Abstract

The search for safer foods has led to increased research attention to discover natural alternatives to synthetic additives that are used in the food industry. Natural preservatives, such as essential oils (EOs) from plants, could increase fish conservation and even positively affect human health. Therefore, the objective of the study was to evaluate the effect of Mentha piperita EO on the physicochemical characteristics and concentration of microorganisms in chilled tambatinga (Colossoma macropomum × Piaractus brachypomum) meat. Mentha piperita EO was prepared at three concentrations (0%, 0.25% and 0.50%) in a solution containing distilled water, propylene glycol and Tween. The meat samples remained immersed in this solution for 60 min; then, they were packed in plastic packages and stored under refrigeration (± 0.4 °C) for 14 days. During this storage, pH, total volatile nitrogenous bases (TVB-N), peroxides, thiobarbituric acid reactive substances (TBARS) and counts of strict and facultative aerobic mesophilic microorganisms were determined. The major constituents found in M. piperita EO were geranial (32.28%), neral (18.64%) and geranic acid (6.98%). None of the EO concentrations affected TVB-N, but there were some changes to the pH. Both 0.25% and 0.50% EO reduced the formation of peroxides and TBARS. The growth of microorganisms was reduced by treatment with 0.50% EO. Based on the findings, 0.50% EO was more effective in reducing the deterioration of meat kept refrigerated for up to 14 days.

Keywords:
Fish meat; lipid oxidation; microbial spoilage; natural preservatives; shelf life

Resumo

A busca por alimentos mais seguros levou a uma maior atenção da pesquisa para encontrar alternativas naturais aos aditivos sintéticos usados na indústria alimentícia. Os conservantes naturais, como os óleos essenciais (OE) de plantas, podem aumentar a conservação dos peixes e até afetar positivamente a saúde humana. Portanto, o objetivo do estudo foi avaliar o efeito do OE de Mentha piperita nas características físico-químicas e concentração de microrganismos em carne resfriada de tambatinga (Colossoma macropomum × Piaractus brachypomum). O OE de M. piperita foi preparado em três concentrações (0%, 0,25% e 0,50%) em solução contendo água destilada, propilenoglicol e Tween. As amostras de carne permaneceram imersas nesta solução por 60 min; em seguida, foram acondicionados em embalagens plásticas e armazenados sob refrigeração (± 0,4°C) por 14 dias. Durante esse armazenamento foram determinados pH, bases nitrogenadas voláteis totais (BNVT), peróxidos, substâncias reativas ao ácido tiobarbitúrico (TBARS) e contagens de microrganismos mesófilos aeróbios estritos e facultativos. Os principais constituintes encontrados no OE de M. piperita foram geranial (32,28%), neral (18,64%) e ácido gerânico (6,98%). Nenhuma das concentrações de OE afetou as BNVT, mas houve algumas alterações no pH. Tanto 0,25% quanto 0,50% de OE reduziram a formação de peróxidos e TBARS. O crescimento de microrganismos foi reduzido no tratamento com 0,50% de OE. Com base nos resultados, a concentração de 0,50% de OE foi mais eficaz na redução da deterioração da carne mantida refrigerada por até 14 dias.

Palavras-chave:
Carne de peixe; oxidação lipídica; deterioração microbiana; conservantes naturais; vida de prateleira

1. Introduction

Fish, crustaceans and molluscs are nutritionally valued foods because they contain highquality proteins, lipids, vitamins and minerals. The consumption of these foods is correlated with the improvement in health and life expectancy of populations(¹1 Sarojnalini C, Hei A. Fish as an important food for quality life. In: Lagouri V. (Ed.). Functional Foods. IntechOpen, 2019. 77-97. https://doi.org/10.5772/intechopen.81947
https://doi.org/10.5772/intechopen.81947... ,²2 Tanimoto S, Kondo R, Itonaga S, Domen A, Mabuchi R. Screening plant extracts for quality preservation of dark muscle fish flesh: a simple method. J Food Process Pres 2020; 44:e14315. https://doi.org/10.1111/jfpp.14315
https://doi.org/10.1111/jfpp.14315... ). In Brazil, among the most bred species are Oreochromis niloticus (Nile tilapia) and native species such as Colossoma macropomum (tambaqui), Piaractus mesopotamicus (pacu) and Arapaima gigas (pirarucu)(³3 Peixe BR. Associação Brasileira de Piscicultura: Anuário Brasileiro da Piscicultura PEIXE BR 2022. Available from: https://www.peixebr.com.br/anuario-2021/ (accessed: April 10, 2023).
https://www.peixebr.com.br/anuario-2021/... ). Tambatinga, the species used in this study, is a hybrid developed from the crossing of the native species C. macropomum and Piaractus brachypomus (pirapitinga) that exhibits higher growth and productivity rates than its parents. As such, it has become an important species in the scenario of fish farming in North and Northeast Brazil(⁴4 Andreghetto F, Santana TC, Castro JS, Noleto KS, Teixeira EG. Desempenho zootécnico e bromatologia de tambatinga (Colossoma macropomum x Piaractus brachypomus, Characidae) alimentada com milheto (Pennisetum sp.). Braz J Dev 2020; 6(4):21818-21831. https://doi.org/10.34117/bjdv6n4-376
https://doi.org/10.34117/bjdv6n4-376... ,⁵5 Costa TS, Silva RC, Pretto A, Monteiro OS, Siqueira JC, Baldisserotto B, Lopes JM. Effect of Lippia grata essential oil as a feed additive on the performance of tambatinga juveniles. Acta Amaz 2022; 52(2):122-130. https://doi.org/10.1590/1809-4392202102442
https://doi.org/10.1590/1809-43922021024... ).

