Bovine Colostrum: Human and Animal Health Benefits or Route Transmission of Antibiotic Resistance—One Health Perspective
Abstract
:1. Introduction
2. Importance of Bioactive Components and Animal Health Benefits
3. Human Health Benefits
4. Bovine Colostrum Pathogens
- Normal inhabitants of the mucosa and skin of dam (Streptococcus spp., Staphylococcus, Pasteurella spp., Corynebacterium spp. and Arconobacterium pyogenes);
- Environmental contaminants (gram-negative rods, Bacillus spp. and Micrococcus spp.);
- Fecal contaminants (coliforms, Enterococcus spp., Streptococcus bovis, E. coli and Proteus spp.);
- Mammary pathogens (Streptococcus uberis, Staphylococcus aureus and Streptococcus dysgalactiae);
- During the collection, processing, storage and feeding processes;
- Systemic infections (Listeria spp., Salmonella spp. and Staphylococcus spp.).
5. Antibiotic Residues and Antibiotic-Resistant Bacteria in Colostrum
Presence of Antibiotic-Resistant Bacteria
6. Measures to Mitigate Bacterial Contamination in Bovine Colostrum
7. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Zarcula, S.; Cernescu, H.; Mircu, C.; Tulcan, C.; Morvay, A.; Baul, S.; Popovici, D. Influence of breed, parity and food intake on chemical composition of first colostrum in cow. Anim. Sci. Biotechnol. 2010, 43, 154–157. [Google Scholar]
- McGrath, B.A.; Fox, P.F.; McSweeney, P.L.H.; Kelly, A.L. Composition and properties of bovine colostrum: A review. Dairy Sci. Technol. 2016, 96, 133–158. [Google Scholar] [CrossRef] [Green Version]
- Poonia, A.; Shiva. Bioactive compounds, nutritional profile and health benefits of colostrum: A review. Food Prod. Process. Nutr. 2022, 4, 26. [Google Scholar] [CrossRef]
- Mehra, R.; Garhwal, R.; Sangwan, K.; Guiné, R.P.F.; Lemos, E.T.; Buttar, H.S.; Visen, P.K.S.; Kumar, N.; Bhardwaj, A.; Kumar, H. Insights into the Research Trends on Bovine Colostrum: Beneficial Health Perspectives with Special Reference to Manufacturing of Functional Foods and Feed Supplements. Nutrients 2022, 14, 659. [Google Scholar] [CrossRef] [PubMed]
- Linehan, K.; Ross, R.P.; Stanton, C. Bovine Colostrum for Veterinary and Human Health Applications: A Critical Review. Annu. Rev. Food Sci. Technol. 2023, 14, 387–410. [Google Scholar] [CrossRef]
- Tsioulpas, A.; Grandison, A.S.; Lewis, M.J. Changes in physical properties of bovine milk from the colostrum period to early lactation. J. Dairy Sci. 2007, 90, 5012–5017. [Google Scholar] [CrossRef]
- Stelwagen, K.; Carpenter, E.; Haigh, B.; Hodgkinson, A.; Wheeler, T.T. Immune components of bovine colostrum and milk. J. Anim. Sci. 2009, 87, 3–9. [Google Scholar] [CrossRef] [Green Version]
- OuYang, X.; Yang, C.Y.; Xiu, W.L.; Hu, Y.H.; Mei, S.S.; Lin, Q. Oropharyngeal administration of colostrum for preventing necrotizing enterocolitis and late-onset sepsis in preterm infants with gestational age ≤ 32 weeks: A pilot single-center randomized controlled trial. Int. Breastfeed. J. 2021, 16, 59. [Google Scholar] [CrossRef]
- Abd El-Fattah, A.M.; Abd Rabo, F.H.; El-Dieb, S.M.; El-Kashef, H.A. Changes in composition of colostrum of Egyptian buffaloes and Holstein cows. BMC Vet. Res. 2012, 8, 19. [Google Scholar] [CrossRef] [Green Version]
