ORIGINAL RESEARCH ARTICLE - Environmental contribution to antimicrobial resistance: A largely ignored global health issue

Adam Mustapha, Ibrahim A. Allamin, Haruna Y. Ismail, Ukpai A. Eze, Muhammad M. Ibrahim, Rabi Y. Bello, Aminatu U Faruq


Environmental contribution to the continued occurrence of antibiotic resistance has been largely unexplored. There has been much focus on clinical isolates for their resistant nature but non-clinical bacterial isolates in the environment have been considered as the chief contributing factors that facilitate the spread and dissemination of antibiotic-resistant bacteria (ABR) and antibiotic-resistant genes (ARGs). The natural environment acts as a reservoir for bacteria, providing them with a favourable condition for their emergence and breeding of resistance. One such environmental leverage is inter/intra-specie exchange of genes encoding resistance factors. It was argued that human activities aid immensely in the emergence of antibiotic resistance in the environment. The rationale for this review is to examine extensively the complex interplay of antibiotic resistance from the natural environmental perspective and factors that influence the occurrence and dissemination of such resistance. It also seeks to stress the biological factors that facilitate the emergence of resistance and link it to general biological processes. The review has been structured to capture the general threat posed by the circulation of antibiotic-resistant bacteria and their genes, as well as the influence of the environment in contributing to this global health threat. In addition, the review looked at the effective methods used to tackle the “silent pandemic”, by controlling the spread of resistance in the environment. Environmental stakeholders and policymakers are recommended to be included in tackling the development of antibiotic resistance.


Antimicrobial resistance, Natural environment, Non-clinical bacterial isolates, multidrug resistance genes, Wastewater

Full Text:



De Kraker ME, Stewardson AJ, Harbarth S (2016). Will 10 Million People Die a Year due to Antimicrobial Resistance by 2050? PLoS medicine. 13(11): 1-6. 2. Jasovský D, Littmann J, Zorzet A, Cars O (2016). Antimicrobial resistance-a threat to the world's sustainable development. Ups J. Med Sci. 121(3):159-164.

Al-Bahry SN, Mahmoud IY, Paulson JR, Al-Musharafi SK (2015). Antibiotic resistance in terrestrial and aquatic environment: A review. The Int Arabic J Antimicrobial Agents. 4(3):1-11.

Singer AC, Shaw H, Rhodes V, Hart A (2016). Review of Antimicrobial Resistance in the Environment and Its Relevance to Environmental Regulators. Front. Microbiol. 7(1728):1-22.

Ferri M, Ranucci E, Romagnoli P, Giaccone V (2017). Antimicrobial Resistance: A global Emerging Threat to Public Health System. Crit. Rev. Food Sci and Nutr. 57(13): 2857-2876.

The Proceedings of the Nigerian Academy of Science 76

Mubbunu L, Siyumbi S, Katango C, Mwambungu A (2014). Waste waters as reservoir of antibiotic Resistant microorganism: A case of Luanshya wastewaters ponds. Int. J Res Med Health Sciences. 4(9):15-20.

Aminov RI (2009). The role of antibiotics and antibiotic resistance in nature. Environ Microbiol. 11(12):2970-2988.

Waseem H, Williams MR, Stedtfeld RD, Hashsham SA (2017). Antimicrobial Resistance in the Environment. Water Env Res. 89(10): 921-941.

Klein EY, Van Boeckel TP, Martinez EM, Pant S, Gandra S, Levin SA, Goossens H, Laxminarayan R (2018). Global increase and geographic convergence in antibiotic consumption between 2000 and 2015. PNAS. 115(15):3463-3470.

World Bank. Nigeria Population Databank. 2016. (https://data.worldbank.org/country/NG) [Last accessed 24th Dec. 2018].

National Population Commission (NPC) (2017). Nigerian Demographics and Population Census.

O'Neill J. Review on Antimicrobial Resistance Antimicrobial Resistance: Tackling a crisis for the health and wealth of nations. London: 2014. [E-Book]. Available: Wellcomecollection.e-book.

Abat C, Rolain JM, Dubourg G,Fournier PE, Chaudet H, Raoult D (2017). Evaluating the clinical burden and mortality attributable to antibiotic resistance: the disparity of empirical data and simple model estimations. Clin Infect Dis. 65(1):58-63.

Jensen US, Muller A, Brandt CT, Frimodt-Moller N, Hammerum AM, Monnet DL (2010). Effect of generics on price and consumption of ciprofloxacin in primary healthcare: the relationship to increasing resistance. J Antimicrob Chemother. 65(6):1286-1291.

