Introduction
Cheese is one of the most commonly used food products worldwide since it can be produced from a wide range of milk types, and with various technologies, people can achieve considerable product varieties. People have shown an increasing inclination to consume this product due to its scrumptious, great protein level and being perceived as a healthy food (Gouvea et al., 2017). However, this food product is easily contaminated and spoils by pathogenic microorganisms, adversely affecting shelf life and jeopardizing the consumer’s health. It was documented that Listeria monocytogenes, Staphylococcus aureus and Salmonella spp. are often associated with food-borne diseases due to cheese consumption (Gouvea et al., 2017).
White cheese is manufactured by using different kinds of milk. This product is constantly in the human diet, rich in protein, calcium, minerals and vitamins. Cheese consumption has experienced a dramatic rise worldwide during the past several years. However, its physical, sensory, color and chemical properties have been proven to result from biological and biochemical reactions throughout storage.
White cheese is somewhat susceptible to contamination and spoilage by pathogenic microorganism-induced contamination, which is likely to decrease shelf life and pose a severe threat to the health of human beings. The bacteria, molds, and yeasts are usually responsible for this contamination, decreasing flavor and cheese quality. This outcome usually occurs when the product is stored without packing (El-Sayed & El-Sayed, 2021).
Using modified atmosphere packaging (MAP) has gained more popularity in increasing the shelf life of various foods due to consumers’ increased demands for preservative-free, “clean label” foods. Modifying the gas content surrounding a food product during storage, including N2 and CO2, will result in comparatively lower physiological deterioration, oxidation reactions, and microbial growth rate (Brown et al., 2018).
Presently, various preservation methods have promoted the shelf storage of food products, the most promising of which is packaging. Certain important functions are attributed to the packaging process, including prevention of deterioration by microbial and chemical changes and development in handling and marketing of packaged goods. Currently, the purpose of food packaging extends beyond convenience and protection attributes (Khoshgozaran et al., 2012). MAP has gained a significant position in research areas as a pragmatic method to preserve the quality of various food products and satisfy customers’ growing demands for fresh and preservative-free food (Khoshgozaran et al., 2012). Moreover, this technique is characterized by several crucial outcomes, including retaining the quality of fresh products, promoting the visual and appearance properties of the product, extending the shelf life and minimizing the application of additives and preservatives (Khoshgozaran et al., 2012).
In recent years, the application of natural antimicrobial agents for food preservation has gained wide acceptance due to the public unpopularity of synthetic additives, which are frequently used to inhibit microbial proliferation in food products. Essential oils (EOs) are extracted from medicinal plants with significant antimicrobial activity against various pathogenic and damaging microorganisms (Artiga-Artigas et al., 2017).
Cuminum cyminum is a small, herbaceous, annual plant that belongs to the Umbelliferae family (Petretto et al., 2018). This plant is found in Asia, North Africa, Europe, and America and has also been cultivated in Middle Eastern countries, India, China and the Mediterranean countries (Petretto et al., 2018; Akrami et al., 2015). The seeds of this plant are constantly used as a flavoring spice in various recipes belonging to different cultures (Petretto et al., 2018), particularly in cooking and making salads (Karimirad et al., 2019). Moreover, different varieties of this plant are of extensive use in both traditional and veterinary medicine as stimulant, carminative, astringent and as a treatment for indigestion, flatulence, and diarrhea (Akrami et al., 2015; Derakhshan et al., 2008). C. cyminum essential oil (CCE) has high levels of γ-terpinene, p-cymene, pinene, cumin aldehyde, safranal, and cuminal with antimicrobial and antioxidant properties (Karimirad et al., 2019). CCE has an appropriate antimicrobial and antioxidant activity that can be applied as a suitable food preservative agent (Petretto et al., 2018).
The current study aimed to assess (i) the combined effect of CCE and MAP for the control of L. monocytogenes inoculated to white Iranian white cheese and (ii) the possible shelf life extension of white Iranian white cheese using the mentioned combination.
Materials and Methods
Plant material
C. cyminum seeds were collected from Kerman City, Iran, in the summer of 2020. Taxonomic identification of plant material was carried out by the Institute of Medicinal Plants, University of Tehran, Iran.
