Characterization and Phylodiversity of Implicated Enteric Bacteria Strains in Retailed Tomato (Lycopersicon esculentum Mill.) Fruits in Southwest Nigeria
DOI:
https://doi.org/10.3889/oamjms.2021.5657Keywords:
Antibiotic resistance, Foodborne pathogens, Food safety, Pylo-diverse strains, Tomato fruits, Public healthAbstract
BACKGROUND: Tomatoes (Lycopersicon esculentum Mill.) have very huge health-promoting benefits due to high nutritional composition; however, these fruits are potential reservoir of enteric food-borne pathogens causing major public health concerns.
AIM: Characterization and phylo-analysis of implicated enteric bacteria strains in retailed Tomato fruits in southwest Nigeria were studied.
METHODS: Ready to be retailed fresh tomato fruits were purchased from common food markets in southwest, Nigeria, which lies between latitudes 6° 21′ to 8° 30′ N and longitudes 2° 30′ to 5° 30′ E. Observation of sample storage potentials at different conditions and bio-typing of associated bacterial strains were carried out for consecutive 14 days. Enteric bacteria strains were genotyped with 16S rRNA assay and further profiled for antibiotic susceptibility to common antibiotics. High population rate frequently consume tomatoes.
RESULTS: Early spoilage characterized with yellow fluid, fungal growth and visible lesions were observed at 25°C storage compare to few patches of lesion at 4°C after 14 days. Higher bacterial count of 4.0–7.18 Log CFU/g was recorded at ambient storage compare to refrigerated samples with more than 10% occurrence rate of Citrobacter spp., Klebsiella spp. and Enterobacter spp. Identified Citrobacter spp. and Klebsiella spp. showed 100% resistant to beta-lactam antibiotics (ceftazidime, cefuroxime, cefixime, ciprofloxacin, and amoxicillin-clavulanic acid). Two-resistant enteric bacteria strains, Klebsiella aerogenes B18 and Citrobacter freundii B27 obtained from Nigerian tomato clustered with Citrobacter strains in food (China), water strains (India, Poland, Malaysia), milk (Germany), and human fecal (China).
CONCLUSION: Implicated multidrug-resistant enteric bacilli in retailed tomatoes can cause severe food-borne diseases which public oriented awareness, strategic farm to market surveillance are needed to be intensified.
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Angadi V, Rai PK, Bara BM. Effect of organic manures and biofertilizers on plant growth, seed yield and seedling characteristics in tomato (Lycopersicon esculentum Mill.). J Pharmacogn Phytochem. 2017;6(3):807-10.
Tan J, Kerr WL. Rheological properties and microstructure of tomato puree subject to continuous high-pressure homogenization. J Food Eng. 2015;166:45-54. https://doi.org/10.1016/j.jfoodeng.2015.05.025 DOI: https://doi.org/10.1016/j.jfoodeng.2015.05.025
Çolak NG, Eken NT, Ülger M, Frary A, Doğanlar S. Mapping of quantitative trait loci for antioxidant molecules in tomato fruit: Carotenoids, Vitamins C and E, glutathione, and phenolic acids. Plant Sci. 2020;292:110393. h t t p s : / / d o i . o r g / 1 0 . 1 0 1 6 / j . p l a n t s c i . 2 0 1 9 . 11 0 3 9 3 PMid:32005398
Chaudhary P, Sharma A, Singh B, Nagpal AK. Bioactivities of phytochemicals present in tomato. J Food Sci Technol. 2018;55(8):2833-49. https://doi.org/10.1007/s13197-018-3221-z PMid:30065393 DOI: https://doi.org/10.1007/s13197-018-3221-z
Martí R, Leiva-Brondo M, Lahoz I, Campillo C, Cebolla- Cornejo J, Roselló S. Polyphenol and L-ascorbic acid content in tomato as influenced by high lycopene genotypes and organic farming at different environments. Food Chem. 2018;239:148- 56. https://doi.org/10.1016/j.foodchem.2017.06.102 PMid:28873552 DOI: https://doi.org/10.1016/j.foodchem.2017.06.102
Ahmed FA, Sipes BS, Alvarez AM. Postharvest diseases of tomato and natural products for disease management. Afr J Agric Res. 2017;12(9):684-91. DOI: https://doi.org/10.5897/AJAR2017.12139
Obafemi YD, Ajayi AA, Taiwo OS, Olorunsola SJ, Isibor PO. Isolation of Polygalacturonase-producing bacterial strain from tomatoes (Lycopersicon esculentum Mill.). Int J Microbiol. 2019;2019:7505606. https://doi.org/10.1155/2019/7505606 PMid:30766603 DOI: https://doi.org/10.1155/2019/7505606
