Cited by 49Microbial infections and disease researchAnimal health and immunologyPneumonia and Respiratory Infections

Differences in the association of cough and other clinical signs with ultrasonographic lung consolidation in dairy, veal, and beef calves

Open access
Lowie, T., Van Leenen, K., Jourquin, S., Pas, M.L., Bokma, J., Pardon, B.·2022·Journal of Dairy Science

Abstract

Bovine respiratory disease (BRD) continues to be a leading cause of economic loss, hampered animal welfare, and intensive antimicrobial use in cattle operations worldwide. Reduction of antimicrobial use is hindered because it is still unclear which clinical signs are best monitored to reliably detect pneumonia. Also, these clinical signs may vary according to age and between breeds. The objective of this cross-sectional study was to identify clinical signs associated with ultrasound-confirmed pneumonia (lung consolidation ≥1 cm depth) pre- and postweaning in different production types (dairy, beef, and veal) and breeds. A total of 956 calves (70% Holstein-Friesian dairy and 30% Belgian Blue beef) from 84 herds were clinically examined using 24 parameters, scored using the Wisconsin and California BRD clinical scoring systems and subjected to thoracic ultrasonography. Of the calves, 42.8% and 19.5% had a lung consolidation ≥1 cm and ≥3 cm, respectively. Cough, both spontaneous and induced, was the only and best-performing clinical sign statistically associated with lung consolidation in all production types. Fever (rectal temperature ≥39.4°C) was the second most promising factor, being significant in beef and veal calves but not in dairy calves. Postweaning, none of the clinical signs studied were statistically associated with pneumonia, with the exception of cough in dairy calves. Spontaneous or induced cough as a single clinical sign outperformed any combination of clinical signs, including the Wisconsin and California respiratory disease scoring systems, but sensitivity remained low. This information can be useful to select appropriate clinical signs for continuous monitoring in precision livestock applications, targeted to a given breed and age. As a cross-sectional measurement, diagnostic accuracy of spontaneous cough (accuracy = 65.1%, sensitivity = 37.4%, specificity = 85.7%) is too low to be used as a criterion to select animals with pneumonia for antimicrobial treatment. At the group level, cough monitoring holds potential as an early warning sign, after which lung ultrasonography should follow.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3168/jds.2021-21570

Cites

10 of 10 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Animals affected with BRD complex display a spectrum of signs including fever, lethargy, and anorexia.

    “Animals affected with BRD complex display a spectrum of signs, including fever, lethargy, and anorexia [24,52,53,54].”

    From Strategies for Bovine Respiratory Disease (BRD) Diagnosis and Prognosis: A Comprehensive Overview (2024) · cites this paper as [52]

    The Abstract identifies fever as a clinical sign in calves with BRD, and the clinical-signs table includes depressed mentation, consistent with lethargy. The Discussion says appetite was not included in the study, so this paper does not support the anorexia part of the cited sentence. (LLM, conf=0.87)

    Experimental — accuracy not yet measured
  • In severe cases, BRD leads to strenuous, accelerated, open-mouthed breathing.

    “In severe cases, the disease leads to strenuous, accelerated, open-mouthed breathing [24,52,53,54].”

    From Strategies for Bovine Respiratory Disease (BRD) Diagnosis and Prognosis: A Comprehensive Overview (2024) · cites this paper as [52]

    The Introduction says BRD can range from subclinical inflammation to life-threatening pneumonia, and the Discussion says increased respiratory rate may occur during a BRD episode. Neither passage describes strenuous or open-mouthed breathing, or establishes that accelerated breathing occurs specifically in severe cases. Page numbers are unavailable in our copy. (LLM, conf=0.84)

    Experimental — accuracy not yet measured
  • Other manifestations of BRD are coughing, along with nasal and ocular discharges.

    “Other manifestations of BRD are coughing, along with nasal and ocular discharges [24,52,53,54].”