Butler MS, Cooper MA (2013). Antibiotics in the clinical pipeline in 2011. J Antibiotic. 64:413-425.

WHO Global action plans on antimicrobial resistance (2015). Available from World Health Organization, Geneva.

Pew charitable trusts (2015). Antibiotics currently in clinical development. Available from www.pewtrusts.org/en/multimedia/data-visualizations/2014/antibiotics-currently-in-clinical-development.

Sahoo KC, Tamhankar AJ, Johansson E, Lundborg CS (2012). Community perceptions of infectious diseases, antibiotic use and antibiotic resistance in context of environmental changes: a study in Odisha, India. Health Expect. 17:651-663.

He LY, Ying GG, Liu YS, Su HC, Chen J, Liu SS, Zhao JL (2016). Discharge of swine wastes risks water quality and food safety: antibiotics and antibiotic resistance genes from swine sources to the receiving environments. Environ. Int. 92:210-219.

Jia S, Zhang X, Miao Y, Zhao Y, Ye L, Li B, Zhang T (2017). Fate of antibiotic resistance genes and their association in livestock breeding, wastewater and its receiving river water. Water Res. 124:259-268.

The Proceedings of the Nigerian Academy of Science 77

Shakibaie MR, Jalilzadeh KA, Yamakanamardi SM (2009). Horizontal transfer of antibiotic resistance genes among gram negative bacteria in sewage and lake water and influence of some physico-chemical parameters of water on conjugation process. J Environ Biol. 30:45-49.

Aali R, Nikaeen M, Khanahmad H, Hassanzadeh A (2014). Monitoring and comparison of antibiotic resistant bacteria and their resistance genes in municipal and hospital wastewaters. Inter J Prev Med. 5(7):887-894.

Zhang QQ, Ying GG, Pan CG,Liu YS, Zhao JL (2015). Comprehensive evaluation of antibiotics emission and fate in the river basins of China: source analysis, multimedia modeling, and linkage to bacterial resistance. Environ Sci Tech. 49(11):6772-6782.

Wellington EMH, Boxall AB, Cross P, Feil EJ, Gaze WH, Hawkey PM, Johnson-Rollings AS, Jones DL, Lee NM, Otten E, et al (2013). The role of the natural environment in the emergence of antibiotic resistance in Gram-negative bacteria. Lancet Infect Dis. 13(2):155-165. 25. Rosi EJ, Bechtold HA, Snow D, Rojas M, Reisinger AJ, Kelly JJ (2018). Urban stream microbial communities show resistance to pharmaceutical exposure. Ecosphere. 109(9Pt 1):1-16.

Dantas G, Sommer MO, Oluwasegun RD, Church GA (2008). Bacteria subsisting on antibiotics. Science. 320(5872):100-103.

Dolliver H, Gupta S (2008). Antibiotic losses in leaching and surface runoff from manure-amended agricultural land. J Environ Qual. 37(3):1227-1237.

Larsson DG (2014). Antibiotics in the environment. Upsala J Med Sci. 119(2):108-112.

Capozzi C, Maurici M, Pana A (2019). Antimicrobial resistance: It is a global crisis, “a slow tsunami”. Ig Sanita Pubbl. 75(6): 429-450.

Akiba M, Sekizuka T, Yamashita A, Kuroda, M, Fujii Y, Murata M, Lee K, Joshua DI, Balakrishna K, Bairy I, et al (2016). Distribution and relationships of antimicrobial resistance determinants among extended-spectrum-cephalosporin resistant or carbapenem resistant Escherichia coli isolates from rivers and sewage treatment plants in India. Antimicrobial Agents Chemo. 60(5):2972-2980.

Goulas A, Livoreil B, Grall N, Benoit P, Couderc-Obert C, Dagot C, Paturau D, Petit F, Cedric L, Andremont A, et al (2018). What are the effective solutions to control the dissemination of antibiotic resistance in the environment? A systematic review protocol. Environ Evidence. 7(1):1-9.

McEwen SA, Collingnon PJ (2018). Antimicrobial resistance: a one Health Perspective. Microbial Spectrum. 6:1-2.

USDA (2014). Antimicrobial Resistance Action Plan. (Available from www.usda.gov) 34. Said KB, Al-Jarbou AN, Alrouji M, Al-harbi HO (2014). Surveillance of antimicrobial resistance among clinical isolates recovered from a tertiary care hospital in Al Qassim, Saudi Arabia. Interl J Health Sci. 8(1):3-12.

The Proceedings of the Nigerian Academy of Science 78

Dafopoulou K., Tsakris A, Pournaras S (2018). Changes in antimicrobial resistance of clinical isolates of Acinetobacterbaumannii group isolated in Greece, 2010-2015. J Med Microbiol. 67(4)496-498.