- Godden, S.M.; Lombard, J.E.; Woolums, A.R. Colostrum Management for Dairy Calves. Vet. Clin. N. Am. Food Anim. Pract. 2019, 35, 535–556. [Google Scholar] [CrossRef]
- Lopez, A.J.; Heinrichs, A.J. Invited review: The importance of colostrum in the newborn dairy calf. J. Dairy Sci. 2022, 105, 2733–2749. [Google Scholar] [CrossRef]
- Morrill, K.M.; Conrad, E.; Lago, A.; Campbell, J.; Quigley, J.; Tyler, H. Nationwide evaluation of quality and composition of colostrum on dairy farms in the United States. J. Dairy Sci. 2012, 95, 3997–4005. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Puppel, K.; Gołębiewski, M.; Grodkowski, G.; Slósarz, J.; Kunowska-Slósarz, M.; Solarczyk, P.; Łukasiewicz, M.; Balcerak, M.; Przysucha, T. Composition and Factors Affecting Quality of Bovine Colostrum: A Review. Animals 2019, 9, 1070. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Renaud, D.L.; Steele, M.A.; Genore, R.; Roche, S.M.; Winder, C.B. Passive immunity and colostrum management practices on Ontario dairy farms and auction facilities: A cross-sectional study. J. Dairy Sci. 2020, 103, 8369–8377. [Google Scholar] [CrossRef] [PubMed]
- Denholm, K. A review of bovine colostrum preservation techniques. J. Dairy Res. 2022, 89, 345–354. [Google Scholar] [CrossRef]
- Bartkiene, E.; Bartkevics, V.; Ikkere, L.E.; Pugajeva, I.; Zavistanaviciute, P.; Lele, V.; Ruzauskas, M.; Bernatoniene, J.; Jakstas, V.; Klupsaite, D.; et al. The effects of ultrasonication, fermentation with Lactobacillus sp., and dehydration on the chemical composition and microbial contamination of bovine colostrum. J. Dairy Sci. 2018, 101, 6787–6798. [Google Scholar] [CrossRef] [PubMed]
- Hasegawa, M.; Iwabuchi, E.; Yamamoto, S.; Esaki, H.; Kobayashi, K.; Ito, M.; Hirai, K. Prevalence and characteristics of Listeria monocytogenes in bovine colostrum in Japan. J. Food Prot. 2013, 76, 248–255. [Google Scholar] [CrossRef]
- Cunha, S.; Soares, R.; Maia, M.; Igrejas, G.; Silva, F.; Miranda, C.; Poeta, P. Presence of antibiotic-resistant Enterococcus faecalis in colostrum supplied to calves? In Proceedings of the 1st International Electronic Conference on Antibiotics—The Equal Power of Antibiotics and Antimicrobial Resistance, Online, 8–17 May 2021; MDPI: Basel, Switzerland. [Google Scholar]
- EFSA Panel on Biological Hazards (BIOHAZ); Ricci, A.; Allende, A.; Bolton, D.; Chemaly, M.; Davies, R.; Fernández Escámez, P.S.; Girones, R.; Koutsoumanis, K.; Lindqvist, R.; et al. Risk for the development of Antimicrobial Resistance (AMR) due to feeding of calves with milk containing residues of antibiotics. EFSA J. 2017, 15, e04665. [Google Scholar]
- Ulfman, L.H.; Leusen, J.H.W.; Savelkoul, H.F.J.; Warner, J.O.; Van Neerven, R.J. Effects of bovine immunoglobulins on immune function, allergy, and infection. Front. Nutr. 2018, 5, 52. [Google Scholar] [CrossRef] [Green Version]
- Borad, S.G.; Singh, A.K. Immunoglobulins. In Encyclopedia of Dairy Sciences, 3rd ed.; McSweeney, P.L.H., McNamara, J.P., Eds.; Academic Press: Oxford, UK, 2022; pp. 894–900. [Google Scholar]
