Effect of Changes in Veterinary Feed Directive Regulations on Violative Antibiotic Residues in the Tissue of Food Animals from the Inspector-Generated Sampling in the United States
Abstract
:1. Introduction
2. Materials and Methods
2.1. Data Source
2.2. Data Preparation and Variables
2.3. Statistical Analyses
3. Results
3.1. Univariable Logistic Regression Results
3.2. Multivariable Logistic Regression Results
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Landers, T.F.; Cohen, B.; Wittum, T.E.; Larson, E.L. A Review of Antibiotic Use in Food Animals: Perspective, Policy, and Potential. Public Health Rep. 2012, 127, 4–22. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- McEwen, S.A.; Fedorka-Cray, P.J. Antimicrobial Use and Resistance in Animals. Clin. Infect. Dis. 2002, 34, S93–S106. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Swartz, M.N. Human Health Risks with the Subtherapeutic Use of Penicillin or Tetracyclines in Animal Feed; The National Academies Press: Washington, DC, USA, 1989. [Google Scholar] [CrossRef]
- Manyi-Loh, C.; Mamphweli, S.; Meyer, E.; Okoh, A. Antibiotic Use in Agriculture and Its Consequential Resistance in Environmental Sources: Potential Public Health Implications. Molecules 2018, 23, 795. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gibbons, S.N.; Kaneene, J.B.; Lloyd, J.W. Patterns of chemical residues detected in US beef carcasses between 1991 and 1993. J. Am. Vet. Med. Assoc. 1996, 209, 589–593. [Google Scholar] [PubMed]
- FDA, U. Guidance for Industry# 213, New Animal Drugs and New Animal Drug Combination Products Administered in or on Medicated Feed or Drinking Water of Food-Producing Animals: Recommendations for Drug Sponsors for Voluntarily Aligning Product Use Conditions with GFI# 209; Center for Veterinary Medicine: Rockville, MD, USA, 2013. Available online: https://www.fda.gov/media/83488/download (accessed on 28 May 2022).
- Raut, R.; Mandal, R.K.; Kaphle, K.; Pant, D.; Nepali, S.; Shrestha, A. Assessment of antibiotic residues in the marketed meat of Kailali and Kavre of Nepal. Int. J. Appl. Sci. Biotechnol. 2017, 5, 386–389. [Google Scholar] [CrossRef] [Green Version]
- Ekakoro, J.E.; Caldwell, M.; Strand, E.B.; Okafor, C.C. Perceptions of Tennessee cattle producers regarding the Veterinary Feed Directive. PLoS ONE 2019, 14, e0217773. [Google Scholar] [CrossRef]
- Wierup, M. The Swedish Experience of the 1986 Year Ban of Antimicrobial Growth Promoters, with Special Reference to Animal Health, Disease Prevention, Productivity, and Usage of Antimicrobials. Microb. Drug Resist. 2001, 7, 183–190. [Google Scholar] [CrossRef] [Green Version]
- A McEwen, S.; Angulo, F.J.; Collignon, P.J.; Conly, J.M. Unintended consequences associated with national-level restrictions on antimicrobial use in food-producing animals. Lancet Planet. Health 2018, 2, e279–e282. [Google Scholar] [CrossRef] [Green Version]
- Lauderdale, T.L.; Shiau, Y.R.; Wang, H.Y.; Lai, J.F.; Huang, I.W.; Chen, P.C.; Chen, H.Y.; Lai, S.S.; Liu, Y.F.; Ho, M. Effect of banning vancomycin ana-logue avoparcin on vancomycin-resistant enterococci in chicken farms in Taiwan. Environ. Microbiol. 2007, 9, 819–823. [Google Scholar] [CrossRef] [PubMed]
- National Residue Program. Available online: https://www.fsis.usda.gov/node/1982 (accessed on 28 May 2022).
