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Bacteriological quality and antimicrobial resistance of Staphylococcus spp. and Escherichia coli isolated from organic and conventional fresh cheese

Abstract

One of the appeals of the rising organic market is the guarantee of offering healthier foods with less impact on the environment, from a more sustainable production method. Dairy market is one of the most popular in the sector but studies on organic dairy products safety are still scarce. The objective of this study was to evaluate the microbiological quality of organic and conventional Minas Frescal cheese samples, and the antimicrobial sensitivity of isolated strains of Escherichia coli and coagulase-positive Staphylococcus to different antimicrobials. Listeria spp. and Salmonella spp. was not detected in any of the samples analyzed. Regarding coagulase-positive Staphylococcus, 70% showed higher counts than that is established by Brazilian legislation, but with no significant difference between the systems. In the determination of the Most Probable Number of E. coli was observed significant difference between the systems, with a higher contamination index in cheeses derived from the organic system. All strains isolated showed 100% resistance to β-lactams and both in the conventional and organic systems were observed multiple resistance characteristics. Considering the similarity of the results obtained, it is necessary to analyze other parameters such as production system, herd health and good manufacturing practices to compare deeply both systems.

Keywords:
organic dairy; foodborne pathogens; antimicrobials; multiple resistance

1 Introduction

The trend towards healthy eating has had a major impact on food production, generally linked to concerns about animal welfare and environmental issues. This aspect is considered to increase the demand for organic foods, seen as healthier and with less impact on the environment, coming from a more sustainable production method than the conventional one (de-Magistris & Gracia, 2016de-Magistris, T., & Gracia, A. (2016). Consumers’ willingness to pay for light, organic and PDO cheese: An experimental auction approach. British Food Journal, 118(3), 560-571. http://dx.doi.org/10.1108/BFJ-09-2015-0322.
http://dx.doi.org/10.1108/BFJ-09-2015-03...
).

In the organic market, milk and dairy products are considered to represent the second largest share, behind only of the largest of them, the fruit and vegetable sector (Research Institute of Organic Agriculture, 2018Research Institute of Organic Agriculture - FiBL, & Organic International - IFOAM. (2018). The World of Organic Agriculture: Statistics & Emerging Trends 2018. Retrieved from https://www.organic-world.net/yearbook/yearbook-2018.html
https://www.organic-world.net/yearbook/y...
). Organic-certified foods occupy the “premium” food market segment, targeting consumers willing to pay higher prices for selected products, considered to be of better quality and safety (Heckman, 2019Heckman, J. R. (2019). Securing fresh food from fertile soil, challenges to the organic and raw milk movements. Renewable Agriculture and Food Systems, 34(5), 472-485. http://dx.doi.org/10.1017/S1742170517000618.
http://dx.doi.org/10.1017/S1742170517000...
).

Significantly higher prices are justified not only by the market rising but also by the higher production cost when compared to the conventional system (Badruddoza et al., 2022Badruddoza, S., Carlson, A. C., & McCluskey, J. J. (2022). Long‐term dynamics of US organic milk, eggs, and yogurt premiums. Agribusiness, 38(1), 45-72. http://dx.doi.org/10.1002/agr.21723.
http://dx.doi.org/10.1002/agr.21723...
). Although the requirements for the certification of an organic product vary according to the regulatory agency of each country, the requirements commonly demanded are expensive and require specialized labor (Rotz et al., 2007Rotz, C. A., Kamphuis, G. H., Karsten, H. D., & Weaver, R. D. (2007). Organic dairy production systems in Pennsylvania: a case study evaluation. Journal of Dairy Science, 90(8), 3961-3979. http://dx.doi.org/10.3168/jds.2006-527. PMid:17639008.
http://dx.doi.org/10.3168/jds.2006-527...
).

