Antibiotics in poultry manure and their associated health issues: a systematic review

Abstract

Purpose

Antibiotics are growing environmental contaminants leading to public health concern. Antibiotics are commonly used as growth promoters and therapeutic agents in poultry feed that are not completely metabolized in the body tissues of chicken, get deposited in meat as parent compounds, and ultimately excreted via poultry droppings into the environment. These antibiotics in the soil result into the creation of antibiotic resistance in bacteria via activation of antibiotic resistance genes (ARGs). The development of ARGs and antibiotic-resistant bacteria (ARB) lead to huge physical and economic losses, as these bacteria cannot be treated with commonly used antibiotics. Moreover, these antibiotics after entering into food chains seriously affect the human immune system, growth, and metabolism of the body. Therefore, to reduce the future health risks of antibiotics, there is a dire need to understand the fate of poultry antibiotics and spread of ARGs in the soil environment.

Materials and methods

In this manuscript, we reviewed the existing literature about the antibiotics used in the poultry sector, soil contamination through application of poultry manures, and development of ARB in environment. An attempt has been done to present a better understanding of emerging contaminants (ARGs, ARB) in the soil environment and their associated human health effects.

Results and discussion

In this paper, we summarized the use of antibiotics in the poultry sector, persistence of antibiotics in animal body, and their release into environment. Transfer mechanism of antibiotics and their metabolites to the human body and their fatal effects have been investigated. Developments of ARB and ARGs in the soil due to excessive use of veterinary antibiotics have been highlighted.

Conclusions

Poultry antibiotics are causing human health risks by development of ARGs and ARB. Such antibiotic resistance cannot be treated with common antibiotics. Therefore, effective measures are needed to control this emerging problem by improving the efficiency of antibiotics, reducing the spread of resistance genes, and proper monitoring of antibiotics in poultry feed and manure. Manure composting and biochar application are the possible ways to reduce the risk and spread of ARGs in environment due to manure application in agriculture field. The pathways that allow antibiotic, ARGs, and ARB to move through the environment are not fully understood and there is a need for further research to make clear the reservoirs and routes of antibiotic-related contaminants in the ecosystem.

This is a preview of subscription content, access via your institution.

Fig.1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Ahmad M, Vithanage M, Kim K, Cho J-S, Lee YH, Joo YK, Lee SS, Ok YS (2014) Inhibitory effect of veterinary antibiotics on denitrification in groundwater: a microcosm approach. Sci World J 2014:1–7. https://doi.org/10.1155/2014/879831

    Article  Google Scholar 

  2. Ahmed MBM, Rajapaksha AU, Lim JE, Vu NT, Kim IS, Kang HM, Ok YS (2015) Distribution and accumulative pattern of tetracyclines and sulfonamides in edible vegetables of cucumber, tomato, and lettuce. J Agric Food Chem 63(2):398–405

    CAS  Google Scholar 

  3. Allaire SE, Del CJ, Juneau V (2006) Sorption kinetics of chlortetracycline and tylosin on sandy loam and heavy clay soils. J Environ Qual 35:969–972

    CAS  Google Scholar 

  4. Barnes KK, Kolpin DW, Furlong ET, Zaugg SD, Meyer MT, Barber LB (2008) A national reconnaissance of pharmaceuticals and other organic wastewater contaminants in the United States- (I) ground water. Sci Total Environ 402(2–3):192–200

    CAS  Google Scholar 

  5. Bartlett JG, Gilbert DN, Spellberg B (2013) Seven ways to preserve the miracle of antibiotics. Clin Infect Dis 56(10):1445–1450

    CAS  Google Scholar 

  6. Berendonk TU, Manaia CM, Merlin C, Fatta-Kassinos D, Cytryn E, Walsh F, Kreuzinger N (2015) Tackling antibiotic resistance: the environmental framework. Nat Rev Microbiol 13(5):310–317

    CAS  Google Scholar 

  7. Bhaskaran N, Quigley C, Paw C, Butala S, Schneider E, Pandiyan P (2018) Role of short chain fatty acids in controlling tregs and immunopathology during mucosal infection. Front Microbiol 9:1995

    Google Scholar 

  8. Boerlin P, White DB (2013) Antimicrobial resistance and its epidemiology chapter 3 in book antimicrobial therapy in veterinary medicine, fifth edition by Giguère S, Prescott JF. Dowling PM. https://doi.org/10.1002/9781118675014.ch3