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 42

  1. Andrani, F., M. Aiello, G. Bertorelli, E. Crisafulli, and A. Chetta. 2019. Cough, a vital reflex. Mechanisms, determinants and mea- surements. Acta Biomed. 89:477-480. https: / / doi .org/ 10 .23750/ abm .v89i4 .6182. · DOI
  2. Bokma, J., R. Boone, P. Deprez, and B. Pardon. 2019. Risk factors for antimicrobial use in veal calves and the association with mor- tality. J. Dairy Sci. 102:607-618. https: / / doi .org/ 10 .3168/ jds .2018 -15211. · DOI
  3. Buczinski, S., G. Forté, and A. M. Bélanger. 2013. Short communica- tion: Ultrasonographic assessment of the thorax as a fast technique to assess pulmonary lesions in dairy calves with bovine respiratory disease. J. Dairy Sci. 96:4523-4528. https: / / doi .org/ 10 .3168/ jds .2013 -6577. · DOI · Paper page
  4. Buczinski, S., G. Forté, D. Francoz, and A. M. Bélanger. 2014. Com- parison of thoracic auscultation, clinical score, and ultrasonogra- phy as indicators of bovine respiratory disease in preweaned dairy calves. J. Vet. Intern. Med. 28:234-242. https: / / doi .org/ 10 .1111/ jvim .12251. · DOI · Paper page
  5. Buczinski, S., T. L. Ollivett, and N. Dendukuri. 2015. Bayesian esti- mation of the accuracy of the calf respiratory scoring chart and ultrasonography for the diagnosis of bovine respiratory disease in pre-weaned dairy calves. Prev. Vet. Med. 119:227-231. https: / / doi .org/ 10 .1016/ j .prevetmed .2015 .02 .018. · DOI · Paper page
  6. Buczinski, S., and B. Pardon. 2020. Bovine respiratory disease diag- nosis: What progress has been made in clinical diagnosis? Vet. Clin. North Am. Food Anim. Pract. 36:399-423. https: / / doi .org/ 10 .1016/ j .cvfa .2020 .03 .004. · DOI · Paper page
  7. Callan, R. J., and F. B. Garry. 2002. Biosecurity and bovine respira- tory disease. Vet. Clin. North Am. Food Anim. Pract. 18:57-77. https: / / doi .org/ 10 .1016/ S0749 -0720(02)00004 -X. · DOI
  8. Carpentier, L., D. Berckmans, A. Youssef, D. Berckmans, T. van Wa- terschoot, D. Johnston, N. Ferguson, B. Earley, I. Fontana, E. Tullo, M. Guarino, E. Vranken, and T. Norton. 2018. Automatic cough detection for bovine respiratory disease in a calf house. Biosyst. Eng. 173:45-56. https: / / doi .org/ 10 .1016/ j .biosystemseng .2018 .06 .018. · DOI
  9. Catry, B., J. Dewulf, D. Maes, B. Pardon, B. Callens, M. Vanrobaeys, G. Opsomer, A. De Kruif, and F. Haesebrouck. 2016. Effect of antimicrobial consumption and production type on antibacterial resistance in the bovine respiratory and digestive tract. PLoS One 11:e0146488. https: / / doi .org/ 10 .1371/ journal .pone .0146488. · DOI
  10. Divers, T.J. 2008. Respiratory diseases. Pages 79-129 in Rebhun's Diseases of Dairy Cattle. 2nd ed. T. J. Divers and S. F. Peek, ed. https: / / doi .org/ 10 .1016/ B978 -141603137 -6 .50007 -7. · DOI
  11. Dubrovsky, S. A., A. L. Van Eenennaam, S. S. Aly, B. M. Karle, P. V. Rossitto, M. W. Overton, T. W. Lehenbauer, and J. G. Fadel. 2020. Preweaning cost of bovine respiratory disease (BRD) and cost-benefit of implementation of preventative measures in calves on California dairies: The BRD 10K study. J. Dairy Sci. 103:1583- 1597. https: / / doi .org/ 10 .3168/ jds .2018 -15501. · DOI
  12. Eberhart, N. L., J. M. Storer, M. Caldwell, A. M. Saxton, and P. D. Krawczel. 2017. Behavioral and physiologic changes in Holstein steers experimentally infected with Mannheimia haemolytica. Am. J. Vet. Res. 78:1056-1064. https: / / doi .org/ 10 .2460/ ajvr .78 .9 .1056. · DOI · Paper page
  13. Ferrari, S., R. Piccinini, M. Silva, V. Exadaktylos, D. Berckmans, and M. Guarino. 2010. Cough sound description in relation to respira- tory diseases in dairy calves. Prev. Vet. Med. 96:276-280. https: / / doi .org/ 10 .1016/ j .prevetmed .2010 .06 .013. · DOI
  14. Gille, L., J. Callens, K. Supré, F. Boyen, F. Haesebrouck, L. Van Driessche, K. van Leenen, P. Deprez, and B. Pardon. 2018. Use of a breeding bull and absence of a calving pen as risk factors for the presence of Mycoplasma bovis in dairy herds. J. Dairy Sci. 101:8284-8290. https: / / doi .org/ 10 .3168/ jds .2018 -14940. · DOI
  15. Grissett, G. P., B. J. White, and R. L. Larson. 2015. Structured litera- ture review of responses of cattle to viral and bacterial pathogens causing bovine respiratory disease complex. J. Vet. Intern. Med. 29:770-780. https: / / doi .org/ 10 .1111/ jvim .12597. · DOI · Paper page