Fish meat, sold in different ways, is the final product of fishing and fish farming, requiring care from the capture of the fish to its distribution, with special attention to sanitary aspects, storage conditions and conservation of the product(⁶6 Gonçalves AA. Tecnologia do pescado: Ciência, Tecnologia, Inovação Legislação. São Paulo: Editora Atheneu; 2011. 608 p.). Fresh fish is a very perishable meat and has a short shelf life as several processes such as protein degradation, fat oxidation and decomposition by microbes or by endogenous enzymes contribute to the deterioration of meat(⁷7 Dang HTT, Gudjonsdóttir M, Karlsdóttir MG, Nguyen MV, Tómasson T, Arason S. Stability of Golden redfish (Sebastes marinus) during frozen storage as affected by raw material freshness and season of capture. Food Sci Nutr 2018; 6(4):1065-1076. https://doi.org/10.1002/fsn3.648
https://doi.org/10.1002/fsn3.648... ,⁸8 Mattje LGB, Tormen L, Bombardelli MCM, Corazza ML, Bainy EM. Ginger essential oil and supercritical extract as natural antioxidants in tilapia fish burger. J Food Process Pres 2019; 43(5):e13942. https://doi.org/10.1111/jfpp.13942
https://doi.org/10.1111/jfpp.13942... ). For this reason, one or more adequate preservation methods are required in order to maintain the safety and quality and extend the shelf life of such products(⁹9 Hassoun A, Karoui R. Quality evaluation of fish and other seafood by traditional and nondestructive instrumental methods: Advantages and limitations. Crit Rev Food Sci Nutr 2017; 57(9):1976-1998. https://doi.org/10.1080/10408398.2015.1047926
https://doi.org/10.1080/10408398.2015.10... ). In this sense, the use of processes that reduce oxidative events (formation of hydroperoxides, aldehydes, alkanes, conjugated dienes) and fish deterioration (formation of biogenic amines, sensory changes, discoloration, loss of nutrients and water) can improve their conservation(¹⁰10 Huang Z, Liu X, Jia S, Zhang L, Luo Y. The effect of essential oils on microbial composition and quality of grass carp (Ctenopharyngodon idellus) fillets during chilled storage. Int J Food Microbiol 2018; 266:52-59. https://doi.org/ 10.1016/j.ijfoodmicro.2017.11.003
https://doi.org/ 10.1016/j.ijfoodmicro.2... ,¹¹11 Ribeiro JS, Santos MJMC, Silva LKR, Pereira LCL, Santos IA, Lannes SCS, Silva MV. Natural antioxidants used in meat products: A brief review. Meat Sci 2019; 148:181-188. https://doi.org/10.1016/j.meatsci.2018.10.016
https://doi.org/10.1016/j.meatsci.2018.1... ,¹²12 Vieira BB, Mafra JF, Bispo ASR, Ferreira MA, Silva FL, Rodrigues AVN, Evangelista-Barreto NS. Combination of chitosan coating and clove essential oil reduces lipid oxidation and microbial growth in frozen stored tambaqui (Colossoma macropomum) fillets. LWT - Food Sci Technol 2019; 116:108546. https://doi.org/10.1016/j.lwt.2019.108546
https://doi.org/10.1016/j.lwt.2019.10854... ).

The application of synthetic antioxidants such as butylated hydroxytoluene (BHT), butylated hydroxyanisol (BHA), sorbate and benzoate, commonly used to increase the oxidative stability of fish and derived products, is now being discouraged due to the risk of diseases that they can cause(¹²12 Vieira BB, Mafra JF, Bispo ASR, Ferreira MA, Silva FL, Rodrigues AVN, Evangelista-Barreto NS. Combination of chitosan coating and clove essential oil reduces lipid oxidation and microbial growth in frozen stored tambaqui (Colossoma macropomum) fillets. LWT - Food Sci Technol 2019; 116:108546. https://doi.org/10.1016/j.lwt.2019.108546
https://doi.org/10.1016/j.lwt.2019.10854... ,¹³13 Singh S, Chaurasia PK, Bharati SL. Functional roles of essential oils as an effective alternative of synthetic food preservatives: a review. J Food Process Pres 2022; 46:e16804. https://doi.org/10.1111/jfpp.16804
https://doi.org/10.1111/jfpp.16804... ). On the other hand, substances of natural origin (extracted from spices or herbs) such as essential oils (EOs) have received special attention in the food industry and in human nutrition as they present molecules capable of reducing the chemical and microbiological decomposition of fish meat and derived formulations(¹⁰10 Huang Z, Liu X, Jia S, Zhang L, Luo Y. The effect of essential oils on microbial composition and quality of grass carp (Ctenopharyngodon idellus) fillets during chilled storage. Int J Food Microbiol 2018; 266:52-59. https://doi.org/ 10.1016/j.ijfoodmicro.2017.11.003
https://doi.org/ 10.1016/j.ijfoodmicro.2... ,²2 Tanimoto S, Kondo R, Itonaga S, Domen A, Mabuchi R. Screening plant extracts for quality preservation of dark muscle fish flesh: a simple method. J Food Process Pres 2020; 44:e14315. https://doi.org/10.1111/jfpp.14315
https://doi.org/10.1111/jfpp.14315... ). Phenolic compounds such as thymol, eugenol, rosmarinic acid, carvacrol, gingerol, menthol and citral, among other molecules present in EOs, have antimicrobial and antioxidant action that is of interest to the food industry(¹³13 Singh S, Chaurasia PK, Bharati SL. Functional roles of essential oils as an effective alternative of synthetic food preservatives: a review. J Food Process Pres 2022; 46:e16804. https://doi.org/10.1111/jfpp.16804
https://doi.org/10.1111/jfpp.16804... ,¹⁴14 Dègnon RG, Allagbé AC, Adjou ES, Dahouenon-Ahoussi E. Antifungal activities of Cymbopogon citratus essential oil against Aspergillus species isolated from fermented fish products of Southern Benin. J Food Qual Hazards Control 2019; 6(2):53-57. https://doi.org/10.18502/jfqhc.6.2.955
https://doi.org/10.18502/jfqhc.6.2.955... ).

