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. 2020 Oct 23;98(11):skaa345. doi: 10.1093/jas/skaa345

Growth performance and hematological changes of weaned beef calves diagnosed with respiratory disease using respiratory scoring and thoracic ultrasonography

Inmaculada Cuevas-Gómez 1, Mark McGee 1, Matthew McCabe 1, Paul Cormican 1, Edward O’Riordan 1, Tara McDaneld 2, Bernadette Earley 1,✉
PMCID: PMC7694598  PMID: 33095858

Abstract

This study investigated 1) the effect of clinical bovine respiratory disease (BRD) and associated lung consolidations on growth performance and hematological profiles of recently weaned beef calves and 2) the relationship between clinical respiratory signs and lung consolidation detected by thoracic ultrasonography (TUS). One hundred and fifty-three weaned beef calves (209 days old [SD: 35.8] and 306 kg [SD: 26.3], at arrival) purchased and transported from auction markets were accommodated indoors in concrete slatted floor pens. Calves were weighed weekly from arrival until day 28 and on day 65 post-arrival. Assessment of BRD and blood sample collection for hematological profiles were performed on scheduled days (at arrival, on days 7, 14, and 28) and on other days upon BRD diagnosis. Animals were assessed for BRD using a total clinical respiratory score (CRS) of five clinical signs (rectal temperature, ear position, cough, nasal secretion, and eye secretion with each ranging from normal [0] to abnormal [3]) and TUS scores (normal [0] to lung consolidation ≥ 1 cm2 [2]). Based on CRS, 35% of calves were CRS+ (CRS ≥ 5) and 65% were CRS− (CRS < 5). Although no lung consolidations (TUS−) were detected at arrival, 34% of calves developed lung consolidation (≥1 cm2) (TUS+) during the first 28 d post-arrival. Only fever (>39.6 °C) and nasal discharge were weakly associated (r = 0.19, P <0.05) with lung consolidation. On the day of BRD detection, neutrophil number and neutrophil:lymphocyte ratio were 58% and 73% greater, respectively, in BRD calves with lung consolidation compared with healthy calves. From day 0 to 65, calf average daily gain (ADG) did not differ (P >0.05) between CRS+ and CRS− calves but was 0.09 kg/d lower (P < 0.05) for TUS+ compared with TUS− calves. Calves classified as BRD (CRS + TUS ≥ 5) with lung consolidation had lower (P < 0.05) ADG from arrival until day 28 than healthy calves and BRD calves without lung consolidation (0.11 ± 0.10 vs. 0.53 ± 0.07 vs. 0.57 ± 0.10 kg/d, respectively); however, no differences in ADG were observed from day 0 to 65. Conventional methods to diagnose BRD failed to detect calves with lung lesions. TUS is a useful tool to detect lung lesions and its implementation in combination with CRS should provide a more accurate and early diagnosis of BRD, which is fundamental to successful treatment, animal welfare, and growth performance.

Keywords: bovine respiratory disease, cattle, growth performance, hematology, thoracic ultrasonography

Introduction

Bovine respiratory disease (BRD) defines a complex, multifactorial syndrome, in which the interaction between infectious etiological agents (bacteria and virus), external stressors, and the animal’s immune system influences the development of the disease (Panciera and Confer, 2010). It is the most prevalent disease of recently weaned feedlot cattle in Ireland (Murray et al., 2017) and internationally (Delabouglise et al., 2017; Hay et al., 2017; Wilson et al., 2017) and causes substantial economic losses due to decreased animal performance, higher mortality rates, and increased costs associated with treatment (Cernicchiaro et al., 2013; Blakebrough-Hall et al., 2020) as well as negatively impacting animal welfare (Wolfger et al., 2015a). The temporal proximity between various stressors in feedlot cattle, such as weaning, transport, housing, and dietary change, results in immunosuppression, thus predisposing the respiratory tract to colonization by infectious pathogens (Lynch et al., 2010; Earley et al., 2017).

Despite the existence of numerous tools such as clinical respiratory scoring systems (Love et al., 2014; McGuirk and Peek, 2014; Maier et al., 2019) and automated monitoring systems of behavior to detect animals affected with BRD (Wolfger et al., 2015a), its diagnosis remains a challenge due to the lack of a gold standard diagnostic method antemortem (Wolfger et al., 2015b). Thoracic ultrasonography (TUS) is being used as a rapid, noninvasive, and on-site diagnostic and prognostic tool for finding lung abnormalities (Ollivett and Buczinski, 2016). Detection of lung abnormalities antemortem using TUS has been correlated with the findings postmortem using necropsy (Abutarbush et al., 2012; Baruch et al., 2019), and TUS is reported to have greater accuracy for BRD diagnosis compared with conventional methods, such as auscultation or clinical scoring criteria (Buczinski et al., 2015, 2016). Furthermore, this methodology requires only minimal training and skills and has a good inter-rater agreement (Buczinski et al., 2018).

Although BRD cannot be diagnosed solely based on hematological profiles, changes in the hemogram may provide useful information for the diagnosis, monitoring, and prognosis of BRD (Richeson et al., 2013; Roland et al., 2014). The presence of ≥4% of neutrophils in the bronchoalveolar lavage fluid of Holstein’s calves has been related with the presence of lung consolidation (Ollivett et al., 2015). Automated blood cell counters are readily accessible nowadays in veterinary practice for diagnosing and monitoring systemic diseases.

