Morganella morganii growth in skipjack tuna under different storage conditions and histamine detection using TLC method

Pertumbuhan Morganella morganii pada cakalang dengan kondisi penyimpanan berbeda dan deteksi histamin metode TLC

Authors

  • Susana Endah Ratnawati Center for Seafood Security and Sustainability, Department of Fisheries, Faculty of Agriculture, Gadjah Mada University https://orcid.org/0000-0003-3874-8631
  • Lutfia Permata Sari Center for Seafood Security and Sustainability, Department of Fisheries, Faculty of Agriculture, Gadjah Mada University
  • Ahmad Awaludin Agustyar Department of Food Science and Technology, School of Agriculture and Biology, Shanghai Jiao Tong University
  • Indun Dewi Puspita Center for Seafood Security and Sustainability, Department of Fisheries, Faculty of Agriculture, Gadjah Mada University https://orcid.org/0000-0003-3637-6870

DOI:

https://doi.org/10.17844/4mms8195

Keywords:

growth rate, non-vacuum packaging, temperature, thin-layer chromatography, vacuum-packaging

Abstract

Morganella morganii, a strong histamine-producing bacterium (HPB), has been frequently detected in seafood, such as skipjack tuna. Temperature fluctuations and improper packaging have resulted in bacterial proliferation and histamine production. This study aimed to determine the effects of different packaging and temperature conditions on M. morganii growth and to examine histamine formation in skipjack tuna. A factorial design with two factors, namely packaging type (vacuum and non-vacuum) and storage temperature (4, 15, 30, and 40°C), was used in this study.  The bacterial growth model over time was analyzed using DMFit software. Histamine production was analyzed using thin-layer chromatography (TLC) combined with ImageJ program visualization. The results indicated that different temperatures significantly affected the bacterial growth rate (p < 0.05). The application of vacuum packaging at 4 °C retarded histamine formation in skipjack tuna cubes. The highest growth rate (0.2652 log CFU-1h-1) was observed in samples under non-vacuum packaging stored at 40 °C. M. morganii. At 15 °C, a 3 to 4 log increase was observed, starting from 3.2 to 7.5 (vacuum packaging) and from 5.8 to 8.3 log CFU-1 mL-1 (non-vacuum packaging) at the end. Nevertheless, the production of histamine in vacuum-packed samples stored at 15°C after days 3 and 4 of incubation were 446 ppm and 443.5 ppm, respectively. These findings highlight the importance of proper packaging of skipjack tuna using a cold chain system during storage. This study also confirmed the potential application of TLC for the detection of histidine and histamine.

References

Altafini, A., Roncada, P., Guerrini, A., Sonfack, G. M., Accurso, D., & Caprai, E. (2022). Development of histamine in fresh and canned tuna steaks stored under different experimental temperature conditions. Foods, 11(24), 4034 https://doi.org/10.3390/foods11244034

Alya’ainun, R., Fathoni, E. Y., & Puspita, I. D. (2021, July 28-29). The effect of pH on bacterial growth and histamine formation by Klebsiella pneumoniae CK02 and Raoultella ornithinolytica TN01 [conference session]. The 4th International Symposium on Marine and Fisheries Research, Yogyakarta, Indonesia. IOP Conference Series: Earth and Environmental Science, 919(1), 012039 https://doi.org/10.1088/1755-1315/919/1/012039

Bancalari, E., Bernini, V., Bottari, B., Neviani, E., & Gatti, M. (2016). Application of impedance microbiology for evaluating potential acidifying performances of starter lactic acid bacteria to employ in milk transformation. Frontiers in Microbiology, 7(1628), 1–11. https://doi.org/10.3389/fmicb.2016.01628

Barbosa, R. G., Gonzaga, L. V., Lodetti, E., Olivo, G., Costa, A. C. O., Aubourg, S. P., & Fett, R. (2018). Biogenic amines assessment during different stages of the canning process of skipjack tuna (Katsuwonus pelamis). International Journal of Food Science and Technology, 53(5), 1236–1245. https://doi.org/10.1111/ijfs.13703