Among the cheeses widely spread in Brazil, Minas Frescal cheese stands out as the third most consumed. As the name classifies, it is a fresh, curdled, unripened, of very high moisture and semi-fat cheese (Brasil, 2004Brasil. Ministério da Agricultura, Pecuária e Abastecimento. (2004). Regulamento técnico para fixação de identidade e qualidade do queijo Minas Frescal (Instrução Normativa n° 4, de 01 de março de 2004). Diário Oficial [da] República Federativa do Brasil.; Empresa Brasileira de Pesquisa Agropecuária, 2019Empresa Brasileira de Pesquisa Agropecuária - EMBRAPA. (2019). Anuário Leite 2019: novos produtos e novas estratégias da cadeia do leite para ganhar competitividade e conquistar os clientes finais. Retrieved from https://www.infoteca.cnptia.embrapa.br/handle/doc/1109959
https://www.infoteca.cnptia.embrapa.br/h...
). Such features provide a favorable growth environment for contaminants, mainly bacterial pathogens (Delorme et al., 2020Delorme, M. M., Guimarães, J. T., Coutinho, N. M., Balthazar, C. F., Rocha, R. S., Silva, R., Margalho, L. P., Pimentel, T. C., Silva, M. C., Freitas, M. Q., Granato, D., Sant’Ana, A. S., Duart, M. C. K. H., & Cruz, A. G. (2020). Ultraviolet radiation: An interesting technology to preserve quality and safety of milk and dairy foods. Trends in Food Science & Technology, 102, 146-154. http://dx.doi.org/10.1016/j.tifs.2020.06.001.
http://dx.doi.org/10.1016/j.tifs.2020.06...
).

The main pathogens isolated from cheeses are Escherichia coli, Staphylococcus spp., Salmonella spp. and Listeria monocytogenes, commonly related to foodborne disease outbreaks worldwide, considered to be one of the main threats to public health (Chavez-Martinez et al., 2019Chavez-Martinez, A., Paredes-Montoya, P., Renteria-Monterrubio, A. L., Corral-Luna, A., Lechuga-Valles, R., Dominguez-Viveros, J., Sánchez-Vega, R., & Santellano-Estrada, E. (2019). Microbial quality and prevalence of foodborne pathogens of cheeses commercialized at different retail points in Mexico. Food Science and Technology (Campinas), 39(suppl 2), 703-710. http://dx.doi.org/10.1590/fst.30618.
http://dx.doi.org/10.1590/fst.30618...
; Lee & Yoon, 2021Lee, H., & Yoon, Y. (2021). Etiological agents implicated in foodborne illness worldwide. Food Science of Animal Resources, 41(1), 1-7. http://dx.doi.org/10.5851/kosfa.2020.e75. PMid:33506212.
http://dx.doi.org/10.5851/kosfa.2020.e75...
). Linked to this, the emergence of multidrug-resistant strains caused by the indiscriminate use of antimicrobials increases the difficulty of clinical treatment of these manifestations (Ge et al., 2022Ge, H., Wang, Y., & Zhao, X. (2022). Research on the drug resistance mechanism of foodborne pathogens. Microbial Pathogenesis, 162, 105306. http://dx.doi.org/10.1016/j.micpath.2021.105306. PMid:34822970.
http://dx.doi.org/10.1016/j.micpath.2021...
).

In conventional animal production, antibiotics are used for therapeutic or prophylactic purposes for diseases that impact animal health and production volume, but when misused, they can be harmful for both the environment and consumers health (Jayarao et al., 2019Jayarao, B., Almeida, R., & Oliver, S. P. (2019). Antimicrobial resistance on dairy farms. Foodborne Pathogens and Disease, 16(1), 1-4. http://dx.doi.org/10.1089/fpd.2019.29011.edi. PMid:30673352.
http://dx.doi.org/10.1089/fpd.2019.29011...
; Sharma et al., 2018Sharma, C., Rokana, N., Chandra, M., Singh, B. P., Gulhane, R. D., Gill, J. P. S., Ray, P., Puniya, A. K., & Panwar, H. (2018). Antimicrobial resistance: its surveillance, impact, and alternative management strategies in dairy animals. Frontiers in Veterinary Science, 4, 237. http://dx.doi.org/10.3389/fvets.2017.00237. PMid:29359135.
http://dx.doi.org/10.3389/fvets.2017.002...
). In organic production, the use of antimicrobials is prohibited, except when the use of permitted alternative medications has no effect and the animal is under suffering or at risk of death (Brasil, 2011Brasil. Ministério da Agricultura, Pecuária e Abastecimento. (2011). Regulamento Técnico para os Sistemas Orgânicos de Produção (Instrução Normativa n° 46, de 6 de outubro de 2011). Diário Oficial [da] República Federativa do Brasil.).

