PERTANIKA JOURNAL OF TROPICAL AGRICULTURAL SCIENCE

 

e-ISSN 2231-8542
ISSN 1511-3701

Home / Regular Issue / JTAS Vol. 46 (3) Aug. 2023 / JTAS-2657-2022

 

Pathogenic Bacterial Communities Isolated and Identified in Stingless Bee (Kelulut) Honey from Selected Farms in Terengganu

Noor Aimi Shazana Mohd Yusoff, Fisal Ahmad, Amir Izzwan Zamri, Samsul Bahri Abdul Razak, Muhammad Fauzi Mahmud and Tuan Zainazor Tuan Chilek

Pertanika Journal of Tropical Agricultural Science, Volume 46, Issue 3, August 2023

DOI: https://doi.org/10.47836/pjtas.46.3.08

Keywords: Food handlers, foodborne illness, kelulut, pathogenic bacteria, stingless bee honey

Published on: 30 August 2023

In Malaysia, stingless bees can be categorised into two genera: Melipona and Trigona, known as “Kelulut”. The high demand for Kelulut honey boosts the production of the honey industry. Previous studies reported that stingless bee (Kelulut) honey and its products were contaminated with pathogenic bacteria during harvesting and processing. This research aims to isolate and identify the pathogenic bacteria in Kelulut honey. Forty-eight samples of Kelulut honey (open and closed pot) and propolis were obtained from selected farms in Terengganu by focusing on a major stingless bee species available in Malaysia, Heterotrigona itama. In addition, the swabbing technique was done on the wooden beehive of the Kelulut to evaluate the environmental contamination. The pathogenic bacteria were isolated using specifically selected agar, such as Bacillus cereus agar (for B. cereus), Baird-Parker agar (for Staphylococcus aureus), and MacConkey agar (for other pathogenic bacteria), which were confirmed through a biochemical test. All samples were analysed, and the results showed that B. cereus (7/48), Pseudomonas aeruginosa (10/48), Pantoea spp. (11/48), Serratia plymuthica (6/48), and S. aureus (9/48) were obtained in the samples. This study indicates that Kelulut honey was contaminated with B. cereus, P. aeruginosa, Pantoea spp., S. plymuthica, and S. aureus. Isolated pathogenic bacteria may exist in the Kelulut honey through food handlers, utensils, and the environment. Hence, the stakeholders should strictly follow good standard operating procedures and guidelines by the Kelulut honey industry to prevent foodborne illness.

  • Adadi, P., & Obeng, A. K. (2017). Assessment of bacterial quality of honey produced in Tamale metropolis (Ghana). Journal of Food and Drug Analysis, 25(2), 369–373. https://doi.org/10.1016/j.jfda.2016.07.005

  • Akkaya, H., Bayrakal, G. M., & Dumen, E. (2020). Investigation of propolis in terms of hygienic quality, some pathogenic bacteria and Nosema spp. Turkish Journal of Veterinary and Animal Science, 44(4), 838-844. https://doi.org/10.3906/vet-2001-20

  • Amin, F. A. Z., Sabri, S., Ismail, M., Chan, K. W., Ismail, N., Esa, N. M., Lila, M. A. M., & Zawawi, N. (2020). Probiotic properties of Bacillus strains isolated from stingless bee (Heterotrigona itama) honey collected across Malaysia. International Journal of Environmental Research and Public Health, 17(1), 278. https://doi.org/10.3390%2Fijerph17010278

  • Andrews, W. H., & Hammack, T. S. (2022). BAM Chapter 1: Food sampling/Preparation of sample homogenate. U. S. Food and Drug Administration. https://www.fda.gov/food/laboratory-methods-food/bam-chapter-1-food-samplingpreparation-sample-homogenate

  • Ashgar, S. S., & El-Said, H. M. (2012). Pathogenic bacteria associated with different public environmental sites in Mecca city. Open Journal Medical Microbiology, 2(4), 133–137. https://doi.org/10.4236/ojmm.2012.24020

  • Augustin, J. C., Kooh, P., Bayeux, T., Guillier, L., Meyer, T., Jourdan-Da Silva, N., Villena, I., Sanaa, M., Cerf, O., & On Behalf of the Anses Working Group on Consumer Information on Foodborne Biological Risks (2020). Contribution of foods and poor food-handling practices to the burden of foodborne infectious diseases in France. Foods, 9(11), 1644. https://doi.org/10.3390/foods9111644

  • Avashia, S. B., Riggins, W. S., Lindley, C., Hoffmaster, A., Drumgoole, R., & Nekomoto, T. (2007). Fatal pneumonia among metalworkers due to inhalation exposure to Bacillus cereus containing Bacillus anthracis toxin genes. Clinical Infection Disease, 44(3), 414–416. https://doi.org/10.1086/510429

