Investigation of doxycycline residues in bones after oral administration to broiler chickens

Gajda, Anna; Szymanek-Bany, Iwona; Nowacka-Kozak, Ewelina; Gbylik-Sikorska, Małgorzata

doi:10.2478/jvetres-2024-0030

Abstract

Introduction

Chicken bones, a by-product of the poultry industry, can directly or indirectly enter the food chain. Bone meal and bone products could be sources of many contaminants. Considering the wide range of uses made of bones in the culinary and food industries, this material needs to be safe and antibiotic residue–free. To determine if such is the case, the concentration of doxycycline in chicken bones was investigated, this antimicrobial being one of the most commonly used in poultry production.

Material and Methods

Ross 308 broilers were grouped into three experimental and one control group. Doxycycline was administered in drinking water at therapeutic and sub-therapeutic doses, as well as via spray treatment. The concentration of doxycycline in bones was determined post slaughter by ultra-high performance liquid chromatography–tandem mass spectrometry.

Results

Doxycycline was quantified at 135 μg/kg 22 days after the last day of antibiotic administration at therapeutic doses; 2,285 μg/kg after sub-therapeutic treatment for 27 days and 9.62 μg/kg 22 days after the end of spray application.

Conclusion

High concentrations and long persistence of doxycycline in bones were found in this study. Doxycycline can contaminate all bone-derived products in the food and fertiliser industries.