In some studies, the main constituents found in the EO of Mentha piperita were menthol, menthone and menthyl acetate, and these molecules revealed significant antimicrobial activity against bacteria and pathogenic fungi in humans(¹⁵15 Reddy DN, Al-Rajab AJ, Sharma M, Moses MM, Reddy GR, Albratty M. Chemical constituents, in vitro antibacterial and antifungal activity of Mentha piperita L (peppermint) essential oils. J King Saud Univ Sci 2019; 31(4):528-533. https://doi.org/10.1016/j.jksus.2017.07.013
https://doi.org/10.1016/j.jksus.2017.07.... ) and also against bacteria and parasites in fish(¹⁶16 Ferreira LC, Cruz MG, Lima TBC, Serra BNV, Chaves FCM, Chagas EC, Ventura AS, Jerônimo GT. Antiparasitic activity of Mentha piperita (Lamiaceae) essential oil against Piscinoodinium pillulare and its physiological effects on Colossoma macropomum (Cuvier, 1818). Aquaculture 2019; 512:734343. https://doi.org/10.1016/j.aquaculture.2019.734343
https://doi.org/10.1016/j.aquaculture.20... ,¹⁷17 Souza Silva LT, Pereira UP, Oliveira HM, Brazil EM, Pereira SA, Chagas EC, Jesus GFA, Cardoso L, Mouriño JLP, Martins ML. Hemato-immunological and zootechnical parameters of Nile tilapia fed essential oil of Mentha piperita after challenge with Streptococcus agalactiae. Aquaculture 2019; 506:205-211. https://doi.org/10.1016/j.aquaculture.2019.03.035
https://doi.org/10.1016/j.aquaculture.20... ). Spearmint essential oil applied to fillets of Sciaenops ocellatus in the form of steam prevents the breakdown of proteins and the formation of biogenic amines and decreases the development of microorganisms in refrigerated fish(¹⁸18 Cai L, Cao A, Li Y, Song Z, Leng L, Li J. The effects of essential oil treatment on the biogenic amines inhibition and quality preservation of red drum (Sciaenops ocellatus) fillets. Food Control 2015; 56:1-8. https://doi.org/10.1016/j.foodcont.2015.03.009
https://doi.org/10.1016/j.foodcont.2015.... ). Thus, these natural preservatives such as EOs could perfectly meet the increasing consumer demand for cleanlabel products that are fresh and free of chemical additives.

Therefore, in the present study, we aim to evaluate the effect of the EO of M. piperita in solution applied to fillets of tambatinga, a freshwater fish, on the physicochemical characteristics and total concentration of microorganisms in the meat kept refrigerated.

2. Material and methods

All procedures adopted in the study involving animals were approved by the Animal Use Ethics Committee of the Federal University of Pampa (approval no. 004/2019).

2.1 Essential oil

The EO of M. piperita used in this study was supplied by Vimontti (Santa Maria, Rio Grande do Sul, Brazil). The oil was analysed on a gas chromatograph coupled to a mass spectrometer (GCMS; QP2010 Ultra system, Shimadzu Corporation, Tokyo, Japan), equipped with GCMS-Solution software. The identification of the components was based on the time and linear retention index (series of n-alkanes C8-C40), on the interpretation and comparison of the mass spectra obtained with the Adams(¹⁹19 Adams RP. Identification of essential oil components by gas chromatography/quadrupole mass spectroscopy. 4nd ed. Carol Stream, IL: Allured Publishing Corporation, 2007. 804p.), NIST(²⁰20 NIST/EPA/NIH Mass Spectral Library 2011. 5nd ed. Hoboken, NJ: Wiley, 2011.) and FFNSC 2 libraries as described in detail by Fernandes(²¹21 Fernandes YML, Matos JVS, Lima CA, Tardini AM, Viera FAP, Maia JGS, Monteiro OS, Longato GB, Rocha CQ. Essential oils obtained from aerial Eugenia punicifolia parts: Chemical composition and antiproliferative potential evidenced through cell cycle arrest. J Braz Chem Soc 2021; 32(7):1381-1390. https://doi.org/10.21577/0103-5053.20210036
https://doi.org/10.21577/0103-5053.20210... ).

2.2 Fish and sample preparation

The study was carried out at the Fisheries Laboratory of the Federal University of Maranhão, Chapadinha Campus. Tambatinga specimens (310 ± 11.4 g and 26.05 ± 3.15 cm) were kept in a tank for depuration (density of 11.7 kg m³3 Peixe BR. Associação Brasileira de Piscicultura: Anuário Brasileiro da Piscicultura PEIXE BR 2022. Available from: https://www.peixebr.com.br/anuario-2021/ (accessed: April 10, 2023).
https://www.peixebr.com.br/anuario-2021/...

4 Andreghetto F, Santana TC, Castro JS, Noleto KS, Teixeira EG. Desempenho zootécnico e bromatologia de tambatinga (Colossoma macropomum x Piaractus brachypomus, Characidae) alimentada com milheto (Pennisetum sp.). Braz J Dev 2020; 6(4):21818-21831. https://doi.org/10.34117/bjdv6n4-376
https://doi.org/10.34117/bjdv6n4-376...

5 Costa TS, Silva RC, Pretto A, Monteiro OS, Siqueira JC, Baldisserotto B, Lopes JM. Effect of Lippia grata essential oil as a feed additive on the performance of tambatinga juveniles. Acta Amaz 2022; 52(2):122-130. https://doi.org/10.1590/1809-4392202102442
https://doi.org/10.1590/1809-43922021024...

6 Gonçalves AA. Tecnologia do pescado: Ciência, Tecnologia, Inovação Legislação. São Paulo: Editora Atheneu; 2011. 608 p.

7 Dang HTT, Gudjonsdóttir M, Karlsdóttir MG, Nguyen MV, Tómasson T, Arason S. Stability of Golden redfish (Sebastes marinus) during frozen storage as affected by raw material freshness and season of capture. Food Sci Nutr 2018; 6(4):1065-1076. https://doi.org/10.1002/fsn3.648
https://doi.org/10.1002/fsn3.648...

8 Mattje LGB, Tormen L, Bombardelli MCM, Corazza ML, Bainy EM. Ginger essential oil and supercritical extract as natural antioxidants in tilapia fish burger. J Food Process Pres 2019; 43(5):e13942. https://doi.org/10.1111/jfpp.13942
https://doi.org/10.1111/jfpp.13942...

9 Hassoun A, Karoui R. Quality evaluation of fish and other seafood by traditional and nondestructive instrumental methods: Advantages and limitations. Crit Rev Food Sci Nutr 2017; 57(9):1976-1998. https://doi.org/10.1080/10408398.2015.1047926
https://doi.org/10.1080/10408398.2015.10...

10 Huang Z, Liu X, Jia S, Zhang L, Luo Y. The effect of essential oils on microbial composition and quality of grass carp (Ctenopharyngodon idellus) fillets during chilled storage. Int J Food Microbiol 2018; 266:52-59. https://doi.org/ 10.1016/j.ijfoodmicro.2017.11.003
https://doi.org/ 10.1016/j.ijfoodmicro.2...

