]), and summer (10/95 [10.5%]). Animals represented included mixed breed (42/95, 45.1%), Angus (36/95, 38.7%), Charolais (5/95 [5.3%]), Simmental (3/95 [3.2%]), Limousin (2/95 [2.1%]), South Poll (2/95 [2.1%]), Longhorn (1/95 [1.0%]), Salers (1/95 [1.0%]), and Dexter (1/95 [1.0%]). There was a total of 252 lesions identified, with a median of 3 lesions/calf (range, 0 to 7). When more than 1 lesion was identified within 1 system, duplicate representation of each system were removed to represent the number of system-based lesions. A total of 190 system-based lesions were identified, with a median of 2 systems affected/calf (range, 0 to 5). A total of 3 (3.2%) calves had no identified lesions.

Overall, gross necropsy only was performed on 6.3% (6/95) of cases. Gross necropsy and histopathology were performed on 10.5% (10/95) of cases. Gross necropsy, histopathology and laboratory testing were performed on 82% (78/95) of cases. Most cases (99%; 94/95) were from calves submitted to the VMDL while 1% (1/95) of cases were from field necropsies with samples submitted by the referring veterinarian. Among the calves with no identified lesions, 1 was examined by gross necropsy and histopathology only and 2 were examined by gross necropsy, histopathology, and ancillary laboratory tests.

Among the 252 lesions, digestive system (42.1% [106/252]) lesions were the most common (Table 1), followed by respiratory (12.7% [32/252]), multisystemic (11.1% [28/252]), and CNS (8.3% [21/252]) lesions. Among all systems, congenital abnormalities were noted among 8.4% (8/95) of calves. The most common congenital abnormalities identified included patent foramen ovale (3/8) and patent ductus arteriosus (3/8). When considering the system-based categorization (n = 190), most calves (57.9% [55/95]) had 2 or more system affected while only (38.9% [37/95]) had only 1 affected system. With regard to the calves that had 2 or more systems affected, 26.3% (25/95) had 2 affected systems, 20% (19/95) had 3 affected systems, 9.5% (9/95) had 4 affected systems, and 2.1% (2/95) of calves had 5 affected systems. The majority of calves with only 1 affected system were diagnosed with digestive lesions (73% [27/37]), followed by respiratory lesions (8.1% [3/37]). Among calves with 2 affected systems, the most common combination was digestive and respiratory system lesions (36% [9/25]), followed by a digestive system and other known system lesions (12% [3/25]) and digestive system and multisystemic lesions (12% [3/25]). Among calves with 3 systems involved, the most common combinations included the following: digestive, respiratory, and multisystemic (26.3% [5/19]); digestive, respiratory, and CNS (10.5% [2/19]); and digestive, multisystemic, and other known system (10.5% [2/19]). Among calves with 4 systems involved, the only combination represented more than once was digestive, CNS, musculoskeletal, and multisystemic (22.2% [2/9]). Among calves with 5 systemic involved, 1 of 2 had digestive, respiratory, musculoskeletal, hemolymphatic, and CNS lesions and 1 of 2 had urogenital, hemolymphatic, cardiovascular, CNS, and multisystemic lesions. Among calves with ≥ 3 affected systems diagnosed (n = 30), 43.3% (13/30) were not classified as multisystemic by the pathologist.