Sevillano E, Valderrey C, Canduela MJ, Umaran A, Calvo F, Gallengo L (2006). Resistance to antibiotics in clinical isolates of Pseudomonas aeruginosa. Pathologie Biol. 54(8-9): 493-497.

Paul R, Ray J, Sinha S, Mondal J (2017). Antibiotic resistance pattern of bacteria isolated from various clinical specimens: an eastern Indian study. Interl J Com Med Public Health. 4(4):1367-1371.

Rice LB (2009). The clinical consequences of antimicrobial resistance. Curr Opin Microbiol. 12(5):476-481.

World Health Organization. Global Action Plan on Antimicrobial Resistance. Available from http://www.wpro.who.int/entity/drug_resistance/resources/global_action_plan_eng. (Cited 2015 May 15).

Exner M, Bhattacharya S, Christiansen B, Gebel J, Goroncy-Bernes P, Hartemann P, Heeg P, Illschner C, Kramer A, Larson E, Merkens W, et al. (2017). Antibiotic resistance: What is so special about multidrug-resistant Gram-negative bacteria? GMS Hyg Infect Control. 12:1-24.

Aliyu S (2014). Treating infections caused by carbapenemase producing Gram-negative bacteria. Annals Nig Med. 8(1):1-3.

Hashemi MM, Rovig J, Weber S,Hilton B, Forouzan MM, Svage PB (2017). Susceptibility of Colistin-Resistant, Gram-Negative Bacteria to Antimicrobial Peptides and Ceragenins. Antimicrob A Chemo. 61(8):1-6.

MacNair CR, Stokes JM, Carfrae LA, Fiebig-Comyn AA, Coombe BK, Mulvey MR, Brown ED (2018). Overcoming mcr-1 mediated colistin resistance with colistin in combination with other antibiotics. Nat Comm. 9(1):1-8.

Arjun R, Gopalakrishnan R, Nambi PS, Kumar DS, Madhumitha R, Ramasubramanian V (2017). A study of 24 patients with colistin-resistant Gram-negative isolates in a tertiary care hospital in South India. Indian J Crit Care Med. 21(5):317-321.

Yin W, Li H, Shen Y, Liu Z, Wang S, Shen Z, Zhang R, Walsh TR, Shen J, Wang Y (2017). Novel plasmid-mediated Colistin resistance gene mcr-3 in Escherichia coli. MBio. 8(3):1-8. 46. Liu YY, Wang Y, Walsh TR, Yi LX, Zhang R, Spencer J, Doi Y, Tian G, Dong B, Huang X et al (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.

Wang R, van Dorp L, Shaw LP, Bradly P, Wang Q, Wang X, Jin L, Qing Z, Liu Y, Rieux A, et al (2018). The global distribution and spread of the mobilized colistin resistance gene mcr-1. Nat Comm. 9(1):1-9.

Lázár V,Nagy I, Spohn R, Csorgo B, Gyorkei A, Nyerges A, Horvath B, Voros A, Busa-Fekete R, Hrtyan M et al (2014). Genome-wide analysis captures the determinants of the antibiotic cross-resistance interaction network. Nat Comm. 8(5):1-12.

The Proceedings of the Nigerian Academy of Science 79

Hauhnar L, Pachuau L, Lalhruaitluanga H (2018). Isolation and Characterization of multi-drug Resistant bacteria from Hospital wastewater sites around the city of Aizawl, Mizoram. Adv Biosci Biotech. 9(7):311-321.

Bridgett MW, Liggit P, Daniel LC, Steven NF (2010). Antibiotic Resistance, gene transfer and water quality patterns observed in waterways near Confined Animal Feeding Operations farms and wastewater treatment facilities. Water, air, soil pollution. 217:473-489.

Berglund B (2015). Environmental dissemination of antibiotic resistance genes and correlation to anthropogenic contamination with antibiotics. Infect Ecol Epidemiol. 8(5):1-10.

Martínez JL (2008). Antibiotics and antibiotic resistance genes in natural environments. Sci. 32(5887):365-367.

Rizzo L, Manaia C, Merlin C,Schwartz T, Dagot C, Ploy MC, Micheal I, Fatta-Kassinos D (2013). Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment: a review. Sci Total Environ. 447:345-360.

Rodriguez-Mozaz S, Chamorro S, Marti E, Huerta B, Gros M, Sanchez-Melsio A, Borrego CM, Barcelo D, Balcazzr JL (2015).Occurrence of antibiotics and antibiotic resistance genes in hospital and urban wastewaters and their impact on the receiving river. Water Res. 69:234-242.

