Global prevalence of pathogens isolated from butter and cream samples derived from milk - a systematic review with meta-analysis

Authors

DOI:

https://doi.org/10.5433/1679-0359.2026v47n1p255

Keywords:

Butter, Fresh cream, Foodborne pathogens, Food safety.

Abstract

Microbiological contamination occurring in the milk production chain represents a significant challenge for public health, especially in dairy products such as butter and cream. In this context, and considering the socioeconomic and nutritional relevance of these foods, it is essential to understand the risks involved and to seek effective control strategies. This study is a systematic review with meta-analysis aimed at evaluating the prevalence of pathogenic microorganisms in butter and cream. The research involved five bibliographic databases and initially included 1,275 articles. After applying the exclusion criteria, 21 articles from countries such as Brazil, India, Egypt, Ireland, Turkey, the United Kingdom, and Sweden were included, encompassing regions in Africa, Asia, Europe, and South America. The PRISMA guidelines were used for data selection and analysis. The results highlighted the presence of Escherichia coli and species of Listeria, Staphylococcus, and Pseudomonas in both types of samples, in addition to specific isolates such as Klebsiella spp. in cream and Salmonella spp. in butter. Variability in isolation and confirmation methods was identified. The research showed that hygienic failures and inadequacies in transport and storage are critical factors associated with contamination. The findings reinforce the need for standardization of microbiological analysis methods and for more efficient surveillance strategies. The low representation of continents such as North America and Oceania points to important gaps in the literature. Thus, the implementation of public policies to minimize health risks is necessary, promoting the safety of widely consumed dairy products.

Downloads

Download data is not yet available.

Author Biographies

Giliel Rodrigues Leandro, Universidade Federal de Campina Grande

Ph.D. Student in the Graduate Program in Animal Science and Health, Universidade Federal de Campina Grande (UFCG), Patos, PB, Brazil.

Fernanda Araújo, Universidade Federal de Campina Grande

Ph.D. Student in the Graduate Program in Animal Science and Health, UFCG, Patos, PB, Brazil.

Mikaely Giordanno Medeiros de Araújo, Universidade Federal de Campina Grande

Ph.D. Student in the Graduate Program in Animal Science and Health, UFCG, Patos, PB, Brazil.

Clécio Henrique Limeira, Universidade Federal de Campina Grande

Ph.D., Higher Education Technician, UFCG, Patos, PB, Brazil.

Mônica Adriana Araújo de Souza, Universidade Federal de Campina Grande

Ph.D., Higher Education Technician, UFCG, Patos, PB, Brazil.

Rosália Severo de Medeiros, Universidade Federal de Campina Grande

Prof. Dr. in the Graduate Program in Animal Science, UFCG, Patos, PB, Brazil.

Sergio Santos Azevedo, Universidade Federal de Campina Grande

Prof. Dr. in the Graduate Program in Animal Science and Health, UFCG, Patos, PB, Brazil.

Carolina de Sousa Américo Batista Santos, Universidade Federal de Campina Grande

Prof. Dr. in the Graduate Program in Animal Science and Health, UFCG, Patos, PB, Brazil.

References

Attri, L. K., & Narang, H. H. (2014). Analysis of important dairy products: Isolation and characterization. Research Journal of Pharmaceutical, Biological and Chemical Sciences, 5(1), 698-706. doi: 10.5555/20143067760

Azwai, S. M., Lawila, A. F., Eshamah, H. L., Sherif, J. A., Farag, S. A., Naas, H. T., & Eldaghayes, I. M. (2024). Antimicrobial susceptibility profile of Klebsiella pneumoniae isolated from some dairy products in Libya as a foodborne pathogen. Veterinary World, 17(5), 1168-1176. doi: 10.14202/vetworld.2024.1168-1176

Balduzzi, S., Rücker, G., & Schwarzer, G. (2019). How to perform a meta-analysis with R: a practical tutorial. Evidence-Based Mental Health, 22(3), 153-160. doi: 10.1136/ebmental-2019-300117

Barrow, G. I., & Miller, D. C. (1967). A bacteriological study of fresh cream and cream products in Cornwall. Monthly Bulletin of the Ministry of Health, 26(1), 254-261. doi: 10.5555/19692702691

Berge, A. C., & Baars, T. (2020). Raw milk producers with high levels of hygiene and safety. Epidemiology & Infection, 148, e14. doi: 10.1017/S0950268820000060

Bradshaw, J. G., Peeler, J. T., Corwin, J. J., Hunt, J. M., & Twedt, R. M. (1987). Thermal resistance of Listeria monocytogenes in dairy products. Journal of Food Protection, 50(7), 543-545.