Barria, C., Malecki, M., & Arraiano, C. M. (2013). Bacterial adaptation to cold. Microbiology, 159 (12), 2437–2443. https://doi.org/10.1099/mic.0.052209-0

Berggren, H., Tibblin, P., Yıldırım, Y., Broman, E., Larsson, P., Lundin, D., & Forsman, A. (2022). Fish skin microbiomes are highly variable among individuals and populations but not within individuals. Frontiers in Microbiology, 12, 1-13 https://doi.org/10.3389/fmicb.2021.767770

Bjornsdottir-Butler, K., Abraham, A., Harper, A., Dunlap, P. V., & Benner, R. A. (2018). Biogenic amine production by and phylogenetic analysis of 23 Photobacterium species. Journal of Food Protection, 81(8), 1264–1274. https://doi.org/10.4315/0362-028X.JFP-18-022

Brosnan, M. E., & Brosnan, J. T. (2020). Histidine metabolism and function. Journal of Nutrition, 150, 2570S-2575S. https://doi.org/10.1093/jn/nxaa079

Chakma, S., Rahman, M. A., Mali, S. K., Debnath, S., Hoque, M. S., & Siddik, M. A. B. (2022). Influence of frozen storage period on the biochemical, nutritional, and microbial quality of Skipjack tuna (Katsuwonus pelamis) collected from the Bay of Bengal coast of Bangladesh. Food Chemistry Advances, 1(100139), 1–7. https://doi.org/10.1016/j.focha.2022.100139

Chakraborty, K., Krishna Raola, V., Joy, M., & Makkar, F. (2017). Nutritional attributes in the fillet of skipjack tuna (Katsuwonus pelamis) from the Arabian Sea near the south-west coast of India. Journal of the Marine Biological Association of the United Kingdom, 97(2), 419–432. https://doi.org/10.1017/S0025315416000527

Cruz, R., Pereira, V., Pinho, T., Ferreira, I. M. P. L. V. O., Novais, C., & Casal, S. (2022). Safety and quality of canned sardines after opening: A shelf-stability study. Foods, 11(991), 1-16 https://doi.org/10.3390/foods11070991

Debeer, J., Bell, J. W., Nolte, F., Arcieri, J., & Correa, G. (2021). Histamine limits by country: A survey and review. Journal of Food Protection, 84(9), 1610–1628. https://doi.org/10.4315/JFP-21-129

Dityanawarman, A., Puspita, I. D., Ratnawati, S. E., Ekantari, N., & Tamplin, M. (2020). Growth rate and histamine production of Klebsiella sp. Ck02 isolated from skipjack tuna compared with Morganella morganii ATCC 25830 at various incubation temperatures. Squalen Bulletin of Marine and Fisheries Postharvest and Biotechnology, 15(1), 1–9. https://doi.org/10.15578/squalen.v15i1.441

Emborg, J., & Dalgaard, P. (2008). Growth, inactivation and histamine formation of Morganella psychrotolerans and Morganella morganii — development and evaluation of predictive models. International Journal of Food Microbiology, 128, 234–243. https://doi.org/10.1016/j.ijfoodmi

Enache, E., Kataoka, A., Glenn Black, D., Weddig, L., Hayman, M., & Bjornsdottir-Butler, K. (2013). Heat resistance of histamine-producing bacteria in irradiated tuna loins. Journal of Food Protection, 76(9), 1608–1614. https://doi.org/10.4315/0362-028X.JFP-12-467

European Food Safety Authority. (2015). Scientifica and technical assistance on the evaluation of the temperature to be applied to pre-packed fishery products at retail level. Scientific Report of EFSA, 13(7), 1–48.