  16. Grobet, L., D. Poncelet, L. J. Royo, B. Brouwers, D. Pirottin, C. Mi- chaux, F. Ménissier, M. Zanotti, S. Dunner, and M. Georges. 1998. Molecular definition of an allelic series of mutations disrupting the myostatin function and causing double-muscling in cattle. Mamm. Genome 9:210-213. https: / / doi .org/ 10 .1007/ s003359900727. · DOI
  17. Gustin, P., F. Lomba, J. Bakima, P. Lekeux, and K. P. Van de Woesti- jne. 1987. Partitioning of pulmonary resistance in calves. J. Appl. Physiol. 62:1826-1831. https: / / doi .org/ 10 .1152/ jappl .1987 .62 .5 .1826. · DOI
  18. Hill, T. M., H. G. Bateman II, F. X. Suarez-Mena, T. S. Dennis, and R. L. Schlotterbeck. 2016. Short communication: Changes in body temperature of calves up to 2 months of age as affected by time of day, age, and ambient temperature. J. Dairy Sci. 99:8867-8870. https: / / doi .org/ 10 .3168/ jds .2016 -10994. · DOI
  19. Htun, T. P., Y. Sun, H. L. Chua, and J. Pang. 2019. Clinical features for diagnosis of pneumonia among adults in primary care setting: A systematic and meta-review. Sci. Rep. 9:7600. https: / / doi .org/ 10 .1038/ s41598 -019 -44145 -y. · DOI
  20. Jourquin, S., J. Bokma, L. De Cremer, K. van Leenen, N. Vereecke, and B. Pardon. 2022. Randomized field trial comparing efficacy of florfenicol and oxytetracycline in a natural outbreak of calf pneu- monia using lung reaeration as a cure criterion. J. Vet. Intern. Med. 36:820-828. https: / / doi .org/ 10 .1111/ jvim .16348. · DOI
  21. Kolb, E. A., R. E. Buterbaugh, C. L. Rinehart, D. Ensley, G. A. Perry, K. W. Abdelsalam, and C. C. L. Chase. 2020. Protection against bovine respiratory syncytial virus in calves vaccinated with adju- vanted modified live vaccine administered in the face of maternal antibody. Vaccine 38:298-308. https: / / doi .org/ 10 .1016/ j .vaccine .2019 .10 .015. · DOI
  22. Masmeijer, C., B. Devriendt, T. Rogge, K. van Leenen, L. De Cremer, B. Van Ranst, P. Deprez, E. Cox, and B. Pardon. 2019. Random- ized field trial on the effects of body weight and short transport on stress and immune variables in 2-to 4-week-old dairy calves. J. Vet. Intern. Med. 33:1514-1529. https: / / doi .org/ 10 .1111/ jvim .15482. · DOI · Paper page
  23. McGuirk, S. M., and S. F. Peek. 2014. Timely diagnosis of dairy calf respiratory disease using a standardized scoring system. Anim. Health Res. Rev. 15:145-147. https: / / doi .org/ 10 .1017/ S1466252314000267. · DOI · Paper page
  24. Murphy, D., A. Ricci, Z. Auce, J. G. Beechinor, H. Bergendahl, R. Breathnach, J. Bureš, J. P. Duarte Da Silva, J. Hederová, P. Hek- man, C. Ibrahim, E. Kozhuharov, G. Kulcsár, E. Lander Persson, J. M. Lenhardsson, P. Mačiulskis, I. Malemis, L. Markus-Cizelj, A. Michaelidou-Patsia, M. Nevalainen, P. Pasquali, J. Rouby, J. Schefferlie, W. Schlumbohm, M. Schmit, S. Spiteri, S. Srčič, L. Ta- ban, T. Tiirats, B. Urbain, E. Vestergaard, A. Wachnik-Święcicka, J. Weeks, B. Zemann, A. Allende, D. Bolton, M. Chemaly, P. S. Fernandez Escamez, R. Girones, L. Herman, K. Koutsoumanis, R. Lindqvist, B. Nørrung, L. Robertson, G. Ru, M. Sanaa, M. Sim- mons, P. Skandamis, E. Snary, N. Speybroeck, B. Ter Kuile, H. Wahlström, K. Baptiste, B. Catry, P. S. Cocconcelli, R. Davies, C. Ducrot, C. Friis, G. Jungersen, S. More, C. Muñoz Madero, P. Sanders, M. Bos, Z. Kunsagi, J. Torren Edo, R. Brozzi, D. Candiani, B. Guerra, E. Liebana, P. Stella, J. Threlfall, and H. Jukes. 2017. EMA and EFSA Joint Scientific Opinion on mea- sures to reduce the need to use antimicrobial agents in animal husbandry in the European Union, and the resulting impacts on food safety (RONAFA). EFSA J. 15. https: / / doi .org/ 10 .2903/ j .efsa .2017 .4666. · DOI
  25. Nienaber, J. A., and G. L. Hahn. 2007. Livestock production system management responses to thermal challenges. Int. J. Biometeorol. 52:149-157. https: / / doi .org/ 10 .1007/ s00484 -007 -0103 -x. · DOI
  26. Nowicki, J., and M.T. Murray. 2020. Bronchitis and pneumonia. Pages 1196-1201 in Textbook of Natural Medicine. 5th ed. J. E. Pizzorno and M. T. Murray, ed. https: / / doi .org/ 10 .1016/ B978 -0 -323 -43044 -9 .00155 -2. · DOI
  27. Pardon, B. 2019. A quick scan lung ultrasound method and flow chart as a decision aid for bronchopneumonia diagnosis. Pages 258-260 in XXIV Congreso Internacional ANEMBE de Medicina Bovina, 2019, Sevilla, Spain. Asociación Nacional de Especialistas en Me- dicina Bovina de España (ANEMBE).