Among calves with a digestive lesion (70.5% [67/95]), 43.2% (29/67) had multiple lesions within the digestive tract (Table 2). A total of 106 digestive lesions were identified, with enteritis being the most common (45.3% [48/106]) followed by rumenitis (13.2% [14/106]), peritonitis (5.7% [6/106]), and hepatitis (5.7% [6/106]). Overall, 50.5% (48/95) of calves that were included in this study had enteritis. Among the 48 cases of enteritis, the majority of cases (60.4% [29/48]) had 1 infectious agent type identified, followed by identification of 2 different infectious agent types (35% [17/48]) and identification of 3 different infectious agent types (4.2% [2/48]). The most common infectious agents associated with enteritis were bacteria (54% [26/48]), viruses (44% [21/48]), parasites (27% [13/48]), and unknown agents (15% [7/48]). A total of 77 infectious agents, including bacteria, parasites, and viruses, were detected in the small intestines of calves with enteritis. The most common bacteria isolated from the small intestines of calves with enteritis were E coli (79.2% [38/48]) and Clostridium perfringens (43.8% [21/48]). While these bacterial agents were commonly identified, they were only rarely associated with histologic lesion (Table 3). Cryptosporidium spp was the only parasitic agent and was identified in 22.9% of calves with enteritis (11/48). Salmonella spp were identified in the small intestines of 4 calves with enteritis. Among the Salmonella isolates identified, S enterica serotype Newport was detected in 2 out of 4 calves, while the remaining samples were identified as S enterica serotype Agona (1/4), and S enterica serotype Give (1/4). Viral PCR testing was not performed in all calves with enteritis, including no rotavirus or bovine viral diarrhea virus (BVDV) testing for 8 of 48 and no coronavirus testing for 6 of 48 cases. Among those that were tested for viral enteric pathogens, 26% (11/43) were positive for coronavirus, 34% (14/41) were positive for rotavirus and 0% (0/41) were positive for BVDV.

The most common respiratory lesion identified was pneumonia (72% [23/32]) followed by pleuritis (6% [2/32]). Other respiratory abnormalities identified included bronchiolitis (1/32), laryngitis (1/32), neutrophil sequestration in the lungs (1/32), pulmonary congestion (1/32), pulmonary edema (1/32), pulmonary hemorrhage (1/32), and tracheitis (1/32). Pneumonia cases were further classified as bronchopneumonia (26% [6/23]), multifocal (26% [6/23]), interstitial (18% [4/23]), embolic (4% [1/23]), and other (26% [6/23]). Of the 23 animals with pneumonia 13 had a bacterial culture performed on the lungs and common isolated organisms included Escherichia coli (31% [4/13]), undifferentiated coliforms (31% [4/13]), and Mannheimia haemolytica (15% [2/13]). The presence of these bacterial species was not frequently associated with histopathologic lesions (Table 3).

The most common reason for the system-based categorization of multisystemic was because of signs of sepsis (79% [22/28]). Other lesions that were characterized as multisystemic included bacteremia (3/28 10.7%), neutrophil sequestration in multiple organs (3.6% [1/28]), petechia (3.6% [1/28]), and subcutaneous hemorrhages (3.6% [1/28]). Among calves with a multisystemic diagnosis (n = 23), bacteria were cultured from several organ systems outside the gastrointestinal tract, including the lungs, liver, umbilicus, joints, brain, spleen, and kidneys. The most common bacterial species identified was E coli (78% [18/23]), followed by undifferentiated coliforms (22% [5/23]), and C perfringens (13% [3/23]). S enterica was identified among 17% (4/23) of calves with multisystemic categorization; however, among these cases, Salmonella spp was isolated only from the gastrointestinal tract. Among calves with a system categorization of multisystemic disease, common concurrent lesions included enteritis (61% [14/23]), pneumonia (39% [9/23]), meningitis (17% [4/23]), and septic arthritis (17% [4/23]).

Bacterial cultures were performed on samples from 81% (77/95) of the necropsied calves (Table 3). Among the 287 bacterial isolates recovered, the most common body sites of origin included the small intestines (33% [96/287]), large intestines (15% [43/287]), lung (14% [39/287]), liver (10% [28/287]), brain/CSF (8% [22/287]), and umbilicus (7% [20/287]). The most common bacteria species identified were E coli (37% [106/287]) and C perfringens (16% [46/287]). A total of 12 Salmonella isolates were recovered from 7 (7% [7/95]) calves, with most of the isolates originating from the intestines or feces (75% [9/12]). Salmonella was also isolated from the liver (17% [2/12]) and abomasum (8% [1/12]). Many calves that were culture positive for Salmonella spp also had enteritis (71% [5/7]). Antimicrobial susceptibility testing was performed on 7 Salmonella isolates, but not all isolates were tested for the same antimicrobials. The number of resistant isolates for the following antimicrobials are as follows: penicillin (7/7), sulfadimethoxine (5/5), oxytetracycline (4/7), ampicillin (3/5), ceftiofur (0/5). Antimicrobial susceptibility testing was performed on 9 E coli isolates from septic calves but not all isolates were tested for the same antimicrobials. The number of resistant isolates for the following antimicrobials is as follows: penicillin (9/9), sulfadimethoxine (4/8), oxytetracycline (8/9), ampicillin (6/8), and ceftiofur (0/9). While bacteria was often isolated, depending on organ site, only 25% to 64% of isolates were determined to be associated with a histologic lesion (Table 3).