- Takele, B.; Berihun, T. Rational veterinary drug use: Its significance in public health. J. Vet. Med. Anim. Health 2014, 6, 302–308. [Google Scholar]
- Lee, M.; Lee, H.; Ryu, P. Public health risks: Chemical and antibiotic residues-review. Asian-Australas. J. Anim. Sci. 2001, 14, 402–413. [Google Scholar] [CrossRef]
- Samanidou, V.; Nisyriou, S. Multi-residue methods for confirmatory determination of antibiotics in milk. J. Sep. Sci. 2008, 31, 2068–2090. [Google Scholar] [CrossRef] [PubMed]
- Chen, R.-A.; Wu, W.-K.; Panyod, S.; Liu, P.-Y.; Chuang, H.-L.; Chen, Y.-H.; Lyu, Q.; Hsu, H.-C.; Lin, T.-L.; Shen, T.-C.D.; et al. Dietary Exposure to Antibiotic Residues Facilitates Metabolic Disorder by Altering the Gut Microbiota and Bile Acid Composition. Msystems 2022, 7, e00172-22. [Google Scholar] [CrossRef] [PubMed]
- Riley, L.W.; Raphael, E.; Faerstein, E. Obesity in the United States–dysbiosis from exposure to low-dose antibiotics? Front. Public Health 2013, 1, 69. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Commission Regulation (EU) No 37/2010 of 22 December 2009. Available online: https://health.ec.europa.eu/system/files/2016-11/reg_2010_37_en_0.pdf (accessed on 28 May 2022).
- Hosmer, D.W., Jr.; Lemeshow, S.; Sturdivant, R.X. Applied Logistic Regression; John Wiley & Sons: Hoboken, NJ, USA, 2013; Volume 398. [Google Scholar]
- Dohoo, I.R.; Martin, W.; Stryhn, H.E. Veterinary Epidemiologic Research; VER Inc.: Charlottetown, PE, Canada, 2003. [Google Scholar]
- Thrift, T.A.; Hersom, M.J.; Irsik, M. Florida Cow-Calf and Stocker Beef Safety and Quality Assurance Handbook: Beef Withdrawal Time Chart. EDIS. 2006. Available online: https://edis.ifas.ufl.edu/pdf%5CAN%5CAN17500.pdf (accessed on 28 May 2022).
- Payne, M.A.; Craigmill, A.; Riviere, J.E.; Webb, A.I. Extralabel use of penicillin in food animals. J. Am. Vet. Med. Assoc. 2006, 229, 1401–1403. [Google Scholar] [CrossRef] [Green Version]
- KuKanich, B.; Gehring, R.; Webb, A.I.; Craigmill, A.L.; Riviere, J.E. Effect of formulation and route of administration on tissue residues and withdrawal times. J. Am. Vet. Med. Assoc. 2005, 227, 1574–1577. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- E Vaala, W.; Ehnen, S.J.; Divers, T.J. Acute renal failure associated with administration of excessive amounts of tetracycline in a cow. J. Am. Vet. Med. Assoc. 1987, 191, 1601–1603. [Google Scholar]
- Vivrette, S.; Cowgill, L.D.; Pascoe, J.; Suter, C.; Becker, T. Hemodialysis for treatment of oxytetracycline-induced acute renal failure in a neonatal foal. J. Am. Vet. Med. Assoc. 1993, 203, 105–107. [Google Scholar] [PubMed]
- Al-Amri, I.; Kadim, I.T.; AlKindi, A.; Hamaed, A.; Al-Magbali, R.; Khalaf, S.; Al-Hosni, K.; Mabood, F. Determination of residues of pesticides, anabolic steroids, antibiotics, and antibacterial compounds in meat products in Oman by liquid chromatography/mass spectrometry and enzyme-linked immuno-sorbent assay. Vet. World 2021, 14, 709. [Google Scholar] [CrossRef]