    Google Scholar 

  9. Bolan NS, Adriano DC, Mahimairaja S (2004) Distribution and bioavailability of trace elements in livestock and poultry manure by-products. Crit Rev Environ Sci Technol 34:291–338

    CAS  Google Scholar 

  10. Bowman A, Mueller K, Smith, M (2000) Increased animal waste production from concentrated animal feeding operations: potential implications for public and environmental health. Occasional Paper Series, No, 2. Omaha, USA, Nebraska Centre for Rural Health Research

  11. Boxall ABA, Blackwell P, Cavallo R, Kay P, Tolls J (2002) The sorption and transport of a sulphonamide antibiotic in soil systems. Toxicol Lett 131:19–28

    CAS  Google Scholar 

  12. Camacho-Munoz D, Martin J, Santos JL, Aparicio I, Alonso E (2012) Effectiveness of conventional and low-cost wastewater treatments in the removal of pharmaceutically active compounds. Water Air Soil Pollut 223(5):2611–2621

    CAS  Google Scholar 

  13. Centers for Disease Control and Prevention (CDC) (2013) Antibiotic resistance threats in the United States

  14. Chee-Sanford JC, Mackie RI, Koike S, Krapac I, Maxwell S, Lin YF, Aminov RI (2009) Fate and transport of antibiotic residues and antibiotic resistance genetic determinants during manure storage, treatment, and land application. J Environ Qual 38:1086–1108

    CAS  Google Scholar 

  15. Chee-Sanford JC, Krapac IJ, Yannarell AC, Mackie RI (2012) Environmental impacts of antibiotic use in the animal production industry. Chapter 29:228–268

    Google Scholar 

  16. Chen Q, An X, Li H, Su J, Ma Y, Zhu YG (2016) Long-term field application of sewage sludge increases the abundance of antibiotic resistance genes in soil. Environ Int 92-93:1–10

    CAS  Google Scholar 

  17. Commission Regulation (EEC) No 37/2010 of December (2009) on pharmacologically active substances and their classification regarding maximum residue limits in food stuffs of animal origin. Official Journal of the European Union L15/1, 20/1/2010

  18. De Alwis H, Heller DN (2010) Multiclass, multi residue method for the detection of antibiotic residues in distillers grains by liquid chromatography and ion trap tandem mass spectrometry. J Chromatogr A 1217:3076–3084

    Google Scholar 

  19. Elmund GK, Morrison SM, Grant DW, Nevins MP (1971) Role of excreted chlortetracycline in modifying the decomposition process in feedlot waste. Bull Environ Contam Toxicol 6:129–132

    CAS  Google Scholar 

  20. Environmental Protection Agency (2013) Particulate and turbidity removal technologies. United States Environmental Protection Agency N P, 16 Jan 2013

  21. Erian I, Philips CJ (2017) Public understanding and attitudes towards meat chicken production and relations to consumption. Anim 7(3):20

    Google Scholar 

  22. Fang H, Wang HF, Cai L, Yu YL (2015) Prevalence of antibiotic resistance genes and bacterial pathogens in long-term manured greenhouse soils as revealed by metagenomic survey. Environ Sci Technol 49:1095–1104

    CAS  Google Scholar 

  23. FAO/WHO Joint Expert Committee on Food Additives (JECFA) (2009) Toxicological evaluation of certain veterinary drug residues in food: Tilmicosin. WHO food additives series

  24. FDA, Center for Veterinary Medicine (2001) The human health impact of fluoroquinolone resistant campylobacter attributed to the consumption of chicken. Food and Drug Administration, Washington, DC

  25. Food and Drug Administration (FDA) (2012) The judicious use of medically important antimicrobial drugs in food-producing animals.Guidance #209, P.3

  26. Founou LL, Founou RC, Essack SY (2016) Antibiotic resistance in the food chain: a developing country-perspective. Front Microbiol 7:1881

    Google Scholar 

  27. Franklin AM, Aga DS, Cytryn E, Durso LM, McLain JE, Pruden A, Roberts MC, Rothrock MJ, Snow DD, Watson JE, Dungan RS (2016) Antibiotics in agro-ecosystems: introduction to the special section. J Environ Qual 45(2):377–393