BRD diagnosis in feedlots is mainly performed through subjective evaluation of clinical respiratory signs (Sanderson et al., 2008); however, not all BRD-affected cattle show clinical respiratory signs resulting in subclinical BRD (sBRD) cases going undetected (Thompson et al., 2006; Murray et al., 2017). Animals affected with sBRD also have a lower economic return at slaughter compared with healthy animals (Thompson et al., 2006; Blakebrough-Hall et al., 2020). In preweaned dairy calves, the incorporation of TUS for diagnosing BRD led to the detection of calves with lung consolidation and these animals had reduced average daily gain (ADG) compared with calves without lung consolidation (Cramer and Ollivett, 2019). Few studies with backgrounding indoor feedlot cattle have assessed the relationship between clinical respiratory signs and lung consolidation detected by TUS or have evaluated the impact of BRD diagnosed using both TUS and respiratory signs on animal growth performance and hematology.

Therefore, the objective of this experiment was to investigate 1) the effect of clinical BRD and associated lung consolidations on growth performance and hematological profiles of recently weaned beef calves and 2) the relationship between clinical respiratory signs and lung consolidations detected by TUS.

Material and Methods

Ethical approval

All animals procedures performed in this study were reviewed and approved by the Teagasc Animal Ethics Committee (TAEC-221-2019) and were conducted under experimental license from the Health Products Regulatory Authority, Dublin, Ireland (AE19132-P101) in accordance with the protection of animals used for scientific purposes, that is, Directive 2010/63/EU and S.I. No. 543 of 2012, as amended by S.I. No. 434 of 2013 and S.I. No. 174 of 2014.

Animals management

One-hundred and fifty-three (209 days old [SD: 35.8] and 306 kg [SD: 26.3], at arrival) spring-born weaned “suckler” beef male (n = 79) and female (n = 74) calves were used. Forty-seven were sired by early-maturing breeds (Aberdeen Angus and Hereford) and 106 were late-maturing breeds (Charolais and Limousin). Animals were purchased through auction markets (n = 10) during October 2019, over five consecutive days, and were transported by road (transport duration, 1 to 2.5 h) in five different groups to the research center at Teagasc, Grange (longitude 6°65′W; latitude 53°52′N). At arrival (day −1), calves were housed and penned on concrete slatted floors (n = 32) in groups of five according to group and sex, with an individual space allowance of 2.9 m2 per animal. During the study, the mean indoor and outdoor temperatures were 5.5 °C (range 0 to 11 °C) and 6.1 °C (range 1 to 12 °C), respectively; the ambient outdoor relative humidity ranged from 72% to 97.5%.

Grass silage (in vitro dry matter digestibility 690 g/kg [SD: 18.0]) was offered ad libitum once daily and each animal received 60 g of a mineral and vitamin supplement applied on the forage. The objective was to grow the animals at a moderate ADG during this indoor winter period (backgrounding) and subsequently avail of compensatory growth during the grazing season (McGee et al., 2014). All animals had free access to clean, fresh water. Animals were vaccinated 24 h post-arrival (day 0) against bovine respiratory syncytial virus, parainfluenza-3-virus, Mannheimia haemolytica A1 (Bovilis Bovipast RSP, MSD Animal Health), bovine herpesvirus type 1 (Bovilis IBR marker live, MSD Animal Health), and against clostridial diseases using toxoids (Covexin 10, Zoetis). Animals were dewormed at day 21 post-arrival with a subcutaneous injection of the ivermectin solution (Closamectin, Norbrook). Male calves were castrated on day 30 to 35 by a veterinarian using standard Burdizzo castration management procedures with pain relief (administration of local anesthesia and of nonsteroidal anti-inflammatory drug [NSAID] prior to castration). The study duration was 65 d.

Experimental design

The experimental design of the study is detailed in Figure 1. Individual body weight was measured on days 0, 7, 14, 21, 28, and 65 post-arrival, using a calibrated platform scales (Tru-Test XR3000, load bars XHD 10000, Aukland, New Zealand) placed in the hydraulic squeeze chute (Titan, O’Donovan Engineering, Ireland).

Figure 1.

Figure 1.

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Experimental design. Timeline representing the experimental design from arrival of animals to the Research Centre facilities (day −1) until the last weight was measured (day 65). The BRD evaluation was performed during the first 28 d of the study. ADG was measured in three periods: ADG-1, ADG-2, and ADG-overall. BS, blood sampling.

Clinical and TUS assessment of individual calves was performed on days 0, 7, 14, and 28 post-arrival at the pen side and in the hydraulic squeeze chute. All calves were subjected to clinical respiratory assessment, using the clinical respiratory score (CRS) developed in the University of Wisconsin (McGuirk and Peek, 2014) and TUS by the same trained research veterinarian. At the same time as clinical respiratory assessment, whole blood samples were collected by jugular venipuncture into a 4-mL K3 ethylene diamine tetraacetic acid (K3EDTA) tubes (Vacuette; Cruinn Diagnostics, Dublin, Ireland) for hematological analysis within 1 to 2 h of blood collection. Additionally, from day 0 to 28, calves were visually checked by the research veterinarian once daily, and those with ≥1 visual sign included in the CRS or showing a depressed appearance were temporarily moved from their home pen to the handling chute and subjected to a complete clinical assessment and TUS. Calves continued to be observed on a daily basis by technical research personnel from day 28 until the end of the study.