Charles MT, Arul J, Charlebois D, Yaganza ES, Rolland D, Roussel D, et al. Postharvest UV-C treatment of tomato fruits: Changes in simple sugars and organic acids contents during storage. LWT Food Sci Technol. 2016;65:557-64. https://doi.org/10.1016/j.lwt.2015.08.055 DOI: https://doi.org/10.1016/j.lwt.2015.08.055
Ma L, Zhang M, Bhandari B, Gao Z. Recent developments in novel shelf-life extension technologies of fresh-cut fruits and vegetables. Trends Food Sci Technol. 2017;64:23-38. https:// doi.org/10.1016/j.tifs.2017.03.005 DOI: https://doi.org/10.1016/j.tifs.2017.03.005
Amaechi EC, Ohaeri CC, Ukpai OM, Adegbite RA. Prevalence of parasitic contamination of salad vegetables in Ilorin, North Central, Nigeria. Momona Ethiopian J Sci. 2016;8(2):136-45. https://doi.org/10.4314/mejs.v8i2.3 DOI: https://doi.org/10.4314/mejs.v8i2.3
Bello SI, Aminu D, Olawuyi OJ, Afolabi-Balogun NB, Lawal AO, Azeez AH, et al. Antibiotic sensitivity of bacterial and fungal isolates from tomato (Solanum lycopersicum L.) fruit. Trop Plant Res. 2016;3(1):112-9.
Alegbeleye OO, Singleton I, Sant’Ana AS. Sources and contamination routes of microbial pathogens to fresh produce during field cultivation: A review. Food Microbiol. 2018;73:177-208. https://doi.org/10.1016/j.fm.2018.01.003 PMid:29526204 DOI: https://doi.org/10.1016/j.fm.2018.01.003
Obafemi YD, Ajayi AA, Olasehinde GI, Atolagbe OM, Onibokun EA. Screening and partial purification of amylase from Aspergillus niger isolated from deteriorated tomato (Lycopersicon esculentum Mill.) fruits. Afr J Clin Exp Microbiol. 2018;19(1):47-57. https://doi.org/10.4314/ajcem.v19i1.7 DOI: https://doi.org/10.4314/ajcem.v19i1.7
Lake IR. Food-borne disease and climate change in the United Kingdom. Environ Health. 2017;16(1):117. PMid:29219100 DOI: https://doi.org/10.1186/s12940-017-0327-0
Javed A. Food borne health issues and their relevance to Pakistani society. Am Sci Res J Eng Technol Sci. 2016;26(4):235-51.
Zekar FM, Granier SA, Marault M, Yaici L, Gassilloud B, Manceau C, et al. From farms to markets: Gram-negative bacteria resistant to third-generation cephalosporins in fruits and vegetables in a region of North Africa. Front Microbiol. 2017;8:1569. https://doi.org/10.3389/fmicb.2017.01569 PMid:28883810 DOI: https://doi.org/10.3389/fmicb.2017.01569
European Food Safety Authority and European Centre for Disease Prevention and Control (EFSA and ECDC). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2017. EFSA J. 2018;16(12):e05500. https://doi.org/10.2903/j.efsa.2018.5500 DOI: https://doi.org/10.2903/j.efsa.2018.5500
Kilonzo-Nthenge A, Liu S, Hashem F, Millner P, Githua S. Prevalence of Enterobacteriaceae on fresh produce and food safety practices in small-acreage farms in Tennessee, USA. J Consum Prot Food Saf. 2018;13(3):279-87. https://doi.org/10.1007/s00003-018-1172-y DOI: https://doi.org/10.1007/s00003-018-1172-y
Saksena R, Malik M, Gaind R. Bacterial contamination and prevalence of antimicrobial resistance phenotypes in raw fruits and vegetables sold in Delhi, India. J Food Saf. 2020;40(1):e12739. https://doi.org/10.1111/jfs.12739 DOI: https://doi.org/10.1111/jfs.12739
Al-Kharousi ZS, Guizani N, Al-Sadi AM, Al-Bulushi IM. Antibiotic resistance of Enterobacteriaceae isolated from fresh fruits and vegetables and characterization of their AmpC β-lactamases. J Food Prot. 2019;82(11):1857- 63. https://doi.org/10.4315/0362-028x.jfp-19-089 PMid:31609646 DOI: https://doi.org/10.4315/0362-028X.JFP-19-089
Bello OO, Oni MO, Bello JO, Bello TK. The incidence of extended-spectrum beta-lactamase (ESBL)-producing bacteria in salad vegetables in Ondo city, Nigeria. Asian Food Sci J. 2019;1:1-14. https://doi.org/10.9734/afsj/2019/v9i130003 DOI: https://doi.org/10.9734/afsj/2019/v9i130003
Richter L, Du Plessis EM, Duvenage S, Korsten L. Occurrence, identification, and antimicrobial resistance profiles of extended-spectrum and AmpC β-lactamase-producing Enterobacteriaceae from fresh vegetables retailed in Gauteng Province, South Africa. Foodborne Pathog Dis. 2019;16(6):421-7. https://doi.org/10.1089/fpd.2018.2558 DOI: https://doi.org/10.1089/fpd.2018.2558
Olotu EJ, Aribisala JO, Oluyele O, Ojo OR, Olaniyi BO. Bacteriological and parasitological assessment of fruits and vegetables sold in Akoko South West Local government area of Ondo state Nigeria. Int Res J Gastroenterol Hepatol. 2020;1:11-20.