References

Abrial D., Calavas D., Jarrige N., Ducrot C.: Spatial heterogeneity of the risk of BSE in France following the ban of meat and bone meal in cattle feed. Prev Vet Med 2005, 67, 69–82, doi:10.1016/j.prevetmed.2004.10.004.
Open DOI Search in Google Scholar Back to article
Alao B.O., Falowo A.B., Chulayo A., Muchenje V.: The Potential of Animal By-Products in Food Systems: Production, Prospects and Challenges. Sustainability 2017, 9, 1089–1107, doi: 10.3390/su9071089.
Open DOI Search in Google Scholar Back to article
Bacanli M., Başaran N.: Importance of antibiotic residues in animal food. Food Chem Toxicol 2019, 125, 462–466, doi: 10.1016/j.fct.2019.01.033.
Open DOI Search in Google Scholar Back to article
Bichukale A.D., Koli J.M., Sonavane A.E., Vishwasrao V.V., Pujari K.H., Shingare P.E.: Functional Properties of Gelatin Extracted From Poultry Skin and Bone Waste. Int J Pure App Biosci 2018, 6, 87–101, doi: 10.18782/2320-7051.6768.
Open DOI Search in Google Scholar Back to article
Błądek T., Posyniak A., Jabłoński A., Gajda A.: Pharmacokinetics of tulathromycin in edible tissues of healthy and experimentally infected pigs with Actinobacillus pleuropneumoniae. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 2015, 32, 1823–1832, doi: 10.1080/19440049.2015.1078915.
Open DOI Search in Google Scholar Back to article
Carter L.J., Harris E., Williams M., Ryan J.J., Kookana R.S., Boxall A.B.A.: Fate and uptake of pharmaceuticals in soil-plant systems. J Agric Food Chem 2014, 62, 816–825, doi: 10.1021/jf404282y.
Open DOI Search in Google Scholar Back to article
Cascarosa E., Gea G., Arauzo J.: Thermochemical processing of meat and bone meal: a review. Renew Sustain Energ Rev 2012, 16, 942–957, doi: 10.1016/j.rser.2011.09.015.
Open DOI Search in Google Scholar Back to article
Cornejo J., Pokrant E., Araya D., Briceño C., Hidalgo H., Maddaleno A., Araya-Jordán C., San Martín B.: Residue depletion of oxytetracycline (OTC) and 4-epi-oxytetracycline (4-epi-OTC) in broiler chicken’s claws by liquid chromatography-tandem mass spectrometry (LC-MS/MS). Food Addit Contam Part A Chem Anal Control Expo Risk Assess 2017, 34, 494–500, doi: 10.1080/19440049.2016.1263876.
Open DOI Search in Google Scholar Back to article
Cornejo J., Pokrant E., Krogh M., Briceño C., Hidalgo H., Maddaleno A., Araya-Jordán C., San Martín B.S.: Determination of Oxytetracycline and 4-Epi-Oxytetracycline Residues in Feathers and Edible Tissues of Broiler Chickens Using Liquid Chromatography Coupled with Tandem Mass Spectrometry. J Food Prot 2017, 8, 619–625, doi: 10.4315/0362-028X.JFP-16-320.
Open DOI Search in Google Scholar Back to article
Coutand M., Cyr M., Deydier E., Guilet R., Clastres P.: Characteristics of industrial and laboratory meat and bone meal ashes and their potential applications. J Hazard Mat 2008, 150, 522–532, doi: 10.1016/j.jhazmat.2007.04.133.
Open DOI Search in Google Scholar Back to article
Cycoń M., Mrozik A., Piotrowska-Sefet Z.: Antibiotics in the Soil Environment – Degradation and Their Impact on Microbial Activity and Diversity. Front Microbiol 2019, 10, 338–383, doi: 10.3389/fmicb.2019.00338.
Open DOI Search in Google Scholar Back to article
Duan M., Li H., Gu J., Tuo X., Sun W., Qian X., Wang X.: Effects of biochar on reducing the abundance of oxytetracycline, antibiotic resistance genes, and human pathogenic bacteria in soil and lettuce. Environ Pollut 2017, 224, 787–795, doi: 10.1016/j.envpol.2017.01.021.
Open DOI Search in Google Scholar Back to article
European Commission: Commission Implementing Regulation (EU) 2021/808 of 22 March 2021 on the performance of analytical methods for residues of pharmacologically active substances used in food-producing animals and on the interpretation of results as well as on the methods to be used for sampling and repealing Decisions 2002/657/EC and 98/179/EC. OJEU L 2021, 180, 64, 21/05/2021, 84–109.
Search in Google Scholar Back to article
European Commission Joint Research Centre, Wenzl T., Haedrich J., Schaechtele A., Robouch P., Stroka J.: EUR 28099 Guidance Document on the Estimation of LOD and LOQ for Measurements in the Field of Contaminants in Feed and Food. Publications Office of the European Union, Luxembourg, 2016, JRC102946, doi: 10.2787/8931.
Open DOI Search in Google Scholar Back to article
European Food Safety Authority: EN-1997 Report for 2019 on the results from the monitoring of veterinary medicinal product residues and other substances in live animals and animal products. EFSA support publ 2021, 18, doi: 10.2903/sp.efsa.2021.EN-1997.
Open DOI Search in Google Scholar Back to article
European Food Safety Authority, Brocca D., Salvatore S.: EN-7143 Report for 2020 on the results from the monitoring of veterinary medicinal product residues and other substances in live animals and animal products. EFSA support publ 2022, 19, doi: 10.2903/sp.efsa.2022.EN-7143.
Open DOI Search in Google Scholar Back to article
European Parliament and the Council of European Union: Regulation (EC) No. 1069/2009 of the European Parliament and of the Council of 21 October 2009 laying down health rules as regards animal by-products and derived products not intended for human consumption and repealing Regulation (EC) No. 1774/2002 (Animal by-products Regulation). OJEU L 2009, 300, 52, 14/11/2009, 1–33.
Search in Google Scholar Back to article
Ferreira A., Kunh S.S., Cremonez P.A., Dieter J., Teleken J.G., Sampaio S.C., Kunh P.D.: Brazilian poultry activity waste: destinations and energetic potential. Renew Sustain Energy Rev 2018, 81, 3081–3089, doi: 10.1016/j.rser.2017.08.078.
Open DOI Search in Google Scholar Back to article
Gajda A., Nowacka-Kozak E., Gbylik-Sikorska M., Posyniak A.: Feather analysis as a non-invasive alternative to tissue sampling for surveillance of doxycycline use on poultry farms. Poult Sci 2019, 98, 5971–5980, doi: 10.3382/ps/pez394.
Open DOI Search in Google Scholar Back to article