- Rathe, M.; Müller, K.; Sangild, P.T.; Husby, S. Clinical applications of bovine colostrum therapy: A systematic review. Nutr. Rev. 2014, 72, 237–254. [Google Scholar] [CrossRef]
- Quigley, J. Passive immunity in newborn calves. Adv. Dairy Technol. 2002, 14, 273–292. [Google Scholar]
- Arfuso, F.; Minuti, A.; Liotta, L.; Giannetto, C.; Trevisi, E.; Piccione, G.; Lopreiato, V. Stress and inflammatory response of cows and their calves during peripartum and early neonatal period. Theriogenology 2023, 196, 157–166. [Google Scholar] [CrossRef]
- Sangild, P.T.; Vonderohe, C.; Melendez Hebib, V.; Burrin, D.G. Potential Benefits of Bovine Colostrum in Pediatric Nutrition and Health. Nutrients 2021, 13, 2551. [Google Scholar] [CrossRef]
- Afzal, I.; Khan, A.A.; Khaliq, T.; Hamadani, H.; Shafi, M.; Raja, T.A. Effect of bovine colostrum supplemented diets on performance of broiler chicken. Indian J. Poult. Sci. 2017, 52, 157–160. [Google Scholar] [CrossRef]
- Giffard, C.J.; Seino, M.M.; Markwell, P.J.; Bektash, R.M. Benefits of bovine colostrum on fecal quality in recently weaned puppies. J. Nutr. 2004, 134, 2126S–2127S. [Google Scholar] [CrossRef] [Green Version]
- Gore, A.M.; Satyaraj, E.; Labuda, J.; Engler, R.; Sun, P.; Kerr, W.; Conboy-Schmidt, L. Supplementation of diets with bovine colostrum influences immune and gut function in kittens. Front. Vet. Sci. 2021, 8, 675712. [Google Scholar] [CrossRef] [PubMed]
- Moretti, D.B.; Nordi, W.M.; Machado-Neto, R. Redox balance and tissue development of juvenile Piaractus mesopotamicus subjected to high stocking density and fed dry diets containing nutraceutical food. Lat. Am. J. Aquat. Res. 2019, 47, 423–432. [Google Scholar] [CrossRef]
- Arslan, A.; Kaplan, M.; Duman, H.; Bayraktar, A.; Ertürk, M.; Henrick, B.M.; Frese, S.A.; Karav, S. Bovine Colostrum and Its Potential for Human Health and Nutrition. Front. Nutr. 2021, 8, 651721. [Google Scholar] [CrossRef]
- Ghosh, S.; Iacucci, M. Diverse Immune Effects of Bovine Colostrum and Benefits in Human Health and Disease. Nutrients 2021, 13, 3798. [Google Scholar] [CrossRef] [PubMed]
- Ismail, R.I.H.; Awad, H.A.; Imam, S.S.; Gad, G.I.; Aboushady, N.M.; Abdou, R.M.; Eissa, D.S.; Azzam, N.T.; Barakat, M.M.; Yassin, M.M.; et al. Gut priming with bovine colostrum and T regulatory cells in preterm neonates: A randomized controlled trial. Pediatr. Res. 2021, 90, 650–656. [Google Scholar] [CrossRef] [PubMed]
- Jones, A.W.; March, D.S.; Thatcher, R.; Diment, B.; Walsh, N.P.; Davison, G. The effects of bovine colostrum supplementation on in vivo immunity following prolonged exercise: A randomised controlled trial. Eur. J. Nutr. 2019, 58, 335–344. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- March, D.S.; Marchbank, T.; Playford, R.J.; Jones, A.W.; Thatcher, R.; Davison, G. Intestinal fatty acid-binding protein and gut permeability responses to exercise. Eur. J. Appl. Physiol. 2017, 117, 931–941. [Google Scholar] [CrossRef] [Green Version]
- Tanideh, N.; Abdordideh, E.; Yousefabad, S.L.A.; Daneshi, S.; Hosseinabadi, O.K.; Samani, S.M. Evaluation of the healing effect of honey and colostrum in treatment of cutaneous wound in rat. Comp. Clin. Pathol. 2017, 26, 71–77. [Google Scholar] [CrossRef]