Food and Drug Administration. (2024). Sec. 540.525 Scombrotoxin (histamine)-forming fish and fishery Products-decomposition and histamine (CPG 7108.24) compliance policy guide: guidance for FDA Staff. https://www.fda.gov/inspections-compliance-enforcement-and-criminal-investigations/compliance-

Guizani, N., Al-Busaidy, M. A., Al-Belushi, I. M., Mothershaw, A., & Rahman, M. S. (2005). The effect of storage temperature on histamine production and the freshness of yellowfin tuna (Thunnus albacares). Food Research International, 38(2), 215–222. https://doi.org/10.1016/j.foodres.2004.09.011

Huang, X., Wang, H., & Tu, Z. (2023). A comprehensive review of the control and utilization of aquatic animal products by autolysis-based processes: Mechanism, process, factors, and application. Food Research International, 164, 112325 https://doi.org/10.1016/j.foodres.2022.112325

Lee, Y. C., Chen, Y. F., Huang, Y. L., Kung, H. F., Chen, T. Y., & Tsai, Y. H. (2016). Hygienic quality, adulteration of pork and histamine production by Raoultella ornithinolytica in milkfish dumpling. Journal of Food and Drug Analysis, 24(4), 762–770. https://doi.org/10.1016/j.jfda.2016.04.005

Lee, Y. C., Hsieh, C. Y., Chen, M. L., Wang, C. Y., Lin, C. Saint, & Tsai, Y. H. (2020a). High-pressure inactivation of histamine-forming bacteria Morganella morganii and Photobacterium phosphoreum. Journal of Food Protection, 83(4), 621–627. https://doi.org/10.4315/0362-028X.JFP-19-267

Lee, Y. C., Tseng, P. H., Hwang, C. C., Kung, H. F., Huang, Y. L., Lin, C. Saint, Wei, C. I., & Tsai, Y. H. (2019a). Effect of vacuum packaging on histamine production in Japanese Spanish mackerel (Scomberomorus niphonius) stored at various temperatures. Journal of Food Protection, 82(11), 1931–1937. https://doi.org/10.4315/0362-028X.JFP-19-143

Ma, J. X., Liu, P., Wang, Y. X., Ren, X., Zhang, R., & Li, L. W. (2023). A histidine-rich fusion tag enables real-time monitoring of recombinant protein expression by Pauly reaction-based colorimetric assay. Biochemical and Biophysical Research Communications, 666, 128–136. https://doi.org/10.1016/j.bbrc.2023.05.004

Margareta, G., Ratnawati, S. E., & Puspita, I. D. (2020, February 2020). Growth Rate and Histamine Production of Citrobacter freundii CK01 in Various Incubation Temperatures. The 3rd International Symposium on Marine and Fisheries Research, Yogyakarta, Indonesia. E3S Web of Conferences, 147, 03018 https://doi.org/10.1051/e3sconf/202014703018

Matějková, K., Křížek, M., Vácha, F., & Dadáková, E. (2013). Effect of high-pressure treatment on biogenic amines formation in vacuum-packed trout flesh (Oncorhynchus mykiss). Food Chemistry, 137(1–4), 31–36. https://doi.org/10.1016/j.foodchem.2012.10.011

Mentang, F., Montolalu, R. I., Dien, H. A., Meko, A., & Berhimpon, S. (2022). Shelf life and presence of pathogens in liquid-smoked Skipjack pampis packed in vacuum packaging (VP), modified atmosphere packaging (MAP), and stored at ambient temperature. Nutricion Clinica y Dietetica Hospitalaria, 42(4), 73–78. https://doi.org/10.12873/424mentang

Mohamed, W. A., Hassanen, E. I., Mansour, H. A., & Mahmoud, M. A. (2022). Bacteria forming histamine and shelf life of sardine (Sardina pilchardus) at different temperatures and storage times with an emphasis on histopathological changes in the skeletal musculature. Egyptian Journal of Aquatic Biology & Fisheries, 26(5), 345–360. www.ejabf.journals.ekb.eg

Nei, D. (2014). Evaluation of non-bacterial factors contributing to histamine accumulation in fish fillets. Food Control, 35(1), 142–145. https://doi.org/10.1016/j.foodcont.2013.06.037