The presence of lactic acid bacteria in cheeses is favorable in terms of sensory characteristics, as it imparts flavor, aroma and texture, and in terms of microbiological quality, considering its ability to produce antimicrobial substances, known as bacteriocins (Antônio & Borelli, 2020Antônio, M. B., & Borelli, B. (2020). A importância das bactérias láticas na segurança e qualidade dos queijos Minas artesanais. Revista do Instituto de Latícinios Cândido Tostes, 75(3), 204-221. http://dx.doi.org/10.14295/2238-6416.v75i3.799.
http://dx.doi.org/10.14295/2238-6416.v75...
). Its antagonistic action can be observed against important pathogens, such as Listeria monocytogenes and Staphylococcus aureus (Darbandi et al., 2022Darbandi, A., Asadi, A., Mahdizade Ari, M., Ohadi, E., Talebi, M., Halaj Zadeh, M., Darb Emamie, A., Ghanavati, R., & Kakanj, M. (2022). Bacteriocins: properties and potential use as antimicrobials. Journal of Clinical Laboratory Analysis, 36(1), e24093. http://dx.doi.org/10.1002/jcla.24093. PMid:34851542.
http://dx.doi.org/10.1002/jcla.24093...
).

Given the significant increase of organic cheese consumption in the world and the lack of scientific evidence about the superior quality of the dairy products mentioned, the study aimed to evaluate the bacteriological quality of organic and conventional fresh cheeses, and to estimate the resistance of coagulase-positive Staphylococcus and Escherichia coli to different antimicrobials.

2 Material and methods

2.1 Sample collection and preparing

Thirty samples of Minas Frescal cheese were collected in supermarkets and organic food stores in the state of Rio de Janeiro. Fifteen samples originated from each system were from 5 different brands, which brand collected from three distinct stores and manufacturing dates, from May to July 2021. The packaging of the samples was carried out in isothermal boxes with reusable ice, maintaining the appropriate temperature conditions (from 6 °C to 8 °C) during transport to the Microbiological Control of Animal Origin Products Laboratory, of Universidade Federal Fluminense. The samples were separated and identified according to classification (conventional and organic) and prepared according to the bacteriological analyzes to be performed.

Twenty-five grams of each sample were aseptically homogenized in 225 mL of 0.1% peptone saline solution, obtaining the first dilution (10-1). Subsequent dilutions up to 10-7 were derived from this initial dilution. For the detection of Salmonella spp., 25 g of the sample was aseptically homogenized in 225 mL of 1.0% buffered peptone water, while for Listeria spp., 25 g aliquots were diluted in 225mL of Half Fraser Broth (Himedia, Mumbai, India). The samples were homogenized using a Stomacher® homogenizer (Seward, Worthing, UK) at medium speed for 60 seconds.

2.2 Microbiological evaluation

The determination of the Most Probable Number (MPN) of total coliforms, thermotolerant coliforms and E. coli was performed according to Merck methodology (Merck, 2000Merck. (2000). Microbiology manual (407 p.). Berlin: Merck.), using Fluorocult Lauryl Sulfate Broth (Merck, Germany), confirmed by Kovacs test. All confirmed strains were subcultured into Brain Heart Infusion (BHI) broth (Himedia, Mumbai, India), and then inoculated into Eosin Methylene Blue agar plates (BD, Heidelberg, Germany) for isolation of strains.

Coagulase-positive Staphylococcus counting was performed as described in the Compendium of Methods for the Microbiological Examination of Foods (Bennett et al., 2015Bennett, R. W., Hait, J. M., & Tallent, S. M. Staphylococcus aureus and staphylococcal enterotoxins. In Y. Salfinger & M. L. Tortorello (2015). Compendium of methods for the microbiological examinations of foods (5th ed., Chap. 39, pp. 509-526). Washington: APHA.), by spread plate inoculation in Baird Parker agar (Kasvi, Paraná, Brazil) plates. Five suspected colonies were selected from each plate, confirmed by coagulase and catalase tests and morphotintorial characterization by smear and Gram staining.

The lactic acid bacteria (LAB) count was performed according to methodology described by Frank & Yousef (2004)Frank, J. F., & Yousef, A. E. (2004). Tests for groups of microrganisms. In H. M. Wehr, & J. F. Frank, Standard methods for the examination of dairy products (17th ed., chap. 8, pp. 227-247). Washington, D.C: American Public Health Association. in the Standard Methods for the Examination of Dairy Products from inoculation by overlay on Man, Rogosa and Sharpe agar (Neogen, Michigan, USA).

The detection of Listeria spp. was performed by the plating method described by Ryser & Donnelly (2015)Ryser, E. T., & Donnelly, K. W. (2015). Listeria. In Y. Salfinger, & M. L. Tortorello. Compendium of methods for the microbiological examinations of foods (5th ed., chap. 36, pp. 425-444). Washington: APHA. in the Compendium of Methods for the Microbiological Examination of Foods using Half-Fraser broth in the pre-enrichment step, followed by enrichment in Fraser broth (Himedia, Mumbai, India) and subsequent plating on Modified Oxford agar (Himedia, Mumbai, India) and Listeria acc. Ottaviani & Agosti (Kasvi, Paraná, Brazil).