CRS and TUS assessment

The Wisconsin CRS classifies rectal temperature, presence of cough, appearance of nasal and eye discharges, and ear position with scores ranging from normal (score 0) to very abnormal (score 3) (McGuirk and Peek, 2014), and the sum of all scores of each clinical sign evaluated to form the CRS. TUS was performed using an 8-MHz Wi-Fi linear probe (Tecnoscan SR-1C, Imporvet, Spain) at a maximal depth of 10 cm and a gain of 50 dB. Hair on the thorax was clipped with electric clippers, and isopropyl alcohol (70%) was used as a transducing agent before performing TUS as described by Ollivett and Buczinski (2016). TUS was performed on the left and right sides of the thorax. Since the first to third intercostal spaces could not be scanned in animals of this size, particularly when restrained in a chute, only the fourth, fifth, and sixth intercostal spaces were examined as these are the locations where lung consolidation has been associated with negative outcomes in feedlot cattle (Thompson et al., 2006; Rademacher et al., 2014). The appearance of the lungs in the thoracic ultrasonograms was classified according to a 3-point scale (Figure 2). Aerated lungs without any sign of consolidation or comet tail artifacts were classified as TUS score = 0. The ultrasonogram of the lungs with a TUS score = 0 is characterized by the visualization of the pleura as a hyperechoic line with echogenic lines parallel and below the pleural line representing reverberation artifacts. Lungs with one or more comet tail artifacts were classified as TUS score = 1. Comet tail artifacts were visualized as bright echogenic lines perpendicular to the pleural line. Lungs with any consolidation ≥ 1 cm2 were classified as TUS score = 2. Consolidation is visualized as a hypoechoic area of varying size with an echogenicity similar to that of liver parenchyma, in some cases, developing fluid bronchograms. Visualization of normal lungs and presence of comet tails by TUS were annotated on-site, while a 10-s loop of ultrasound footage was stored when consolidation was visualized in order to evaluate its size off-line by the same researcher after the study period was complete. For measuring consolidation size, squares in the screen representing 1 cm2 each were used.

Figure 2.

Figure 2.

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Ultrasonograms of the three thoracic ultrasound score classification. Echo of lung tissue is observed in the bottom part of each ultrasonogram, separated from the intercostal muscles by the pleura. Two comet tails in TUS = 1 are indicated with arrows and lung consolidations in TUS = 2 are marked with stars. Each square delimited by green lines indicates 1 cm2. ICM, intercostal muscles; P, pleura.

Three classifications according to CRS, TUS scores, and a combination of them were made retrospectively (Figure 3). Calves with a CRS ≥ 5 were CRS+ and calves with a CRS < 5 were CRS−. TUS classification was determined by the presence (TUS+) or absence (TUS−) of lung consolidation ≥ 1 cm2. The combined classification determined the clinical status of animals and was used to determine the need for antibiotic and NSAID therapy. Calves with a sum of both scores (CRS + TUS) ≥5 at any time between 1 and 28 d post-arrival were diagnosed as having clinical BRD (with or without lung consolidation, BRD-con and BRD-no-con, respectively). Once diagnosed, these animals were weighed, blood sampled, and, subsequently, treated with a subcutaneous dose of 2.5 mg/kg tulathromycin (Draxxin, Zoetis) and an intravenous dose of 0.5 mg/kg meloxicam (Metacam, Boehringer Ingelheim). Calves with a sum of both scores (CRS + TUS) <5 and no lung consolidation detected during 28 d post-arrival were considered healthy. Calves that developed lung consolidation (≥ 1 cm2) and a combined score (CRS + TUS) <5 were considered sBRD, did not receive veterinary medication unless they had a combined score ≥ 5, and were thereby classified as BRD. Calves with a combined score (CRS + TUS) ≥5 at least 7 d after initial drug medication were considered relapses and were re-treated with the same drugs. A matched healthy control calf corresponding to each individual BRD case was selected retrospectively from the nearest pen to compare hematology variables at the same sample times and ADG prior to and after treatment.

Figure 3.

Figure 3.

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Criteria for CRS classification, TUS classification, and combined classification. The sum of rectal temperature, nasal, eye, cough, and ear scores form the CRS (McGuirk and Peek, 2014). Calves with CRS < 5 were considered CRS−, and calves with CRS ≥ 5 were considered CRS+. TUS represents the appearance of the lungs. Calves without lung consolidation (TUS = 0 or 1) were considered TUS−, and calves with lung consolidation (TUS = 2) were considered TUS+. The combined classification used both CRS and TUS. Calves with CRS + TUS < 5 without lung consolidation were considered healthy; calves with CRS + TUS < 5 with lung consolidation were considered sBRD; calves with CRS + TUS ≥ 5 without lung consolidation were considered BRD-no-con; and calves with CRS + TUS ≥ 5 with lung consolidation were considered BRD-con.

Hematological analysis

Unclotted K3EDTA whole blood samples were analyzed using an ADVIA hematology analyzer (ADVIA 2120; Bayer Healthcare, Siemens, UK) equipped with software for bovine blood. White blood cell (WBC) count, total neutrophil, lymphocyte, monocyte, basophil, red blood cell (RBC), platelet numbers, hemoglobin concentration, and hematocrit percentage were evaluated. Three time (T) points were selected to analyze the hematological profile. The blood samples obtained 7 d prior to BRD detection are represented by T1, T2 represents the samples collected on the day of BRD diagnosis and treatment, and T3 those obtained 7 d post BRD detection.