11 Ribeiro JS, Santos MJMC, Silva LKR, Pereira LCL, Santos IA, Lannes SCS, Silva MV. Natural antioxidants used in meat products: A brief review. Meat Sci 2019; 148:181-188. https://doi.org/10.1016/j.meatsci.2018.10.016
https://doi.org/10.1016/j.meatsci.2018.1...

12 Vieira BB, Mafra JF, Bispo ASR, Ferreira MA, Silva FL, Rodrigues AVN, Evangelista-Barreto NS. Combination of chitosan coating and clove essential oil reduces lipid oxidation and microbial growth in frozen stored tambaqui (Colossoma macropomum) fillets. LWT - Food Sci Technol 2019; 116:108546. https://doi.org/10.1016/j.lwt.2019.108546
https://doi.org/10.1016/j.lwt.2019.10854...

13 Singh S, Chaurasia PK, Bharati SL. Functional roles of essential oils as an effective alternative of synthetic food preservatives: a review. J Food Process Pres 2022; 46:e16804. https://doi.org/10.1111/jfpp.16804
https://doi.org/10.1111/jfpp.16804...

14 Dègnon RG, Allagbé AC, Adjou ES, Dahouenon-Ahoussi E. Antifungal activities of Cymbopogon citratus essential oil against Aspergillus species isolated from fermented fish products of Southern Benin. J Food Qual Hazards Control 2019; 6(2):53-57. https://doi.org/10.18502/jfqhc.6.2.955
https://doi.org/10.18502/jfqhc.6.2.955...

15 Reddy DN, Al-Rajab AJ, Sharma M, Moses MM, Reddy GR, Albratty M. Chemical constituents, in vitro antibacterial and antifungal activity of Mentha piperita L (peppermint) essential oils. J King Saud Univ Sci 2019; 31(4):528-533. https://doi.org/10.1016/j.jksus.2017.07.013
https://doi.org/10.1016/j.jksus.2017.07....

16 Ferreira LC, Cruz MG, Lima TBC, Serra BNV, Chaves FCM, Chagas EC, Ventura AS, Jerônimo GT. Antiparasitic activity of Mentha piperita (Lamiaceae) essential oil against Piscinoodinium pillulare and its physiological effects on Colossoma macropomum (Cuvier, 1818). Aquaculture 2019; 512:734343. https://doi.org/10.1016/j.aquaculture.2019.734343
https://doi.org/10.1016/j.aquaculture.20...

17 Souza Silva LT, Pereira UP, Oliveira HM, Brazil EM, Pereira SA, Chagas EC, Jesus GFA, Cardoso L, Mouriño JLP, Martins ML. Hemato-immunological and zootechnical parameters of Nile tilapia fed essential oil of Mentha piperita after challenge with Streptococcus agalactiae. Aquaculture 2019; 506:205-211. https://doi.org/10.1016/j.aquaculture.2019.03.035
https://doi.org/10.1016/j.aquaculture.20...

18 Cai L, Cao A, Li Y, Song Z, Leng L, Li J. The effects of essential oil treatment on the biogenic amines inhibition and quality preservation of red drum (Sciaenops ocellatus) fillets. Food Control 2015; 56:1-8. https://doi.org/10.1016/j.foodcont.2015.03.009
https://doi.org/10.1016/j.foodcont.2015....

19 Adams RP. Identification of essential oil components by gas chromatography/quadrupole mass spectroscopy. 4nd ed. Carol Stream, IL: Allured Publishing Corporation, 2007. 804p.

20 NIST/EPA/NIH Mass Spectral Library 2011. 5nd ed. Hoboken, NJ: Wiley, 2011.

21 Fernandes YML, Matos JVS, Lima CA, Tardini AM, Viera FAP, Maia JGS, Monteiro OS, Longato GB, Rocha CQ. Essential oils obtained from aerial Eugenia punicifolia parts: Chemical composition and antiproliferative potential evidenced through cell cycle arrest. J Braz Chem Soc 2021; 32(7):1381-1390. https://doi.org/10.21577/0103-5053.20210036
https://doi.org/10.21577/0103-5053.20210...

22 Dang HTT, Gudjónsdóttir M, Tómasson T, Nguyen MV, Karlsdóttir MG, Arason S. Influence of processing aditives, packaging and storage conditions on the physicochemical stability of frozen Tra catfish (Pangasius hypophthalmus) fillets. J Food Eng 2018: 238: 148-155. https://doi.org/10.1016/j.jfoodeng.2018.06.021
https://doi.org/10.1016/j.jfoodeng.2018....

23 Savay da Silva LK, Riggo R, Martins PE, Galvão JA, Oetterer M. Otimização e padronização do uso da metodologia para determinação de bases nitrogenadas voláteis totais (BNVT) em camarões Xyphopenaeus kroyeri. Braz J Food Technol 2008: 20:138-144.

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37 Brasil. Ministério da Agricultura, Pecuária e Abastecimento. Decreto n° 9.013 de 29 de março de 2017. Dispõe sobre a Inspeção Industrial E Sanitária De Produtos De Origem Animal. Diário Oficial da União. Available from: http://www.planalto.gov.br/ccivil_03/_ato2015-2018/2017/decreto/D9013.htm (accessed: May 15, 2023).
http://www.planalto.gov.br/ccivil_03/_at...

38 Soares KMDP, Gonçalves AA. Qualidade e segurança do pescado. Rev Inst Adolfo Lutz 2012; 71(1):1-10.

39 Karami B, Moradi Y, Motallebi AA, Hosseini E, Soltani M. Effects of frozen storage on fatty acids profile, chemical quality indices and sensory properties of red tilapia (Oreochromis niloticus × Tilapia mosambicus) fillets. Iran J Fish Sci 2013; 12(2):378-388.

40 Afrin F, Islam MM, Rasul MG, Sarkar MSI, Yuan C, Shah AKMA. Effects of seaweed extracts on the quality and shelf life of Nile tilapia (Oreochromis niloticus) fillets during frozen storage. Food Chem Adv 2023; 3:100388. https://doi.org/10.1016/j.focha.2023.100388
https://doi.org/10.1016/j.focha.2023.100...