Salmonella spp. detection was performed by the methodology described in the Compendium of Methods for the Microbiological Examination of Foods (Cox et al., 2015Cox, N. A., Frye, J. G., McMahon, W., Jackson, C. R., Richardson, J., Cosby, D. E., Mead, G., & Doyle, M. P. (2015). Salmonella. In Y. Salfinger & M. L. Tortorello. Compendium of methods for the microbiological examinations of foods (5th ed., Chap. 36, pp. 445-476). Washington (DC): APHA.), starting with pre-enrichment in 1% buffered peptone saline solution, followed by selective enrichment in Mossel (Oxoid, Hants, UK) and Rappaport Vassiliadis broth (Oxoid, Hants, UK), with subsequent selective plating using Brilliant Green, Xylose Lysine Deoxycholate and Salmonella spp. Differential agar (Himedia, Mumbai, India).

All isolated strains of E. coli and Staphylococcus spp. were transferred to BHI broth and kept in a refrigerator at an average temperature of 4 °C for antimicrobial susceptibility test.

2.3 Antimicrobial susceptibility test

The test was performed according to the recommendations of the Clinical & Laboratory Standards Institute (Clinical and Laboratory Standards Institute, 2021Clinical and Laboratory Standards Institute - CLSI. (2021). Performance standards for antimicrobial susceptibility testing (31st ed.). USA: CLSI. CLSI supplement M100.), by the agar disk-diffusion test, also known as Kirby-Bauer Method (Bauer et al., 1966Bauer, A. W., Kirby, W. M., Sherris, J. C., & Turck, M. (1966). Antibiotic susceptibility testing by a standardized single disk method. American Journal of Clinical Pathology, 45(4), 493-496. http://dx.doi.org/10.1093/ajcp/45.4_ts.493. PMid:5325707.
http://dx.doi.org/10.1093/ajcp/45.4_ts.4...
) and the antimicrobials were chosen considering the most relevant antimicrobials in terms of frequency of use and impacts on public health.

Strains were standardized to category one on the McFarland Standards (Probac, Brazil), an universally established scale to standardize the approximate number of bacteria in a liquid suspension, which, in category one represents the concentration of 3 x 108 bacteria/mL, seeded on plates containing Müeller Hinton Agar. The antimicrobial discs arranged in modules, of 6 antimicrobial discs per module (Polisensidisc 24, DME), were superimposed on the plates. For both microorganisms, the following antimicrobials were used: Aztreonam (ATM 30 µg), Cefoxitin (CFO 30µg), Chloramphenicol (CLO 30 µg), Gentamicin (GEN 10 µg) and Tetracycline (TET 30 µg). Specifically for E. coli, were also used: Amikacin (AMI 30 µg), Ampicillin (AMP 10 µg), Cefazolin (CFZ 10 µg), Cefotaxime (CTX 30 µg), Ceftazidime (CAZ 30 µg), Sulfamethoxazole + Trimethoprim (SUT 25 µg) and Ceftriaxone (CRO 30 µg). For Staphylococcus spp., Clindamycin (CLI 02 µg), Erythromycin (ERI 15 µg), Oxacycline (OXA 01 µg), Penicillin G (PEN 10 µg), Teicoplamine (TEC 30 µg) and Vancomycin (VAN 30 µg) were also tested.

After incubation at 35-37 °C for 24 hours, the test was interpreted using standard measures of inhibition halos for each antimicrobial used according to the table established in the CLSI (Clinical and Laboratory Standards Institute, 2021)Clinical and Laboratory Standards Institute - CLSI. (2021). Performance standards for antimicrobial susceptibility testing (31st ed.). USA: CLSI. CLSI supplement M100. using a halometer to classify the strains as resistant, intermediate or sensitive.

2.4 Statistical analysis

For the statistical analysis of the data, non-parametric tests were applied. Friedman's test was applied to compare the values of the two groups, appropriate or inappropriate for consumption, while Pearson's linear correlation coefficient was used to evaluate potential associations between the variables and between conventional and organic matrices, using also Mann-Whitney Test to compare both systems regarding quantitative variables, considering the level of global significance of 5% (p ≤ 0.05). Data were processed using the IBM “Statistical Package for the Social Sciences” (SPSS), version 18.0.

