Antibacterial and antiseptic activities of various spices to the mala food ingredients

Abstract

Chinese Mala dishes, typical and traditional Chinese cuisines, have a high risk of exposure to contaminants due to its characteristic cuisine culture where customers can personally add ingredients into the dish. The main spices added to mala dishes commonly have antibacterial and antiseptic properties. This study was conducted to find spices and concentrations suitable for inhibiting bacterial infection and spoilage of Mala cooking ingredients. Ten types of ingredients bought from professional Mala restaurants were checked for the occurrence of bacteria in the Mala dishes. Six major spices sauce constituting the Mala dishes were added to food ingredients with severe bacterial contamination, and the progression of spoilage was observed for 47 days. E. coli and 9 species of bacteria were found in all ingredients, and 2 species of them were C. geocarposphaerae and E. americana, which known to be found in human wounds. Of the 6 types of spices, Star anise and Sichuan pepper best inhibited the bacteria growth and slowed the spoilage progression of ingredients. In conclusion, Mala cooking ingredients can be contaminated with various bacteria due to its unique storage method, but Star anise or Sichuan pepper could be safely protected the ingredients from bacteria and spoilage.

Keywords:
antibacterial; antiseptic; mala; Sichuan pepper; spice; Star anise

1 Introduction

Chinese mala cuisine is gaining popularity and spreading around the world (Hankyung Economy News, 2019), and in Korean mala cuisine franchise 'La Hua Kungbu', it is growing from 35 in 2018 to 80 in 2019, and 10 stores every month (MK Economy News, 2019). In Malatang restaurants, the ingredients that are added in the dish are on display for the customers to personally pick and choose, which is a characteristic of Chinese restaurant culture. Malatang called Chinese spicy hot pot is a dish in which the diners select fresh vegetables, fish cakes, tofu, noodles, meat, etc., and boil them with various spices (CGTN News, 2019). However, since the ingredients for malatang are stored in a container filled with water and picked with one tong, sources of contamination between ingredients can easily spread and the entire ingredient can be contaminated. According to the investigation conducted by the South Korean Ministry of Food and Drug Safety in July 2019 of 63 restaurants selling ‘Malatang’ and ‘Mala xiang guo’ (spicy stir-fry hot pot), of which 37 places were found in violation of the Food Sanitation Act (Korea, 2019). Thus, restaurants selling Malatang/Mala xiang guo can be health-threatening for hygiene and sanitation, this problem must be solved.

Spices have been used as food and flavoring since ancient times because of their antibacterial properties that increase the safety and shelf life of foods (Manasa et al., 2021). The six main spices that are added in Mala cuisine are Star anise, Clove, Sichuan pepper, Fennel, Cinnamon, and Cumin, all of which come together to create the characteristic taste (DayDayNews, 2019).

Star anise (Illicium verum) has a star shape and its fruit is a very important element as a spice in oriental cuisine. It is highly valued as a medicinal plant in countries such as China and Vietnam and its several biologically important phytochemicals are known. It also has antibacterial, antiviral and antioxidant properties (Patra et al., 2020). Clove (Eugenia caryohyllata) is widely used in oriental medicine as an antiseptic for infectious diseases such as periodontal disease due to its antibacterial activity against oral bacteria (Prastuty et al., 2021), and in the food industry, it is used as a natural additive or preservative to extend the shelf-life of food (Xu et al., 2016). Sichuan pepper (Zanthoxylum bungeanum) is mainly grown in China and Southeast Asian countries and has a unique pungent taste called ‘maa’ and is used as a spice in various Chinese dishes (Rui-Xue, 2011). Sichuan pepper has been traditionally used as an herbal medicine because of the belief that it relieves abdominal pain from ascariasis, promotes stomach health, reduces inflammation, and relieves pain caused by dental caries (Gong et al., 2009). Fennel (Foeniculum vulgare) is widely grown in temperate and the tropical regions and is used as a culinary ingredient (Singh et al., 2006). The essential oil of fennel seeds is known to have significant antifungal and antibacterial activities (Liu et al., 2017). Cinnamon (Cinnamomum zeylanicum) is widely used in savory dishes, pickles and soups (Ranasinghe et al., 2012). The three main compounds of cinnamon are cinnamaldehyde, cinnamyl acetate and cinnamyl alcohol (Khasnavis & Pahan, 2012) and due to their antibacterial activities, cinnamon is used in cosmetics or food products (Nabavi et al., 2015) as well as to treat diseases such as inflammation, gastrointestinal disorders and urinary infections (Brierley & Kelber, 2011; Al-Jiffri et al., 2011). Cumin (Cuminum cyminum) has been used as food ingredients in the Middle East since ancient time and cumin seeds have been used as antiseptic and disinfectant in India (Mohammad Reza et al., 2015; Feng et al., 2020). The major bioactive components of cumin essential oils are cuminaldehyde, cymene and terpenoids (Allahghadri et al., 2010).