41 Chandra H, Farooq Ah A. Lipoxigenase inhibitory, antioxidant, and antimicrobial activities of selected essential oils. Asian J Pharm Clin Res 2014; 7:79-83.

42 El-Hanafy AEA, Shawky HA, Ramadan MF. Preservation of Oreochromis niloticus fish using frozen green tea extract: impact on biochemical, microbiological and sensory characteristics. J Food Process Pres 2011; 35:639-646. https://doi.org/10.1111/j.1745-4549.2011.00513.x
https://doi.org/10.1111/j.1745-4549.2011... -¹1 Sarojnalini C, Hei A. Fish as an important food for quality life. In: Lagouri V. (Ed.). Functional Foods. IntechOpen, 2019. 77-97. https://doi.org/10.5772/intechopen.81947
https://doi.org/10.5772/intechopen.81947... ) for 48 h. In this process, the average water renewal rate was 6 L min^-1. In addition, dissolved oxygen and water temperature were analysed daily, and the mean values found were 5.87 ± 0.05 mg L^-1 and 28.50 ± 0.86 °C, respectively.

At the end of the depuration period, the fish were slaughtered by hypothermia (water: ice 1: 1) and weighed to calculate weight loss (%). There was a 4.9% reduction in fish weight. The fillet was removed and weighed to calculate the yield (fillet weight/total fish weight × 100). A fillet yield of 34.8% was obtained. The fillet was washed in running water and then in water containing 10 ppm of chlorine.

2.3 Preparation and application of EO to fish meat samples

Fillet samples were separated (750 g treatment^-1, in duplicate) and exposed to a solution containing different EO concentrations: 0% (control), 0.25% or 0.50%. The EO, which had a density of 0.85 g mL^-1, was diluted and emulsified in a solution containing 80% distilled water, 20% propylene glycol and 0.05% Tween. The meat samples remained immersed in 1.5 L of solution for 60 min. This time interval was chosen based on the study by Dang(²²22 Dang HTT, Gudjónsdóttir M, Tómasson T, Nguyen MV, Karlsdóttir MG, Arason S. Influence of processing aditives, packaging and storage conditions on the physicochemical stability of frozen Tra catfish (Pangasius hypophthalmus) fillets. J Food Eng 2018: 238: 148-155. https://doi.org/10.1016/j.jfoodeng.2018.06.021
https://doi.org/10.1016/j.jfoodeng.2018.... ). After exposure, the samples were drained on racks for 5 min, packed in plastic packages and stored under refrigeration at ± 0.4 °C for future analysis of meat quality parameters.

2.4 Physicochemical analysis

On days 0 (initial), 7 and 14 days of refrigeration (± 0.4 °C), the pH (hydrogen potential) of the samples was analysed using a previously calibrated portable meat pH meter (Akso Electronic Products, Rio Grande do Sul, Brazil). Total volatile nitrogenous bases (TVB-N) were determined as described by Savay da Silva(²³23 Savay da Silva LK, Riggo R, Martins PE, Galvão JA, Oetterer M. Otimização e padronização do uso da metodologia para determinação de bases nitrogenadas voláteis totais (BNVT) em camarões Xyphopenaeus kroyeri. Braz J Food Technol 2008: 20:138-144.). Protein nitrogen was precipitated with trichloroacetic acid. The filtered material containing the volatile nitrogen was alkalised, received in a solution of boric acid and mixed indicator (methyl red and bromocresol green) and titrated with standardised sulphuric acid solution.

Peroxides were measured according to Chapman and Mackay(²⁴24 Chapman RA, Mackay K. The estimation of peroxides in fats and oils by the ferric thiocyanate method. JAOCS J Am Oil Chem Soc 1949; 26:360-363.). Fat was extracted from fillets and dissolved (200 μL) in a benzene:methanol solution (70: 30, v/v), followed by the addition of 30% ammonium thiocyanate (10 μL) and ferrous chloride (10 μL). The samples were incubated (50 °C for 2 min) and absorbance was assessed at 520 nm. The results were calculated from the standard curve of iron solution (0.7 to 7.1 μmol).

Thiobarbituric acid reactive substances (TBARS) were evaluated according to Buege and Aust(²⁵25 Buege JA, Aust SD. Microsomal lipid peroxidation. Meth Enzymol 1978; 52:302-310.). The sample (1 g) was homogenised in 1.15% potassium chloride solution (1: 5, w/v) and centrifuged at 3000 rpm for 10 min. The supernatant (0.75 mL) was incubated in a water bath (100 °C for 15 min) with 30% trichloroacetic acid solution and 0.67% thiobarbituric acid. Next, n-butyl alcohol (1.5 mL) was added to extract the coloured product. Absorbance was measured at 535 nm. The results were calculated from the standard curve of malondialdehyde (MDA) solution (0.6 to 12 nmol).

2.5 Microbiological analysis

The standard count of strict and facultative aerobic mesophilic microorganisms in the fillets was conducted according to the methodology proposed by the Brazilian Ministry of Agriculture, Livestock and Supply(²⁶26 Brasil. Ministério da Agricultura, Pecuária e Abastecimento. Instrução Normativa n° 62 de 26 de agosto de 2003. Dispõe sobre os Métodos Analíticos Oficiais para Análises Microbiológicas para Controle de Produtos de Origem Animal e Água. Diário Oficial da União. (https://www.normasbrasil.com.br/norma/instrucaonormativa-62-200375165.html) (accessed: 16 May, 2023).
https://www.normasbrasil.com.br/norma/in... ): 25 g of sample was diluted and homogenised in 0.1% peptone saline solution (1: 10 w/v). A sample (1 mL) of each dilution (10^-1, 10^-2 and 10^-3) was pipetted onto the surface of the plates containing the agar culture medium for counting (PCA), in duplicate. The plates were incubated for 48 h at 36 °C and then the colonies formed were counted. The results are expressed in colony-forming units (CFU) g^-1.

2.6 Statistical analysis

The data were subjected to the normality test, followed by two-way analysis of variance (ANOVA) (the factors were essential oil concentration and refrigeration time). Means were compared using Tukey’s test (p < 0.05), using the statistical program Statistica 7.0.