Essential oil extraction and analysis
In the preparation phase, 100 g of powdered seeds were mixed with 1000 mL of distilled water. The CCE was obtained via the ‘clevenger apparatus’ for 3 hours. Dehydration of CCE was done by adding sodium sulfate. The collected CCE was stored in dark glass at 4 °C for further analysis (Karimirad et al., 2019; Akrami et al., 2015). The gas chromatography-mass spectrometry analysis was performed according to the method described by Akrami et al., (2015).
Preparation of test microorganisms
L. monocytogenes (ATCC1918) was inoculated in brain heart infusion (BHI) broth. After 24 h incubation at 35 °C, the second subculture was prepared and incubated for 24 h at 35 °C. The L. monocytogenes broth culture was placed in a sterile cuvette and optical density (OD) was adjusted to an absorbance of 0.1 using a spectrophotometer (Jenway, UK). Then, the number of cells in the suspension was estimated by duplicate plating from 10-fold serial dilutions on BHI agar and counting the colonies after 24 h incubation at 35 °C and then the suspension was diluted to 4 logs CFU/mL using 0.1% peptone water preparation of white cheese.
Fresh and whole cow’s milk was pasteurized to produce Iranian white cheese at 72±2 °C for 15 s. Before starting the different stages of cheese-making, the milk temperature was raised to 35 °C and 10 L of milk was added to the cheese-making container. After that, the 0.5% (V/V) starter was added to the milk samples simultaneously. After half an hour, the amount of 0.02% (weight by volume) of calcium chloride (CaCl2) (weight by volume) in 20 mL of sterile distilled water at a temperature of 40 °C was added to the milk. Finally, 0.001% (W/V) rennet was added and the milk temperature was maintained at around 35 °C during the clot formation. After one hour, the formed clot was cut into 1-2 cubic cm pieces and according to the instructions for making Iranian white cheeses, it was put under 10 kg pressure for 6 hours to absorb water. Then, the clot was cut into pieces with dimensions of 6×8×12 cm and placed in 2% sterile salt water for 42 days at a temperature of 4 °C. Immediately after spraying, all blocks were packaged in plastic trays and sealed by a sealing machine. Finally, the samples were air-packaged and gas-flushed with 30% CO2+70% N2, sealed using a MAP machine, and stored at 4 °C so the tests could be carried out on day 35 (Govaris et al., 2011).
Microbiological characteristics of white cheese throughout storage
About 25 g of cheese samples were homogenized with 225 mL of sterile tri-sodium citrate (2.00% w/v) for 1 min. After that, decimal dilution with 9 mL sterile NaCl (0.85%) was performed.
The microbiological properties of white cheese samples were determined as follows:
LAB count was enumerated by using MRS agar; yeasts and mold counts were determined on Rose Bengal Chloramphenicol agar; TMC and PSB were estimated on plate count agar; L. monocytogenes bacteria counts were determined using PALCAM Listeria selective agar (El-Sayed & El-Sayed, 2021).
Statistical analysis
The experimental data were analyzed by analysis of variance and the significant differences between mean values in different sampling days were evaluated by Duncan’s multiple range test/least significant difference. Data was analyzed using the SPSS software, version 14.
Results
Chemical composition of CCE
The analysis of CCE revealed that the EO yield is 4% (v/w). Among all constituents identified by GC/MS, 1, 4-p-Menthadien-7-al and cumin aldehyde stand as the two major compounds with 32.20% and 29.57% percentages, respectively (Table 1).
Microbiological characteristics of white cheese during the storage period
In general, compared to control samples, all coatings in this experiment exhibited significant antibacterial activity against TMC, PSB, LAB, Enterobacteriaceae and L. monocytogenes in white cheese packed in air and MAP during refrigerated storage (Figures 1, 2, 3, 4 and 5).
Comparatively, higher bacterial counts were present in groups packed in air than in MAP (P<0.05). It can be seen from Figures 1 and 2 that the initial TMC and LAB of white cheese samples were found to be 4.5 and 4.32 log CFU/g, respectively. The TMC and LAB of control samples constantly increased and reached 7.53 and 7.54 log CFU/g after 35 days of storage in air packaging, respectively (Figsures 1 and 2). The TMC and LAB of control samples continuously increased and reached 7.22 and 6.1 log CFU/g after 35 days of storage in MAP packaging, respectively. Packing conditions determined the growth of TMC and LAB. The lowest TMC and LAB belonged samples packed in MAP+0.06% CCE were 6.26 and 5.51 log CFU/g, respectively.