Nurilmala, M., & Ochiai, Y. (2016). Molecular characterization of southern bluefin tuna myoglobin (Thunnus maccoyii). Fish Physiology and Biochemistry, 42(5), 1407–1416. https://doi.org/10.1007/s10695-016-0228-0

Nurilmala, M., Ushio, H., & Ochiai, Y. (2018). pH- and temperature-dependent denaturation profiles of tuna myoglobin. Fisheries Science, 84(3), 579–587. https://doi.org/10.1007/s12562-018-1198-1

Oktariani, A. F., Ramona, Y., Sudaryatma, P. E., Dewi, I. A. M. M., & Shetty, K. (2022). Role of marine bacterial contaminants in histamine formation in seafood products: A Review. In Microorganisms, 10 (6), 11197 https://doi.org/10.3390/microorganisms10061197

Patil, A. R., Chogale, N. D., Pagarkar, A. U., Koli, J. M., Bhosale, B. P., Sharangdhar, S. T., Gaikwad, B. V, & Kulkarni, G. N. (2020). Vacuum packaging is a tool for shelf life extension of fish product : a review. Article in Journal of Experimental Zoology, 23, 807–810. https://www.researchgate.net/publication/339842514

Powell, S. M., Ratkowsky, D. A., & Tamplin, M. L. (2015). Predictive model for the growth of spoilage bacteria on modified atmosphere packaged Atlantic salmon produced in Australia. Food Microbiology, 47, 111–115. https://doi.org/10.1016/j.fm.2014.12.001

Rachmawati, N., Ariyani, F., Triwibowo, R., Januar, H. I., Dwiyitno, D., Yennie, Y., Kusmarwati, A., & Poernomo, A. (2024). Exposure assessment and semi-quantitative risk analysis of histamine in tuna and tuna-like fish from Indonesia. Food Additives and Contaminants - Part A, 41(11), 1498–1508. https://doi.org/10.1080/19440049.2024.2396971

Rachmawati, N., Powell, S. M., Triwibowo, R., Nichols, D. S., Ross, T., & Tamplin, M. L. (2022). Modelling growth and histamine formation of Klebsiella aerogenes TI24 isolated from Indonesian pindang. International Journal of Food Microbiology, 362(109459), 1–9. https://doi.org/10.1016/j.ijfoodmicro.2021.109459

Rachmawati, N., & Triwibowo, R. (2022, 25 March 2022). Histamine Fish Poisoning (HFP) in Indonesia: Current status and challenges. International Food Conference, Surabaya, Indonesia. E3S Web of Conferences, 344, 05001 https://doi.org/10.1051/e3sconf/202234405001

Rahmani, J., Miri, A. L. I., Mohseni-Bandpei, A., Fakhri, Y., Bjørklund, G., Keramati, H., Moradi, B., Amanidaz, N., Shariatifar, N., & Khaneghah, A. M. (2018). Contamination and prevalence of histamine in canned tuna from Iran: A systematic review, meta-analysis, and health risk assessment. Journal of Food Protection, 81(12), 2019–2027. https://doi.org/10.4315/0362-028X.JFP-18-301

Ratnawati, S. E., Kuuliala, L., Walgraeve, C., Demeestere, K., Ragaert, P., & Devlieghere, F. (2023). The effect of high oxygen modified atmospheres on the quality degradation of packed live blue mussels (Mytilus edulis). LWT, 177, 104047 https://doi.org/10.1016/j.lwt.2023.114537

Ryser, L. T., Arias-Roth, E., Perreten, V., Irmler, S., & Bruggmann, R. (2021). Genetic and phenotypic diversity of Morganella morganii isolated from cheese. Frontiers in Microbiology, 12, 1-11 https://doi.org/10.3389/fmicb.2021.738492

Schirone, M., Visciano, P., Tofalo, R., & Suzzi, G. (2017). Histamine food poisoning. In Handbook of Experimental Pharmacology 241, 217–235. Springer New York LLC. https://doi.org/10.1007/164_2016_54