Gajda A., Szymanek-Bany I., Nowacka-Kozak E., Gbylik-Sikorska M.: Risk to Public Health Regarding Doxycycline Residues in Chicken Claws. J Agric Food Chem 2022, 70, 2495–2500, doi: 10.1021/acs.jafc.1c07480.
Open DOI Search in Google Scholar Back to article
Hussain C.M., Paulraj M.S., Nuzhat S.: Chapter 7 - Source reduction and waste minimization in food industry, In: Source Reduction and Waste Minimization. Elsevier, Maryland Heights, MO, USA, 2022, pp. 137–147, doi: 10.1016/B978-0-12-824320-6.00007-1.
Open DOI Search in Google Scholar Back to article
Jayalakshmi K., Paramasivam M., Sasikala M., Tamilam T.V., Sumithra A.: Review on antibiotic residues in animal products and its impact on environments and human health. J Entomol Zool Stud 2017, 5, 1446–1451.
Search in Google Scholar Back to article
Jayathilakan K., Sultana K., Radhakrishna K., Bawa A.S.: Utilization of byproducts and waste materials from meat, poultry and fish processing industries: a review. J Food Sci Technol 2012, 49, 278–293, doi: 10.1007/s13197-011-0290-7.
Open DOI Search in Google Scholar Back to article
Jeng A.S., Haraldsen T.K., Grønlund A., Pedersen P.A.: Meat and bone meal as nitrogen and phosphorus fertilizer to cereals and ryegrass. Nutr Cycl Agroecosystems 2006, 76, 183–191, doi: 10.1007/s10705-005-5170-y.
Open DOI Search in Google Scholar Back to article
Kühne M., Körner U.: Bound chlortetracycline residues in bones: release under acidic conditions. Food Chem 2001, 72, 41–44, doi: 10.1016/S0308-8146(00)00198-9.
Open DOI Search in Google Scholar Back to article
Kühne M., Wegmann S., Kobe A., Fries R.: Tetracycline residues in bones of slaughtered animals. Food Control 2000, 11, 175–180, doi: 10.1016/S0956-7135(99)00092-4.
Open DOI Search in Google Scholar Back to article
Mondini C., Cayuela M.L., Sinicco T., Sánchez-Monedero M.A., Bertolone E., Bardi L.: Soil application of meat and bone meal. Short-term effects on mineralisation dynamics and soil biochemical and microbiological properties. Soil Biol Biochem 2008, 40, 462–474, doi: 10.1016/j.soilbio.2007.09.010.
Open DOI Search in Google Scholar Back to article
Monro J.A., Leon R., Puri B.K.: The risk of lead contamination in bone broth diets. Med Hypotheses 2013, 80, 389–390, doi: 10.1016/j.mehy.2012.12.026.
Open DOI Search in Google Scholar Back to article
Nogalska A., Załuszniewska A.: The Effect of Meat and Bone Meal (MBM) on Crop Yields, Nitrogen Content and Uptake, and Soil Mineral Nitrogen Balance. Agronomy 2021, 11, 2307, doi: 10.3390/agronomy11112307.
Open DOI Search in Google Scholar Back to article
Odore R., De Marco M., Gasco L., Rotolo L., Meucci V., Palatucci A.T., Rubino V., Ruggiero G., Canello S., Guidetti G., Centenaro S., Quarantelli A., Terrazzano G., Schiavone A.: Cytotoxic effects of oxytetracycline residues in the bones of broiler chickens following therapeutic oral administration of a water formulation. Poult Sci 2015, 94, 1979–1985, doi: 10.3382/ps/pev141.
Open DOI Search in Google Scholar Back to article
Pan M., Chu L.M.: Leaching behavior of veterinary antibiotics in animal manure-applied soils. Sci Total Environ 2017, 579, 466–473, doi: 10.1016/j.scitotenv.2016.11.072.
Open DOI Search in Google Scholar Back to article
Pereira de Souza F.F., Cavalcante F.L., Castro-Silva I.I., Coelho da Silva A.L., Moreira de Souza Filho M.: Poultry by-products as source of collagen, nanokeratin and bioapatite for biomedical use. Rev Ciênc Agron 2021, 52, e20207565, doi: 10.5935/1806-6690.20210049.
Open DOI Search in Google Scholar Back to article
Pokrant E., Riquelme R., Maddaleno A., San Martín B., Cornejo J.: Residue Depletion of Florfenicol and Florfenicol Amine in Broiler Chicken Claws and a Comparison of Their Concentrations in Edible Tissues Using LC–MS/MS. Molecules 2018, 23, 2211, doi: 10.3390/molecules23092211.
Open DOI Search in Google Scholar Back to article
Rana M.S., Lee S.Y., Kang H.J., Hur S.J.: Reducing Veterinary Drug Residues in Animal Products: A Review. Food Sci Anim Resour 2019, 39, 687–703, doi: 10.5851/kosfa.2019.e65.
Open DOI Search in Google Scholar Back to article
Robles-Jimenez L.E., Aranda-Aguirre E., Castelan-Ortega O.A., Shettino-Bermudez B.S., Ortiz-Salinas R., Miranda M., Li X., Angeles-Hernandez J.C., Vargas-Bello-Pérez E., Gonzalez-Ronquillo M.: Worldwide Traceability of Antibiotic Residues from Livestock in Wastewater and Soil: A Systematic Review. Animals 2021, 12, 60, doi: 10.3390/ani12010060.
Open DOI Search in Google Scholar Back to article
Rusu A., Buta E.L.: The Development of Third-Generation Tetracycline Antibiotics and New Perspectives. Pharmaceutics 2021, 13, 2085, doi: 10.3390/pharmaceutics13122085.
Open DOI Search in Google Scholar Back to article
Saeid A., Labuda M., Chojnacka K., Górecki H.: Valorization of Bones to Liquid Phosphorus Fertilizer by Microbial Solubilization. Waste Biomass Valor 2014, 5, 265–272, doi: 10.1007/s12649-013-9238-7.
Open DOI Search in Google Scholar Back to article
Schwartz A.V.: Marrow fat and bone: review of clinical findings. Front Endocrinol 2015, 6, 40, doi: 10.3389/fendo.2015.00040.
Open DOI Search in Google Scholar Back to article
Shurson G.C., Dierenfeld E.S., Dou Z.: Rules are meant to be broken – Rethinking the regulations on the use of food waste as animal feed. Resour Conserv Recycl 2023, 199, 107273, doi: 10.1016/j.resconrec.2023.107273.
Open DOI Search in Google Scholar Back to article
Tajchman K., Ukalska-Jaruga A., Bogdaszewski M., Pecio M., Dziki-Michalska K.: Accumulation of Toxic Elements in Bone and Bone Marrow of Deer Living in Various Ecosystems. A Case Study of Farmed and Wild-Living Deer. Animals 2020, 10, 2151, doi: 10.3390/ani10112151.
Open DOI Search in Google Scholar Back to article
Toldrá F., Reig M., Mora L.: Management of meat by- and co-products for an improved meat processing sustainability. Meat Sci 2021, 181, 108608, doi: 10.1016/j.meatsci.2021.108608.
Open DOI Search in Google Scholar Back to article