- Fecteau, G.; Baillargeon, P.; Higgins, R.; Paré, J.; Fortin, M. Bacterial contamination of colostrum fed to newborn calves in Québec dairy herds. Can. Vet. J. 2002, 43, 523–527. [Google Scholar]
- Baltrukova, S.; Zagorska, J.; Eihvalde, I. Preliminary study of bovine colostrum quality in Latvia. Res. Rural Dev. 2019, 1, 234–240. [Google Scholar]
- Poulsen, K.P.; Foley, A.L.; Collins, M.T.; McGuirk, S.M. Comparison of passive transfer of immunity in neonatal dairy calves fed colostrum or bovine serum-based colostrum replacement and colostrum supplement products. J. Am. Vet. Med. Assoc. 2010, 237, 949–954. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Alegbeleye, O.O.; Guimarães, J.T.; Cruz, A.G.; Sant’Ana, A.S. Hazards of a ‘Healthy’ Trend? An Appraisal of the Risks of Raw Milk Consumption and the Potential of Novel Treatment Technologies to Serve as Alternatives to Pasteurization. Trends Food Sci. Technol. 2018, 82, 148–166. [Google Scholar] [CrossRef]
- Šlosárková, S.; Pechová, A.; Staněk, S.; Fleischer, P.; Zouharová, M.; Nejedlá, E. Microbial contamination of harvested colostrum on Czech dairy farms. J. Dairy Sci. 2021, 104, 11047–11058. [Google Scholar] [CrossRef] [PubMed]
- Elizondo-Salazar, J.A.; Heinrichs, A.J. Review: Heat treating bovine colostrum. Prof. Anim. Sci. 2008, 24, 530–538. [Google Scholar] [CrossRef]
- Lima, S.F.; Teixeira, A.G.V.; Lima, F.S.; Ganda, E.K.; Higgins, C.H.; Oikonomou, G.; Bicalho, R.C. The bovine colostrum microbiome and its association with clinical mastitis. J. Dairy Sci. 2017, 100, 3031–3042. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cummins, C.; Berry, D.P.; Murphy, J.P.; Lorenz, I.; Kennedy, E. The effect of colostrum storage conditions on dairy heifer calf serum immunoglobulin G concentration and preweaning health and growth rate. J. Dairy Sci. 2017, 100, 525–535. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Abuelo, A.; Havrlant, P.; Wood, N.; Hernandez-Jover, M. An investigation of dairy calf management practices, colostrum quality, failure of transfer of passive immunity, and occurrence of enteropathogens among Australian dairy farms. J. Dairy Sci. 2019, 102, 8352–8366. [Google Scholar] [CrossRef]
- Godden, S. Colostrum management for dairy calves. Vet. Clin. N. Am. Food Anim. Pract. 2008, 24, 19–39. [Google Scholar] [CrossRef]
- Brunton, L.A.; Duncan, D.; Coldham, N.G.; Snow, L.C.; Jones, J.R. A survey of antimicrobial usage on dairy farms and waste milk feeding practices in England and Wales. Vet. Rec. 2012, 171, 296. [Google Scholar] [CrossRef]
- Gonggrijp, M.; Scherpenzeel, C.; Kappert, C.; Heuvelink, A.; Holtstege, M.; Nijenhuis, E.; Tijs, S.; Keurentjes, J.; Lam, T.; Velthuis, A. Resistentieontwikkeling bij Jonge Kalveren; Report Research Number OND1358162; GD Animal Health: Deventer, The Netherlands, 2015. (In Dutch) [Google Scholar]
- Aust, V.; Knappstein, K.; Kunz, H.J.; Kaspar, H.; Wallmann, J.; Kaske, M. Feeding untreated and pasteurized waste milk and bulk milk to calves: Effects on calf performance, health status and antibiotic resistance of faecal bacteria. J. Anim. Physiol. Anim. Nutr. 2013, 97, 1091–1103. [Google Scholar] [CrossRef] [PubMed]