There was a significant association between median age and system affected (P = 0.012; Figure 1). Pairwise comparisons indicated that calves with CNS lesions were younger than calves with digestive lesions (P = 0.029). The χ² or Fisher exact test (when needed) also identified that calves with digestive lesions were less likely to have urogenital lesions (P = 0.001) and cardiovascular lesions (P = 0.003). Calves with CNS lesions were less likely to have musculoskeletal lesions (P = 0.002), while calves with urogenital lesions were more likely to have musculoskeletal lesions (P = 0.014). No seasonal effects were identified.

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Mean age (± 1 SD) of calves (n = 95) included in the study by system-based lesion categorization. *Significant (P < 0.05) differences among mean ages.

Citation: Journal of the American Veterinary Medical Association 260, 13; 10.2460/javma.22.03.0139

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Discussion

Overall, the majority of lesions in this retrospective study were digestive, respiratory, and multisystemic in origin. This is in contrast to producer-driven data that identified weather-related causes, unknown causes, and digestive problems as the most common causes of calf loss in the first 3 weeks of life unrelated to birthing problems.⁸ This discrepancy could be based on case selection, as calves that have died during a difficult weather event are unlikely to be presented for necropsy. However, the addition of gross and histopathologic findings were able to help classify the death of necropsied calves that would otherwise likely be reported as unknown by producers. It should be noted that most calves had at least 1 lesion identified, while only 3 (3.2%) calves had no lesions identified. This finding supports the utility of necropsy data to help classify likely causes of death in neonatal calves.

Enteritis was the most common reported digestive disorder in this study. This is similar to a Canadian study¹⁰ that reported enteritis as the most common digestive disorder; however, that study had a much lower prevalence than our study. Overall, 45.3% of cases with digestive lesions included in this retrospective evaluation had enteritis,⁹ while only 16% of older calves (those that lived > 3 days) had enteritis in the Canadian study.¹⁰ A high proportion of enteritis cases in this study were associated with E coli, C perfringens, and Cryptosporidium sp. The significance of the identification of these bacterial organisms on culture of the intestines is questionable since E coli and C perfringens are normal inhabitants of the gastrointestinal tract and the latter can also rapidly overgrow shortly after death. Additional characterization of these bacterial species would be necessary to determine their virulence potential. Additional characterization of C perfringens was pursued in only 2 cases of suspected clostridial enteritis by enterotoxin ELISA, both of which were negative. Viral pathogens, coronavirus and rotavirus, were commonly identified among enteritis cases, 26% and 34%, respectively. Reports of prevalence of both coronavirus and rotavirus in beef calves are sparse, but a previous study¹⁰ found a higher prevalence of coronavirus (62%) in Canadian beef calves than what is reported in this study.

Respiratory disease is one of the most common causes of disease in preweaned calves and is one of the major reasons for antimicrobial usage in calves prior to weaning.^2,11 Most previous studies^2,11 base their classification of respiratory disease on producer records. Few studies have characterized the lesions within the lungs, and in the 1 study¹⁰ that did, cases were classified broadly as pneumonia. While bronchopneumonia is thought to be a common cause of disease in preweaned beef calves and is often associated with summer heat, little data can be found to determine the prevalence of bronchopneumonia among young calves. In this study, the majority of lesions classified as pneumonia were not characterized as bronchopneumonia, with 74% of cases being classified as either interstitial, multifocal, other, or embolic pneumonias. Multifocal and embolic lesions are likely related to a septic spread of disease rather than originating from the respiratory tract. Factors that have been proposed to have an impact on respiratory disease in preweaned calves include maternal transfer of immunity, dystocia, environmental stressors, and maternal nutrient restriction.¹²