- Jalal, H.; Para, P.; Ganguly, S.; Gogai, M.; Bhat, M.; Praveen, P.; Bukhar, S. Chemical residues in meat and meat products: A review. World J. Pharm. Life Sci. 2015, 1, 106–122. [Google Scholar]
- Beyene, T. Veterinary Drug Residues in Food-animal Products: Its Risk Factors and Potential Effects on Public Health. J. Vet. Sci. Technol. 2016, 7, 1. [Google Scholar] [CrossRef]
- Paturkar, A.; Waskar, V.; Mokal, K.; Zende, R. Antimicrobial drug residues in meat and their public health significance—A review. Indian J. Anim. Sci. 2005, 75, 1103–1111. [Google Scholar]
- Martin-jimenez, T.; Arthur, D.; Craigmill, L.; Riviere, P.J.E.; Pharmacokinetlc, P.N. FARAD Digest Extralabel Use of Oxytetracycline. J. Am. Vet. Med. Assoc. 1997, 211, 42–44. [Google Scholar]
- Kebirungi, P.; Nyombi, A.; Omara, T.; Adaku, C.; Ntambi, E. Oxytetracycline residues in bovine muscles, liver and kidney tissues from selected slaugh-ter facilities in South Western Uganda. Bull. Natl. Res. Cent. 2022, 46, 17. [Google Scholar] [CrossRef]
- Abasi, M.M.; Rashidi, M.R.; Javadi, A.; Amirkhiz, M.B.; Mirmahdavi, S.; Zabihi, M. Levels of tetracycline residues in cattle meat, liver, and kidney from a slaughterhouse in Tabriz, Iran. Turk. J. Vet. Anim. Sci. 2009, 33, 345–349. [Google Scholar] [CrossRef]
- El-Ghareeb, W.; Mulla, Z.S.; Meligy, A.; Darwish, W.; Edris, A. Antibiotic residue levels in camel, cattle and sheep tissues using LC-MS/MS method. JAPS J. Anim. Plant Sci. 2019, 29, 943–952. [Google Scholar]
- Zhang, Y.; Lu, J.; Yan, Y.; Liu, J.; Wang, M. Antibiotic residues in cattle and sheep meat and human exposure assessment in southern Xinjiang, China. Food Sci. Nutr. 2021, 9, 6152–6161. [Google Scholar] [CrossRef]
- Ruegg, P. Antimicrobial Residues and Resistance: Understanding and Managing Drug Usage on Dairy Farms; University of Winsconsin, Dept. of Dairy Scinece: Madison, WI, USA, 2013. [Google Scholar]
- Landfried, L.K.; Pithua, P.; Emo, B.; Lewis, R.; Jacoby, J.A.; King, C.; Baskin, C.R. How Under-testing of ethnic meat might contribute to antibiotic environmental pollution and antibiotic resistance: Tetracycline and aminoglycoside residues in domestic goats slaughtered in Missouri. J. Environ. Health 2017, 80, 20–25. [Google Scholar]
- Martin, K.L.; Clapham, M.O.; Davis, J.L.; Baynes, R.E.; Lin, Z.; Vickroy, T.W.; Riviere, J.E.; Tell, L.A. Extralabel drug use in small ruminants. J. Am. Vet. Med. Assoc. 2018, 253, 1001–1009. [Google Scholar] [CrossRef] [Green Version]
- K. Landfried, L.; K. Barnidge, E.; Pithua, P.; D. Lewis, R.; A. Jacoby, J.; C. King, C.; R. Baskin, C. Antibiotic use on goat farms: An investigation of knowledge, attitudes, and behaviors of Missouri goat farmers. Animals 2018, 8, 198. [Google Scholar] [CrossRef] [Green Version]