- Langford, F.M.; Weary, D.M.; Fisher, L. Antibiotic resistance in gut bacteria from dairy calves: A dose response to the level of antibiotics fed in milk. J. Dairy Sci. 2003, 86, 3963–3966. [Google Scholar] [CrossRef] [Green Version]
- Pereira, R.V.; Siler, J.D.; Ng, J.C.; Davis, M.A.; Warnick, L.D. Effect of preweaned dairy calf housing system on antimicrobial resistance in commensal Escherichia coli. J. Dairy Sci. 2014, 97, 7633–7643. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Berge, A.C.; Moore, D.A.; Sischo, W.M. Field trial evaluating the influence of prophylactic and therapeutic antimicrobial administration on antimicrobial resistance of fecal Escherichia coli in dairy calves. Appl. Environ. Microbiol. 2006, 72, 3872–3878. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Duse, A.; Waller, K.P.; Emanuelson, U.; Unnerstad, H.E.; Persson, Y.; Bengtsson, B. Risk factors for antimicrobial resistance in fecal Escherichia coli from preweaned dairy calves. J. Dairy Sci. 2015, 98, 500–516. [Google Scholar] [CrossRef] [Green Version]
- He, Z.; Yang, S.; Ma, Y.; Zhang, S.; Cao, Z. Detection of CTX-M-15 Extended-Spectrum β-Lactamases Producing Escherichia coli Isolates from Colostrum and Faeces of Newborn Dairy Calves in China. Pathogens 2021, 10, 1162. [Google Scholar] [CrossRef]
- Oh, S.I.; Ha, S.; Roh, J.H.; Hur, T.Y.; Yoo, J.G. Dynamic Changes in Antimicrobial Resistance in Fecal Escherichia coli from Neonatal Dairy Calves: An Individual Follow-Up Study. Animals 2020, 10, 1776. [Google Scholar] [CrossRef]
- Jarrige, N.; Cazeau, G.; Bosquet, G.; Bastien, J.; Benoit, F.; Gay, E. Effects of antimicrobial exposure on the antimicrobial resistance of Escherichia coli in the digestive flora of dairy calves. Prev. Vet. Med. 2020, 185, 105177. [Google Scholar] [CrossRef] [PubMed]
- Afema, J.A.; Davis, M.A.; Sischo, W.M. Antimicrobial use policy change in pre-weaned dairy calves and its impact on antimicrobial resistance in commensal Escherichia coli: A cross sectional and ecological study. BMC Microbiol. 2019, 19, 217. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Uyama, T.; Renaud, D.L.; Morrison, E.I.; McClure, J.T.; LeBlanc, S.J.; Winder, C.B.; de Jong, E.; McCubbin, K.D.; Barkema, H.W.; Dufour, S.; et al. Associations of calf management practices with antimicrobial use in Canadian dairy calves. J. Dairy Sci. 2022, 105, 9084–9097. [Google Scholar] [CrossRef] [PubMed]
- Chee-Sanford, J.C.; Mackie, R.I.; Koike, S.; Krapac, I.G.; Lin, Y.F.; Yannarell, A.C.; Maxwell, S.; Aminov, R.I. Fate and transport of antibiotic residues and antibiotic resistance genes following land application of manure waste. J. Environ. Qual. 2009, 38, 1086–1108. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Firth, C.L.L.; Kremer, K.; Werner, T.; Käsbohrer, A. The Effects of Feeding Waste Milk Containing Antimicrobial Residues on Dairy Calf Health. Pathogens 2021, 10, 112. [Google Scholar] [CrossRef]
- Stewart, S.; Godden, S.; Bey, R.; Rapnicki, P.; Fetrow, J.; Farnsworth, R.; Scanlon, M.; Arnold, Y.; Clow, L.; Mueller, K.; et al. Preventing bacterial contamination and proliferation during the harvest, storage, and feeding of fresh bovine colostrum. J. Dairy Sci. 2005, 88, 2571–2578. [Google Scholar] [CrossRef] [Green Version]