3. Results

3.1 Chemical composition of EO

By analysing the chemical composition, it was possible to identify the major constituents of the EO, highlighting citral, which is a mixture of neral (18.51%) and geranial (32.05%) isomers, which together represented 58% of the composition. It was also possible to identify a mixture of neranic acid and geranic acid (about 7.83%). Low concentrations of piperitone (0.44%), 6-methyl-hep-5-en-2-one (0.13%) and sabinene (0.09%) were found. Due to the high concentration of citral in the EO, there is a strong indication that its biological activity is attributed to this mixture of isomers.

3.2 Physicochemical analysis

There was a reduction in pH in fillet samples exposed to 0.25 and 0.50% EO at the initial evaluation period (Table 1). After seven days, this reduction was only observed in the samples exposed to 0.25% EO. Fillet samples exposed to control (0%) and 0.50% EO had a higher pH. After 14 days of refrigeration, samples treated with 0.50% EO had a lower pH; it did not differ significantly from the control samples, but was significantly lower than the samples treated with 0.25% EO (Table 1).

The concentration of TVB-N was not altered in fillets exposed to EO in relation to meat from the control treatment (0% EO), in any of the evaluated refrigeration periods. The TVB-N concentration also did not change in the treatments with the passage of refrigeration time (Figure 1). At baseline, values ranged from 8.68 to 9.57 mg %^-1. After seven days under refrigeration, the TVB-N content varied from 8.97 to 10.89 mg %^-1 and in the final evaluation, at 14 days, the values varied from 9.12 to 10.33 mg %^-1.

In relation to the products of fat oxidation, the peroxide content was reduced in meat exposed to both concentrations of EO compared to samples from the control treatment (0% EO), in the initial period and after 7 and 14 days under refrigeration (Figure 2A). In the initial evaluation, the peroxide content found in the control treatment was 0.96 ± 0.11 mEq kg lipid^-1. In meat exposed to EO, values of 0.61 ± 0.06 mEq kg lipid^-1 (0.25% treatment) and 0.57 ± 0.14 mEq kg lipid^-1 (0.50% treatment) were observed. In general, these molecules increased with the storage time of the meat, with the exception of the evaluation at seven days of refrigeration, when lower values of peroxides were found in all treatments (around 0.20 mEq kg lipid^-1).

Likewise, the concentration of TBARS in the tambatinga fillets was reduced on exposure to EO, for all refrigeration periods evaluated (Figure 2B). In the initial evaluation, the values found in the meat (mg MDA kg^-1) were: 3.21 ± 0.25 for the control treatment; 2.07 ± 0.20 for the 0.25% EO treatment; and 1.32 ± 0.17 in the 0.50% EO treatment. As the refrigeration period went on, the concentration of TBARS increased in all treatments, but in a less accentuated way in the fillets exposed to the EO of M. piperita (Figure 2B).

3.3 Microbiological analysis

There were fewer colonies in fillets exposed to 0.50% EO during all periods of refrigerated storage (Table 2).

4. Discussion

The major constituents found in the EO of M. piperita used in the present study were geranial, neral and geranic acid. Neranic acid, piperitone and sabinene were present in low concentrations. The oil was extracted from a plant grown in southern Brazil (RS) and the characterization of the constituents and their concentration differ from those found in the EO of two varieties of M. piperita grown in northeastern Brazil (Ceará). For the chocolate mint variety, the major constituents found were menthofuran (23.7%), menthone (17.2%), D-neo isomenthol (14.3%) and pulegone (10.7%). For the grapefruit mint variety, linalyl acetate (51.3%) and linalool (25.4%) were identified in higher concentrations(²⁷27 Sousa Barros A, Morais SM, Ferreira PAT, Vieira IGP, Craveiro AA, Fontenelle ROS, Menezes JESA, Silva FWF, Sousa HA. Chemical composition and functional properties of essential oils from Mentha species. Ind Crops Prod 2015; 76:557-564. https://doi.org/10.1016/j.indcrop.2015.07.004
https://doi.org/10.1016/j.indcrop.2015.0... ). The same authors also observed that other Mentha species (M. aquatica, M. spicata (menthol mint), leaf spearmint, homegrown mint varieties) had carvone (31-58%) and limonene (20-37%) as major constituents. In another study, Chagas(²⁸28 Chagas EC, Majolo C, Monteiro PC, Oliveira MR, Gama PE, Bizzo HR, Chaves FCM. Composition of essential oils of Mentha species and their antimicrobial activity against Aeromonas spp. J Essent Oil Res 2020; 32(3):209-215. https://doi.org/10.1080/10412905.2020.1741457
https://doi.org/10.1080/10412905.2020.17... ) reported higher concentrations of menthol (33.8%), menthone (15.2%), menthyl acetate (13%) and pulegone (8.3%) in the EO of M. piperita cultivated in north Brazil (Manaus), whereas low concentrations of geranial (1.1%), neral (1.3%), piperitone (1.6%) and sabinene (0.2%) were observed. The authors report that environmental factors such as altitude, soil, temperature, light, fertilization and interactions with predators are conditions that influence metabolic pathways in plants and can change the composition of the EO(²⁹29 Agostini F, Santos ACA, Rossato M, Pansera MR, Santos PL, Serafini LA, Molon R, Moyna P. Essential oil yield and composition of Lamiaceae species growing in Southern Brazil. Braz Arch Biol Technol 2009; 52(2):473-478. https://doi.org/10.1590/S1516-89132009000200026
https://doi.org/10.1590/S1516-8913200900... ,³⁰30 Freire MM, Jham GN, Dhingra OD, Jardim CM, Barcelos RC, Valente VMM. Composition, antifungal activity and main fungitoxic components of the essential oil of Mentha piperita L. J Food Saf 2012. 32:29-36. https://doi.org/10.1111/j.1745-4565.2011.00341.x
https://doi.org/10.1111/j.1745-4565.2011... ). In addition, aspects such as plant geographical origin, genotype, age and vegetative cycle, as well as the plant organ and extraction method used, may cause significant variations in the composition found(³¹31 Souza CF, Baldissera MD, Baldisserotto B, Heinzmann BM, Martos-Sitcha JA, Mancera JM. Essential Oils as Stress-Reducing Agents for Fish Aquaculture: A Review. Front Physiol 2019; 10:1-17. https://doi.org/10.3389/fphys.2019.00785
https://doi.org/10.3389/fphys.2019.00785... ).