Multisystemic disease was the third most common system categorization in the population of necropsied calves in this study. This retrospective study¹⁰ has a higher prevalence of septic calves than what has been previously reported for neonatal beef calves (7.4%). Enteritis, pneumonia, meningitis, and septic arthritis were often identified among cases with septic lesions in this study, which is similar to previous data.¹³ This data support the notion that a focal site of infection is an important risk factor for sepsis in neonatal calves.^14,15

Major risk factors for illness in neonatal calves include dystocia, calving in confinement, failure of transfer of passive immunity, poor maternal milk production, or weather-related conditions that make it challenging for the calf to nurse.^16–18 While no studies in the US have investigated the prevalence of failure of transfer of passive immunity in beef calves, studies from Ireland^19–21 have reported a failure of passive transfer prevalence of 22% to 29% which is higher than the 19.2% reported for US dairy herds. Identified factors that contribute to failure of transfer of passive immunity in beef calves include dystocia, poor mothering ability, parity of the dam, and nutrition of the dam.^4,18,19 One study found that even mild complications in the birthing process that do not require assistance increase the risk of failure of transfer of passive immunity, highlighting how small difficulties in calving can impact the life and productivity of a beef calf.¹⁹ It is estimated that up to 20% of 2-year-old heifers may abandon their calf or not allow them to nurse and 12% of neonatal beef calf losses could be attributed to mothering problems.^4,22 Furthermore, primiparous dams and those dams that have been nutrient restricted in the prepartum period have been shown to have decreased colostrum quality, which increases the risk of failure of transfer of passive immunity.¹⁸ Unfortunately, in this study, transfer of passive immunity status was not available for review.

Overall, lesions that likely contributed to illness were identified in a high proportion of cases. Previous research has identified noninfectious disease processes to be more common than infectious among necropsies done across all age groups of calves (abortions, still births, perinatal calves and neonatal calves).¹⁰ The results of this study differ, in that infectious diseases were common. This is not surprising because the previously mentioned study found that infectious causes increased as calves aged. Among perinatal calf deaths this previous report found lesions in the thyroid, cardiac muscle, and skeletal muscle, and therefore the role of trace minerals and vitamins in overall disease was speculated.¹⁰ Lesions in these organ systems were not common among the sample population in our study, but underlying trace mineral imbalances may be a factor to consider. No trace mineral profiles were performed among cases included in this study.

Limitations of this study include its retrospective nature and lack of uniformity of necropsy data. Standardizing nomenclature based on postmortem findings in simple and consistent terms can provide more useful information about significant lesions that may be associated with death.²³ Additionally, the results of the gross, histopathologic, and ancillary tests are all listed in this study, however these results do not always agree, making interpretation challenging. For example, bacterial species are frequently isolated from body sites; however, they are less frequently associated with a lesion at that specific location. While, having access to common organisms identified from different organ systems may be useful to veterinarians when addressing sick calves, it is important for veterinarians to evaluate whether the bacterial species is associated with a lesion and therefore significant. Furthermore, there is an inherit bias of calves who presented for necropsy evaluation, as these may have been calves coming from outbreak situations or situations in which a presumptive diagnosis of the cause of death was made on farm and may not accurately represent the overall calf population. Finally, the inclusion criteria for this study required an age to have been recorded for each calf. This criterion may have led to a bias, as this selects for producers that maintain accurate records and delivered that information to the laboratory.

In conclusion, this study reports gross necropsy, histopathologic, and ancillary test results from beef calves submitted to a veterinary diagnostic laboratory. Common systems affected are in line with previous reports of digestive and respiratory diseases being common systems affected. Multisystemic diseases (ie sepsis) may be more common in calf populations than previously thought and could account for the high proportion of calf losses when producers cannot identify a cause of death. Future studies should focus on clinical prospective investigation to identify risk factors for these disease processes in neonatal beef calves.