Assessment of the Microbiological Profile, Species Diversity and Antimicrobial Susceptibility of Recovered Bacteria from Retail Honeys in Turkey

PDF (English)
DOI: https://doi.org/10.12681/jhvms.26763
HS GURAN
Department of Food Hygiene and Technology, Faculty of Veterinary Medicine, Dicle University, Diyarbakir, Turkey
G DURUKAN
Department of Food Hygiene and Technology, Faculty of Veterinary Medicine, Dicle University, Diyarbakir, Turkey
D MANN
Department of Food Hygiene and Technology, Faculty of Veterinary Medicine, Dicle University, Diyarbakir, Turkey
Resumen

The aim of this study was to assess the microbiological profile, coliform and staphylococcal species diversity, and the antimicrobial susceptibility of coliform and other Gram-negative bacteria recovered from retail honeys in Turkey. A total of 150 honey samples, including extracted honey and comb honey samples, were purchased from honey sellers. The honey samples were analyzed for total mesophilic aerobic bacteria (TMAB), total mesophilic anaerobic bacteria (TMAnB), coliforms, Escherichia coli (E. coli), Staphylococcus spp., lactic acid bacteria (LAB), yeasts, and molds. All presumptive coliform and Staphylococcus isolates were identified at species level and then Gram-negative isolates were screened for antimicrobial susceptibility. TMAB, TMAnB, LAB, yeasts and molds mean counts (log cfu/g) in the samples were 3.26±1.08, 3.0±0.89, 2.93±0.52, 2.90±0.83, 1.80±0.53, respectively. Eighteen point seven percent and 15.3% of extracted and comb honey contained coliform and Staphylococcus spp., respectively, with a mean count (MPN/g) of 8.06±1.23 and 0.71±0.66. TMAB, Staphylococcus spp. and yeast contamination rates were significantly higher in the extracted honeys (P<0.05). Presumptive coliform and Staphyloccus spp. isolates were mostly identified as Klebsiella pneumoniae, Proteus mirabilis, Serratia marcescens, and Staphylococcus hominis and Staphylococcus epidermidis, respectively. Among coliform and non-coliform Gram-negative recovered isolates, antimicrobial resistance was highest against ceftriaxone (92.4%) and cefepime (91.5%) followed by tigecyclin (46.2%). The results obtained in this study provide insight on the microbiological profile of honey and the diversity of coliform and Staphylococcus species in honey samples. Moreover, these results show that honey, which is considered beneficial for human health, may contain antibiotic-resistant bacteria.

Article Details
  • Sección
  • Research Articles
Creative Commons License

Esta obra está bajo una licencia internacional Creative Commons Atribución-NoComercial 4.0.

Authors who publish with this journal agree to the following terms:

· Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution Non-Commercial License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.

· Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g. post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.

· Authors are permitted and encouraged to post their work online (preferably in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work.