3 Results and discussion

The results, described in Table 1, were compared with the microbiological standards for foods pre-established in Brazil by IN n°60 (Normative Instruction n° 60, of December 23, 2019, of Anvisa), based on the category of cheeses with moisture above 46%, classifying the samples as appropriate or inappropriate for consumption (Brasil, 2019Brasil. Ministério da Saúde, Agência Nacional de Vigilância Sanitária. (2019). Estabelece as listas de padrões microbiológicos para alimentos (Instrução Normativa nº 60, de 23 de dezembro de 2019). Diário Oficial [da] República Federativa do Brasil.).

Table 1
Mean bacterial counts of organic and conventional Minas Fresh cheese.

Coagulase-positive Staphylococcus counts ranged from 0 to 7.4 log CFU/g in conventional cheeses and from 0 to 7.9 log CFU/g in organic cheeses. Of the 30 samples analyzed, 21 samples (70%), being 13 (43.4%) conventional and 8 (26.6%) organic, presented counts higher than the recommended in Brazilian legislation, of 3 log CFU/g, as described in Figure 1. Therefore, they were unfit for consumption (Brasil, 2019Brasil. Ministério da Saúde, Agência Nacional de Vigilância Sanitária. (2019). Estabelece as listas de padrões microbiológicos para alimentos (Instrução Normativa nº 60, de 23 de dezembro de 2019). Diário Oficial [da] República Federativa do Brasil.), but with no statistical difference between the production systems regarding consumption suitability (p > 0.05).

Figure 1
Suitability of conventional and organic Minas Frescal Cheese samples according to IN 60 (Brasil, 2019Brasil. Ministério da Saúde, Agência Nacional de Vigilância Sanitária. (2019). Estabelece as listas de padrões microbiológicos para alimentos (Instrução Normativa nº 60, de 23 de dezembro de 2019). Diário Oficial [da] República Federativa do Brasil.) for coagulase-positive Staphylococcus and Escherichia coli counts.

Mullen et al. (2013)Mullen, K. A. E., Sparks, L. G., Lyman, R. L., Washburn, S. P., & Anderson, K. L. (2013). Comparisons of milk quality on North Carolina organic and conventional dairies. Journal of Dairy Science, 96(10), 6753-6762. http://dx.doi.org/10.3168/jds.2012-6519. PMid:23932134.
http://dx.doi.org/10.3168/jds.2012-6519...
stated that despite differences in herd management, the prevalence of Staphylococcus spp. in the herd was remarkably similar between the organic and conventional dairies surveyed, and that conventional and organic dairy farmers face similar challenges in mastitis management and the quality of milk produced. Similarities in the systems were also reported by Malissiova et al. (2017)Malissiova, E., Papadopoulos, T., Kyriazi, A., Mparda, M., Sakorafa, C., Katsioulis, A., Katsiaflaka, A., Kyritsi, M., Zdragas, A., & Hadjichristodoulou, C. (2017). Differences in sheep and goats milk microbiological profile between conventional and organic farming systems in Greece. The Journal of Dairy Research, 84(2), 206-213. http://dx.doi.org/10.1017/S0022029917000103. PMid:28294933.
http://dx.doi.org/10.1017/S0022029917000...
, in a study about differences in the microbiological profile of milk from sheep and goats between conventional and organic farming systems in Greece.

In conventional cheese, the MPN of Escherichia coli ranged from 0 to 1.5 log NMP/g, and in none of the 15 samples analyzed was a count higher than that determined in the legislation of 3.0 log MPN/g. In the organic cheeses, the MPN ranged from 0 to 11.9 log MPN/g and two of the 15 samples were inappropriate for consumption. The significant difference in total coliforms and E. coli count was observed between the systems (p = 0.002 and p = 0.042, respectively), with a higher contamination index in cheeses derived from the organic system. Higher absolute levels of E. coli contamination in organic cheeses were also reported by Kukułowicz (2018)Kukułowicz, A. (2018). Comparison of microbiological quality of milk products from organic and conventional production. Rocz Naukowe Stow Ekonomistów Rol Agrobiz, 20(6), 147-153. http://dx.doi.org/10.5604/01.3001.0012.7744.
http://dx.doi.org/10.5604/01.3001.0012.7...
and Wanniatie et al. (2019)Wanniatie, V., Sudarwanto, M. B., Purnawarman, T., & Jayanegara, A. (2019). Comparison of microbiological quality between organic and conventional goat milk: a study case in Bogor, Indonesia. Advances in Animal and Veterinary Sciences, 7(7), 593-598. http://dx.doi.org/10.17582/journal.aavs/2019/7.7.593.598.
http://dx.doi.org/10.17582/journal.aavs/...
in comparative studies about different organic dairy products and organic goat milk, respectively. On the other hand, no statistical difference was observed in both related studies.