Data management and statistical analyses

Statistical analyses were conducted using SAS v.9.4 software (SAS Institute, Inc.). The experimental unit was the individual animal. The outcomes of interest were the hematology variables and ADG. Calf ADG was determined for different periods: day 0 to 28 (ADG1), day 28 to 65 (ADG2), and day 0 to 65 (ADG-overall). Additionally, ADG prior to detection and treatment of BRD was calculated from day 1 to the day of BRD diagnosis (ADG-PRE), and ADG-POST was calculated from BRD diagnosis to day 65. Calf ADG-PRE and ADG-POST were calculated retrospectively in matched healthy control animals that were weighed on the same days as the BRD cases. Categorical explanatory variables included clinical status obtained from combined classification (treatment classifier [healthy, sBRD, BRD-con, and BRD-no-con]) and categorical dichotomous explanatory variables included CRS classification (+/−) and TUS classification (+/−). Three calves (one sBRD and two BRD-con) were removed from the study after day 28 due to injury not related to treatment classification; their ADG and blood data are included from period 1 only. Data were checked for normality and homogeneity of variance by histograms, q–q plots, and formal statistical tests as part of the UNIVARIATE procedure of SAS. Data that were not normally distributed were transformed by raising the variable to the power of lambda. The appropriate λ value was obtained by conducting a Box–Cox transformation analysis using the TRANSREG procedure of SAS. Data subjected to transformation were used to calculate P-values. Associations between explanatory variables and the outcomes of interest were evaluated using mixed-effects linear models (PROC MIXED). Group was included as a random effect, and age, sex, and breed as fixed effects. There was no effect of age (P > 0.05) and it was excluded from the model. Hematological variables were analyzed according to combined classification at T1 (Pre-BRD detection), T2 (BRD detection), and T3 (7 d post-BRD). Values of healthy matched controls were used corresponding with T1, T2, and T3 of BRD calves. As six sBRD calves were detected at day 28, they were not evaluated 7 d post-BRD so that T3 was not analyzed in sBRD calves. Number (×103 cells/µL) of WBC, neutrophils, lymphocytes, basophils, monocytes, eosinophils, RBC, platelets, neutrophil:lymphocyte ratio (N:L), concentration of hemoglobin, and hematocrit percentage were analyzed using repeated measures mixed models (PROC MIXED) where time point defined the repeated measure. A Tukey adjustment was used to correct for multiple testing. Multivariable linear regression models (PROC GLM with MANOVA) for ADG1, ADG2, and ADG-overall were conducted including CRS and TUS variables. To evaluate the prevalence of BRD disorders, the clinical parameters included in the CRS and the TUS were used. Scores recorded at days 0, 7, 14, and 28 were expressed as percentages (PROC FREQ) of calves that showed each abnormal clinical disorder. Cough, nasal, eye, and ear score were considered abnormal when ≥1. Rectal temperature score of 3 was considered abnormal (fever, >39.6 °C). Lung consolidation ≥ 1cm2 (TUS score = 2) was considered abnormal compared with absence of lung consolidation (TUS score = 0) or presence of comet tails (TUS score = 1). Association between clinical disorders and the presence of lung consolidation recorded at days 7, 14, and 28 was evaluated by calculating correlation coefficients between variables using Pearson correlation (PROC CORR). Data were considered statistically significant when P < 0.05. A statistical trend was considered when P-values ranged from 0.05 to 0.10. Least square means (Lsmeans) are reported with a standard error.

Results

BRD incidence using different diagnostic methods

Using CRS classification, 35% (54/153) and 65% (99/153) of calves were classified as CRS+ and CRS−, respectively (Table 1). Although no lung consolidation was detected at arrival, 34% (52/153) calves developed lung consolidation ≥ 1 cm2 (TUS+), and 66% (101/153) were TUS− in the 28 d post-arrival based on TUS classification. Using the combined classification, 68 calves (44.4%) were classified as BRD cases, of which 30 BRD-no-con and 38 BRD-con. Fourteen (9.2%) calves were classified as sBRD and 71 (46.4%) were healthy. Of 68 BRD cases, 8 (12%) calves relapsed once after the first BRD medication and no calves required any further BRD medication. Fifty percent (34/68) of BRD cases were detected within the first 7 d post-arrival and 81% (55/68) within the first 14 d (Figure 4). Lung consolidations were not found in 60.5% (23/38) of BRD calves post-antibiotic treatment. Conversely, lung consolidation was detected in all subsequent evaluation of sBRD calves diagnosed before day 28. No further cases of BRD were detected after day 28.

Table 1.

Distribution of 153 weaned beef calves according to their CRS and TUS status

CRS status1
TUS status2 − +
No consolidation 71 30
Consolidation 28 24
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1CRS from the study of McGuirk and Peek (2014). Calves were considered CRS+ when the score was ≥5.

2TUS consolidation was defined as ≥1 cm2.

Figure 4.

Figure 4.

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Distribution of BRD detection. Representation of the number of bovine respiratory disease (Nº BRD) cases (x axis) detected each day (y axis) from arrival (day −1) until day 28. Fifty percent of cases were detected within the first 7 d while 80% within the first 14 d post-arrival.

Prevalence of clinical disorders and associations

Descriptive statistics for BRD-associated disorders recorded on days 0, 7, 14, and 28 are reported in Table 2. A relatively low prevalence (<10%) of cough, eye discharge, and ear drooping was observed. The greatest percentages of calves with fever were observed on days 7 and 14 (28.1% and 26.8%, respectively). The percentage of calves that showed nasal discharge on days 0 (31.4%) and 7 (59.5%) decreased to 9% and 10% by days 14 and 28, respectively. No lung consolidations were detected by TUS on day 0; however by day 28, 18% of calves were TUS+. Fever was correlated (P < 0.05) with the presence of lung consolidation ≥ 1 cm2 on day 7 (Table 3). There was no correlation between the percentage of calves with clinical respiratory signs and lung consolidation at days 14 and 28 post-arrival (P > 0.05).

Table 2.

Prevalence (%) of clinical signs associated with BRD in 153 weaned beef calves evaluated at four stages within the first 28 d post-arrival

% Clinical scores1 Day 0 Day 7 Day 14 Day 28
Fever (>39.6 °C) 9.2 28.1 26.8 9.2
Cough 1.3 7.8 5.9 6.5
Nasal discharge 31.4 59.5 9.15 9.8
Eye discharge 2.6 9.8 2.6 7.2
Ear drooping 0 2.6 2.6 0.7
TUS evaluation
% Consolidation2 ≥ 1cm2 0 9.8 19.0 17.7
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1Percentage of calves with evidence of each clinical sign associated with BRD.

2Percentage of calves with lung consolidation ≥ 1 cm2.

Table 3.