As described above, the spices added to mala dishes have antibacterial and antiseptic effects in common, which can help to solve the hygiene problem of food materials in Chinese restaurants. Therefore, this study was conducted to find out a safe storage method to prevent bacterial contamination and spoilage of food ingredients displayed mainly in Chinese restaurants using these spices.

2 Materials and methods

2.1 Preparation of food ingredients

Oyster mushroom, winter mushroom, black mushroom, tofu, starch noodle, bean sprouts, lotus root, spinach, beef and lamb meat that were on display at Mala Restaurant (Malagongbang, South Korea) were purchased and placed in separate plastic bags. The 10 types of purchased ingredients were stored at 4 °C after less than an hour of leaving the restaurant.

2.2 Preparation of spices

1 g each of cinnamon, cloves, fennel, Star anise, cumin, and Sichuan pepper, which are main spices added to mala dishes, and 100 mL of distilled water were put in a beaker, mixed with a magnetic stirrer for 5 minutes and filtered through filter paper (Whatman, UK) to separate the solution.

2.3 Bacterial contamination test of food ingredients

Each of the 10 food ingredients was put into a beaker, distilled water 10 times the mass of each ingredient was added and the mixture was mixed with a magnetic stirrer for 5 minutes. 1 mL of each mixture was dropped onto a Coliform Count Plate (3M^TM petrifilm^TM) and after 48 hours of cultivation in room temperature, the bubble number of CO₂ generated was counted.

A 10 µL loop was immersed in a solution of various food ingredients, inoculated in TSA plate and incubated at room temperature for 48 hours. The colonies generated on the TSA plate were classified and pure culture was performed. After that, it was analyzed by Macrogen Co., Ltd (South Korea) to identify bacteria through 16s rRNA analysis and BLASTN test.

2.4 Antibacterial activity test of spices

200 µL of each spice solution was added to 1800 μL of each food ingredient solution, and incubated at room temperature for 48 hours. 1 mL of the cultivated solution was dropped onto a Coliform Count Plate (3M^TM petrifilm^TM), cultivated for 48 hours in room temperature, and then the CO₂ bubble number was counted.

In addition, 1%, 2%, 3%, and 4% solutions of Sichuan peppers and Star anise were put in 20% bean sprouts solution, respectively, and incubated at room temperature for 48 hours. Thereafter, the cultured solution was inoculated on a TSA plate and incubated for another 48 hours.

2.5 Antiseptic activity test of spices

After preparing seven 100 mL glass bottles, 5 g of beef, 5 g of lamb, 1g of winter mushroom, 0.4 g of bean sprouts, 4g of starch noodles were added to each glass bottle. 1.5 g of each of the six spices were put in another bottle, and another one did not have spices added. The lids were sealed, and the changes in the ingredients’ conditions inside were photographed to check the spoilage state over time.

3 Results

3.1 Bacterial contamination of food ingredients

Mala dish restaurants display and store ingredients in open environments for customers to pick and choose. In such environments, ingredients are vulnerable to bacterial contamination. The degree of bacterial contamination of ingredients directly purchased from a restaurant specializing in Mala cuisine were investigated.

1. A

   Escherichia coli

There is a total of 10 food ingredients, consisting of 3 types of mushrooms, 4 types of vegetables, 2 types of meat, and starch noodles. The number of E. coli colonies generated per 1 mL of tofu, starch noodles and bean sprouts solution were 105, 128, and 150, respectively, the highest among all the test ingredients (Figure 1). In the 3 types of mushrooms, a similar amount of E. coli was present, and there were relatively low levels of E. coli in lotus root, spinach and the 2 types of meat. The 2 types of meat were not in an open container but stored separately in the kitchen, which might have contributed to their relatively low E. coli levels. It was confirmed that storing ingredients in an open environment increases the E. coli contamination.

Figure 1
The number of E. coli colonies generated from each ingredient (Note: The number of E. coli colonies was generated in 1 mL of a solution in which each ingredient was mixed in 100 times distilled water).

1. B

   General bacteria

The general bacteria contamination of the food ingredients was compared using TSA plates. Various types of bacterial colonies were observed, and a total 9 bacterial colonies were classified according to 7 categories; shape, color, margin, elevation, size, texture, optical properties. By observing the distribution of bacteria for each ingredient, one or more bacteria strains were found in all ingredients (Table 1). Four types of bacteria were found in tofu, bean sprouts, and lotus root among various ingredients, indicating that these 3 ingredients were contaminated with the most bacterial species.

Table 1
Distribution of bacterial colonies generated in each ingredient.

	Vegetable				Mushroom		Meat
	tofu	bean sprouts	lotus root	spinach	oyster mushroom	winter mushroom	beef	lamb
Strains	4	4	4	2	2	2	1	1

The 4 most common bacterial colonies were identified through genetic analysis (Table 2). The Bacteria species were confirmed as Chryseobacterium geocarposphaerae, Ewingella americana, Pseudomonas extremaustralis, Variovorax boronicumulans respectively. C. geocarposphaerae, P. extremaustralis, V. boronicumulans are, in general, present in soil and water. It can be presumed the bacteria were introduced from the food ingredients (Park et al., 2006; Ivanova et al., 2002; Miwa et al., 2008). In contrast, C. geocarposphaerae and E. americana are commonly known to be found in human clinical samples (Holmes et al., 2013; Grimont et al., 1983), suggesting that contamination is possibly originated from humans. Additionally, all four bacterial species can survive in body temperatures, which gives a possibility for them to be re-contaminated to humans. These findings support that food ingredients stored in exposed environments and handled by lots of people can cause bacterial contamination, which can be re-transferred to people.