Geranial (alpha-citral) and neral (beta-citral) are the two isomeric aldehydes that make up citral, a monoterpene that occurs naturally in herbs, plants and citrus fruits(³²32 Tajidin NE, Ahmad SH, Rosenani AB, Azimah H, Munirah M. Chemical composition and citral content in lemongrass (Cymbopogon citratus) essential oil at three maturity stages. Afr J Biotechnol 2012; 11(11):2685-2693. https://doi.org/10.5897/AJB11.2939
https://doi.org/10.5897/AJB11.2939... ,³³33 Lu W-C, Huang D-W, Wang C-CR, Yeh C-H, Tsai J-C, Huang Y-T, Li P-H. Preparation, characterization, and antimicrobial activity of nanoemulsions incorporating citral essential oil. J Food Drug Anal 2018; 26(1):82-89. https://doi.org/10.1016/j.jfda.2016.12.018
https://doi.org/10.1016/j.jfda.2016.12.0... ). Citral (3, 7-dimethyl-2,6-octadienal) is found in the EO of several botanical species such as Cymbopogon flexuosus(³⁴34 Rampelotto C, Speroni CS, Conte L, Pianesso D, Machado IS, Rodrigues R, Minuzzi NM, Adorian TJ, Klein B, Wagner R, Baldisserotto B, Silva LP, Heinzmann BM, Menezes CR, Emanuelli T. Microencapsuled lemongrass (Cymbopogon flexuosus) essential oil supplementation on quality and stability of silver catfish fillets during frozen storage. J Aquat Food Prod 2021; 30(9):1124-1141. https://doi.org/10.1080/10498850.2021.1974137
https://doi.org/10.1080/10498850.2021.19... ), Aloysia triphylla, Lippia alba and Zingiber officinale, among others(¹⁷17 Souza Silva LT, Pereira UP, Oliveira HM, Brazil EM, Pereira SA, Chagas EC, Jesus GFA, Cardoso L, Mouriño JLP, Martins ML. Hemato-immunological and zootechnical parameters of Nile tilapia fed essential oil of Mentha piperita after challenge with Streptococcus agalactiae. Aquaculture 2019; 506:205-211. https://doi.org/10.1016/j.aquaculture.2019.03.035
https://doi.org/10.1016/j.aquaculture.20... ). In plants such as lemongrass and verbena, strong antibacterial activity is associated with a high citral content (above 35%). In the EO of these plants, antifungal and antioxidant action has also been found(³⁵35 Lis-Balchin M, Deans SG, Eaglesham E. Relationship between bioactivity and chemical composition of commercial essential oils. Flavour Frag J 1998; 13(2):98-104. https://doi.org/10.1002/(SICI)1099-1026(199803/04
https://doi.org/10.1002/(SICI)1099-1026(... ).

The main physicochemical parameters used to determine the degree of freshness of fish are pH and TVB-N(³⁶36 Kuroda CN, Pretto A, Camargo ACC, Stefanello CM, Rosa GM, Ferrigolo FRG, Gollino GP, Ribeiro VB, Bender ABB. Conservation and quality of grumatã (Prochilodus lineatus) fillets after different depuration periods and frozen storage. Cienc Anim Bras 2020; 21:e-62701. https://doi.org/10.1590/1809-6891v21e-62701
https://doi.org/10.1590/1809-6891v21e-62... ). Brazilian legislation(³⁷37 Brasil. Ministério da Agricultura, Pecuária e Abastecimento. Decreto n° 9.013 de 29 de março de 2017. Dispõe sobre a Inspeção Industrial E Sanitária De Produtos De Origem Animal. Diário Oficial da União. Available from: http://www.planalto.gov.br/ccivil_03/_ato2015-2018/2017/decreto/D9013.htm (accessed: May 15, 2023).
http://www.planalto.gov.br/ccivil_03/_at... ) establishes that fish considered fresh must have a pH below 7.0 and a TVB-N of up to 30 mg%. Fish with an excellent state of freshness should have between 5 and 10 mg% TVB-N. In this sense, our results showed that the tambatinga fillets were in an excellent state of freshness until the end of the refrigeration period (14 days). Mentha piperita EO did not affect the TVB-N content, but there were specific changes in the pH of the fillets. The main reasons may be related to the low pH of the meat after rigor mortis, resulting from the anaerobic breakdown of glycogen into lactic acid(³⁸38 Soares KMDP, Gonçalves AA. Qualidade e segurança do pescado. Rev Inst Adolfo Lutz 2012; 71(1):1-10., ³⁹39 Karami B, Moradi Y, Motallebi AA, Hosseini E, Soltani M. Effects of frozen storage on fatty acids profile, chemical quality indices and sensory properties of red tilapia (Oreochromis niloticus × Tilapia mosambicus) fillets. Iran J Fish Sci 2013; 12(2):378-388.), in addition to the adequate process of fish slaughter and meat processing and the evaluated storage time. However, specific changes observed in the pH of tambatinga fillets during refrigeration may be associated with autolytic and bacterial degradation processes, which lead to the generation of alkaline molecules and, consequently, increased the pH of the meat(³⁸38 Soares KMDP, Gonçalves AA. Qualidade e segurança do pescado. Rev Inst Adolfo Lutz 2012; 71(1):1-10., ³⁹39 Karami B, Moradi Y, Motallebi AA, Hosseini E, Soltani M. Effects of frozen storage on fatty acids profile, chemical quality indices and sensory properties of red tilapia (Oreochromis niloticus × Tilapia mosambicus) fillets. Iran J Fish Sci 2013; 12(2):378-388., ⁴⁰40 Afrin F, Islam MM, Rasul MG, Sarkar MSI, Yuan C, Shah AKMA. Effects of seaweed extracts on the quality and shelf life of Nile tilapia (Oreochromis niloticus) fillets during frozen storage. Food Chem Adv 2023; 3:100388. https://doi.org/10.1016/j.focha.2023.100388
https://doi.org/10.1016/j.focha.2023.100... ). Rampelotto(³⁴34 Rampelotto C, Speroni CS, Conte L, Pianesso D, Machado IS, Rodrigues R, Minuzzi NM, Adorian TJ, Klein B, Wagner R, Baldisserotto B, Silva LP, Heinzmann BM, Menezes CR, Emanuelli T. Microencapsuled lemongrass (Cymbopogon flexuosus) essential oil supplementation on quality and stability of silver catfish fillets during frozen storage. J Aquat Food Prod 2021; 30(9):1124-1141. https://doi.org/10.1080/10498850.2021.1974137
https://doi.org/10.1080/10498850.2021.19... ) did not observe any effects of C. flexuosus EO (containing 45.6% geranial and 32.1% neral) on the pH of Rhamdia quelen fillets stored frozen for 12 months. The fish had been fed diets containing 1 or 3 mL EO kg^-1 diet for 20 days before slaughter. The authors reported that the initial pH of the fillets was 6.36, reaching 6.68 after nine months of storage.