    CAS  Google Scholar 

  28. Gilbert N (2012) Rules tighten on use of antibiotics on farms. Nature 481(7380):125

    CAS  Google Scholar 

  29. Gilchrist MJ, Greko C, Wallinga DB, Beran GW, Riley DG, Thorne PS (2007) The potential role of concentrated animal feeding operations in infectious disease epidemics and antibiotic resistance. Environ Health Perspect 115:313–316

    Google Scholar 

  30. Grenni P, Ancona V, Caracciolo AB (2018) Ecological effects of antibiotics on natural ecosystems: a review. Microchem J 136:25–39

    CAS  Google Scholar 

  31. Guan Y, Wang B, Gao Y, Liu W, Zhao X, Huang X, Yu J (2017) Occurrence and fate of antibiotics in the aqueous environment and their removal by constructed wetlands in China: A review. Pedosphere 27(1):42–51

    Google Scholar 

  32. Gupta G, Charles S (1999) Trace elements in soils fertilized with poultry litter. Poult Sci 78:1695–1698

    CAS  Google Scholar 

  33. Gupta SK, Le XC, Kachanosky G, Zuidhof MJ, Siddique T (2018) Transfer of arsenic from poultry feed to poultry litter: a mass balance study. Sci Total Environ 630:302–307

    CAS  Google Scholar 

  34. Hamscher G, Pawelzick HT, Hoper H, Nau H (2005) Different behavior of tetracyclines and sulfonamides in sandy soils after repeated fertilization with liquid manure. An international journal. Environ Toxicol Chem 24:861–868

    CAS  Google Scholar 

  35. Hass A, Gonzalez JM, Lima IM, Godwin HW, Halvorson JJ, Boyer DG (2012) Chicken manure biochar as liming and nutrient source for acid Appalachian soil. J Environ Qual 41(4):1096–1106

    CAS  Google Scholar 

  36. Hektoen H, Berge JA, Hormazabal V, Yndestad M (1995) Persistence of antibacterial agents in manure sediments. Aquaculture 133:175–184

    CAS  Google Scholar 

  37. Ho YB, Zakaria MP, Latif PF, Saari N (2013) Degradation of veterinary antibiotics and hormone during broiler manure composting. Bioresour Technol 131:476–484

    CAS  Google Scholar 

  38. Holzel CS, Müller C, Harms KS, Mikolajewski S, Schäfer S, Schwaiger K, Bauer J (2012) Heavy metals in liquid pig manure in light of bacterial antimicrobial resistance. Environ Res 113:21–27

    Google Scholar 

  39. Hu HW, Han XM, Shi XZ, Wang JT, Han LL, Chen D, He JZ (2016) Temporal changes of antibiotic-resistance genes and bacterial communities in two contrasting soils treated with cattle manure. FEMS Microbiol Ecol 92(2). https://doi.org/10.1093/femsec/fiv169

    Google Scholar 

  40. Huang X, Liu C, Li K, Liu F, Liao D, Liu L, Zhu G, Liao J (2013) Occurrence and distribution of veterinary antibiotics and tetracycline resistance genes in farmland soils around swine feedlots in Fujian Province, China. Environ Sci Pollut Res 20:9066–9074

    CAS  Google Scholar 

  41. Hughes P, Heritage J (2004) Antibiotic growth-promoters in food animals. In assessing quality and safety of animal feeds. Rome, Italy: FAO, pp 129–151

  42. Jiang JQ, Zhou Z, Sharma VK (2013) Occurrence, transportation, monitoring and treatment of emerging micro-pollutants in waste water — a review from global views. Microchem J 110:292–300

    CAS  Google Scholar 

  43. Jjemba PK, Lauren AW, Weicheng EW, Mark WL (2010) Regrowth of potential opportunistic pathogens and algae in reclaimed water distribution systems. Agric Ecosyst Environ 91:67–78

    Google Scholar 

  44. Khan S, Cao Q (2012) Human health risk due to consumption of vegetables contaminated with carcinogenic polycyclic aromatic hydrocarbons. J Soils Sediments 12:178–184

    Google Scholar 

  45. Kim KR, Owens G, Ok YS, Park WK, Lee DB, Kwon SI (2012) Decline in extractable antibiotics in manure-based composts during composting. Waste Manag 32(1):110–116

    CAS  Google Scholar 

  46. Kim JH, Kuppusamy S, Kim SY, Kim SC, Kim HT, Lee YB (2017) Occurrence of sulfonamide class of antibiotics resistance in Korean paddy soils under long-term fertilization practices. J Soils Sediments 17(6):1618–1625

