Effect of Coxiella burnetii infection on milk constituents and cow behaviour
Momena Khatun
A B C * , Sergio C. García A , Peter C. Thomson D , Alysia M. Parker D , Rupert M. Bruckmaier C and Katrina L. Bosward D
+ Author Affiliations
- Author Affiliations
A School of Life and Environmental Sciences and Sydney Institute of Agriculture, The University of Sydney, Camden, NSW 2570, Australia.
B Bangladesh Agricultural University, Mymensingh 2202, Bangladesh.
C Veterinary Physiology, Vetsuisse Faculty, University of Bern, 3012 Bern, Switzerland.
D Sydney School of Veterinary Science, The University of Sydney, Camden, NSW 2570, Australia.
* Correspondence to: momena.khatun@vetsuisse.unibe.ch, monarahman24@bau.edu.bd
Handling Editor: Keith Pembleton
Animal Production Science - https://doi.org/10.1071/AN21236
Submitted: 6 May 2021 Accepted: 11 March 2022 Published online: 2 May 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Context: The role of Coxiella burnetii in intramammary infection (IMI) in dairy cows is not fully understood.
Aims: The objective of this study was to investigate changes in milk constituents and behaviour such as daily activity (arbitrary unit/day) and daily rumination (min/day) in cows exposed to C. burnetii.
Methods: In total, 1029 quarter milk samples were manually collected from 48 cows before and after alveolar milk ejection in the automatic milking rotary at the University of Sydney’s dairy farm. Each milk sample was analysed for the following parameters: immunoglobulin G (cIgG) against C. burnetii via ELISA, somatic cell count (SCC), total immunoglobulin G (tIgG), lactate dehydrogenase (LDH), serum albumin (SA), milk protein%, milk fat%, and subjected to microbiological culture. The daily activity and daily rumination changes were recorded using heat- and rumination long-distance tags across 21 days before detection of IMI (n = 42 cows). Linear and logistic mixed models were used, with ‘cow’ and ‘quarter nested within cow’ as random effects.
Results: The presence of cIgG was quarter-specific; the cIgG+ quarters (n = 64) had significantly greater tIgG (P < 0.001), LDH (P < 0.001), SA (P < 0.001) and milk protein% (P = 0.002) than did cIgG− quarters (n = 279). The cIgG+ quarters had significantly greater SCC, tIgG, LDH and SA responses than did controls (P < 0.05), but lower responses than did Gram-negative coliform IMI (P < 0.05). Gram-positive IMI caused by coagulase positive/negative Staphylococcus, Streptococcus uberis, Streptococcus dysgalactiae, Corynebacterium spp. in cIgG+ quarters resulted in greater tIgG, LDH and SA responses than in control quarters (P < 0.05). Coagulase-positive Staphylococcus IMI was associated with the presence of cIgG as assessed by Fisher’s exact test (P < 0.05). The cIgG+ group had a significant (P < 0.05) reduction in daily rumination compared with the cIgG− group in the study period.
Conclusions and implications: The cIgG antibody responses are quarter specific with greater tIgG, LDH, SA and milk protein in the affected quarters, as well as behavioural changes in the cow, and therefore might be useful for detection of C. burnetii IMI.
Keywords: Coxiella burnetii, daily activity, daily rumination, immunoglobulin G, intramammary infection, lactate dehydrogenase, serum albumin, somatic cell count.
References
Anderson A, Bijlmer H, Fournier P-E, Graves S, Hartzell J, Kersh GJ, Limonard G, Marrie TJ, Massung RF, McQuiston JH, Nicholson WL, Paddock CD, Sexton DJ (2013) Diagnosis and management of Q fever – United States, 2013: recommendations from CDC and the Q Fever Working Group. MMWR Recommendations and Reports 62, 1–30. http://www.ncbi.nlm.nih.gov/pubmed/23535757Angelakis E, Raoult D (2010) Q fever. Veterinary Microbiology 140, 297–309.