Pal C, Bengtsson-Palme J, Kristiansson, E, Larssson DGJ (2016). The structure and diversity of human, animal and environmental resistomes. Microbiome. 4(54):1-15.

Hocquet D, Muller A, Bertrand X (2016). What happens in hospitals does not stay in hospitals: antibiotic-resistant bacteria in hospital wastewater systems. J Hosp Infect. 93(4):395-402.

Hall BG, Barlow M (2004). Evolution of the serine beta-lactamases: past, present and future. Drug Resist Updat. 7(2):111-123.

Kümmerer K (2004). Resistance in the environment. J Antimicrob Chemother. 54(2):311-320.

Davis S, Fowler T, Watson J, Livermore DM, Walker D.et al (2013). Annual Report of Chief Medical Officer: infection and the rise of antimicrobial resistance. The Lancet. 381(9878):1606-1609.

Priest Amy (2018). Antibiotic resistant bacteria in water environments in Louisville, Kentucky. College of Arts and Sciences. Senior Honor Thesis, 89 P.

Birosova L, Mikulasova L (2009). Development of triclosan and antibiotic resistance in Salmonella enteric serovar Typhimurium. J Med Microbiol. 58(4): 436-471.

Rozos G, Voidarou C, Stavropoulou E, Skoufos I, Tzora A, Alexopoulos A, Bezirtzoglou E (2018). Biodiversity and Microbial Resistance of Lactobacilli Isolated From the Traditional Greek Cheese Kopanisti. Front Microbiol. 22 (9):1-8.

Baquero F, Martinez JL, Canton R (2008). Antibiotics and antibiotic resistance in water environments. Curr Opinion Biotech. 19(3):260-265.

Berendonk TU, Manaia CM, Merlin C, Fatta-Kassinos D, Cytryn E, Walsh F, Burgmann H, Sorum H, Norstrom M, Pons MN, et al (2015). Tackling antibiotic resistance: the environmental framework. Nat Rev Microbiol. 13(5):310-317.

The Proceedings of the Nigerian Academy of Science 80

Sugumar RB, Anandharaj K (2016). Assessment of Bacterial Load in the Fresh Water Lake System of Tamil Nadu. Interl J Curr Microbiol App Sci. 5(6):236-246.

Mustapha A, Isa T, Bello HS, Ismail HY (2016). Resistance profile of bacteria isolated from wastewater in the University of Maiduguri Teaching Hospital. J Biotech Res. 2(7): 49-54.

Elmanama AA, El kichariu AY, Mohsin M (2006). Contribution of hospital wastewater to the spread of antibiotic resistance in comparison to non-health institution. J AL-Aqsa University. 10:108-121.

Martinez JL (2009). Environmental pollution by antibiotics and by antibiotic resistance determinants. Environ Pollut. 157(11):2893-2902. 69. Burke V, Richter D, Greskowiak J, Mehrtens A, Schulzz L, Massmann G (2016). Occurrence of Antibiotics in Surface and Groundwater of a Drinking Water Catchment Area in Germany. Water Environ Res. 88(7):652-659. 70. Nguyen-Dang GC, Sebesvari Z, Renaud F, Rosendahl I, Minh QH, Amelung W (2015). Occurrence and Dissipation of the Antibiotics Sulfamethoxazole, Sulfadiazine, Trimethoprim, and Enrofloxacin in the Mekong Delta, Vietnam. PLoS ONE. 10(7):1-24.

Le TX, Munekage Y (2004). Residues of selected antibiotics in water and mud from shrimp ponds in mangrove areas in Vietnam. Marine Pol Bulletin. 49(11-12):922-929.

Förster M, Laabs V, Lamshöft M, Groeneweg J, Zuhlke S, Spiteller M, Krauss M, Kaupenjohann M, Amelung W (2009). Sequestration of manure-applied sulfadiazine residues in soils. Environ Sci Technol. 43(6):1824-1830. 73. Jessick AM, Moorman TB, Coats JR (2013). Fate of erythromycin in sediment-containing surface water microcosms: how does aged erythromycin in sediment influence bioavailability? Evaluating Veterinary Pharmaceutical Behavior in the Environment. ACS Symposium Series. 1126(7):161–178.

Sukul P, Spiteller M (2007). Fluoroquinolone antibiotics in the environment. Rev Environ Contamination Toxicol. 191:131-162.

Barkovskii A, Babb C, Hurley D (2014). Origins and environmental mobility of antibiotic resistance genes, virulence factors and bacteria in a tidal creek's watershed. J App Microbiol. 118(3):764-776.