The presence of E. coli in dairy products, an indicator of fecal contamination, is mainly associated with the use of raw or improperly pasteurized milk and poor hygienic-sanitary practices during processing (Hammad et al., 2022Hammad, A. M., Eltahan, A., Hassan, H. A., Abbas, N. H., Hussien, H., & Shimamoto, T. (2022). Loads of coliforms and fecal coliforms and characterization of Thermotolerant Escherichia coli in fresh raw milk cheese. Foods, 11(3), 332. http://dx.doi.org/10.3390/foods11030332. PMid:35159482.
http://dx.doi.org/10.3390/foods11030332...
), determinant factors in both production systems.

Regardless of the cheeses origin, Salmonella spp. and Listeria spp. were not detected in the analyzed samples, in accordance with the provisions of national legislation (Brasil, 2019Brasil. Ministério da Saúde, Agência Nacional de Vigilância Sanitária. (2019). Estabelece as listas de padrões microbiológicos para alimentos (Instrução Normativa nº 60, de 23 de dezembro de 2019). Diário Oficial [da] República Federativa do Brasil.) and with what was reported by Messias et al. (2022)Messias, T. B. O. N., Magnani, M., Pimentel, T. C., Silva, L. M. D., Alves, J., Gadelha, T. S., Morgano, M. A., Pacheco, M. T. B., Oliveira, M. E. G., & Queiroga, R. C. R. E. (2022). Typical Brazilian cheeses: safety, mineral content and adequacy to the nutritional labeling. Food Science and Technology, 42, e37121. https://doi.org/10.1590/fst.37121.
https://doi.org/10.1590/fst.37121...
, in an analysis of different typical Brazilian cheeses and by Kukułowicz (2018)Kukułowicz, A. (2018). Comparison of microbiological quality of milk products from organic and conventional production. Rocz Naukowe Stow Ekonomistów Rol Agrobiz, 20(6), 147-153. http://dx.doi.org/10.5604/01.3001.0012.7744.
http://dx.doi.org/10.5604/01.3001.0012.7...
, who, when comparing different dairy products of conventional and organic origin, did not detect the presence of Salmonella spp. in any of the samples analyzed. Sosnowski & Osek (2021)Sosnowski, M., & Osek, J. (2021). Microbiological safety of food of animal origin from organic farms. Journal of Veterinary Research, 65(1), 87-92. http://dx.doi.org/10.2478/jvetres-2021-0015. PMid:33817400.
http://dx.doi.org/10.2478/jvetres-2021-0...
observed that despite reports by several authors about the presence of Listeria spp. in different organic and conventional matrices there is no significant difference between the production systems on the presence of Listeria spp.

Van Loo et al. (2012)Van Loo, E. J., Alali, W., & Ricke, S. C. (2012). Food safety and organic meats. Annual Review of Food Science and Technology, 3(1), 203-225. http://dx.doi.org/10.1146/annurev-food-022811-101158. PMid:22385165.
http://dx.doi.org/10.1146/annurev-food-0...
considered that organic production poses a risk in relation to microbiological safety arising from system particularities such as restriction of the use of antimicrobials and antiparasitics and outdoor breeding, favoring the spread of zoonosis due to greater exposure of the animal. Disagreeing, Galdino et al. (2012)Galdino, M. C., Domingues, P. F., & Ferreira, B. L. S. (2012). A produção de leite orgânico e aspectos de segurança alimentar. Veterinária e Zootecnia, 490-501. reported that such obstacles can be mitigated by the adoption of strict hygiene practices and the application of complementary therapy, such as homeopathy, acupuncture and herbal medicine. Furthermore, Schwendel et al. (2015)Schwendel, B. H., Wester, T. J., Morel, P. C. H., Tavendale, M. H., Deadman, C., Shadbolt, N. M., & Otter, D. E. (2015). Invited review: Organic and conventionally produced milk — an evaluation of factors influencing milk composition. Journal of Dairy Science, 98(2), 721-746. http://dx.doi.org/10.3168/jds.2014-8389. PMid:25497795.
http://dx.doi.org/10.3168/jds.2014-8389...
reported that numerous factors must be considered when evaluating the differences between organic and conventional dairy, from minimal factors such as animal breed and diet composition to production and post-processing handling.