Descargas
Los datos de descargas todavía no están disponibles.
Citas
Aljadi AM, Kamaruddin MY (2004) Evaluation of the phenolic contents and antioxidant capacities of two Malaysian floral honeys. Food Chem 85:513-518.
Armbruster CE, Smith SN, Johnson AO, De Ornellas V, Eaton KA, Yep A, Mobley HL (2017) The Pathogenic Potential of Proteus Mirabilis is Enhanced by Other Uropathogens During Polymicrobial Urinary Tract İnfection. Infect Immun 85:E00808-16.
Baki F, Saner G, Adanacıoğlu H, Güler D (2017) Türkiye’de süzme çam balına yönelik tüketici tercihlerinin konjoint analizi: İzmir ili örneği. Balkan and Near Eastern J Soc Sci 3: 50-57.
Becker K, Heilmann C, Peters G (2014) Coagulase-negative staphylococci. Clin. Microbiol Rev 27:870-926.
Bezirtzoglou E, Voidarou C, Stavropoulou E (2016) Emerging antibiotic resistance in honey as a hazard for human health. J Bacteriol Mycol 2:6-12.
Bhatta DR, Cavaco LM, Nath G, Kumar K, Gaur A, Gokhale S, Bhatta DR (2016) Association of Panton Valentine Leukocidin (PVL) genes with methicillin resistant Staphylococcus aureus (MRSA) in Western Nepal: a matter of concern for community infections (a hospital based prospective study). BMC Infect Dis 16:199.
Boussaid A, Chouaibi M, Rezig L, Hellal R, Donsì F, Ferrari G, Hamdi S (2018) Physicochemical and bioactive properties of six honey samples from various floral origins from Tunisia. Arab J Chem 11:265-274.
Ceauşi C, Ţogoe I, Tudor L, Furnaris F (2009) The evaluation of microbiological quality of some bee honey sorts. Bull Univ Agric Sci Vet 66:273-277.
Chakir A, Romane A, Marcazzan GL, Ferrazzi P (2016) Physicochemical properties of some honeys produced from different plants in Morocco. Arab J Chem 9:946-954.
Combarros-Fuertes P, Valencia-Barrera RM, Estevinho LM, Dias LG, Castro JM, Tornadijo ME, Fresno JM (2019) Spanish honeys with quality brand: a multivariate approach to physicochemical parameters, microbiological quality and floral origin. J Apic Res 58:92-103.
Cosgrove SE (2006) The relationship between antimicrobial resistance and patient outcomes: mortality, length of hospital stay, and health care costs. Clin Infect Dis 42:82-89.
Duman AB, Sezer Ç, Oral NB (2008) Kars’ta Satışa Sunulan Süzme Balların Kalite Niteliklerinin Araştırılması. Kafkas Univ Vet Fak Derg 14:89-94.
Dümen E, Akkaya H, Öz GM, Sezgin FH (2013) Microbiological and parasitological quality of honey produced in İstanbul. Turk. J Vet Anim Sci 37:602-607.
El Sohaimy SA, Masry SHD, Shehata MG (2015). Physicochemical characteristics of honey from different origins. Ann Agric Sci 60:279-287.
Erkan ME, Vural A, Guran HS, Durmusoglu H (2015) Microbiological investigation of honey collected from Şırnak province of Turkey. J Hell Vet Med Soc 66:22-26.
European Commission (2005) Commission Regulation (EC) No 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs. Official Journal of the European Union, 338: 1-26.
Fernandez LA, Ghilardi C, Hoffmann B, Busso C, Gallez LM (2017) Microbiological quality of honey from the Pampas region throughout the extraction process. Rev Argent Microbiol 49:55-61.
Gallez L, Fernández LA (2009) Mieles Del Sistema Serrano De Ventania: Evaluación De La Calidad Microbiológica En El Circuito De La Planta De Extracción. Rev Argent Microbiol 41:163-167.
Garcia NL (2018) The current situation on the International honey market. Bee World 95:89-94.
Gasper J, Terentjeva M, Kántor A., Ivanišová E, Kluz M, Kačániová M (2017) Identification of Apis mellifera Gut Microbiota with MALDI-TOF MS Biotyper. Scientific Papers Animal Science & Biotechnologies 50:192-196.
Gomes S, Dias LG, Moreira LL, Rodrigues P, Estevinho L (2010) Physicochemical, microbiological and antimicrobial properties of commercial honeys from Portugal. Food Chem Toxicol 48:544-548.
Grabowski NT, Klein G (2017) Microbiology and foodborne pathogens in honey. Crit Rev Food Sci Nutr 57:1852-1862.
Hennekinne JA, De Buyser ML, Dragacci S (2012) Staphylococcus aureus and its food poisoning toxins: characterization and outbreak investigation. FEMS Microbiol Rev 36:815-836.
ISO (2003) EN ISO 4833 Microbiology of Food and Animal Feeding Stuffs- Horizontal Methods for Enumeration of Microorganisms-Colony-Count Technique at 30 Degrees, International Standardization Organization, Geneva.
Kačániová M, Gasper J, Brindza, Schubertová Z, Ivanišová E (2017) Bacteria of Apis mellifera gastrointestinal tract: counts, identification and their antibiotic resistance. Agrobiodivers. Improv Nutr Health Life Qual 1:210-215.
Kačániová M, Hleba L, Džugan M, Pasternakiewicz A, Kňazovická V, Pavelková A, Felsöciová S, Petrová J, Rovná K, Kluz M, Grabek-Lejko D (2012) Microbiological properties and antimicrobial effect of Slovakian and Polish honey having regard to the water activity and water content. J Microbiol Biotechnol Food Sci 2:272-281.