Sheng, M., Frurip, D., & Gorman, D. (2015). Reactive chemical hazards of diazonium salts. Journal of Loss Prevention in the Process Industries, 38, 114–118. https://doi.org/10.1016/j.jlp.2015.09.004

Tamasi, J., Balla, Z., Csuka, D., Kalabay, L., & Farkas, H. (2022). The missing link: A case of severe adverse reaction to histamine in food and beverages. American Journal of Case Reports, 23(1), 1-7 https://doi.org/10.12659/AJCR.934212

Tao, Z., Sato, M., Han, Y., Tan, Z., Yamaguchi, T., & Nakano, T. (2011). A simple and rapid method for histamine analysis in fish and fishery products by TLC determination. Food Control, 22(8), 1154–1157. https://doi.org/10.1016/j.foodcont.2010.12.014

Tao, Z., Wu, X., Liu, W., Takahashi, H., Xie, S., Ohshima, C., & He, Q. (2022a). Prevalence of histamine-forming vacteria in two kinds of salted fish at town markets of Guangdong Province of South China. Journal of Food Protection, 85(6), 956–960. https://doi.org/10.4315/JFP-21-215

Velut, G., Delon, F., Mérigaud, J. P., Tong, C., Duflos, G., Boissan, F., Watier-Grillot, S., Boni, M., Derkenne, C., Dia, A., Texier, G., Vest, P., Meynard, J. B., Fournier, P. E., Chesnay, A., & De Santi, V. P. (2019). Histamine food poisoning: A sudden, large outbreak linked to fresh yellowfin tuna from Reunion Island, France, April 2017. Eurosurveillance, 24(22), 1-8 https://doi.org/10.2807/1560-7917.ES.2019.24.22.1800405

Wang, D., Yamaki, S., Kawai, Y., & Yamazaki, K. (2020). Histamine production behaviors of a psychrotolerant histamine-producer, Morganella psychrotolerans, in various environmental conditions. Current Microbiology, 77(3), 460–467. https://doi.org/10.1007/s00284-019-01853-y

Wongsariya, K., Bunyapraphatsara, N., Yasawong, M., & Chomnawang, M. T. (2016). Development of molecular approach based on PCR assay for detection of histamine producing bacteria. Journal of Food Science and Technology, 53(1), 640–648. https://doi.org/10.1007/s13197-015-1982-1

Yoshikawa, T., Nakamura, T., Shibakusa, T., Sugita, M., Naganuma, F., Iida, T., Miura, Y., Mohsen, A., Harada, R., & Yanai, K. (2014). Insufficient intake of L-histidine reduces brain histamine and causes anxiety-like behaviors in male mice. Journal of Nutrition, 144(10), 1637–1641. https://doi.org/10.3945/jn.114.196105

Yu, H., Zhuang, D., Hu, X., Zhang, S., He, Z., Zeng, M., Fang, X., Chen, J., & Chen, X. (2018). Rapid determination of histamine in fish by thin-layer chromatography-image analysis method using diazotized visualization reagent prepared with: P-nitroaniline. Analytical Methods, 10(27), 3386–3392. https://doi.org/10.1039/c8ay00336j

Zhang, B., Deng, S. gui, Gao, M., & Chen, J. (2015). Effect of slurry ice on the functional properties of proteins related to quality loss during skipjack tuna (Katsuwonus pelamis) chilled storage. Journal of Food Science, 80(4), C695–C702. https://doi.org/10.1111/1750-3841.12812

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Published

2025-12-03

How to Cite

Ratnawati, S. E., Sari, L. P. ., Agustyar, A. A. ., & Puspita, I. D. . (2025). Morganella morganii growth in skipjack tuna under different storage conditions and histamine detection using TLC method: Pertumbuhan Morganella morganii pada cakalang dengan kondisi penyimpanan berbeda dan deteksi histamin metode TLC. Jurnal Pengolahan Hasil Perikanan Indonesia, 28(11). https://doi.org/10.17844/4mms8195