Pearson correlation coefficients between clinical signs associated with respiratory disease and lung consolidation detected by ultrasonography simultaneously in 153 recently weaned beef calves

Lung consolidation2 ≥ 1 cm2
Clinical scores1 TUS7 TUS14 TUS28
Fever (>39.6 °C) 0.19* 0.13 0.04
Cough 0.07 0.09 0.02
Nasal discharge −0.13 −0.04 −0.10
Eye discharge −0.03 0.02 0.00
Ear drooping 0.30 0.02 −0.04
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1Clinical sign associated with BRD.

2Lung consolidation ≥ 1 cm2 detected by TUS on days 7, 14, and 28.

*P-value < 0.05.

Hematological variables

There was no effect of treatment (P > 0.05) prior to the development of BRD (T1) on any of the hematological variables except for platelet cell number (Table 4). There was a treatment × time interaction (P < 0.05) for neutrophil number, N:L, and basophil and platelet numbers. On the day of BRD detection (T2), neutrophil number was greater (P < 0.05) in BRD-con calves than in healthy and sBRD calves, with BRD-no-con intermediate (P > 0.05), whereas post-BRD (T3) neutrophil number was greater (P < 0.05) in BRD-con calves than in healthy calves, with BRD-no-con calves intermediate (P > 0.05). Neutrophil number was greater (P <0.05) in BRD-con calves at T2 compared with T1. N:L was greater (P < 0.05) in BRD-con calves compared with healthy and sBRD calves and tended to be greater (P = 0.07) in BRD-no-con calves than in healthy calves at T2. At T3, N:L was greater (P <0.05) in BRD-con calves than in healthy calves without difference (P > 0.05) when compared with BRD-no-con calves. N:L was greater (P < 0.05) in BRD-con at T2 and T3 compared with T1. Basophil number was lower (P < 0.05) in BRD-con compared with sBRD calves at T2, and no differences were found (P > 0.05) with healthy or BRD-no-con calves. Basophil and platelet numbers (P < 0.05) were greater at T3 compared with T1 and T2 in BRD-con calves. At T1, platelet number was greater (P < 0.05) in sBRD calves than in healthy calves, while there was no difference (P > 0.05) with BRD-con or BRD-no-con calves. At T3, platelet number was greater (P < 0.05) in BRD-con calves than in healthy calves and were not different (P >0.05) when compared with BRD-no-con calves.

Table 4.

Hematology variables (Lsmean with pooled SE) in 153 weaned beef calves according to combined classification at three sampling timepoints

Hematology parameter1 Combined classification2 Time 13 Time 24 Time 35 SE Treatment6 (Trt) Time (T) Trt × T
WBCs,
×103 cells/µL		 Healthy 10.4 9.7 9.1 0.34 0.0037 0.3366 0.4437
sBRD 10.3 10.1 — 0.78
BRD-no-con 10.8 10.4 10.1 0.51
BRD-con 10.7 10.8 11.2 0.45
Neutrophils,
×103 cells/µL		 Healthy 3.1 2.6x 2.2x 0.26 0.001 0.1136 0.0018
sBRD 2.7 2.1x – 0.56
BRD-no-con 2.9 3.8xy 2.6xy 0.38
BRD-con 2.7a 4.1b,y 3.8ab,y 0.33
Lymphocytes,
×103 cells/µL		 Healthy 6.9 6.6 6.5 0.21 0.1952 0.0062 0.1241
sBRD 7.1 7.4 7.6 0.48
BRD-no-con 7.6 6.3 7.0 0.32
BRD-con 7.6 6.3 6.9 0.28
N:L Healthy 0.46 0.40x 0.36x 0.05 0.0002 0.0448 0.0004
sBRD 0.39 0.31x – 0.10
BRD-no-con 0.42 0.63xy 0.41xy 0.07
BRD-con 0.36a 0.69b,y 0.62b,y 0.06
Basophils,
×103 cells/µL		 Healthy 0.12 0.12xy 0.12 0.006 0.0334 0.0029 0.0196
sBRD 0.13 0.14x 0.15 0.013
BRD-no-con 0.12 0.09y 0.13 0.009
BRD-con 0.12a 0.11a,xy 0.14b 0.007
Monocytes,
×103 cells/µL		 Healthy 0.45 0.41 0.37 0.023 0.1376 0.1685 0.7377
sBRD 0.44 0.49 – 0.053
BRD-no-con 0.46 0.46 0.40 0.035
BRD-con 0.48 0.44 0.46 0.031
Eosinophils,
×103 cells/µL		 Healthy 0.27 0.22 0.25 0.035 0.0935 0.3718 0.1847
sBRD 0.21 0.42 0.33 0.082
BRD-no-con 0.24 0.16 0.33 0.055
BRD-con 0.17 0.17 0.21 0.048
RBCs,
×106 cells/µL		 Healthy 10.7 10.6 10.5 0.16 0.001 0.1131 0.7346
sBRD 10.6 10.4 – 0.37
BRD-no-con 10.5 10.1 10.6 0.24
BRD-con 10.3 9.6 9.9 0.21
Hemoglobin,
g/dL		 Healthy 13.8 13.5 13.5 0.21 0.0072 0.0206 0.8926
sBRD 13.6 13.3 – 0.44
BRD-no-con 13.6 12.9 13.2 0.30
BRD-con 13.5 12.6 12.9 0.27
Hematocrit,
%		 Healthy 36.2 35.3 34.9 0.55 0.0107 0.0058 0.8440
sBRD 35.8 34.7 – 1.19
BRD-no-con 35.6 33.5 34.6 0.80
BRD-con 35.4 33.0 33.5 0.71
Platelets,
×103 cells/µL		 Healthy 503.3x 541.3 556.1x 22.1 <0.0001 0.0132 0.0281
sBRD 692.8y 648.5 – 51.5
BRD-no-con 560.4xy 528.0 609.6xy 33.9
BRD-con 540.2a,xy 539.6a 714.7b,y 29.5
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1WBCs, white blood cells; N:L, neutrophils:lymphocytes; RBCs, red blood cells.