Kavanagh S, Gunnoo J, Passos TM, Stout JC, White B (2019) Physicochemical properties and phenolic content of honey from different floral origins and from rural versus urban landscapes. Food Chem 272:66-75.
Kollef KE, Schramm GE, Wills AR, Reichley RM, Micek ST, Kollef MH (2008) Predictors of 30-day mortality and hospital costs in patients with ventilator-associated pneumonia attributed to potentially antibiotic-resistant gram-negative bacteria. Chest 134:281-287.
Kunová S, Kačániová M, Haščík P, Čuboň J (2015) Microbiological and chemical quality of Slovak and European honey. J Microbiol Biotechnol Food Sci 4:41-44.
Leme LM, Montenegro HR, Dos Santos LDR, Sereia MJ, Valderrama P, Março PH (2018) Relation between near-infrared spectroscopy and physicochemical parameters for discrimination of honey samples from Jatai weyrauchi and Jatai angustula bees. Food Anal Methods 11:1944-1950.
Manges AR (2016) Escherichia coli and urinary tract infections: the role of poultry-meat. Clin Microbiol Infect 22:122-129.
Mercan N, Guvensen A, Celik A, Katircioglu H (2007) Antimicrobial activity and pollen composition of honey samples collected from different provinces in Turkey. Nat Prod Res 21:187-195.
Moujanni A, Terrab Benjelloun A, Eddoha R, Nasser B, Benbachir M (2017) Microbiological quality of moroccan labeled euphorbia resinifera honey. J Microbiol Biotechnol Food Sci 6:1188-1194.
Olaitan PB, Adeleke OE, Iyabo OO (2007) Honey: a reservoir for microorganisms and an inhibitory agent for microbes. Afr Health Sci 7:159-165.
Pucciarelli AB, Schapovaloff ME, Kummritz S, Señuk IA, Brumovsky LA, Dallagnol AM (2014) Microbiological and physicochemical analysis of Yateí (Tetragonisca Angustula) honey for assessing quality standards and commercialization. Rev Argent Microbiol 46:325-332.
Rozanska H, Osek J (2012) Effect of storage on microbiological quality of honey. B Vet I Pulawy 56:161-163.
Sherlock O, Dolan A, Athman R, Power A, Gethin G, Cowman S, Humphreys H (2010) Comparison of the antimicrobial activity of Ulmo honey from Chile and Manuka honey against methicillin-resistant Staphylococcus aureus, Escherichia coli and Pseudomonas aeruginosa. BMC Complement Altern Med 10:1-5.
Silva MS, Rabadzhiev Y, Eller MR, Iliev I, Ivanova I, Santana WC (2017) Microorganisms in honey. In V. De Alencar Arnaut De Toledo (Ed.), Honey analysis, IntechOpen, pp. 233-245.
Snowdon JA, Cliver DO (1996) Microorganisms in Honey. Int J Food Microbiol 31:1-26.
Soylu M, Silici S (2018) Üniversite öğrencilerinin bal tüketim tercihleri. J Hum Sci 15:386-398.
Stagos D, Soulitsiotis N, Tsadila C, Papaeconomou S, Arvanitis C, Ntontos A, Karkanta F, Adamou‑Androulaki S, Petrotos K, Spandidos D, Kouretas D, Mossialos M (2018) Antibacterial and antioxidant activity of different types of honey derived from Mount Olympus in Greece. Int J Mol Med 42:726-734.
TEPGE (2020) Aricilik. No: HU-01. https://arastirma.tarimorman.gov.tr/tepge/Menu/27/Tarim-Urunleri-Piyasalari [accessed 03 February 2020].
Tian B, Fadhil NH, Powell JE, Kwong WK, Moran NA (2012) Longterm exposure to antibiotics has caused accumulation of resistance determinants in the gut microbiota of honeybees. MBio 3:e00377-12.
Tonks AJ, Cooper RA, Jones KP, Blair S, Parton J, Tonks A (2003) Honey stimulates inflammatory cytokine production from monocytes. Cytokine 21:242-247.
TUİK (2016) Turkish Statistical Institute. http://www.tuik.gov.tr [accessed 11 May 2018]
Turkish Food Codex (2011) Communiqué on Microbiological Criteria. https://www.resmigazete.gov.tr/eskiler/2011/12/20111229M3-6.htm [accessed 12 October 2019].
Tysett C, Rosseau M (1981) Problem of microbes, hygiene of commercial honey. Rev Med Vet 132:591-600.
US FDA’s Bacteriological Analytical Manual (FDA/BAM) (2001) Staphylococcus aureus. https://www.fda.gov/food/laboratory-methods-food/bam-staphylococcus-aureus [accessed 21 October 2019].
US FDA’s Bacteriological Analytical Manual (FDA/BAM) (2002) Enumeration of Escherichia coli and the Coliform Bacteria. https://www.fda.gov/food/laboratory-methods-food/bam-4-enumeration-escherichia-coli-and-coliform-bacteria [accessed 21 October 2019].
Vazquez-Quiñones CR, Moreno-Terrazas R, Natividad-Bonifacio I, Quiñones-Ramírez EI, Vázquez-Salinas C (2018) Microbiological assessment of honey in México. Rev Argent Microbiol 50:75-80.
World Health Organization (WHO) (2016) Critically important antimicrobials for human medicine: ranking of antimicrobial agents for risk management of antimicrobial resistance due to non-human use. https://apps.who.int/iris/bitstream/handle/10665/255027/9789241512220-eng.pdf . [accessed 12 June 2019].
Artículos más leídos del mismo autor/a