Thai-Hoang LE, Charmaine NG, Hongjie C (2016). Occurrences and Characterization of Antibiotic-Resistant Bacteria and Genetic Determinants of Hospital Wastewater in a Tropical Country. Antimicrobial AChemo. 60(12):7449-7456.

Basri ZDM, Chua AL, Bwahid AM (2017). Occurrence of antibiotic-resistant bacteria in wastewater treatment plant. Advanced Sci Lett. 23(5):4649-4651.

Turolla A, Cattaneo M, Marazzi F (2018). Antibiotic resistant bacteria in urban sewage: Role of full-scale wastewater treatment plants on environmental spreading. Chemosphere. 19:761-769. 79. Barancheshme F, Munir M (2018). Strategies to Combat Antibiotic Resistance in the wastewater treatment plants. Front Microbiol. 8:1-12.

The Proceedings of the Nigerian Academy of Science 81

Devarajan N, Laffite A, Graham ND,Meijer M, Prabakar K, Mubedi JI, Elongo V, Mpiana PT, Ibelings BW, Wildi W, Pote J (2015). Accumulation of clinically relevant antibiotic-resistance genes, bacterial load, and metals in freshwater lake sediments in Central Europe. Environ Sci Technol. 49(11):6528-6537.

Sharma VK. Johnson N, Cizmas L, McDonald TJ, Kim H (2016). A review of the influence of treatment strategies on antibiotic resistant bacteria and antibiotic resistance genes. Chemosphere. 150:702-714.

Kwak YK, Colque P, Byfors S, Giske CG, Mollby R, Kuhn I (2015). Surveillance of antimicrobial resistance among Escherichia coli in wastewater in Stockholm during1 year: does it reflect the resistance trends in the society? Interl J antimicrobial agents. 45(1):25-32.

Odjadjare EC, Olaniran AO (2015). Prevalence of antimicrobial resistant and virulent Salmonella spp. In treated effluent and receiving aquatic milieu of wastewater treatment plants in Durban, South Africa. Int J Environ Res Public Health. 12(8):9692-9713.

Lien LTQ, Hoa NQ, Chuc NTK, Thoa NTM, Phuc HD, Diwan V, Dat NT, Tamhankar AJ, Lundborg CS (2016). Antibiotics in Wastewater of a Rural and an Urban Hospital before and after Wastewater Treatment, and the Relationship with Antibiotic Use-A One Year Study from Vietnam. Int J Environ Res Public Health. 13(6):1-13.

Mustapha A, Imir T (2019). Detection of Multidrug - Resistance Gram-Negative Bacteria from Hospital sewage in North East, Nigeria. Front Environ Microbiol. 5(1):1-7. doi: 10.11648/j.fem.20190501.11

Gothwal R, Shashidhar T (2014). Antibiotic Pollution in the Environment: A Review. CLEAN - Soil, Air, Water. 43(4):479-489.

Finley RL, Collignon P, Larsson DG, McEwen SA, Li XZ, Gaze WH, Reid-Smith R, Timinouni M, Graham DW, Topp E (2013). The scourge of antibiotic resistance: the important role of the environment. Clin Infect Dis.57(5):704-710.

Laffite A, Kilunga PI, Kayembe JM, Devarajan N, Mulaji CK, Giuliani G, Slaveykova VI, Pote J (2016). Hospital Effluents Are One of Several Sources of Metal, Antibiotic Resistance Genes, and Bacterial Markers Disseminated in Sub-Saharan Urban Rivers. Front Microbiol. 7:1-14.

McCarthy G, Lawlor PG, Gutierrez M, Gardiner GE (2013). Assessing the biosafety risks of pig manure for use as a feedstock for composting. Sci Total Environ. 463:712-719.

Hsu CY, Hsu BM, Ji WT, Chang TY, Kao PM, Tseng SF, Shen TY, Shih FC, Fan CW, Liu JH (2014). A Potential Association between Antibiotic Abuse and Existence of Related Resistance Genes in Different Aquatic Environments. Water, Air & Soil Pollution. 2014;226(1):1-10.

Van Boeckel TP, Brower C, Gilbert M, Grenfell BT, Levin SA, Robinson TP, Teillant A, Laxminarayan R (2015). Global trends in antimicrobial use in food animals. PNAS. 112(18):5649-5654. 92. Van-Boeckel TP, Glennon EE, Chen D, Gilbert M, Robinson TP, Grenfell BT, Levin SA, Bonhoeffer S, Laxminarayn R (2017). Reducing antimicrobial use in food animals. Science. 357 (6358):1350-1352.