2Classification is based on the combination of CRS and TUS score. Healthy (n = 68), sBRD (n = 14), BRD-no-con (n = 38), and BRD-con (n = 30). A matched healthy control calf corresponding to each individual BRD case was selected retrospectively from the nearest pen to compare hematology variables at the same sample times.

3Seven days before BRD detection.

4Day of BRD diagnosis.

5Seven days of BRD detection.

6Treatment (TRT) refers to classification groups (Healthy, sBRD, BRD-no-con, and BRD-con).

a–cWithin rows, Lsmeans differ from pre-BRD baseline by P ≤ 0.05.

x–zWithin columns, Lsmeans differ between treatments by P ≤ 0.05.

Lsmeans with the same letter are not significantly different.

There was no treatment × time interaction (P > 0.05) for WBC, eosinophil and RBC numbers, hemoglobin concentration, and hematocrit percentage. No differences (P > 0.05) in lymphocyte and monocyte numbers were found between treatment groups. Eosinophil numbers tended to be lower (P = 0.09) in BRD calves with lung consolidation compared with sBRD calves. WBC number was greater, while RBC number, hemoglobin concentration, and hematocrit percentage were lower (P < 0.05) in BRD-con calves compared with healthy calves, while no differences (P >0.05) were found when values were compared with sBRD and BRD-no-con calves.

Growth performance

Least squares means for ADG according to the clinical classification of calves are presented in Table 5. The ADG1 of calves classified as BRD-con was 0.42 and 0.46 kg lower (P < 0.05) than healthy calves and BRD-no-con calves, respectively; however, no difference (P >0.05) was found between healthy, sBRD, BRD-no-con, and BRD-con calves in ADG2 or ADG-overall. Regarding ADG prior to and after BRD treatment, BRD-no-con and BRD-con calves had a lower (P < 0.05) ADG-PRE compared with healthy calves, whereas ADG-POST was greater (P < 0.05) for BRD-no-con and BRD-con calves than healthy calves.

Table 5.

Least squares mean (SE) of ADG (kg) calculated in different periods

Clinical status1 n ADG1 ADG2 ADG-overall ADG-PRE ADG-POST
Healthy 71 0.53a (0.07) 0.17 (0.04) 0.32 (0.03) 0.16a (0.10) 0.26a (0.04)
sBRD2 14 0.45ab (0.14) 0.09 (0.09) 0.23 (0.07) — —
BRD-no-con3 30 0.57a (0.10) 0.22 (0.07) 0.37 (0.05) −0.26b (0.15) 0.48b (0.06)
BRD-con4 38 0.11b (0.10) 0.30 (0.06) 0.26 (0.05) −0.44b (0.13) 0.44b (0.06)
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1A matched healthy control calf corresponding to each individual BRD case was selected retrospectively from the nearest pen to compare ADG prior to and after treatment at the same times. ADGs calculated with individual body weights from day 0 to 28 (ADG1), day 28 to 65 (ADG2) and ADG-overall.

2Calves diagnosed as sBRD: CRS + TUS < 5 and lung consolidation ≥ 1 cm2.

3Calves diagnosed with BRD (CRS + TUS ≥ 5) without lung consolidation.

4Calves diagnosed with BRD (CRS + TUS ≥ 5) with lung consolidation ≥ 1 cm2.

a,bWithin columns, Lsmeans differ between treatments by P ≤ 0.05.

Multivariable linear regression evaluating the association between ADG and CRS status as well as TUS status is presented in Table 6. Although there was no difference (P > 0.05) in calf ADG according to CRS status, ADG1 was 0.28 kg lower and ADG-overall was 0.09 kg lower (P < 0.05) in TUS+ compared with TUS− calves.

Table 6.

Multivariable linear regression model for ADG1, ADG2, and ADG-overall1 in 153 weaned beef calves according to their CRS status2 and TUS status3

Variable ADG1 ADG2 ADG-overall
Estimate ADG (kg/d) SE P-value Estimate ADG (kg/d) SE P-value Estimate ADG (kg/d) SE P-value
Intercept 0.54 0.055 <0.0001 0.17 0.035 <0.0001 0.32 0.027 <0.0001
CRS status
− Referent Referent Referent
+ 0.01 0.088 0.9029 0.03 0.057 0.6316 0.02 0.043 0.5745
TUS status
− Referent Referent Referent
+ −0.28 0.088 0.0016 0.05 0.057 0.4028 −0.09 0.043 0.0346
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1ADGs calculated with individual body weights (kg) from day 0 to 28 (ADG1), day 28 to 65 (ADG2) and ADG-overall.

2Classification is based on the CRS developed by McGuirk and Peek (2014). Calves with CRS ≥ 5 were CRS+.

3Classification is based on the thoracic ultrasound evaluation. Animals with lung consolidation ≥ 1 cm2 in at least one ultrasound evaluation were TUS+.

Discussion

Currently, there is no “gold standard” antemortem method for diagnosing BRD meaning that delayed and under-detection of BRD are a significant problem in feedlot cattle (Wolfger et al., 2015b; Blakebrough-Hall et al., 2020). In this study, the evaluation of clinical respiratory signs, which is widely used as a BRD diagnostic method in feedlots (Sanderson et al., 2008; Leruste et al., 2012), was used in conjunction with TUS, a measure of the presence of lung consolidation. The TUS method is a novel technique that can be used for the early detection of BRD but is rarely used in feedlot studies to date (Abutarbush et al., 2012; Timsit et al., 2019).