In the present study, PSB count in the control group was found to increase from an initial count of 5.43 log CFU/g to 7.9 log CFU/g at the end of chilled storage in air packaging and an initial count of 5.43 log CFU/g to 6.09 log CFU/g at the end of chilled storage in MAP packaging. The smallest PSB count belonged to samples packed in air +0.06% CCE (6.72) after 35 days of storage. The lowest PSB count was obtained for samples packed in MAP+0.06% CCE (5.72) after 35 days of storage (Figure 3).
In the present study, mold and yeast counts in the control group were increased from an initial count of 6.77 log CFU/g to 8.37 log CFU/g at the end of chilled storage in air packaging and an initial count of 6.77 log CFU/g to 7.73 log CFU/g at the end of chilled storage in MAP packaging. The lowest mold and yeast count belonged to samples packed in air +0.06% CCE after 35 days of storage. The lowest mold and yeast count was achieved in the case with samples packed in MAP+0.06% CCE after 35 days of storage (Figure 4).
In the present study, L. monocytogenes count in the control group was found to increase from an initial count of 4.22 log CFU/g to 8.23 log CFU/g at the end of chilled storage in air packaging and an initial count of 4.22 log CFU/g to 6.98 log CFU/g at the end of chilled storage in MAP packaging. The lowest L. monocytogenes count was determined to belong to samples packed in air +0.06 % CCE (6.87 log CFU/g) after 35 days of storage. The lowest L. monocytogenes count was achieved in the case with samples packed in MAP+0.06 % CCE after 35 days of storage (Figure 5).
No coliforms were detected in any batch of cheese produced for the shelf life experiments.
Discussion
The analysis of used CCE revealed that 1, 4-p-menthadien-7-al and cumin aldehyde stand as the two major compounds of this essential oil (Table 1). This finding agrees with Karimirad et al., (2019), who reported cumin aldehyde at 23.6% and γ-terpinen-7-al at 22.23% are the major components of CCE. Petretto et al., (2018) noted 25 compounds identified with γ-Terpinen-7-al as the major CCE component. Derakhshan et al., (2008) noted declacumin aldehyde with 25.2%, p-mentha-1,3-dien-7-al with 13% and p-mentha-1,4-dien-7-al with 16.6%. Also, El-Sayed & El-Sayed, (2021) noted cumin aldehyde (30.9%), sabinene (14.3%), p-cymene (13.3%), γ-terpinene (12.6%), cuminyl alcohol (11.5%) and p-cymen-7-ol (8.8%).
According to certain studies, the quality and quantity of certain EOs can be affected by factors such as harvesting season, geographic location, soil conditions, and essential oil extraction technique (Kalemba & Kunicka, 2003; Kizil et al., 2010).
Furthermore, as reported by Eikani et al. (1999), cumin aldehyde and cuminyl alcohol have potent antimicrobial and antioxidant properties with an extensive range. As a result, they may be considered appropriate candidates for preserving agents and are promising to the food industry.
Monoterpenes compounds, such as cumin aldehyde, were reported to be responsible for C. cyminum EO’s antimicrobial activity. The antibacterial effect of EO plants may be associated with the hydrophobicity nature of constituent’s EO, especially oxygenated monoterpenes, and their capability to disrupt the lipid layer of the cell membrane and interact with membrane proteins and intracellular targets of microorganisms. This phenomenon is believed to be able to change the bacterial phospholipid membrane and, as a result, reduce cellar uptake of ethidium bromide while increasing leakage of potassium ions, ATP, and carboxyfluorescein (Kakaei & Shahbazi, 2016).
Hydrocarbon derivatives have been reported to have a low antimicrobial function when used alone. Their low water solubility and limited hydrogen-bound capacity are responsible for this phenomenon. However, the compounds mentioned before can potentiate the activity of terpenoids such as cumin aldehyde, γ-terpinen7-al and γ-terpinene (monoterpene aldehydes), which exhibit a higher antimicrobial potential owing to their functional groups. For instance, aldehyde moiety by amino groups can link with DNA and proteins and interfere with their normal function. Furthermore, it has been stated that hydrocarbon monoterpenes like p-cymene promote the entrance of other compounds into the cell wall via swelling of the cell membrane (Karimirad et al., 2019).
Regarding crucial foods and pathogens, only a limited number of studies have been conducted on this essential oil.
De et al. (2003) examined the antimicrobial properties of some Indian spices and investigated the antimicrobial properties of C. cyminum against the microbes tested (Bacillus subtilis, Escherichia coli), resulting in the approval of its usage as a disinfectant food preservative.