  • Bakar, M. F. A, Sanusi, S. B., Bakar, F. I. A, Cong, O. J., & Mian, Z. (2017). Physicochemical and antioxidant potential of raw unprocessed honey from Malaysian stingless bees. Pakistan Journal of Nutrition, 16(11), 888–894. https://doi.org/10.3923/pjn.2017.888.894

  • Boorn, K. L., Khor, Y.-Y., Sweetman, E., Tan, F., Heard, T. A., & Hammer, K. A. (2010). Antimicrobial activity of honey from the stingless bee Trigona carbonaria determined by agar diffusion, agar dilution, broth microdilution and time-kill methodology. Journal of Applied Microbiology, 108(5), 1534–1543. https://doi.org/10.1111/j.1365-2672.2009.04552.x

  • Cavicchioli, R., Ripple, W. J., Timmis, K. N., Azam, F., Bakken, L. R., Bayliss, M., Bahrenfeld, M. J., Boetius, A., Boyd, P. W., Classen, A. T, Crowther, T. W., Danovaro, R., Foreman, C. M., Huisman, J., Hutchins, D. A., Jansson, J. K., Karl, D. M., Koskella, B., Welch, D. B. M., … Webster, N. S. (2019). Scientists’ warning to humanity: Microorganisms and climate change. Nature Review Microbiology, 17, 569–586. https://doi.org/10.1038/s41579-019-0222-5

  • Colombari, V., Mayer, M. D. B., & Laicini, Z. M. (2007). Foodborne outbreak caused by Staphylococcus aureus: Phenotypic and genotypic characterization of strains of food and human sources. Journal of Food Protection, 70(2), 489–493. https://doi.org/10.4315/0362-028x-70.2.489

  • Dinges, M. M., Orwin, P. M., & Schlievert, P. M. (2000). Exotoxins of Staphylococcus aureus. Clinical Microbiology Review, 13(1), 16–34. https://doi.org/10.1128/cmr.13.1.16

  • Engelhart, S., Saborowski, F., Krakau, M., Scherholz-Schlösser, G., Heyer, I., & Exner, M. (2003). Severe Serratia liquefaciens sepsis following vitamin C infusion treatment by a naturopathic practitioner. Journal of Clinical Microbiology, 41(8), 3986–3988. https://doi.org/10.1128/jcm.41.8.3986-3988.2003

  • Erkan, M. E., Vural, A., Guran, H. S., & Durmusoglu, H. (2017). Microbiological investigation of honey collected from Şırnak province of Turkey. Journal of the Hellenic Veterinary Medical Society, 66(1), 22-26. https://doi.org/10.12681/jhvms.15579

  • Feng, P. C. S., & Hartman, P. A. (1982). Fluorogenic assays for immediate confirmation of Escherichia coli. Applied and Environmental Microbiology, 43(6), 1320-1329. https://doi.org/10.1128/aem.43.6.1320-1329.1982

  • Gaur, A. H., Patrick, C. C., McCullers, J. A., Flynn, P. M., Pearson, T. A., & Razzouk, B. I. (2001). Bacillus cereus bacteremia and meningitis in immunocompromised children. Clinical Infection Disease, 32(10), 1456–1462. https://doi.org/10.1086/320154

  • Hongu, N., Suzuki, A., Alcance, K. A. A., & Martinez, C. L. (2017). Is honey the same as sugar? https://extension.arizona.edu/sites/extension.arizona.edu/files/pubs/az1577-2017.pdf

  • Jalil, M. A. A., Kasmuri, A. R., & Hadi, H. (2017). Stingless bee honey, the natural wound healer: A review. Skin Pharmacology and Physiology, 30(2), 66-75. https://doi.org/10.1159/000458416

  • Kordiyeh, H. (2018). How do rodents play role in transmission of foodborne diseases? Nutrition and Food Science International Journal, 6(2), 555683. https://doi.org/10.19080/NFSIJ.2018.06.555683

  • Leber, A. L. (Ed.) (2016). Biochemical tests for the identification of aerobic bacteria. In Clinical microbiology procedures handbook (Vol. 1-3, 4th ed.). American Society for Microbiology. https://doi.org/10.1128/9781555818814.ch3.17.1

  • Loir, L. Y., Baron, F., & Gautier, M. (2003). Staphylococcus aureus and food poisoning. Genetics and Molecular Research, 2(1), 63-76.