The incidence of BRD based on evaluation of solely clinical respiratory signs obtained in the current experiment (35%) is intermediate to the range in values (15% to 53%) reported for feedlot studies (Wittum et al., 1996; Thompson et al., 2006; Fulton et al., 2009; Ball et al., 2019; Blakebrough-Hall et al., 2020). In feedlot studies, the incidence of BRD based on clinical respiratory signs is much lower than the prevalence of lung lesions at slaughter. For example, Thompson et al. (2006) reported that 22.6% of animals had clinical BRD, whereas 42.8% had lung lesions at slaughter, and Blakebrough-Hall et al. (2020) reported that 17% of animals showed clinical respiratory signs, whereas 68% had lung lesions at slaughter. This underlines the importance of including TUS to detect lung lesions as not all BRD-affected animals are diagnosed when evaluated using only clinical respiratory signs during their productive life.

When comparing CRS and TUS in the current study, 28% of calves classified as CRS− had lung consolidation, whereas 56% of calves classified as CRS+ had no lung consolidation detected by TUS. Similarly, Abutarbush et al. (2012) evaluating BRD cases and healthy controls in feedlot cattle found that 16% of healthy controls had lung consolidation, whereas 72% of BRD cases had no lung consolidation detected by TUS. Given that cranial lung lobes could not be evaluated in this study due to the size of animals, it is possible that more calves classified as CRS− could have had lung consolidation. Using the combined classification (CRS + TUS) in this study, 54% of calves had BRD or sBRD, which implied a detection of 18% (28/153) additional calves that would have not been detected using CRS alone. Similarly, when Thompson et al. (2006) used the combined definition of clinical BRD (treated animals) and sBRD (never treated but with lesions at slaughter), they obtained a BRD incidence of 53%. Thus, the combination of CRS with TUS used in this study has shown that both methods are necessary to provide a better classification of BRD cases (calves that show clinical signs without evidence of lung consolidation detectable by TUS, calves with lung consolidation detected by TUS without evidence of clinical signs, and calves with both clinical signs and lung consolidation).

Interestingly, in this study, 60.5% (22/38) of lung consolidation detected in treated BRD-con calves were not detected in the ultrasound evaluation at day 28. However, lung consolidation was present in sBRD calves that were evaluated at least twice, suggesting that consolidation could have responded to treatment in some of the BRD-con treated calves. Similarly in feedlot cattle, Abutarbush et al. (2012) found that 49% of lung consolidations were not detected in subsequent evaluations by TUS in BRD animals after receiving treatment. Lung tissue is reported to have extensive capacity to repair and regenerate damaged cells after injury or disease both in humans and mice (Herriges and Morrisey, 2014; Zacharias et al., 2018), though more investigation is needed in this regard in cattle.

In the current study, the greatest incidence of BRD cases occurred within the first 14 d post-arrival. Previous authors have reported that BRD incidence was greatest in the first week after arrival to the feedlot and decreased subsequently (Sanderson et al., 2008). Management practices conducted at feedlots such as transport or commingling predispose calves to BRD development in an early stage after entry (Taylor et al., 2010). In the present study, although calves were visually checked once daily during 28 d post-arrival to detect clinical respiratory signs, a greater number of BRD cases (53/82) were detected on the 4 days when the combined score was used (days 0, 7, 14, and 28) than on the intervening days when solely CRS was used (29/82 calves detected). Thus, the evaluation of feedlot calves using CRS with TUS detected a greater number of BRD-affected animals at the early stage of the infection (from 7 to 14 d).

In the present study, the most prevalent clinical disorders associated with BRD were nasal discharge at days 0 and 7 post-arrival and fever at days 7 and 14 post-arrival. The rest of the clinical signs had a low prevalence during the first 28 d. The poor correlations between calf clinical signs and the simultaneous presence of lung consolidation detected by TUS are in agreement with the study of Leruste et al. (2012), who found weak correlations (rsp from 0.16 to 0.40) between clinical signs of BRD and moderate-to-severe lung consolidation at slaughter in feedlot cattle. Therefore, clinical signs are not accurate indicators of lung consolidation, thereby making it necessary to use TUS to detect lung consolidations antemortem. Due to the limitation of TUS as a routinely diagnostic tool, particularly in large high throughput facilities, advances in TUS-related technology in the future may facilitate an early detection of lung consolidation in cattle.

The greatest changes in the hematology profile were observed in neutrophil number and N:L. Calves that were classified as BRD-con had a 52% and 92% increase in neutrophil number and N:L, respectively, the day that they were diagnosed with BRD compared with the day of arrival when they were healthy. This increase is substantially greater than the values reported in beef calves (neutrophil, 5%; N:L, 12%, increase) following a combination of standard postweaning management practices, including housing and adapting to a new diet (Lynch et al., 2011). Moreover, BRD-con calves had a greater number of neutrophils (58%) and N:L ratio (73%) compared with healthy calves on the day of BRD diagnosis and post-BRD (73% and 72% greater, respectively). Ollivett et al. (2015) reported a greater percentage of neutrophils (14.0%) in the bronchoalveolar lavage fluid of Holstein’s calves with lung consolidation compared with calves with completely normal lungs (1.2%). However, the neutrophil number in sBRD calves in this study did not differ from the neutrophil number in healthy calves. This could indicate that not only lung consolidation but also clinical disease symptoms are necessary to detect the differences in neutrophil number. The neutrophil and N:L profiles are in agreement with previous studies, where higher values have been reported in calves affected by BRD compared with healthy calves (Burciaga-Robles et al., 2010; Lindholm-Perry et al., 2018). Previous authors reported low eosinophil and high RBC numbers in blood samples at arrival to facilities as indicators of calves at a greater risk of developing clinical signs of BRD (Richeson et al., 2013). In the present study at arrival, eosinophil numbers tended to be lower in BRD-con calves compared with sBRD calves. However, BRD-con calves had lower RBC number than healthy calves. Thus, changes in blood neutrophil number and N:L could be useful indicators of respiratory disease in calves that develop lung consolidation following natural infection.