Al-Kharousi ZS, Guizani N, Al-Sadi AM, Al-Bulushi IM, Shaharoona B. Hiding in fresh fruits and vegetables: Opportunistic pathogens may cross geographical barriers. Int J Microbiol. 2016;2016:4292417. https://doi.org/10.1155/2016/4292417 DOI: https://doi.org/10.1155/2016/4292417
Adekanle MA, Effedua HI, Oritogun KS, Adesiji YO, Ogunledun A. A study of microbial analysis of fresh fruits and vegetables, in Sagamu markets South-West, Nigeria. Agrosearch. 2015;15(2):1-12. https://doi.org/10.4314/agrosh.v15i2.1 DOI: https://doi.org/10.4314/agrosh.v15i2.1
Adepoju AO. Post-harvest losses and welfare of tomato farmers in Ogbomosho, Osun state, Nigeria. J Stored Prod Postharvest Res. 2014;5(2):8-13. https://doi.org/10.5897/jsppr2014.0160 DOI: https://doi.org/10.5897/JSPPR2014.0160
Izah SC, Aigberua AO. Microbial and heavy metal hazard analysis of edible tomatoes (Lycopersicon esculentum) in Port Harcourt, Nigeria. Toxicol Environ Health Sci. 2020;12(4):371- 80. https://doi.org/10.1007/s13530-020-00060-8 DOI: https://doi.org/10.1007/s13530-020-00060-8
Adewuyi SA, Adekunle CP. Socio-economic determinants of tomato retail marketing in Ibadan Southwest Local Government area of Oyo State, Nigeria. Afr J Agric Sci. 2015;10(13):1619- 24. https://doi.org/10.5897/ajar2015.9529 DOI: https://doi.org/10.5897/AJAR2015.9529
Gizaw Z. Public health risks related to food safety issues in the food market: A systematic literature review. Environ Health Prevent Med. 2019;24(1):68. https://doi.org/10.1186/s12199-019-0825-5 PMid:31785611 DOI: https://doi.org/10.1186/s12199-019-0825-5
Meléndez-Martínez AJ, Stinco CM, Mapelli-Brahm P. Skin carotenoids in public health and nutricosmetics: The emerging roles and applications of the UV radiation-absorbing colourless carotenoids phytoene and phytofluene. Nutrients. 2019;11(5):1093. https://doi.org/10.3390/nu11051093 PMid:31100970 DOI: https://doi.org/10.3390/nu11051093
Obeng FA, Gyasi PB, Olu-Taiwo M, Ayeh-Kumi FP. Microbial assessment of tomatoes (Lycopersicon esculentum) sold at some central markets in Ghana. Biomed Res Int. 2018;2018:6743826. https://doi.org/10.1155/2018/6743826 DOI: https://doi.org/10.1155/2018/6743826
Oyedepo SO, Adeyemi GA, Olawole OC, Ohijeagbon OI, Fagbemi OK, Solomon R, et al. A GIS-based method for assessment and mapping of noise pollution in Ota metropolis, Nigeria. MethodsX. 2019;6:447-57. https://doi.org/10.1016/j.mex.2019.02.027 DOI: https://doi.org/10.1016/j.mex.2019.02.027
Mitruka BM. Methods of Detection and Identification of Bacteria. Boca Raton: CRC Press; 2017.