The Proceedings of the Nigerian Academy of Science 82

Woolhouse M, Ward M, van Bunnik B, Farrar J (2015). Antimicrobial resistance in humans, livestock and the wider environment. Philosophical Transaction Royal Society. 370(1670):1-7. 94. Ibrahim A, Junaidu A, Garba M (2018). Multiple antibiotic residues in meat from slaughtered cattle in Nigeria. The Internet J Vet. Med. 8(1):1-5.

Galadima HB, Geidam YA, Shamaki BU, Hauwa AB, Ibrahim B, Waziri A (2018). Survey of Antimicrobial Residue in Table Eggs among Layer Poultry Farmers in Maiduguri Metropolis, Borno State. Asian J Animal and Vet Advances. 13(2):101-108.

An XL, Su JQ, Li B, Ouyang WY, Zhao Y, Chen QL, Cui L, Chen H, Gillings MR, Zhang T, et al (2018). Tracking antibiotic resistome during wastewater treatment using high throughput quantitative PCR. Environ Int. 117:146–153.

Zhu YG, Zhao Y, Zhu D, Richard M, Penuelas J, Ok YS, Banwart SA (2019). Soil biota, antimicrobial resistance and planetary health. Environ Int. 131:1-7.

McCann MC, Christgen B, Robert JA, Su JQ, Arnold KE, Gray ND, Zhu YG, Graham DW (2019). Understanding drivers of antibiotic resistance genes in High Arctic soil ecosystems. Environ Int. 125:497–504.

Audrain B, Farang MA, Ryu CM, Ghigo JM (2015). Role of bacterial volatile compounds in bacterial biology. FEMS Microbiol Rev. 39(2):222–233.

Lorena B, Corcione S, Pacini G, Perri GD, D’Avolio A, DeRosa FG (2014). A 30-years review on pharmacokinetics of antibiotics: is the right time for pharmacogenetics? Curr Drug Met. 15(6):581–598.

Guzman JD, Bucar GA, Gibbons S, Bhakta S (2012). Antimycobacterials from natural sources: ancient times, antibioticera and novel scaffolds. Front Biosci. 17:1861–1881.

Tong Z, Ivask A, Guo K, McCormick S, Lombi E, Priest C, Voelcker NH (2017). Crossed flow microfluidics for high throughput screening of bioactive chemical-cell interactions. Lab on Chip. 17(3):501–510.

Hautbergue T, Jamin EL, Debrauwer L, Puel O, Oswald IP (2018). From genomics to metabolomics, moving toward an integrated strategy for the discovery of fungal secondary metabolites. Nat Prod Rep. 35(2):147–173.

Andersson DI, Hughes D (2010). Antibiotic resistance and its cost: is it possible to reverse? Nat Rev Microbiol. 8(4):260-271.

Wright GD (2010). Antibiotic resistance in the environment: a link to the clinic. Curr Opin Microbiol. 13(5):589–594.

D'Costa VM, King CE, Kalan L, Morar M, Sung WWL, Schwarz C, Froese D, Zazula G, Calmels F, Debruyne R, et al (2011). Antibiotic resistance is ancient. Nat. 477(7365):457–461.

Blair JM, Webber MA, Baylay AJ, Ogbolu DO, Piddock LJV (2015). Molecular mechanisms of antibiotic resistance. Nat Rev Microbiol. 13(1):42–51.

The Proceedings of the Nigerian Academy of Science 83

Galán JC, Gonzálezcandelas F, Rolain JM, Canton R (2013). Antibiotics as selectors and accelerators of diversity in the mechanisms of resistance: from the resistome to genetic plasticity in the β-lactamases world. Front Microbiol. 4(9):1-17.

Goethem MWV, Pierneef R, Bezuidt KIO, De-Peer YVD, Cowan DA, Makhalanyane TP (2018). A reservoir of ‘historical’ antibiotic resistance genes inremote pristine Antarctic soils. Microbiome. 6:1-12.

Centres for Disease Control and Prevention CDC (2017). Antibiotic use in the United States progress and opportunities. 24 (7). Available from www.cdc.gov/antibiotic-use/stewardship-report

Peterson E, Kaur P (2018). Antibiotic resistance mechanisms in bacteria: relationships between resistance determinants of antibiotic producers, environmental bacteria, and clinical pathogens. Front Microbiol. 9:1-21.

Forsberg KJ, Reyes A, Wang B, Selleck EM, Sommer MOA, Dantas G (2012). The shared antibiotic resistome of soil bacteria and human pathogens. Sci. 337(6098):1107–1111.