    CAS  Google Scholar 

  47. Kumar K, Gupta SC, Baidoo SK, Chander Y, Rosen CJ (2005a) Antibiotic uptake by plants from soil fertilized with animal manure. J Environ Qual 34:2082–2085

    CAS  Google Scholar 

  48. Kumar K, Gupta SC, Chander Y, Singh AK (2005b) Antibiotic use in agriculture and its impact on the terrestrial environment. Adv Agron 87:1–54

    CAS  Google Scholar 

  49. Kummerer (2009) Antibiotics in the aquatic environment -a review–part II. Chemosphere 75:435–441

    Google Scholar 

  50. Lee YK, Menezes JS, Umesaki Y, Mazmanian SK (2011) Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proc Natl Acad Sci U S A 108(Suppl. 1):4615–4622

    CAS  Google Scholar 

  51. Li Y, Zhu GB, Ng WJ, Tan SK (2014) A review on removing pharmaceutical contaminants from wastewater by constructed wetlands: design, performance and mechanism. Sci Total Environ 468:908–932

    Google Scholar 

  52. Liu YY, Wang Y, Walsh TR, Yi LX, Zhang R, Spencer J, Doi Y, Tian G, Dong B, Huang X, Yu LF (2016) Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. Lancet Infect Dis 16(2):161–168

    Google Scholar 

  53. Luby E, Ibekwe AM, Zilles J, Pruden A (2016) Molecular methods for assessment of antibiotic resistance in agricultural ecosystems: prospects and challenges. J Environ Qual 45(2):441–453

    CAS  Google Scholar 

  54. Madikizela LM, Ncube S, Chimuka L (2018) Uptake of pharmaceuticals by plants grown under hydroponic conditions and natural occurring plant species: a review. Sci Total Environ 636:477–486

    CAS  Google Scholar 

  55. Marengo J, Kok R, Obrien K, Velagaleti R, Stamm J (1997) Aerobic biodegradation of 14C sarafloxacin hydro chloride in soil. Environ Toxicol Chem 16:462–471

    CAS  Google Scholar 

  56. Marti R, Scott A, Tien YC, Murray R, Sabourin L, Zhang Y, Topp E (2013) The impact of manure fertilization on the abundance of antibiotic-resistant bacteria and frequency of detection of antibiotic resistance genes in soil, and on vegetables at harvest. Appl Environ Microbiol AEM-01682

  57. Migliore L, Civitareale C, Brambilla SC, Casoria P, Gaudio L (1997) Effects of sulphadimethoxine on cosmopolitan weeds (Ameranthus retroflexus L., Plantago major L. and Rumex acetosella L.). Agric Ecosyst Environ 65:163–168

    CAS  Google Scholar 

  58. Mohammad J, Khan S, Shah MT, Islam-ud-din, Ahmed A (2015) Essential and non-essential metal concentrations in morel mushroom (Morchella esculenta) in Dir-Kohistan, Pakistan. Pak J Bot SI (47):133–138

  59. Moyane J, Jideani A, Aiyegoro O (2013) Antibiotics usage in food-producing animals in South Africa and impact on human: antibiotic resistance. Afr J Microbiol Res 7:2990–2997

    Google Scholar 

  60. Pan M, Chu LM (2017) Fate of antibiotics in soil and their uptake by edible crops. A review. Sci Total Environ 599:500–512

    Google Scholar 

  61. Parente CE, Azeredo A, Vollú RE, Zonta E, Azevedo-Silva CE, Brito EM, Malm O (2019) Fluoroquinolones in agricultural soils: multi-temporal variation and risks in Rio de Janeiro upland region. Chemosphere 219:409–417

    CAS  Google Scholar 

  62. Pedersen J, Yeager M, Suffet I (2003) Xenobiotic organic compounds in runoff from fields irrigated with treated wastewater. J Agric Food Chem 51:1360–1372

    CAS  Google Scholar 

  63. Peng W, Li X, Xiao S, Fan W (2018) Review of remediation technologies for sediments contaminated by heavy metals. J Soils Sediments 18(4):1701–1719

    CAS  Google Scholar 

  64. Robert C, Gillard N, Brasseur PY, Ralet N, Dubois M, Delahaut P (2015) Rapid multiresidue and multi-class screening for antibiotics and benzimidazoles in feed by ultra-high-performance liquid chromatography coupled to tandem mass spectrometry. Food Control 50:509–515