So W, Shurko J, Galega R, Quilitz R, Greene JN, Lee GC. Mechanisms of high-level ceftolozane/ tazobactam resistance in Pseudomonas aeruginosa from a severely neutropenic patient and treatment success from synergy with tobramycin. J Antimicrob Chemother. 2019;74(1):269-71. https://doi.org/10.1093/jac/dky393 PMid:30295837 DOI: https://doi.org/10.1093/jac/dky393
Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing. 29th ed., Vol. 29. Wayne, PA: Clinical and Laboratory Standards Institute; 2018. p. 320.
Singh RP, Jha P, Jha PN. The plant-growth-promoting bacterium Klebsiella sp. SBP-8 confers induced systemic tolerance in wheat (Triticum aestivum) under salt stress. J Plant Physiol. 2015;184:57-67. https://doi.org/10.1016/j.jplph.2015.07.002 PMid:26217911 DOI: https://doi.org/10.1016/j.jplph.2015.07.002
NCBI Resource Coordinators. Database resources of the national center for biotechnology information. Nucleic Acids Res. 2018;46(D1):D8-13. https://doi.org/10.1093/nar/gks1189 PMid:29140470 DOI: https://doi.org/10.1093/nar/gks1189
Dasgupta CN, Singh VK, Nayaka S, Kishore S, Lavania S. Molecular phylogeny of a commercially important thermophilic microalga Chlorella sorokiniana LWG002615 and associated bacterium Aquimonas sp. NBRI01 isolated from Jeori thermal spring, Shimla, India. Nucleus. 2020;63:203-10. https://doi.org/10.1007/s13237-019-00286-z DOI: https://doi.org/10.1007/s13237-019-00286-z
Obayelu OA, Adegboyega OM, Sowunmi FA, Idiaye CO. Factors explaining postharvest loss of hot pepper under tropical conditions. Int J Veg Sci. 2021;2021:1-10. https://doi.org/10.1080/19315260.2021.1879342 DOI: https://doi.org/10.1080/19315260.2021.1879342
Obebe OO, Aluko OO, Falohun OO, Akinlabi KB, Onyiche TE. Parasitic contamination and public health risk of commonly consumed vegetables in Ibadan-Nigeria. Pan Afr Med J. 2020;36:126. https://doi.org/10.11604/pamj.2020.36.126.19364
Agbalaka PI, Ejinaka OR, Yakubu DP, Obeta UM, Jwanse RI, Dawet A. Prevalence of parasites of public health significance in vegetables sold in Jos metropolis, Plateau State, Nigeria. Am J Public Health. 2019;7(2):48-57.
El-Ramady HR, Domokos-Szabolcsy É, Abdalla NA, Taha HS, Fári M. Postharvest management of fruits and vegetables storage. In: Sustainable Agriculture Reviews. Cham: Springer; 2015. p. 65-152. https://doi.org/10.1007/978-3-319-09132-7_2 DOI: https://doi.org/10.1007/978-3-319-09132-7_2
Mohan MG, Sutar RF, Mohan RJ. Impact of storage temperature 7°C and post-harvest pre-treatment on quality characteristics and storage life of tomato (Lycopersicon esculentum) fruits. Int J Agric Sci Res. 2017;7(4):23-30. https://doi.org/10.24247/ijasraug20174 DOI: https://doi.org/10.24247/ijasraug20174
Tsang YP, Choy KL, Wu CH, Ho GT, Lam HY, Tang V. An intelligent model for assuring food quality in managing a multi-temperature food distribution centre. Food Control. 2018;90:81- 97. https://doi.org/10.1016/j.foodcont.2018.02.030 DOI: https://doi.org/10.1016/j.foodcont.2018.02.030
Kayode RM, Afolayan AJ. Microbiological and chemical evaluation of decomposed open pollinated tomato (Lycopersicon esculentum) fruits in storage. J Pure Appl Microbiol. 2014;8(6):4441-9.
Brasil IM, Siddiqui MW. Postharvest quality of fruits and vegetables: An overview. In: Preharvest Modulation of Postharvest Fruit and Vegetable Quality. Cambridge: Academic Press; 2018. p. 1-40. https://doi.org/10.1016/b978-0-12-809807-3.00001-9 DOI: https://doi.org/10.1016/B978-0-12-809807-3.00001-9
Chinedu SM, Enya E. Isolation of microorganisms associated with deterioration of tomato (Lycopersicon esculentum) and pawpaw (Carica papaya) fruits. Int J Curric Microbiol Appl Sci. 2016;3(5):501-12.