- Avery, B.P.; Rajić, A.; McFall, M.; Reid-Smith, R.J.; Deckert, A.E.; Irwin, R.J.; McEwen, S.A. Antimicrobial use in the Alberta sheep industry. Can. J. Vet. Res. 2008, 72, 137. [Google Scholar] [PubMed]
Predictor | Categories | Violation N (%) | Non-Violation N (%) | OR | 95% CI | p-Value |
---|---|---|---|---|---|---|
VFD rule change | 0.116 | |||||
Before VFD rule change (2014–2016) | 460 (72) | 182 (28) | Referent | |||
After VFD rule change (2017–2019) | 452 (68) | 216 (32) | 0.82 | 0.65, 1.04 | 0.117 | |
Animal production class | 0.501 | |||||
Bob veal | 58 (65) | 31 (35) | 0.91 | 0.57, 1.45 | 0.704 | |
Beef cow | 74 (73) | 27 (27) | 1.33 | 0.83, 2.14 | 0.225 | |
Dairy cow | 430 (67) | 210 (33) | Referent | |||
Bull | 117 (71) | 47 (29) | 1.21 | 0.83, 1.77 | 0.309 | |
Heifer | 131 (64) | 75 (36) | 0.85 | 0.61, 1.18 | 0.343 | |
Steer | 17 (74) | 6 (26) | 1.38 | 0.53, 3.56 | 0.501 | |
Goat | 2 (50) | 2 (50) | 0.48 | 0.06, 3.49 | 0.475 | |
Sheep | 4 (100) | 0 (0) | 1 | NA | NA | |
Swine | 36 (100) | 0 (0) | 1 | NA | NA | |
Turkey | 43 (100) | 0 (0) | 1 | NA | NA | |
Type of tissue sampled | <0.001 | |||||
Muscle | 34 (32) | 73 (68) | Referent | |||
Kidney | 878 (73) | 325 (27) | 5.8 | 3.78, 8.88 | <0.001 |
Predictor | Categories | Violation N (%) | Non-Violation N (%) | OR | 95% CI | p-Value |
---|---|---|---|---|---|---|
VFD rule change | 0.244 | |||||
Before VFD rule change (2014–2016) | 40 (8) | 465 (92) | Referent | |||
After VFD rule change (2017–2019) | 48 (10) | 430 (90) | 1.29 | 0.83, 2.01 | 0.245 | |
Animal production class | <0.001 | |||||
Bob veal | 13 (5) | 267 (95) | 0.45 | 0.22, 0.90 | 0.024 | |
Beef cow | 17 (10) | 150 (90) | 1.05 | 0.55, 2.00 | 0.863 | |
Dairy cow | 27 (10) | 252 (90) | Referent | |||
Bull | 10 (12) | 75 (88) | 1.24 | 0.57, 2.68 | 0.578 | |
Heifer | 7 (7) | 96 (93) | 0.68 | 0.28, 1.61 | 0.383 | |
Steer | 1 (5) | 19 (95) | 0.49 | 0.06, 3.81 | 0.497 | |
Goat | 8 (40) | 12 (60) | 6.22 | 2.33, 16.55 | <0.001 | |
Sheep | 5 (83) | 1 (17) | 46.66 | 5.25, 414.23 | 0.001 | |
Swine | 0 (0) | 12 (100) | 1 | NA | NA | |
Turkey | 0 (0) | 11 (100) | 1 | NA | NA | |
Type of tissue sampled | 0.002 | |||||
Kidney | 80 (8) | 882 (92) | Referent | |||
Others (muscle) | 8 (38) | 13 (62) | 6.78 | 2.73, 16.85 | <0.001 |
Predictor | Categories | Violation N (%) | Non-Violation N (%) | OR | 95% CI | p-Value |
---|---|---|---|---|---|---|
VFD rule change | 0.014 | |||||
Before VFD rule change (2014–2016) | 417 (87) | 64 (13) | Referent | |||
After VFD rule change (2017–2019) | 339 (81) | 81 (19) | 0.64 | 0.44, 0.91 | 0.015 | |
Animal production class | 0.082 | |||||
Bob veal | 188 (91) | 19 (9) | 2.01 | 1.16, 3.48 | 0.012 | |
Beef cow | 42 (88) | 6 (12) | 1.42 | 0.57, 3.50 | 0.441 | |
Dairy cow | 290 (83) | 59 (17) | Referent | |||
Bull | 70 (79) | 19 (21) | 0.74 | 0.42, 1.33 | 0.329 | |
Heifer | 100 (78) | 28 (22) | 0.72 | 0.43, 1.20 | 0.214 | |
Steer | 33 (83) | 7 (17) | 0.95 | 0.40, 2.27 | 0.924 | |
Goat | 7 (78) | 2 (22) | 0.71 | 0.14, 3.51 | 0.677 | |