Cardak, A. D. (2013). Gross composition and the presence of Listeria monocytogenes and Salmonella spp. in raw milk and dairy products in Aydin, Turkey. Journal of Food, Agriculture and Environment, 11(3-4), 55-62. https://www.wflpublisher.com/Abstract/4602

Colenso, R., Court, G., & Henderson, R. J. (1966). Fresh cream in Worcestershire: a bacteriological study. Monthly Bulletin of the Ministry of Health and the Emergency Public Health Laboratory Service, 25(1), 153-161. doi: 10.5555/19682703352

De Klerk, J. N., & Robinson, P. A. (2022). Drivers and hazards of consumption of unpasteurised bovine milk and milk products in high-income countries. PeerJ, 10, e13426. doi: 10.7717/peerj.13426

Deeks, J. J., Higgins, J. P., & Altman, D. G. (2019). Analysing data and undertaking meta-analyses. In J. P. T. Higgins, J. Thomas, J. Chandler, M. Cumpston, T. Li, M. J. Page, & V. A. Welch (Eds.), Cochrane handbook for systematic reviews of interventions (pp. 241-284). John Wiley & Sons. doi: 10.1002/9781119536604.ch10

El Marrakchi, A., Hamama, A., & El Othmani, F. (1993). Occurrence of Listeria monocytogenes in milk and dairy products produced or imported into Morocco. Journal of Food Protection, 56(3), 256-259. doi: 10.4315/0362-028X-56.3.256

Food and Agriculture Organization (2023). FAOSTAT - Food balances 2023. FAO. https://www.fao.org/faostat/en/#data/FBS

Fotopoulou, E. T., Jenkins, C., Painset, A., & Amar, C. (2024). Listeria monocytogenes: the silent assassin. Journal of Medical Microbiology, 73(3), 001800. doi: 10.1099/jmm.0.001800

Frece, J., Markov, K., Čvek, D., Kolarec, K., & Delaš, F. (2010). Comparison of conventional and molecular methods for the routine confirmation of Listeria monocytogenes in milk products produced domestically in Croatia. Journal of Dairy Research, 77(1), 112-116. doi: 10.1017/S0022029909990379

Fusco, V., Chieffi, D., Fanelli, F., Logrieco, A. F., Cho, G. S., Kabisch, J., & Franz, C. M. (2020). Microbial quality and safety of milk and milk products in the 21st century. Comprehensive Reviews in Food Science and Food Safety, 19(4), 2013-2049. doi: 10.1111/1541-4337.12568

Gamal, H., El-Diasty, M., Dapgh, A., El-Sherbini, M., El-Baz, A., & Abdelkhalek, A. (2022). Virulence genes of multi-drug resistance Pseudomonas species isolated from milk and some dairy products. Journal of Advanced Veterinary Research, 12(4), 415-421. https://advetresearch.com/index.php/AVR/article/view/1037/696

Gerken, A., Coleman, J. C., & Winner, H. I. (1968). Bacteriological impurity of dairy-cream samples in London. The Lancet, 291(7543), 634. doi: 10.1016/S0140-6736(68)91252-X

Jenkins, H. R., & Henderson, R. J. (1969). The source of bacteria in fresh cream, and the methylene blue reduction test as a guide to hygienic quality. Epidemiology & Infection, 67(3), 401-408. doi: 10.1017/s0022172400041814

Kataria, D., & Singh, G. (2024). Health benefits of ghee: review of Ayurveda and modern science perspectives. Journal of Ayurveda and Integrative Medicine, 15(1), 100819. doi: 10.1016/j.jaim.2023.100819

Lanciotti, R., Massa, S., Guerzoni, M. E., & Di Fabio, G. (1992). Light butter: natural microbial population and potential growth of Listeria monocytogenes and Yersinia enterocolitica. Letters in Applied Microbiology, 15(6), 256-258. doi: 10.1111/j.1472-765X.1992.tb00777.x

Lindberg, A. M., Ljungh, Å., Ahrne, S., Löfdahl, S., & Molin, G. (1998). Enterobacteriaceae found in high numbers in fish, minced meat and pasteurised milk or cream and the presence of toxin encoding genes. International Journal of Food Microbiology, 39(1-2), 11-17. doi: 10.1016/S0168-1605(97)00104-9

McHugh, A. J., Feehily, C., Fenelon, M. A., Gleeson, D., Hill, C., & Cotter, P. D. (2020). Tracking the dairy microbiota from farm bulk tank to skimmed milk powder. mSystems, 5(2), e00120-20. doi: 10.1128/msystems.00226-20

McLauchlin, J., Aird, H., Elliott, A., Forester, E., Jørgensen, F., & Willis, C. (2020). Microbiological quality of raw drinking milk and unpasteurised dairy products: results from England 2013-2019. Epidemiology & Infection, 148, e135. doi: 10.1017/S0950268820001016

Medeiros, J. M. S. de, Câmpelo, M. C. S., & Silva, J. B. A. da. (2017). Good manufacturing practices of artisanal products in Northeastern Brazil. Food Control, 1(4), 103-108. doi: 10.26656/fr.2017.4.050

Meshref, A. M. S. (2010). Microbiological quality and safety of cooking butter in Beni-Suef governorate, Egypt. African Health Sciences, 10(2), 193-198. doi: 10.4314/ahs.v10i2.57147