  28. Pardon, B., S. Buczinski, and P. R. Deprez. 2019. Accuracy and inter- rater reliability of lung auscultation by bovine practitioners when compared with ultrasonographic findings. Vet. Rec. 185:109. https: / / doi .org/ 10 .1136/ vr .105238. · DOI
  29. Pardon, B., J. Callens, J. Maris, L. Allais, W. Van Praet, P. Deprez, and S. Ribbens. 2020. Pathogen-specific risk factors in acute out- breaks of respiratory disease in calves. J. Dairy Sci. 103:2556-2566. https: / / doi .org/ 10 .3168/ jds .2019 -17486. · DOI
  30. Pardon, B., B. Catry, R. Boone, H. Theys, K. De Bleecker, J. Dewulf, and P. Deprez. 2014. Characteristics and challenges of the modern Belgian veal industry. Vlaams Diergeneeskd. Tijdschr. 83:155-163. https: / / doi .org/ 10 .21825/ vdt .v83i4 .16641. · DOI
  31. Pardon, B., B. Catry, J. Dewulf, D. Persoons, M. Hostens, K. De Bleecker, and P. Deprez. 2012. Prospective study on quantitative and qualitative antimicrobial and anti-inflammatory drug use in white veal calves. J. Antimicrob. Chemother. 67:1027-1038. https: / / doi .org/ 10 .1093/ jac/ dkr570. · DOI
  32. Pardon, B., K. De Bleecker, J. Dewulf, J. Callens, F. Boyen, B. Catry, and P. Deprez. 2011. Prevalence of respiratory pathogens in dis- eased, non-vaccinated, routinely medicated veal calves. Vet. Rec. 169:278. https: / / doi .org/ 10 .1136/ vr .d4406. · DOI
  33. Peek, S.F., T.L. Ollivett, and T.J. Divers. 2018. Respiratory diseases. Pages 94-167 in Rebhun's Diseases of Dairy Cattle. 3rd ed. S. F. Peek and T. J. Divers, ed. https: / / doi .org/ 10 .1016/ B978 -0 -323 -39055 -2 .00004 -8. · DOI
  34. Polverino, M., F. Polverino, M. Fasolino, F. Andò, A. Alfieri, and F. De Blasio. 2012. Anatomy and neuro-pathophysiology of the cough reflex arc. Multidiscip. Respir. Med. 7:5. https: / / doi .org/ 10 .1186/ 2049 -6958 -7 -5. · DOI
  35. Radaelli, E., M. Luini, G. R. Loria, R. A. J. Nicholas, and E. Scan- ziani. 2008. Bacteriological, serological, pathological and immuno- histochemical studies of Mycoplasma bovis respiratory infection in veal calves and adult cattle at slaughter. Res. Vet. Sci. 85:282-290. https: / / doi .org/ 10 .1016/ j .rvsc .2007 .11 .012. · DOI
  36. Smith, B. P., A. A. Gunn, S. M. McGuirk, and M. Izzo. 2015. Manifes- tations and management of disease in neonatal ruminants. Pages 303-306 in Large Animal Internal Medicine. 5th ed. B. P. Smith, ed. Elsevier.
  37. van Leenen, K., J. Jouret, P. Demeyer, L. Van Driessche, L. De Cre- mer, C. Masmeijer, F. Boyen, P. Deprez, and B. Pardon. 2020b. Associations of barn air quality parameters with ultrasonographic lung lesions, airway inflammation and infection in group-housed calves. Prev. Vet. Med. 181:105056. https: / / doi .org/ 10 .1016/ j .prevetmed .2020 .105056. · DOI
  38. van Leenen, K., J. Jouret, P. Demeyer, P. Vermeir, D. Leenknecht, L. Van Driessche, L. De Cremer, C. Masmeijer, F. Boyen, P. Deprez, E. Cox, B. Devriendt, and B. Pardon. 2021. Particulate matter and airborne endotoxin concentration in calf barns and their as- sociation with lung consolidation, inflammation, and infection. J. Dairy Sci. 104:5932-5947. https: / / doi .org/ 10 .3168/ jds .2020 -18981. · DOI
  39. van Leenen, K., L. Van Driessche, L. De Cremer, C. Masmeijer, F. Boyen, P. Deprez, and B. Pardon. 2020a. Comparison of bron- choalveolar lavage fluid bacteriology and cytology in calves classi- fied based on combined clinical scoring and lung ultrasonography. Prev. Vet. Med. 176:104901. https: / / doi .org/ 10 .1016/ j .prevetmed .2020 .104901. · DOI
  40. Vandermeulen, J., C. Bahr, D. Johnston, B. Earley, E. Tullo, I. Fon- tana, M. Guarino, V. Exadaktylos, and D. Berckmans. 2016. Early recognition of bovine respiratory disease in calves using automated continuous monitoring of cough sounds. Comput. Electron. Agric. 129:15-26. https: / / doi .org/ 10 .1016/ j .compag .2016 .07 .014. · DOI
  41. Wang, M., L. G. Schneider, K. J. Hubbard, and D. R. Smith. 2018. Cost of bovine respiratory disease in preweaned calves on US beef cow-calf operations (2011-2015). J. Am. Vet. Med. Assoc. 253:624-631. https: / / doi .org/ 10 .2460/ javma .253 .5 .624. · DOI
  42. Weary, D. M., J. M. Huzzey, and M. A. G. von Keyserlingk. 2009. Board-Invited Review: Using behavior to predict and identify ill health in animals. J. Anim. Sci. 87:770-777. https: / / doi .org/ 10 .2527/ jas .2008 -1297. · DOI