Iseppi R, de Niederhäusern S, Bondi M, Messi P, Sabia C. Extended-spectrum β-lactamase, AmpC, and MBL-producing gram-negative bacteria on fresh vegetables and ready-to-eat salads sold in local markets. Microbial Drug Resist. 2018;24(8):1156-64. https://doi.org/10.1089/mdr.2017.0198 DOI: https://doi.org/10.1089/mdr.2017.0198
Dey M, Mokbul M, Ismail I, Alim SR. Identification of antibiotic resistant gram-negative bacteria in a popular street-food item (Chatpati) in Dhaka university campus, Bangladesh. Front Environ Microbiol. 2018;4(2):75. https://doi.org/10.11648/j.fem.20180402.15 DOI: https://doi.org/10.11648/j.fem.20180402.15
Jung D, Rubin JE. Identification of antimicrobial resistant bacteria from plant-based food products imported into Canada. Int J Food Microbiol. 2020;1:08509. https://doi.org/10.1016/j.ijfoodmicro.2020.108509 DOI: https://doi.org/10.1016/j.ijfoodmicro.2020.108509
Belay Z, Gelgelu E, Chala B. Assessment of microbiological quality and drug resistance patterns of raw vegetables irrigated with Hasassa River, West Arsi Zone, Oromia Region, Ethiopia. Afr J Microbiol Res. 2020;14(9):507-15. https://doi.org/10.5897/ajmr2019.9205 DOI: https://doi.org/10.5897/AJMR2019.9205
Balali GI, Yar DD, Dela VG, Adjei-Kusi P. Microbial contamination, an increasing threat to the consumption of fresh fruits and vegetables in today’s world. Int J Microbiol. 2020;2020:3029295. https://doi.org/10.1155/2020/3029295 DOI: https://doi.org/10.1155/2020/3029295
Aggarwal D, Upadhyay SK, Kaur L, Kumar A, Bhalla H, Singh R. Assessment of microbial burden on vegetable salads for food safety and human health. Bull Pure Appl Sci Zool. 2020;39:130- 6. https://doi.org/10.5958/2320-3188.2020.00015.7 DOI: https://doi.org/10.5958/2320-3188.2020.00015.7
Nithya A, Babu S. Prevalence of plant beneficial and human pathogenic bacteria isolated from salad vegetables in India. BMC Microbiol. 2017;17(1):1-16. https://doi.org/10.1186/ s12866-017-0974-x DOI: https://doi.org/10.1186/s12866-017-0974-x
Callejón RM, Rodriguez-Naranjo MI, Ubeda C, Hornedo- Ortega R, Garcia-Parrilla MC, Troncoso AM. Reported foodborne outbreaks due to fresh produce in the United States and European Union: Trends and causes. Foodborne Pathog Dis 2015;12(1):32-38. https://doi.org/10.1089/fpd.2014.1821 DOI: https://doi.org/10.1089/fpd.2014.1821
Folster JP, Grass JE, Bicknese A, Taylor J, Friedman CR, Whichard JM. Characterization of resistance genes and plasmids from outbreaks and illness clusters caused by Salmonella resistant to ceftriaxone in the United States, 2011- 2012. Microbial Drug Resist.2017;23(2):188-93. https://doi.org/10.1089/mdr.2016.0080 PMid:27828730 DOI: https://doi.org/10.1089/mdr.2016.0080
Akinduti PA, Olasehinde GI, Ejilude O, Taiwo OS, Obafemi YD. Fecal carriage and phylodiversity of community-acquired blaTEM enteric bacilli in Southwest Nigeria. Infect Drug Resist. 2018;11:2425-33. https://doi.org/10.2147/idr.s178243 PMid:30568469 DOI: https://doi.org/10.2147/IDR.S178243
Duvenage S, du Plessis E, Kgoale D, Ratshilingano M, Baloyi T, Richter L, et al. Formal and informal spinach safety from farm to fork: A South African case study. In: IAFP European Symposium on Food Safety. United States: Global Association for Food Protection; 2019.
Hjikarim F, Dallal MM, Pourmand MR, Abdi M. An investigation of extended-spectrum β-lactamases (ESBLs) in Klebsiella isolated from foodborne outbreaks in Iran. Gene Rep. 2020;2020:100632. https://doi.org/10.1016/j.genrep.2020.100632 DOI: https://doi.org/10.1016/j.genrep.2020.100632
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