- Renaud, D.L.; Kelton, D.F.; LeBlanc, S.J.; Haley, D.B.; Jalbert, A.B.; Duffield, T.F. Validation of commercial luminometry swabs for total bacteria and coliform counts in colostrum-feeding equipment. J. Dairy Sci. 2017, 100, 9459–9465. [Google Scholar] [CrossRef] [Green Version]
- Malik, M.I.; Rashid, M.A.; Raboisson, D. Heat treatment of colostrum at 60 °C decreases colostrum immunoglobulins but increases serum immunoglobulins and serum total protein: A meta-analysis. J. Dairy Sci. 2022, 105, 3453–3467. [Google Scholar] [CrossRef]
- Donahue, M.; Godden, S.M.; Bey, R.; Wells, S.; Oakes, J.M.; Sreevatsan, S.; Stabel, J.; Fetrow, J. Heat treatment of colostrum on commercial dairy farms decreases colostrum microbial counts while maintaining colostrum immunoglobulin G concentrations. J. Dairy Sci. 2012, 95, 2697–2702. [Google Scholar] [CrossRef] [Green Version]
Bioactive Component | Functions |
---|---|
Fat | Body temperature regulate and energy |
Lactose | Body temperature regulate and energy, stimulate of the nervous system |
Protein (Immunoglobulins) | Immune response |
Other protein (casein and albumin) | Muscle development and energy |
Nonspecific antimicrobial factors | Immune response |
Growth factors | Muscle development and energy |
Leucocyte populations | Immune response |
Hormones | Growth performance |
Vitamins | Immune response and antioxidant |
Nutrients | Muscle development and energy |
Cytokines (Interleukin 6) | Immune and anti-inflammatory response |
Enzymes (lysozyme, lactoferrin and lactoperoxidase) | Antimicrobial response |
Minerals | Growth performance |
Bacterial Pathogens | |
---|---|
Gram-Positive | Gram-Negative |
Staphylococcus aureus | Escherichia coli |
Streptococcus uberis | Salmonella Enteritidis |
Streptococcus parauberis | Campylobacter jejuni |
Streptococcus dysgalactiae | Mycoplasma bovis |
Enterococcus faecalis | |
Enterococcus feacium | |
Listeria innocua | |
Listeria monocytogenes | |
Mycobacterium avium subsp. paratuberculosis |
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Miranda, C.; Igrejas, G.; Poeta, P. Bovine Colostrum: Human and Animal Health Benefits or Route Transmission of Antibiotic Resistance—One Health Perspective. Antibiotics 2023, 12, 1156. https://doi.org/10.3390/antibiotics12071156
Miranda C, Igrejas G, Poeta P. Bovine Colostrum: Human and Animal Health Benefits or Route Transmission of Antibiotic Resistance—One Health Perspective. Antibiotics. 2023; 12(7):1156. https://doi.org/10.3390/antibiotics12071156
Chicago/Turabian StyleMiranda, Carla, Gilberto Igrejas, and Patrícia Poeta. 2023. "Bovine Colostrum: Human and Animal Health Benefits or Route Transmission of Antibiotic Resistance—One Health Perspective" Antibiotics 12, no. 7: 1156. https://doi.org/10.3390/antibiotics12071156
APA StyleMiranda, C., Igrejas, G., & Poeta, P. (2023). Bovine Colostrum: Human and Animal Health Benefits or Route Transmission of Antibiotic Resistance—One Health Perspective. Antibiotics, 12(7), 1156. https://doi.org/10.3390/antibiotics12071156