  • Ngalimat, M. S., Rahman, R. N. Z. R. A, Yusof, M. T., Syahir, A., & Sabri, S. (2019). Characterisation of bacteria isolated from the stingless bee, Heterotrigona itama honey, bee bread and propolis. PeerJ, 7, e7478. https://doi.org/10.7717/peerj.7478

  • Ngalimat, M. S., Rahman, R. N. Z. R. A., Yusof, M. T., Hamzah, A. S. A., Zawawi, N., & Sabri, S. (2020). A review on the association of bacteria with stingless bees. Sains Malaysiana, 49(8), 1853-1863. https://doi.org/10.17576/jsm-2020-4908-08

  • Pandey, P. K., Kass, P. H., Soupir, M. L., Biswas, S., & Singh, V. P. (2014). Contamination of water resources by pathogenic bacteria. AMB Express, 4, 51. https://doi.org/10.1186/s13568-014-0051-x

  • Pucciarelli, A. S., Schapovaloff, M. E., Kummritz, S., Señuk, I. A., Brumovsky, L. A., & Dallagnol, A. M. (2014). Microbiological and physicochemical analysis of yateí (Tetragonisca angustula) honey for assessing quality standards and commercialization. Revista Argentina de Microbiología, 46(4), 325-332. https://doi.org/10.1016/S0325-7541(14)70091-4

  • Putri, M. S., & Susanna, D. (2021). Food safety knowledge, attitudes, and practices of food handlers at kitchen premises in the port ‘X’ area, North Jakarta, Indonesia 2018. Italian Journal of Food Safety, 10(4), 9215. https://doi.org/10.4081/ijfs.2021.9215

  • Rivera-Gomis, J., Bubnic, J., Ribarits, A., Moosbeckhofer, R., Alber, O., Kozmus, P., Jannoni-Sebastianini, R., Haefeker, W., Köglberger, H., Smodis Skerl, M. I., Tiozzo, B., Pietropaoli, M., Lubroth, J., Raizman, E., Lietaer, C., Zilli, R., Eggenhoeffner, R., Higes, M., Muz, M. N., … Formato, G. (2019). Good farming practices in apiculture. Revue Scientifique et Technique, 38(3), 879–890. https://doi.org/10.20506/rst.38.3.3032

  • Salatino, A., Pereira, L. R. L., & Salatino, M. L. F. (2019). The emerging market of propolis of stingless bees in tropical countries. MOJ Food Processing and Technology, 7(1), 27-29. https://doi.org/10.15406/mojfpt.2019.07.00215

  • Sanders, E. R. (2012). Aseptic laboratory techniques: Plating methods. Journal of Visualized Experiments, (63), e3064. https://doi.org/10.3791/3064

  • Shamsudin, S., Selamat, J., Sanny, M., Razak, S.-B. A., Jambari, N. N., Mian, Z., & Khatib, A. (2019). Influence of origins and bee species on physicochemical, antioxidant properties and botanical discrimination of stingless bee honey. International Journal of Food Properties, 22(1), 239-264. https://doi.org/10.1080/10942912.2019.1576730

  • Tiemersma, E. W., Bronzwaer, S. L. A. M., Lyytikäinen, O., Degner, J. E., Schrijnemakers, P., Bruinsma, N., Monen, J., Witte, W., & Grundmann, H. (2004). Methicillin-resistant Staphylococcus aureus in Europe, 1999-2002. Emerging Infectious Disease, 10(9), 1627-1634.

  • Willes, C., Nye, K., Aird, H., Lamph, D., & Fox, A. (2013). Examining food, water and environmental samples from healthcare environments. Public Health England. https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/865369/Hospital_F_W_E_Microbiology_Guidelines_Issue_3_February_2020__1_.pdf

  • Wu, Y.-M., Hsu, P.-C., Yang, C.-C., Chang, H.-J., Ye, J.-J., Huang, C.-T., & Lee, M.-H. (2013). Serratia marcescens meningitis: Epidemiology, prognostic factors and treatment outcomes. Journal Microbiology Immunological Infection, 46(4), 259-265. https://doi.org/10.1016/j.jmii.2012.07.006

  • Yaacob, S. N. S., Huyop, F., Ibrahim, R. K. R., & Wahab, R. A. (2018). Identification of Lactobacillus spp. and Fructobacillus spp. isolated from fresh Heterotrigona itama honey and their antagonistic activities against clinical pathogenic bacteria. Journal of Apicultural Research, 57(3), 395-405. https://doi.org/10.1080/00218839.2018.1428047

ISSN 1511-3701

e-ISSN 2231-8542

Article ID

JTAS-2657-2022

Download Full Article PDF

Share this article

Related Articles