Lipid oxidation is one of the main non-microbial changes in meat and leads to changes in sensory properties (colour, flavour, odour and acceptability) and shelf life(⁸8 Mattje LGB, Tormen L, Bombardelli MCM, Corazza ML, Bainy EM. Ginger essential oil and supercritical extract as natural antioxidants in tilapia fish burger. J Food Process Pres 2019; 43(5):e13942. https://doi.org/10.1111/jfpp.13942
https://doi.org/10.1111/jfpp.13942... , ¹¹11 Ribeiro JS, Santos MJMC, Silva LKR, Pereira LCL, Santos IA, Lannes SCS, Silva MV. Natural antioxidants used in meat products: A brief review. Meat Sci 2019; 148:181-188. https://doi.org/10.1016/j.meatsci.2018.10.016
https://doi.org/10.1016/j.meatsci.2018.1... ). Fish meat is especially susceptible to lipid oxidation due to its high content of unsaturated fatty acids. In this sense, M. piperita EO proved to be efficient in delaying lipid oxidation, as evidenced by the lower formation of peroxides and TBARS in tambatinga meat stored refrigerated for up to 14 days. According to Lis-Balchin(³⁵35 Lis-Balchin M, Deans SG, Eaglesham E. Relationship between bioactivity and chemical composition of commercial essential oils. Flavour Frag J 1998; 13(2):98-104. https://doi.org/10.1002/(SICI)1099-1026(199803/04
https://doi.org/10.1002/(SICI)1099-1026(... ) and Chandra and Farook Ah(⁴¹41 Chandra H, Farooq Ah A. Lipoxigenase inhibitory, antioxidant, and antimicrobial activities of selected essential oils. Asian J Pharm Clin Res 2014; 7:79-83.), the EO of plants such as C. flexuosus and verbena, species that have citral as one of the main components of their EO, show antioxidant activity in vitro. The isolated constituent (citral) was also tested and showed an increase in antioxidant activity, determined by the Ferric Reducing Antioxidant Power (FRAP) method, as the concentration increased (5-40 mg mL^-1)(⁴¹41 Chandra H, Farooq Ah A. Lipoxigenase inhibitory, antioxidant, and antimicrobial activities of selected essential oils. Asian J Pharm Clin Res 2014; 7:79-83.). Therefore, according to these findings, our hypothesis is that citral is mainly responsible for the antioxidant action of M. piperita EO on tambatinga meat.

In a previous study, supplementation with C. flexuosus EO, containing around 77% citral, directly in the fish diet did not show a protective effect against lipid oxidation (based on the content of conjugated dienes, peroxides and hexanal) or protein oxidation (total content of sulphhydryl groups reduced and carbonyl protein) in silver catfish meat(³⁴34 Rampelotto C, Speroni CS, Conte L, Pianesso D, Machado IS, Rodrigues R, Minuzzi NM, Adorian TJ, Klein B, Wagner R, Baldisserotto B, Silva LP, Heinzmann BM, Menezes CR, Emanuelli T. Microencapsuled lemongrass (Cymbopogon flexuosus) essential oil supplementation on quality and stability of silver catfish fillets during frozen storage. J Aquat Food Prod 2021; 30(9):1124-1141. https://doi.org/10.1080/10498850.2021.1974137
https://doi.org/10.1080/10498850.2021.19... ). The authors observed a variable response according to the EO concentration used: fish fed with 1 mL EO kg^-1 showed a slight increase in the lipid oxidation of the meat over 12 months under freezing. In contrast, the meat of fish fed 3 mL EO kg^-1 showed an increase in protein oxidation over the storage period.

In addition to freshness and oxidative stability analyses, microbiological evaluation of fish meat is important to demonstrate its quality and durability, because spoilage in fish occurs mainly as a result of bacteriological activity(⁴²42 El-Hanafy AEA, Shawky HA, Ramadan MF. Preservation of Oreochromis niloticus fish using frozen green tea extract: impact on biochemical, microbiological and sensory characteristics. J Food Process Pres 2011; 35:639-646. https://doi.org/10.1111/j.1745-4549.2011.00513.x
https://doi.org/10.1111/j.1745-4549.2011... ). The use of 0.50% M. piperita EO kept the microorganism count in tambatinga meat low during the entire refrigeration period. The count for this treatment was 2-4-fold lower compared with the fillets treated with 0% or 0.25% EO. According to in vitro studies, the high antibacterial and antifungal activity of C. flexuosus is related to the strong activity of citral, which is the main monoterpene in its EO(³⁵35 Lis-Balchin M, Deans SG, Eaglesham E. Relationship between bioactivity and chemical composition of commercial essential oils. Flavour Frag J 1998; 13(2):98-104. https://doi.org/10.1002/(SICI)1099-1026(199803/04
https://doi.org/10.1002/(SICI)1099-1026(... ,⁴¹41 Chandra H, Farooq Ah A. Lipoxigenase inhibitory, antioxidant, and antimicrobial activities of selected essential oils. Asian J Pharm Clin Res 2014; 7:79-83.). The antimicrobial action of M. piperita EO found in the present study is consistent with this information.

5. Conclusion

Mentha piperita EO displayed the constituent forms of citral (geranial and neral) as the most abundant molecules. Treating tambatinga fillets with this EO helped reduce lipid oxidation and the development of microorganisms. The concentration of 0.50% of this EO in solution was more effective in reducing the deterioration of meat kept refrigerated.

References

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