The use of TUS is more common in the studies of preweaned dairy heifers. Recent experiments show that compared with preweaned dairy heifers without lung consolidation, those exhibiting consolidation had reduced (0.12 kg) ADG during the preweaning period (Cramer and Ollivett, 2019), produced 525 kg less milk in their first lactation (Dunn et al., 2018), and had a higher probability of being culled by the end of first lactation (Teixeira et al., 2017). In contrast, there is limited information relating TUS findings with the growth outcomes of feedlot calves. Abutarbush et al. (2012) did not find an association between lung consolidation detected by TUS in feedlot cattle and growth performance; however, they only performed TUS on one side of the thorax using a 3.5-MHz sectorial probe and they evaluated frozen images, which could have affected the diagnostic accuracy (Rademacher et al., 2014).

In the current study, calves with lung consolidation detected at least once by TUS, regardless of their CRS status, had a reduction of growth rate by 28.1% (0.23 vs. 0.32 kg/d) during the first 65-d post-arrival compared with those without lung consolidation. Timsit et al. (2019) reported that severity of lung consolidation as measured using TUS in feedlot cattle was negatively related with ADG (−34 g/cm lung consolidation depth) and was associated with a higher risk of BRD relapse after first BRD antibiotic treatment (odds ratio, 1.337/cm lung consolidation depth). Moreover, studies have reported the impact of lung lesions identified at slaughter on the growth performance of feedlot cattle; compared with animals without lung lesions during the late fattening period, those with severe lung lesions had a reduction of growth rate by 5.3% (1.67 vs. 1.58 kg/d) (Thompson et al., 2006) and 16.7% (1.8 vs. 1.5 kg/d) (Blakebrough-Hall et al., 2020).

Considering the combined classification in the present study, BRD-con calves had reduced ADG during the first 28 d post-arrival compared with healthy and BRD-no-con calves. However, whether the day of BRD diagnosis and treatment is considered, BRD-no-con and BRD-con calves (clinically ill calves) had lower ADG than healthy calves prior to BRD treatment with calves having increased ADG above healthy calves after BRD treatment. In the present study, it is recognized that the ADG measurement duration is short. Additionally, the absolute growth rates are relatively low as the animals were on a “backgrounding” phase in order to minimize feed costs and exploit subsequent compensatory growth at pasture during the following grazing season (McGee et al., 2014). The changes in ADG may be attributed to reduced gut fill at the time of BRD diagnosis due to the lower intake of sick calves compared with healthy calves (Wolfger et al., 2015a), resulting in an increased apparent weight gain post-treatment when appetite resumed. Previous authors have reported that dairy calves reduced their visits to the feeder during 3 d prior to BRD detection and tended to reduce those visits 7 d post BRD detection (Johnston et al., 2016). In beef feedlot calves, mean meal intake and frequency of visits to the feeder were reduced 7 d before BRD detection (Wolfger et al., 2015a). On the other hand, animals could have experienced a physiological compensatory growth after a period of reduced intake caused by BRD (Hornick et al., 2000). Therefore, a low intake caused by BRD may have triggered a compensatory growth, which may have led to BRD calves growing faster after BRD treatment so that, eventually, no difference in ADG was found from day 0 to 65 between calves diagnosed as BRD and healthy calves. Moreover, the success of BRD treatment could have caused a recovery of growth in BRD calves. In this study, sBRD calves, which were not treated, had a numerically lower ADG than healthy and BRD calves in all growth periods evaluated. However, these differences were not statistically significant, which could be due to the low number (n = 14) of sBRD calves present in this study. Thompson et al. (2006) reported that BRD feedlot cattle that were treated tended to grow faster in the finishing period than those with subclinical disease that were not treated. Further research should be directed toward the evaluation of compensatory growth and the effect of antibiotic treatment in calves diagnosed as having BRD using both CRS and TUS.

Conclusions

A greater number of BRD-affected calves were detected using TUS and CRS when compared with CRS alone. Moreover, an increased N:L ratio could be a useful indicator of respiratory disease in calves which develop lung consolidation. The detection of lung consolidation antemortem can only be confirmed using TUS and this is important since TUS+ calves had lower growth performance than TUS− calves, while no differences in ADG were observed between CRS+ and CRS− calves. The current detection of BRD in feedlots through CRS alone may lead to calves going undetected with lung consolidation due to the weak correlation between clinical signs and lung consolidation. Accordingly, TUS could be implemented in feedlots to detect BRD-associated lung consolidation during the first weeks post-entry, when animals are at greater risk of developing BRD. Future research should focus on the evolution of lung consolidation after therapy and its effect on growth performance as well as exploiting the recent advances in sequencing technologies to characterize the microbiome and virome associated with the development of BRD in this cattle population.

Acknowledgment

We acknowledge funding support through the US-Ireland (Department of Agriculture, Food and the Marine (DAFM)) Tri-Partite grant (project number 2018US-IRL200). The authors would like to extend their thanks to: the farm staff for the care and management of the animals, the field technicians (Eddie Mulligan and John Horan) for assistance with blood sampling and Margaret Murray for hematology analyses, at Teagasc AGRIC Grange.

Glossary

Abbreviations

ADG

average daily gain

BRD

bovine respiratory disease

CRS

clinical respiratory score

NSAID

Nonsteroidal anti-inflammatory drugs

sBRD

subclinical BRD

TUS

thoracic ultrasonography

Conflict of interest statement

The authors declare that they have no competing interests.

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