| Q fever.Crossref | GoogleScholarGoogle Scholar | 19875249PubMed |
Barlow J, Rauch B, Welcome F, Kim SG, Dubovi E, Schukken Y (2008) Association between Coxiella burnetii shedding in milk and subclinical mastitis in dairy cattle. Veterinary Research 39, 23
| Association between Coxiella burnetii shedding in milk and subclinical mastitis in dairy cattle.Crossref | GoogleScholarGoogle Scholar | 18252189PubMed |
Bewley JM, Boyce RE, Hockin J, Munksgaard L, Eicher SD, Einstein ME, Schutz MM (2010) Influence of milk yield, stage of lactation, and body condition on dairy cattle lying behaviour measured using an automated activity monitoring sensor. Journal of Dairy Research 77, 1–6.
| Influence of milk yield, stage of lactation, and body condition on dairy cattle lying behaviour measured using an automated activity monitoring sensor.Crossref | GoogleScholarGoogle Scholar |
Bruckmaier RM, Ontsouka CE, Blum JW (2004) Fractionized milk composition in dairy cows with subclinical mastitis. Veterinarni Medicina 49, 283–290.
| Fractionized milk composition in dairy cows with subclinical mastitis.Crossref | GoogleScholarGoogle Scholar |
Burton JL, Erskine RJ (2003) Immunity and mastitis. Some new ideas for an old disease. Veterinary Clinics of North America: Food Animal Practice 19, 1–45.
| Immunity and mastitis. Some new ideas for an old disease.Crossref | GoogleScholarGoogle Scholar |
Butler DG, Cullis BR, Gilmour AR, Gogel BG, Thompson R (2017) ASReml-R Reference Manual Version 4. (VSN International Ltd: Hemel Hempstead, UK).
Chaplin S, Munksgaard L (2001) Evaluation of a simple method for assessment of rising behaviour in tethered dairy cows. Animal Science 72, 191–197.
| Evaluation of a simple method for assessment of rising behaviour in tethered dairy cows.Crossref | GoogleScholarGoogle Scholar |
Dhaka P, Malik SVS, Yadav JP, Kumar M, Barbuddhe SB, Rawool DB (2020) Apparent prevalence and risk factors of coxiellosis (Q fever) among dairy herds in India. PLoS ONE 15, e0239260
| Apparent prevalence and risk factors of coxiellosis (Q fever) among dairy herds in India.Crossref | GoogleScholarGoogle Scholar | 32931511PubMed |
Eldin C, Mélenotte C, Mediannikov O, Ghigo E, Million M, Edouard S, Mege J-L, Maurin M, Raoult D (2017) From Q fever to Coxiella burnetii infection: a paradigm change. Clinical Microbiology Reviews 30, 115–190.
| From Q fever to Coxiella burnetii infection: a paradigm change.Crossref | GoogleScholarGoogle Scholar | 27856520PubMed |
Guatteo R, Beaudeau F, Berri M, Rodolakis A, Jolyc A, Seegers H (2006) Shedding routes of Coxiella burnetii in dairy cows: implications for detection and control. Veterinary Research 37, 827–833.
| Shedding routes of Coxiella burnetii in dairy cows: implications for detection and control.Crossref | GoogleScholarGoogle Scholar | 16973121PubMed |
Günther J, Petzl W, Bauer I, Ponsuksili S, Zerbe H, Schuberth H-J, Brunner RM, Seyfert H-M (2017) Differentiating Staphylococcus aureus from Escherichia coli mastitis: S. aureus triggers unbalanced immune-dampening and host cell invasion immediately after udder infection. Scientific Reports 7, 4811
| Differentiating Staphylococcus aureus from Escherichia coli mastitis: S. aureus triggers unbalanced immune-dampening and host cell invasion immediately after udder infection.Crossref | GoogleScholarGoogle Scholar | 28684793PubMed |
Hernández-Castellano LE, Wall SK, Stephan R, Corti S, Bruckmaier RM (2017) Milk somatic cell count, lactate dehydrogenase activity, and immunoglobulin G 2 concentration associated with mastitis caused by different pathogens: a field study. Schweizer Archiv für Tierheilkunde 159, 283–290.