Cited by

Sorted by citations

Authors
Lowie, T., Van Leenen, K., Jourquin, S., Pas, M. L., Bokma, J., & Pardon, B.
Affiliations
Ghent University (BE)
Corresponding author
Lowie, T.
Venue
Journal of Dairy Science
Published
2022-07
Volume
105
Issue
7
Pages
6111-6124
ISSN
0022-0302 (ISSN-L)
OpenAlex
W4229032099
Cited by
49
References
10
Citations by year
2026: 10 · 2025: 13 · 2024: 11 · 2023: 9 · 2022: 5 · 2012: 1
FWCI
5.95
Type
journal article
Language
en
Open access
Locations
  • Journal of Dairy Science (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Ghent University Academic Bibliography (Ghent University) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Universiteit Gent
  • Agentschap Innoveren en Ondernemen (HBC.2019.2876 KRIS:04570416)
Topics
  • Life Sciences › Immunology and Microbiology › Microbiology › Microbial infections and disease research
  • Health Sciences › Veterinary › Small Animals › Animal health and immunology
  • Health Sciences › Medicine › Epidemiology › Pneumonia and Respiratory Infections
Keywords
bovine respiratory disease, calf pneumonia, lung consolidation, thoracic ultrasound, cough, clinical signs, fever, dairy calves, veal calves, beef calves, Belgian Blue, Holstein cows, post-weaning period, precision livestock farming, early warning signs, antimicrobial use reduction
MeSH terms
Red Meat, Animals, Anti-Bacterial Agents, Cattle, Cattle Diseases, Cough, Cross-Sectional Studies, Lung, Lung Diseases, Pneumonia

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review