    CAS  Google Scholar 

  65. Ronquillo MG, Hernandez JCA (2017) Antibiotic and synthetic growth promoters in animal diets: review of impact and analytical methods. Food Control 72:255–267

    Google Scholar 

  66. Schmitt H, Haapakangas H, van Beelen P (2005) Effects of antibiotics on soil microorganisms: time and nutrients influence pollution- induced community tolerance. Int Soil Biol Biochem 37:1882–1892

    CAS  Google Scholar 

  67. Shukla SD, Budden KF, Neal R, Hansbro PM (2017) Microbiome effects on immunity, health and disease in the lung. Clin Trans Immunology 6(3):133

    Google Scholar 

  68. Skurnik D, Ruimy R, Ready D, Ruppe E, Bernede-Bauduin C, Djossou F, Guillemot D, Pier GB, Andremont A (2010) Is exposure to mercury a driving force for the carriage of antibiotic resistance genes. J Med Microbiol 59:804–807

    CAS  Google Scholar 

  69. Steinfeld H, Gerber P, Wassenaar TD, Castel V, De Haan C (2006) Livestock’s long shadow: environmental issues and options. Food & Agriculture Org

  70. Su JQ, Wei B, Xu CY, Qiao M, Zhu YG (2014) Functional metagenomic characterization of antibiotic resistance genes in agricultural soils from China. Environ Int 65:9–15

    CAS  Google Scholar 

  71. Su JQ, Wei B, Ou Yang WY, Huang FY, Zhao Y, Xu HJ, Zhu YG (2015) Antibiotic resistome and its association with bacterial communities during sewage sludge composting. Environ Sci Technol 49:7356–7363

    CAS  Google Scholar 

  72. Tang X, Lou C, Wang S, Lu Y, Liu M, Hashmi MZ, Liang X, Li Z, Liao Y, Qin W, Fan F, Xu J, Brookes PC (2015) Effects of long-term manure applications on the occurrence of antibiotics and antibiotic resistance genes (ARGs) in paddy soils: evidence from four field experiments in south of China. Soil Biol Biochem 90:179–187

    CAS  Google Scholar 

  73. Tasho RP, Cho JY (2016) Veterinary antibiotics in animal waste, its distribution in soil and uptake by plants: a review. Sci Total Environ 563:366–376

    Google Scholar 

  74. Uslu MO, Jasim S, Arvai A, Bewtra J, Biswas N (2013) A survey of occurrence and risk assessment of pharmaceutical substances in the Great Lakes Basin. Ozone Sci Eng 35:249–262

    CAS  Google Scholar 

  75. Van Boeckel TP, Brower C, Gilbert M, Grenfell BT, Levin SA, Robinsoni TP, Laxminarayan R (2015) Global trends in antimicrobial use in food animals. Proc Natl Acad Sci U S A 112(18):5649–5654

    Google Scholar 

  76. Van den Belt K, Wester PW, van der Ven L, Verheyen R, Witters H (2002) Effects of ethynylestradiol on the reproductive physiology in zebrafish (Daniorerio): time dependency and reversibility. Environ Toxicol Chem 21(4):767–775

    Google Scholar 

  77. Wang X, Yang G, Feng Y, Ren G, Han X (2012) Optimizing feeding composition and carbon–nitrogen ratios for improved methane yield during anaerobic co-digestion of dairy, chicken manure and wheat straw. Biomagn Res Technol 120:78–83

    CAS  Google Scholar 

  78. Wang F, Che R, Xu Z, Wang Y, Cui X (2019) Assessing soil extracellular DNA decomposition dynamics through plasmid amendment coupled with real-time PCR. J Soils Sediments 19(1):91–96

    CAS  Google Scholar 

  79. Wasteson Y, Skjerve E, Yazdankhah SP, Eckner KF, Kapperud G, Lassen JF, kjerdal T (2017) The link between antimicrobial resistance and the content of potentially toxic metals in soil and fertilizing products. Opinion of the panel on biological hazards of the Norwegian Scientific Committee for Food Safety. VKM Report

  80. WHO (2015) Draft global action plan on antimicrobial resistance WHA 68.7

  81. WHO (World Health Organization) (2004) First global report on antibiotic resistance and worldwide threats to public health. 30th April, 2004 Geneva

  82. WHO/FAO/OIE (2003) Joint FAO/OIE/WHO expert workshop on non-human antimicrobial usage and antimicrobial resistance: scientific assessment, Geneva, December 1-5, 2003