| Milk somatic cell count, lactate dehydrogenase activity, and immunoglobulin G 2 concentration associated with mastitis caused by different pathogens: a field study.Crossref | GoogleScholarGoogle Scholar |
Hogan J, Gonzalez R, Harmon R, Nickerson S, Oliver S, Pankey J, Smith K (1999) ‘Laboratory Handbook on Bovine Mastitis.’ (National Mastitis Council: Madison, WI, USA)
Khademi P, Ownagh A, Mardani K, Khalili M (2019) Prevalence of Coxiella burnetii in milk collected from buffalo (water buffalo) and cattle dairy farms in Northwest of Iran. Comparative Immunology, Microbiology and Infectious Diseases 67, 101368
| Prevalence of Coxiella burnetii in milk collected from buffalo (water buffalo) and cattle dairy farms in Northwest of Iran.Crossref | GoogleScholarGoogle Scholar | 31627037PubMed |
Khatun M, Bruckmaier RM, Thomson PC, House J, García SC (2019) Suitability of somatic cell count, electrical conductivity, and lactate dehydrogenase activity in foremilk before versus after alveolar milk ejection for mastitis detection. Journal of Dairy Science 102, 9200–9212.
| Suitability of somatic cell count, electrical conductivity, and lactate dehydrogenase activity in foremilk before versus after alveolar milk ejection for mastitis detection.Crossref | GoogleScholarGoogle Scholar | 31351709PubMed |
Kopecny L, Bosward KL, Shapiro A, Norris JM (2013) Investigating Coxiella burnetii infection in a breeding cattery at the centre of a Q fever outbreak. Journal of Feline Medicine and Surgery 15, 1037–1045.
| Investigating Coxiella burnetii infection in a breeding cattery at the centre of a Q fever outbreak.Crossref | GoogleScholarGoogle Scholar | 23651605PubMed |
Lehmann M, Wall SK, Wellnitz O, Bruckmaier RM (2015) Changes in milk L-lactate, lactate dehydrogenase, serum albumin, and IgG during milk ejection and their association with somatic cell count. Journal of Dairy Research 82, 129–134.
| Changes in milk L-lactate, lactate dehydrogenase, serum albumin, and IgG during milk ejection and their association with somatic cell count.Crossref | GoogleScholarGoogle Scholar |
McQuiston JH, Childs JE (2002) Q Fever in humans and animals in the United States. Vector-Borne and Zoonotic Diseases 2, 179–191.
| Q Fever in humans and animals in the United States.Crossref | GoogleScholarGoogle Scholar | 12737547PubMed |
McQuiston JH, Holman RC, Mccall CL, Childs JE, Swerdlow DL, Thompson HA (2006) National surveillance and the epidemiology of human Q fever in the United States, 1978–2004. American Journal of Tropical Medicine and Hygiene 75, 36–40.
| National surveillance and the epidemiology of human Q fever in the United States, 1978–2004.Crossref | GoogleScholarGoogle Scholar |
Nguyen D-AD, Neville MC (1998) Tight junction regulation in the mammary gland. Journal of Mammary Gland Biology and Neoplasia 3, 233–246.
| Tight junction regulation in the mammary gland.Crossref | GoogleScholarGoogle Scholar |
Nielsen NI, Larsen T, Bjerring M, Ingvartsen KL (2005) Quarter health, milking interval, and sampling time during milking affect the concentration of milk constituents. Journal of Dairy Science 88, 3186–3200.
| Quarter health, milking interval, and sampling time during milking affect the concentration of milk constituents.Crossref | GoogleScholarGoogle Scholar | 16107409PubMed |
Ontsouka CE, Bruckmaier RM, Blum JW (2003) Fractionized milk composition during removal of colostrum and mature milk. Journal of Dairy Science 86, 2005–2011.
| Fractionized milk composition during removal of colostrum and mature milk.Crossref | GoogleScholarGoogle Scholar | 12836936PubMed |
Parisi A, Fraccalvieri R, Cafiero M, Miccolupo A, Padalino I, Montagna C, Capuano F, Sottili R (2006) Diagnosis of Coxiella burnetii-related abortion in Italian domestic ruminants using single-tube nested PCR. Veterinary Microbiology 118, 101–106.
| Diagnosis of Coxiella burnetii-related abortion in Italian domestic ruminants using single-tube nested PCR.Crossref | GoogleScholarGoogle Scholar | 16891064PubMed |
Porter SR, Czaplicki G, Mainil J, Guattéo R, Saegerman C (2011) Q Fever: current state of knowledge and perspectives of research of a neglected zoonosis. International Journal of Microbiology 2011, 248418
| Q Fever: current state of knowledge and perspectives of research of a neglected zoonosis.Crossref | GoogleScholarGoogle Scholar | 22194752PubMed |
Rahimi E, Doosti A, Ameri M, Kabiri E, Sharifian B (2010) Detection of Coxiella burnetii by nested PCR in bulk milk samples from dairy bovine, ovine, and caprine herds in Iran. Zoonoses and Public Health 57, e38–e41.