Zhao Y, Su JQ, An XL, Huang F, Rensing C, Brandt KK, Zhu YG (2017). Feed additives shift gut microbiota and enrich antibiotic resistance in swine gut. Sci Total Environ. 621:1224–1232.

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 swine farms. PNAS. 110 (9):3435–3440.

Qiao M, Ying GG, Singer AC, Zhu YG (2017). Review of antibiotic resistance in China and its environment. Environ Int. 110:160–172.

Wang FH, Qiao M, Lv ZE, Guo GX, Jia YSu YH, Zhu YG (2014). Impact of reclaimed water irrigation on antibiotic resistance in public parks, Beijing, China. Environ Pollut. 184:247–253.

Insam H, Gomez-Brandon M, Ascher J (2015). Manure-based biogas fermentation residues- friend or foe of soil fertility? Soil Biol Biochem. 84: 1–14.

Li J, Cao J, Zhu YG, Chen QL, Shen F, Wu Y, Xu S, Fan H, Da G, Huang RJ, et al (2018). Global survey of antibiotic resistance genes in air. Environ Sci Technol. 52(19):10975–10984.

Zhang J, Sui Q, Tong J, Zhog J, Wang H, Chen M, Wei Y (2018). Soil types influence the fate of antibiotic-resistant bacteria and antibiotic resistance genes following the land application of sludge composts. Environ Int. 118:34–43.

Food and Agriculture Organization of the United Nations FAO (). Antimicrobial Resistance in Food and Agriculture. FCC-EMPRES | Information Sheets | 04 | APRIL | 2017. Available on: http://www.fao.org/antimicrobial-resistance. Last accessed 12 June, 2020.

Anthony DS, Ramachandran R, David CL, Korinek A, Fry JP, Heaney CD (2016). A Framework for Costing the Lowering of Antimicrobial Use in Food Animal Production,” Baltimore, USA: Johns Hopkins Center for a Livable Future. 1-62.

Kumar KC, Gupta S, Chander Y, Singh A (2005). Antibiotic Use in Agriculture and Its Impact on the Terrestrial Environment. Advances in Agronomy. 87:1–54.

The Proceedings of the Nigerian Academy of Science 84

Sarkar DJ, Mukherjee I, Shakil N, Rana VS, Kaushik P, Debnath (2018). Antibiotics in Agriculture: Use and Impact. Indian J Ethno Phyto Pharm. 4:4-19.

Centre for Disease Control and Prevention CDC (2020). Antibiotic /Antimicrobial Resistance (AR/AMR).Centers for Disease Control and Prevention, National Center for Emerging and Zoonotic Infectious Diseases (NCEZID), Division of Healthcare Quality Promotion (DHQP). Available on: https://www.cdc.gov/drugresistance/food.html. Last accessed 20.May.2020.

Topp E (2017). Agriculture and Agri-Food Canada’s research program on antimicrobial resistance. Canada Communicable Disease Rep. 43:224-227.

Abdelgader SA, Shi D, Chen M,Zhang L, Hejair HMA, Mumhammad U, Yao H, Zhang W (2018). Antibiotics Resistance Genes Screening and Comparative Genomics Analysis of Commensal Escherichia coli Isolated from Poultry Farms between China and Sudan. BioMed Res Internl. 1-10.

Durso LM, Miller DN, Wienhold B (2012). Distribution and Quantification of Antibiotic Resistant Genes and Bacteria across Agricultural and Non-Agricultural Metagenomes. PLoS ONE. 7(11):1-12.

Berendsen BJ, Wegh RS, Memelink J, Zuidema T, Stolker LAM (2015). The analysis of animal faeces as a tool to monitor antibiotic usage. Talanta. 132:258–268.

Cerqueira F, Matamoros V, Bayona JM, Berendonk TU, Elsinga G, Hornstra LM, Pina B (2019). Antibiotic resistance gene distribution in agricultural fields and crops. A soil-to-food analysis. Environ Res. 177:1-10.

Thanner S, Drissner D, Walsh F (2016). Antimicrobial resistance in agriculture. MBio. 7:1-7.

Silbergeld E, Aidara-Kane A, Dailey J (2017). Agriculture and Food Production as Drivers of the Global Emergence and Dissemination of Antimicrobial Resistance. OneHealth. 4:1-13.

Davies R, Wales A (2019). Antimicrobial Resistance on Farms: A Review Including Biosecurity and the Potential Role of Disinfectants in Resistance Selection. Comprehensive Rev Food Sci Food Safety. 18(3):753-774.