  83. Williams-Nguyen J, Sallach J, Bartlelt-Hunt S, Boxall ABA, Durso LM, McLain JE, Singer R, Snow DD, Zilles J (2016) Antibiotics and antibiotic resistance in agroecosystems: state of the science. J Environ Qual 45:394–406

    CAS  Google Scholar 

  84. World Health Organization (2006) WHO consultation to develop a strategy to estimate the global burden of foodborne diseases, pp 3

  85. Xie WY, Shen Q, Zhao FJ (2018) Antibiotics and antibiotic resistance from animal manures to soil: a review. Eur J Soil Sci 69(1):181–195

    Google Scholar 

  86. Yang Y, Fu J, Peng H, Hou L, Liu M, Zhou JL (2011) Occurrence and phase distribution of selected pharmaceuticals in the Yangtze estuary and its coastal zone. J Hazard Mater 190:588–596

    CAS  Google Scholar 

  87. Yeom JR, Yoon SU, Kim CJ (2017) Quantification of residual antibiotics in cow manure being spread over agriculture land and assessment of their behavioral effects on antibiotics resistance bacteria. Chemosphere 182:771–780

    CAS  Google Scholar 

  88. Zhang Y, Geißen SU, Gal C (2008) Carbamazepine and diclofenac: removal in wastewater treatment plants and occurrence in water bodies. Chemosphere 73:1151–1161

    CAS  Google Scholar 

  89. Zhang H, Liu P, Feng Y, Yang F (2013) Fate of antibiotics during wastewater treatment and antibiotic distribution in the effluent-receiving waters of the Yellow Sea, northern China. Mar Pollut Bull 73:282–290

    CAS  Google Scholar 

  90. Zhang D, Gersberg RM, Ng WJ, Tan SK (2014) Removal of pharmaceuticals and personal care products in aquatic plant-based systems: a review. Environ Pollut 184:620–639

    CAS  Google Scholar 

  91. Zhang YJ, Hu HW, Gou M, Wang JT, Chen D, He JZ (2017) Temporal succession of soil antibiotic resistance genes following application of swine, cattle and poultry manures spiked with or without antibiotics. Environ Pollut 231:1621–1632

    CAS  Google Scholar 

  92. Zhao L, Dong YH, Wang H (2010) Residues of veterinary antibiotics in manures from feedlot livestock in eight provinces of China. Sci Total Environ 408:1069–1075

    CAS  Google Scholar 

  93. Zhu YG, Johnson TA, Su JQ, Qiao M, Guo GX, Stedtfeld RD, Hashsham SA, Tiedje JM (2013) Diverse and abundant antibiotic resistance genes in Chinese swinefarms. Proc Natl Acad Sci 110:3435–3440

    CAS  Google Scholar 

  94. Zhu B, Chen Q, Chen S, Zhu YG (2017a) Does organically produced lettuce harbor higher abundance of antibiotic resistance genes than conventionally produced. Environ Int 98:152–159

    CAS  Google Scholar 

  95. Zhu YG, Gillings M, Simonet P, Stekel D, Banwart S, Penuelas J (2017b) Microbial mass movements. Science 357:1099–1100

    CAS  Google Scholar 

Download references

Funding

Financial support is provided by Planning and Development Department, Government of Khyber Pakhtunkhwa, through Sustainable Development Unit (SDU), for project on “Low cost and environmentally friendly remediation technology for antibiotics and toxic metals from manure and manure applied agriculture soil, Khyber Pakhtunkhwa” under the Development Project “Piloting Innovative Ideas to Address Key Issues of Khyber Pakhtunkhwa, the Higher Education Commission, Islamabad, Pakistan, and Institute of Urban Environment, Chinese Academy of Sciences, China.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Sardar Khan.

Additional information

SOILS, SEC 5•SOIL AND LANDSCAPE ECOLOGY•REVIEW ARTICLE

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Responsible editor: Jizheng He

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Muhammad, J., Khan, S., Su, J.Q. et al. Antibiotics in poultry manure and their associated health issues: a systematic review. J Soils Sediments 20, 486–497 (2020). https://doi.org/10.1007/s11368-019-02360-0

Download citation

Keywords

  • Antibiotic-resistant bacteria
  • Antibiotic resistance genes
  • Antibiotics
  • Health problems
  • Poultry manure