| Detection of Coxiella burnetii by nested PCR in bulk milk samples from dairy bovine, ovine, and caprine herds in Iran.Crossref | GoogleScholarGoogle Scholar | 19968851PubMed |
Raven CFH, Hautvast JLA, Herremans T, Leenders ACAP, Schneeberger PM (2012) Solitary IgM phase II response has a limited predictive value in the diagnosis of acute Q fever. Epidemiology and Infection 140, 1950–1954.
| Solitary IgM phase II response has a limited predictive value in the diagnosis of acute Q fever.Crossref | GoogleScholarGoogle Scholar |
Rodolakis A, Berri M, Héchard C, Caudron C, Souriau A, Bodier CC, Blanchard B, Camuset P, Devillechaise P, Natorp JC, Vadet JP, Arricau-Bouvery N (2007) Comparison of Coxiella burnetii shedding in milk of dairy bovine, caprine, and ovine herds. Journal of Dairy Science 90, 5352–5360.
| Comparison of Coxiella burnetii shedding in milk of dairy bovine, caprine, and ovine herds.Crossref | GoogleScholarGoogle Scholar | 18024725PubMed |
Schneeberger PM, Hermans MHA, van Hannen EJ, Schellekens JJA, Leenders ACAP, Wever PC (2010) Real-time PCR with serum samples is indispensable for early diagnosis of acute Q fever. Clinical and Vaccine Immunology 17, 286–290.
| Real-time PCR with serum samples is indispensable for early diagnosis of acute Q fever.Crossref | GoogleScholarGoogle Scholar | 20032219PubMed |
Stangaferro ML, Wijma R, Caixeta LS, Al-Abri MA, Giordano JO (2016) Use of rumination and activity monitoring for the identification of dairy cows with health disorders: Part III. Metritis. Journal of Dairy Science 99, 7422–7433.
| Use of rumination and activity monitoring for the identification of dairy cows with health disorders: Part III. Metritis.Crossref | GoogleScholarGoogle Scholar | 27372583PubMed |
Szymańska-Czerwińska M, Jodełko A, Zaręba-Marchewka K, Niemczuk K (2019) Shedding and genetic diversity of Coxiella burnetii in Polish dairy cattle. PLoS ONE 14, e0210244
| Shedding and genetic diversity of Coxiella burnetii in Polish dairy cattle.Crossref | GoogleScholarGoogle Scholar | 30629637PubMed |
Verbyla AP, Cullis BR, Kenward MG, Welham SJ (1999) The analysis of designed experiments and longitudinal data by using smoothing splines. Journal of the Royal Statistical Society Series C: Applied Statistics 48, 269–311.
| The analysis of designed experiments and longitudinal data by using smoothing splines.Crossref | GoogleScholarGoogle Scholar |
Vicari N, Faccini S, Ricchi M, Garbarino C, Decastelli L, Boldini M, Rosignoli C, Dalmasso A, Bronzo V, Fabbi M (2013) Occurrence of Coxiella burnetii in bulk tank milk from northwestern Italy. Veterinary Record 172, 687
| Occurrence of Coxiella burnetii in bulk tank milk from northwestern Italy.Crossref | GoogleScholarGoogle Scholar |
Wellnitz O, Arnold ET, Bruckmaier RM (2011) Lipopolysaccharide and lipoteichoic acid induce different immune responses in the bovine mammary gland. Journal of Dairy Science 94, 5405–5412.
| Lipopolysaccharide and lipoteichoic acid induce different immune responses in the bovine mammary gland.Crossref | GoogleScholarGoogle Scholar | 22032363PubMed |
Wellnitz O, Arnold ET, Lehmann M, Bruckmaier RM (2013) Short communication: Differential immunoglobulin transfer during mastitis challenge by pathogen-specific components. Journal of Dairy Science 96, 1681–1684.
| Short communication: Differential immunoglobulin transfer during mastitis challenge by pathogen-specific components.Crossref | GoogleScholarGoogle Scholar | 23295119PubMed |