Sheep | 1 (100) | 0 (0) | 1 | |||
Swine | 20 (83) | 4 (17) | 1.01 | 0.33, 3.08 | 0.976 | |
Turkey | 5 (83) | 1 (17) | 1.01 | 0.11, 8.86 | 0.988 | |
Type of tissue sampled | NA | |||||
Others (muscle/liver) | 642 (82) | 145 (18) | Referent | |||
Kidney | 114 (100) | 0 (0) | 1 | NA | NA |
Predictor | Categories | OR | 95% CI | p-Value |
---|---|---|---|---|
VFD rule change | 0.030 | |||
Before VFD rule change (2014–2016) | Referent | |||
After VFD rule change (2017–2019) | 0.76 | 0.59, 0.97 | 0.031 | |
Type of tissue sampled | <0.001 | |||
Others (muscle) | Referent | |||
Kidney | 6.01 | 3.91, 9.23 | <0.001 | |
VFD rule change*type of tissue sampled | 0.3009283 | 0.11, 0.80 | 0.017 |
Predictor | Categories | OR | 95% CI | p-Value |
---|---|---|---|---|
Before the VFD rule change (2014–2016), n = 642 | ||||
Type of tissue sampled | Others (muscle) | Referent | ||
Kidney | 3.95 | 2.32, 6.73 | <0.001 | |
After the VFD rule change (2017–2019), n = 668 | ||||
Type of tissue sampled | Others (muscle) | Referent | ||
Kidney | 13.14 | 5.75, 30.02 | <0.001 |
Predictor | Categories | OR | 95% CI | p-Value |
---|---|---|---|---|
VFD rule change | 0.092 | |||
Before VFD rule change (2014–2016) | Referent | |||
After VFD rule change (2017–2019) | 1.54 | 0.93, 2.55 | 0.092 | |
Animal production class | 0.001 | |||
Dairy cow | Referent | |||
Bob veal | 0.36 | 0.17, 0.76 | 0.007 | |
Beef-cow | 0.97 | 0.50, 1.88 | 0.942 | |
Bull | 0.98 | 0.43, 2.20 | 0.962 | |
Heifer | 0.56 | 0.22, 1.39 | 0.218 | |
Steer | 0.54 | 0.06, 4.24 | 0.562 | |
Goat | 6.11 | 2.27, 16.47 | <0.001 | |
Sheep | 40.24 | 4.45, 363.69 | 0.001 | |
Swine | 1 | |||
Turkey | 1 | |||
Type of tissue sampled | <0.001 | |||
Kidney | Referent | |||
Others (muscle) | 7.71 | 3.02, 19.70 | <0.001 |
Predictor | Categories | OR | 95% CI | p-Value |
---|---|---|---|---|
VFD rule change | 0.014 | |||
Before VFD rule change (2014–2016) | Referent | |||
After VFD rule change (2017–2019) | 0.64 | 0.44, 0.91 | 0.015 |
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Sarkar, S.; Okafor, C.C. Effect of Changes in Veterinary Feed Directive Regulations on Violative Antibiotic Residues in the Tissue of Food Animals from the Inspector-Generated Sampling in the United States. Microorganisms 2022, 10, 2031. https://doi.org/10.3390/microorganisms10102031
Sarkar S, Okafor CC. Effect of Changes in Veterinary Feed Directive Regulations on Violative Antibiotic Residues in the Tissue of Food Animals from the Inspector-Generated Sampling in the United States. Microorganisms. 2022; 10(10):2031. https://doi.org/10.3390/microorganisms10102031
Chicago/Turabian StyleSarkar, Shamim, and Chika C. Okafor. 2022. "Effect of Changes in Veterinary Feed Directive Regulations on Violative Antibiotic Residues in the Tissue of Food Animals from the Inspector-Generated Sampling in the United States" Microorganisms 10, no. 10: 2031. https://doi.org/10.3390/microorganisms10102031