In another study, Chaudhry Ahmed et al. (2008) examined the antibacterial properties of extracts of a few plants such as Shab-kur, C. cyminum, and Poppy against 188 species of bacteria such as B. subtilis, Saccharomyces cerevisiae, and E. coli, via disk diffusion method (DDM). They concluded that green cumin extract had the greatest inhibitory effect (73%) on bacteria.
According to Sadeghi et al. (2008), CCE was reported to contain 29.02% cumin aldehyde, 20.70% Alpha-terpinene, and 12.94% gamma-terpinene. It was also observed that the growth rate of S. aureus can significantly be reduced in cheese during 75 days of storage compared to the control group by adding 30 mL/100 µL of CCE.
In another study, the antimicrobial effects of CCE against 10 bacterial strains belonging to 8 different species and 6 yeast strains from 4 species were examined by Petretto et al., (2018). LAB exhibited great resistance to all EO tested, while the CCE showed a strong antifungal activity that affected both maximum specific growth rate and lag time.
Dairy products are categorized as the most popular food, and nutritionists highly recommend them. This food category is critically perishable; therefore, it is crucial to increase its shelf life to make it fresher. As a result of consumers’ increased knowledge about the threats of preservatives, technologists and researchers have attempted to introduce novel preservative-free methods, one of which is MAP, which modifies the natural gas surrounding the product in the package to delay deteriorative changes.
Since CO2 inhibits various spoilage and pathogenic microorganisms, especially gram-negative bacteria and molds, it is usually employed in MAP. Inhibition of microbial growth by CO2 has been provided in the MAP of perishable foods, improving the shelf life. However, CO2 inhibition activity against microbial growth increases under chilled conditions since CO2 is more soluble in food at lower temperatures (Lee et al., 2008). In addition to controlling and to retard microbial growth, the presence of CO2 in the package’s headspace also leads to the change in the microbial content to bacteria with lower spoilage capacity (McMillin, 2008). Low temperature during storage helps this capacity.
Several studies have confirmed the effect of MAP in the development of the shelf life of dairy products, especially cheese, and a variety of gas compositions has been suggested for MAP of cheese. The storage stability of 24-month-old portioned-packed Parmigiano Reggiano cheese, packed in nylon/polyethylene bags and stored for 3 months at 4 °C, was examined by Romani et al. (1999). No particular change occurred in the quality of different packed products, though samples packed in a 100 % N2 atmosphere exhibited flavor profiles quite distant from freshly cut, unpacked cheese. The fungal growth and mycotoxin production on commercial sliced cheddar cheese under modified atmospheres were examined by Taniwaki et al. (2001). Eight fungal species were incubated under conditions of decreasing levels of O2 (5% to packed in aluminum foil and modified atmospheres (100% N2, 30% CO2/70% N2, 50% CO2/50% N2, 70% CO2/30% N2, 100% CO2, 30% CO2/60% N2/10% O2, 70% CO2/20% N2/10% O2 using oriented polyethylene polyamide as the packaging material) as well as in vacuum. The proliferation of coli bacteria was observed in the experimented cheese in aluminum foil. In contrast, the population of the coli group remained unchanged in other samples during the storage period, irrespective of the applied gas mixture.
In another relevant study, the shelf life of Mozzarella cheese was examined by Alam and Goyal (2007) in different atmospheres (air, vacuum, 100% CO2, 100% N2, and 50% N2/50% CO2) packed in high-barrier bags and stored at ₋10 °C to ₋15 °C. According to their observations, Mozzarella cheese under MAP showed a significant increase in its shelf life compared to that of kept in a conventional air package (14–16, 90, 75 and 65 days under air, 100% CO2, 50% N2/50% CO2 and 100% N2, respectively).