The lactic acid bacteria count ranged from 4.9 to 9.0 log CFU/g in conventional cheeses and from 5.1 to 10.6 log CFU/g in organic cheeses. Result that, when analyzed using Pearson's correlation method with the count of E. coli and coagulase-positive Staphylococcus, did not establish a correlation (r = +0.28; p = 0.12 for E. coli and r = -0.24 and p = 0.19 for coagulase-positive Staphylococcus), indicating that the presence of LAB had no influence over the presence of pathogens. Differently from the reported by Pato et al. (2022)Pato, U., Riftyan, E., Ayu, D. F., Jonnaidi, N. N., Wahyuni, M. S., Feruni, J. A., & Abdel-Wahhab, M. A. (2022). Antibacterial efficacy of lactic acid bacteria and bacteriocin isolated from Dadih’s against Staphylococcus aureus. Food Science and Technology (Campinas), 42, e27121. http://dx.doi.org/10.1590/fst.27121.
http://dx.doi.org/10.1590/fst.27121...
when evaluating the antimicrobial activity of lactic acid bacteria and bacteriocins isolated from Dadih (traditional fermented milk from Indonesia) on Staphylococcus aureus strains, in which all 12 isolated strains were able to suppress the growth of S. aureus. Santos et al. (2019)Santos, D. S., Calaça, P. R. A., Porto, A. L. F., Souza, P. R. E., & Cavalcanti, M. T. H. (2019). Caracterização parcial probiótica e molecular de bactérias ácido lácticas isoladas de queijo de coalho da cidade de Arcoverde-Pernambuco. Iniciação Científica Cesumar, 21(1), 7-14. http://dx.doi.org/10.17765/1518-1243.2019v21n1p7-14.
http://dx.doi.org/10.17765/1518-1243.201...
, in a study on the probiotic and molecular characterization of LAB isolated from cheese, noted that probiotic characterization is extremely necessary since not all LAB have antimicrobial characteristics. In the aforementioned study, of the 11 bacteria isolated, only two showed probiotic potential. According to the parameters published by the National Health Surveillance Agency (Brasil, 1999Brasil. Agência Nacional de Vigilância Sanitária. (1999). Regulamento Técnico que Estabelece as Diretrizes Básicas para Análise e Comprovação de Propriedades Funcionais e ou de Saúde Alegadas em Rotulagem de Alimentos (Resolução ANVS/MS nº 18, de 30 de abril de 1999). Diário Oficial [da] República Federativa do Brasil.), to classify a product as a probiotic the minimum concentration of viable probiotic microorganisms need to be achieved, of 8 to 9 log CFU/mL, persistent till the end of the shelf life.

The characterization of the antimicrobial resistance of coagulase-positive Staphylococcus strains to different antimicrobials is described in Table 2. All strains isolated from conventional and organic cheeses showed multi-resistance and there was no statistical difference between the systems.

Table 2
Susceptibility of coagulase-positive Staphylococcus to antimicrobials.

The class of antimicrobials that showed the lowest efficacy on isolated coagulase-positive Staphylococcus strains was the β-lactams such as oxacyclin, penicillin and aztreonam. Similar results were reported by Abreu et al. (2021)Abreu, A. C. S., Matos, L. G., Cândido, T. J. S., Barboza, G. R., de Souza, V. V. M. A., Nuñez, K. V. M., & Silva, N. C. C. (2021). Antimicrobial resistance of Staphylococcus spp. isolated from organic and conventional Minas Frescal cheese producers in São Paulo, Brazil. Journal of Dairy Science, 104(4), 4012-4022. http://dx.doi.org/10.3168/jds.2020-19338. PMid:33516545.
http://dx.doi.org/10.3168/jds.2020-19338...
when analyzing the antimicrobial resistance of strains of Staphylococcus spp. isolated from conventional and organic Minas Frescal cheese, which consider that there are several factors that influence the sensitivity of microorganisms isolated in dairy products, such as contamination by handlers during processing, and that the ineffectiveness of β-lactams is justified by the popularity and extensive use of the class in the country, ineffectiveness also reported by Keyvan et al. (2020)Keyvan, E., Yurdakul, O., Demirtas, A., Yalcin, H., & Bilgen, N. (2020). Identification of methicillin-resistant Staphylococcus aureus in bulk tank milk. Food Science and Technology (Campinas), 40(1), 150-156. http://dx.doi.org/10.1590/fst.35818.
http://dx.doi.org/10.1590/fst.35818...
.

Of the six strains of E. coli isolated in the research, five belonged to organic cheeses while only one strain was isolated from conventional cheeses. The strain resistance profile is described in Table 3.