Mogford, H. (1971). The hygiene and marketing of fresh cream as assessed by the methylene blue test. Epidemiology & Infection, 69(2), 155-170. doi: 10.1017/S0022172400021392

Mohan, M. S., O'Callaghan, T. F., Kelly, P., & Hogan, S. A. (2021). Milk fat: opportunities, challenges, and innovation. Critical Reviews in Food Science and Nutrition, 61(14), 2411-2443. doi: 10.1080/10408398.2020.1778631

N'Guessan, E., Godrie, T., De Laubier, J., Ringuet, M., & Sindic, M. (2015). A survey of bacteria found in Belgian dairy farm products. Biotechnologie, Agronomie, Société et Environnement, 19(4), 346-354. doi: 10.25518/1780-4507.12356

Organisation for Economic Co-operation and Development / Food and Agriculture Organization of the United Nations (2025). OECD-FAO Agricultural Outlook 2025-2034. OECD Publishing/FAO. https://doi.org/10.1787/601276cd-en

R Core Team (2019). R: a language and environment for statistical computing. R Foundation for Statistical Computing. https://www.r-project.org/

Rahimi, E., Sepehri, S., Dehkordi, F. S., Shaygan, S., & Momtaz, H. (2014). Prevalence of Yersinia species in traditional and commercial dairy products in Isfahan Province, Iran. Jundishapur Journal of Microbiology, 7(4), e9249. doi:10.5812/jjm.9249

Rios-Muñiz, D., Cerna-Cortes, J. F., Lopez-Saucedo, C., Angeles-Morales, E., Bobadilla-Del Valle, M., Ponce-De Leon, A., & Estrada-Garcia, T. (2022). Isolation of Staphylococcus aureus, uropathogenic Escherichia coli, and nontuberculous Mycobacteria strains from pasteurized cheeses and unpasteurized cream sold at traditional open markets in Mexico City. Journal of Food Protection, 85(12), 1848-1854. doi: 10.4315/JFP-22-168

Sagdic, O., Ozturk, I., Bayram, O., Kesmen, Z., & Yilmaz, M. T. (2010). Characterization of butter spoiling yeasts and their inhibition by some spices. Journal of Food Science, 75(9), M597-M603. doi: 10.1111/j.1750-3841.2010.01871.x

Silva Viana, I. P., Vieira, C. P., Rosario, I. L. S., Monteiro, N. B., Vieira, I. R. S., Conte, C. A., Jr., & Costa, M. P. (2024). Typhoid fever and non-typhoidal Salmonella outbreaks: a portrait of regional socioeconomic inequalities in Brazil. Current Microbiology, 81(2), 57. doi: 10.1007/s00284-023-03559-8

Sivakumar, M., Abass, G., Vivekanandhan, R., Singh, D. K., Bhilegaonkar, K., Kumar, S., & Dubal, Z. (2021). Extended-spectrum beta-lactamase (ESBL)-producing and multidrug-resistant Escherichia coli in street foods: a public health concern. Journal of Food Science and Technology, 58, 1247-1261. doi: 10.1007/s13197-020-04634-9

Talbot, J. C., Wauchob, D. W., Robertson, L., & Farrell, I. D. (1967). A milk-borne outbreak of food poisoning due to Salmonella paratyphi B. var. Java. Public Health, 81(4), 191-197. doi: 10.1016/s0033-3506(67)80185-9

Timlin, M., Brodkorb, A., O'Callaghan, T. F., Harbourne, N., Drouin, G., Pacheco-Pappenheim, S., & Hogan, S. A. (2024). Pasture feeding improves the nutritional, textural, and techno-functional characteristics of butter. Journal of Dairy Science, 107(8), 5376-5392. doi: 10.3168/jds.2023-24092

Tirloni, E., Stella, S., Celandroni, F., Mazzantini, D., Bernardi, C., & Ghelardi, E. (2022). Bacillus cereus in dairy products and production plants. Foods, 11(17), 2572. doi: 10.3390/foods11172572

World Health Organization (2015). WHO estimates of the global burden of foodborne diseases: foodborne disease burden epidemiology reference group 2007-2015. WHO. https://iris.who.int/handle/10665/199350

Yilma, Z., Loiseau, G., & Faye, B. (2007). Manufacturing efficiencies and microbial properties of butter and Ayib-Ethiopian cottage cheese. Livestock Research for Rural Development, 19(7), Artigo 88. https://pmc.ncbi.nlm.nih.gov/articles/PMC1700062/

Downloads

Published

2026-06-19

How to Cite

Leandro, G. R., Araújo, F., Araújo, M. G. M. de, Limeira, C. H., Souza, M. A. A. de, Medeiros, R. S. de, … Santos, C. de S. A. B. (2026). Global prevalence of pathogens isolated from butter and cream samples derived from milk - a systematic review with meta-analysis . Semina: Ciências Agrárias, 47(1), 255–274. https://doi.org/10.5433/1679-0359.2026v47n1p255

Issue

Section

Articles

Funding data