In the current study, the PSB count in the control group increased from 5.43 log CFU/g to 7.9 log CFU/g at the end of chilled storage in air packaging and an initial count of 5.43 log CFU/g to 6.09 log CFU/g at the end of storage period in MAP. It was demonstrated by Alves et al. (1996) that MAP (100% CO2) could decrease just the beginning of the PSB growth in Mozzarella cheese, which was similar to other studies (Pintado and Malcata 2000 on Requeijão cheese; Gammariello et al. 2009 on Apulian fresh cheeses). Moreover, Eliot et al. (1998) reported the presence of PSB during the first weeks of storage for the products with the modified atmospheres (10%, 25%, 50%, 75%, 100% N2) since PSB is a complicated population and species in Mozzarella cheeses are resistant to CO2 inhibitory effect. In addition, various storage temperatures (10 °C by Moir et al. 1993 on Cottage cheese; 7 °C by Alves et al., 1996 on Mozzarella cheese; 10 °C by Eliot et al., 1998 on Cameros cheese; 4 °C by Gonzalez-Fandos et al. 2000 on Cameros cheese) have been evaluated as a possible contributor means for MAP in controlling PSB growth and applying low temperatures were found as an effective way in combination with MAP. Due to lower temperatures, a higher inhibitory effect of CO2 can be achieved by higher CO2 solubility.
These findings are in line with the studies noted for whey cheese (Dermiki et al., 2008), fresh goat cheese (Gonzalez-Fandos et al. 2000) and Mozzarella (Alam & Goyal, 2011) cheese, where psychrotolerant growth was lower when the CO2 concentration increased, with 100% CO2 conditions was the most effective in the growth inhibition. These findings agree with the article which showed that most psychrotolerant bacteria in dairy products are aerobic, gram-negative, and usually more sensitive to CO2 than gram-positive ones (Rosenthal et al., 1991).
In the present study, mold and yeast counts in the control group were found to increase from 6.77 log CFU/g at the beginning of the study to 8.37 log CFU/g after 35 days of storage at chilled storage in air packaging and an initial count of 6.77 logs CFU/g to 7.73 logs CFU/g at the end of refrigerated storage in MAP packaging. The lowest mold and yeast count belonged to samples packed in air +0.06% CCE (7.7) after 35 days of storage. The inhibition and decrease in yeast and mold population under modified atmospheres compared with growth when packaged under air were confirmed by the previous reports for Mozzarella kept under the same conditions (Alam & Goyal, 2011). The controlling effect of CO2 on the count of bacteria and yeast is also in line with the previous reports (Alves et al., 1996; Eliot et al., 1998; Dermiki et al., 2008).
Since the 1970s, L. monocytogenes has been considered an important food-borne pathogen. Foods such as vegetables, meat, and even certain cheeses are ideal for Listeria growth (Genigeorgis et al., 1991; Mossel et al., 1995). Outbreaks of listeriosis following the consumption of Mexican-style cheese from California (James et al. 1985), Mexican soft cheeses (Linnan et al. 1988) and Vacherin Mont D’Or (Bille, 1990) have led to concerns toward L. monocytogenes. The inhibitory effect of CO2 on L. monocytogenes was reported by Chen and Hotchkiss (1991), especially in a hurdle technology with cold-temperature storage (4 °C) and pH in Cottage cheese. In the present study, L. monocytogenes count in the control group increased from 4.22 log CFU/g to 8.23 log CFU/g at the end of the study period in air packaging and an initial count of 4.22 log CFU/g to 6.98 log CFU/g at the end of refrigerated storage in MAP. According to the study of Brown et al., 2018 which evaluated the effect of MAP on L. monocytogenes on fresh cheese, the mean of L. monocytogenes counts increased to levels significantly higher than inoculation on cheeses stored under MAP conditions.
Enterobacteriaceae are suggested to indicate fecal contamination within food analysis, including zoonotic bacteria such as Salmonella spp., Yersinia spp. and E. coli. Enterobacteriaceae can cause serious infections in humans, while many of the major important members of the genus of this family are resistant to many of the available antimicrobials (Paterson, 2006). Coliforms were not isolated in this study’s Iranian white cheese batch.
Conclusion
The result of the current investigation indicated that the combination of CCE and MAP conditions had a strong antimicrobial effect on L. monocytogenes and extended their shelf life. Accordingly, MAP+0.06% CCE exhibited the best inhibitory effects on the microbial population.
Ethical Considerations
Compliance with ethical guidelines
There were no ethical considerations to be considered in this research.
Funding
This research was financially supported by the Research Council of the University of Tehran, Tehran, Iran (Grant No.: 27931/6/16).
Authors' contributions
Writing the original draft: Leila Khaji and Negin Noori; Supervision: Negin Noori and Ashkan Jebelli Javan; Methodology: Hassan Gandomi; Data analysis and visualization:Ali Khanjari.
Conflict of interest
The authors declared no conflict of interest.
Acknowledgments
The authors acknowledge the staff of the Department of Food Hygiene and Control Laboratory of the Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran.
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