Leibler JH, Dalton K, Pekosz A, Gray GC, Silbergeld EK (2016). Epizootics in Industrial Livestock Production: Preventable Gaps in Biosecurity and Biocontainment. Zoonoses Public Health. 64(2):137-145.

Liu X, Steele JC, Meng XZ (2017). Usage, residue, and human health risk of antibiotics in Chinese aquaculture: A review. Environ Pollut. 223:161–169.

Burridge L, Weis JS, Cabello F, Pizarra J, Bostick K (2010). Chemical use in salmon aquaculture: A review of current practices and possible environmental effects. Aquaculture. 306 (1-4):7-23.

Schmidt AS, Bruun MS, Dalsgaard I, Larsen JL (2001). Incidence, distribution, and spread of tetracycline resistance determinants and integron-associated antibiotic resistance genes among motile aeromonads from a fish farming environment. Appl Environ Microbiol. 67(12):5675–5682.

The Proceedings of the Nigerian Academy of Science 85

Zhang XX, Zhang T (2011). Occurrence, abundance, and diversity of tetracycline resistance genes in 15 sewage treatment plants across China and other global locations. Environ Sci Technol. 45(7):2598–2604.

Gardner M, Jones V, Comber S, Scrimshaw MD, Coello-Garcia T, Cartmell E, Lester J, Ellor B (2013). Performance of UK wastewater treatment works with respect to trace contaminants. Sci Total Environ. 456-457:359–369.

Binh CT, Heuer H, Kaupenjohann M, Smalla K (2008). Piggery manure used for soil fertilization is a reservoir for transferable antibiotic resistance plasmids. FEMS Microbiol Ecol. 66(1):25–37.

Ding GC, Radl V, Schloter-Hai B, Jechalke S, Heuer H, Smalla K, Schloter M (2014). Dynamics of soil bacterial communities in response to repeated application of manure containing sulfadiazine. PLoS One. 9(3):1-10.

Tasho RP, Cho JY (2016). Veterinary antibiotics in animal waste, its distribution in soil and uptake by plants: A review. Sci Total Environ. 563-564:366–376.

Azanu D, Mortey C, Darko G, Weisser JJ, Styrishave B, Abaidoo RC (2016). Uptake of antibiotics from irrigation water by plants. Chemosphere. 157:107–114.

Cerqueira F, Matamoros V, Bayona JM, Elsinga G, Hornstra LM, Pina B (2019). Distribution of antibiotic resistance genes in soils and crops. A field study in legume plants (Viciafaba L.) grown under different watering regimes. Environ Res. 170:16–25.

Chantziaras I, Boyen F, Callens B, Dewulf J (2014). Correlation between veterinary antimicrobial use and antimicrobial resistance in food-producing animals: a report on seven countries,” J Antimicrobial Chemother. 69(3):827-834.

Shi W, Liu Y, Li J,Zhang H, Shi R, Chen J, Li H (2020). Distribution pattern of antibiotic resistance genes and bacterial community in agricultural soil samples of Wuliangsuhai watershed China. Agriculture Ecosyst Environ. 295:1-7.

Armalyte J, Skerniškyte J, Bakiene E, Krasauskas R, Siugzudiniene R, Kareiviene V, Kerziene S, Klimiene I, Suziedeliene E, Ruzauskas M (2019). Microbial Diversity and Antimicrobial Resistance Profile in MicrobiotaFrom Soils of Conventional and Organic Farming Systems. Front Microbiol. 10(892):1-12.

Chang Q, Wang W, Regev-Yochay G, Lipsitch M, Hanage WP (2014). Antibiotics in agriculture and the risk to human health: how worried should we be?. Evol Appl. 8(3):240–245.

Ter-Kuile BH, Kraupner N, Brul S (2016). The risk of low concentrations of antibiotics in agriculture for resistance in human health care. FEMS Microbiol Lett. 363(19):1-7.

Spoor LE, McAdam PR, Weinert L, Rambaut A, Hasman H, Aarestrup FM, Kearns AM, Larsen AR, Skov R, Fitzgerald JR (2013). Livestock origin for a human pandemic clone of community-associated methicillin-resistant Staphylococcus aureus. mBio. 4(4):1-7.

Manyi-Loh C, Mamphweli S, Meyer E, Okoh A (2018). Antibiotic Use in Agriculture and Its Consequential Resistance in Environmental Sources: Potential Public Health Implications. Molecules. 23(4):1-48.

The Proceedings of the Nigerian Academy of Science 86

Meena HR, Kumar V (2019). Antimicrobial Resistance and Rational Use of Antimicrobials in Livestock: Developing Countries’ perspectives. Livestock Health and Farming. Intechopen. p 1-14.


  • There are currently no refbacks.