Table 3
Susceptibility of E. coli to antimicrobials.

All strains isolated showed multidrug resistance, with 100% resistance to ampicillin, cefazolin, aztreonam and cefoxitin in both production systems. The disparity in the number of strains isolated from conventional and organic cheeses made statistical analysis of the data difficult when comparing the systems.

The predominance of E. coli resistance to ampicillin in milk and dairy products was also reported by Gundogan & Avci (2014)Gundogan, N., & Avci, E. (2014). Occurrence and antibiotic resistance of Escherichia coli, Staphylococcus aureus and Bacillus cereus in raw milk and dairy products in Turkey. International Journal of Dairy Technology, 67(4), 562-569. http://dx.doi.org/10.1111/1471-0307.12149.
http://dx.doi.org/10.1111/1471-0307.1214...
, who justified this incidence by the routine use of β-lactams in the treatment of E. coli infections in both humans and animals and by the strains ability to produce extended-spectrum β-lactamases, enzymes capable of inactivating antimicrobials of the class.

Almeida et al. (2021)Almeida, C. C., Financi, T. P., Cardozo, M. V., Pizauro, L. J. L., Pereira, N., Valmorbida, M. K., Borzi, M. M., Weiss, B., & Ávila, F. A. (2021). Enterobacteriaceae in calves, cows and milking environment may act as reservoirs of virulence and antimicrobial resistance genes. Food Science and Technology (Campinas), 41(2), 376-380. http://dx.doi.org/10.1590/fst.37819.
http://dx.doi.org/10.1590/fst.37819...
, when evaluating the presence and antimicrobial resistance of Enterobacteriaceae in calves, cows and the milking environment, observed a high rate of ampicillin resistance and multidrug resistance in all isolates. Characteristics that, according to Poirel et al. (2018)Poirel, L., Madec, J. Y., Lupo, A., Schink, A. K., Kieffer, N., Nordmann, P., & Schwarz, S. (2018). Antimicrobial resistance in Escherichia coli. Microbiology Spectrum, 6(4), 1-27. http://dx.doi.org/10.1128/microbiolspec.ARBA-0026-2017. PMid:30003866.
http://dx.doi.org/10.1128/microbiolspec....
, are extremely important from a One Health perspective due to the worldwide spread of E. coli, commonly associated with food, in which resistance to multiple classes of antimicrobials leads to difficult-to-treat infections.

Results contrasting with those found by Sato et al. (2005)Sato, K., Bartlett, P. C., & Saeed, M. A. (2005). Antimicrobial susceptibility of Escherichia coli isolates from dairy farms using organic versus conventional production methods. Journal of the American Veterinary Medical Association, 226(4), 589-594. http://dx.doi.org/10.2460/javma.2005.226.589. PMid:15742702.
http://dx.doi.org/10.2460/javma.2005.226...
when analyzing isolates from cows and calves from conventional and organic systems, which reported a low rate of resistance to ampicillin (19.5% in conventional and 10.4% in organic) and cefoxitin (1.4% in conventional and 0.4% in organic) and 100% amikacin sensitivity. Such differences between studies that are just over a decade apart reinforce the advance of antimicrobial resistance, currently considered a pandemic, with projection of causing about 10 million deaths by 2050 (Singhal, 2022Singhal, T. (2022). Antimicrobial Resistance: The 'Other' Pandemic! Indian Journal of Pediatrics: Based on 9th Dr. I. C. Verma Excellence Award for Young Pediatricians Delivered as Oration on 19th Sept. 2021. , 89(6), 600-606. http://dx.doi.org/10.1007/s12098-021-04008-9. PMID: 35064528.
http://dx.doi.org/10.1007/s12098-021-040...
).

4 Conclusions

The significant difference between the production systems regarding E. coli count is more commonly related to poor hygienic-sanitary conditions than to the type of production system. All other similarities found in this research reinforce the need to analyze other parameters that influence food safety such as herd health and good manufacturing practices, in order to justify the appealing of paying more for better quality food.

Regardless of the production system, the use of antimicrobials must be reconsidered in order to stop growing antimicrobial resistance. So that all types of consumers have access to a safe food, mitigating the risks of serious and/or difficult-to-treat foodborne diseases.

  • Practical Application: In view of the widespread consumption of cheeses and the rise of the organic market in the world, it is important to guide consumers about the quality and safety of these products considered superior to conventional products.

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Publication Dates

  • Publication in this collection
    06 Jan 2023
  • Date of issue
    2023

History

  • Received
    14 June 2022
  • Accepted
    05 Nov 2022
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