Table 2
Identification and characteristics of bacterial colonies most generating in the ingredients.

Scientific name	Aero condition	Source	Growth temperature	Gram stain	Origin*
Chryseobacterium geocarposphaerae	Aerobic (Kangale et al., 2021)	Soil, plant (Park et al., 2006), clinical samples (Holmes et al., 2013)	28 °C, 30 °C (Reimer et al., 2019), 37 °C (Kangale et al., 2021)	Negative (Kangale et al., 2021)	bean sprouts, lotus root
Ewingella americana	Facultative anaerobic (Grimont et al., 1983)	Human clinical samples (Grimont et al., 1983)	37 °C (Grimont et al., 1983)	Negative (Grimont et al., 1983)	bean sprout, lotus root, lamb, spinach
Pseudomonas extremaustralis	Aerobic (Ivanova et al., 2002)	Water (Ivanova et al., 2002)	4-37 °C (López et al., 2009)	Negative (Ivanova et al., 2002)	tofu, lotus root
Variovorax boronicumulans	Aerobic (Miwa et al., 2008)	Soil (Miwa et al., 2008)	4-37 °C (Miwa et al., 2008)	Negative (Miwa et al., 2008)	oyster mushroom, spinach, bean sprout

• ^*
  Food ingredients in which each bacteria was found.

3.2 Antibacterial properties of spices

The main 6 types of spices added to mara dishes, cloves, Sichuan pepper, fennel, Star anise, cinnamon, and cumin were prepared and the bacterial growth inhibitory effect of these spices was tested.

First, tofu, starch noodles, and bean sprouts solution and 6 types of spice solutions were combined to check for the growth of E. coli. Compared to the control, Clove, Star anise and Sichuan pepper suppressed the growth of E. coli best (Figure 2).

Figure 2
Number of E. coli colonies occurred in ingredients exposed to spices.

3.3 Food spoilage suppression effect of spices

Even though spices inhibit the growth of bacteria in ingredients, there may be a difference in the spoilage rate of ingredients directly added with spices. Figure 3 show the spoilage degree (ratio) of each ingredient according to the type of spice. For the rate of spoilage scaling, the completely spoiled state being 0 and the intact state being 1.0 degrees ​​were assigned according to the state of each material.

Figure 3
Non-spoilage rate of ingredient according to spice type over time (1, original state; 0, completely spoiled) (A) Control group; (B) Cinnamon treatment group; (C) Clove treatment group; (D) Star anise treatment group; (E) Fennel treatment group; (F) Cumin treatment group; G. Sichuan pepper treatment group.

In the control group, most of the ingredients spoiled more than 80-100% in 5 days (0.2~0), and the shape of the ingredients could not be recognized at the 21^st day. All spices lowered the spoilage rate of ingredient compared to the control group. Among them, Sichuan pepper maintained the spoilage degree of meats up to 0.8 and the starch noodle was 0.6 until 47 days, confirming it to be the spice that most slows ingredient spoilage rate. However, the winter mushroom and bean sprouts soiled rapidly after 12 days even in the presence of Sichuan pepper. Star anise was also effective in slowing the spoilage of ingredients over time, maintaining the spoilage degree of meat and starch noodle at 0.7, and winter mushrooms and bean sprouts at 0.5 on day 12. In addition, cinnamon, clove, fennel, and cumin had better anti-spoilage effect compared to the control group, but not that effective. Therefore, Sichuan pepper and Star Nice were excellent spices for both antibacterial and antiseptic activities.

3.4 Spices and concentrations effective for food ingredient storage

By adding 0~4% of Star anise and Sichuan pepper in bean sprout solution, which had the highest occurrence of bacteria, and checking for the occurrence of E. coli, Sichuan pepper suppressed the growth of E. coli from about 2%, and for Star anise it was 1% (Table 3). In addition, observations from Day 5 showed that E. coli did not occur at all, thereby it was confirmed that Star anise and Sichuan pepper were the most suitable spices for ingredient storage.

Table 3
Number of E. coli colonies occurred in Bean sprout exposed to the Sichuan pepper and Star anise concentrations (at 48 hours).

Spice	0% (No spice)	1%	2%	3%	4%
Sichuan pepper	62	23	0	0	0
Star anise	161	0	0	0	0

4 Conclusion and discussion

Unlike other restaurants, Mala food ingredients are not stored in the kitchen but in exposed environments for customers to personally pick and choose the ingredients. The ingredients are stored in separate containers, but a single set of tongs is used to select the ingredients, making it easy for contamination to happen. Also, used tongs are not washed but immediately re-used by the next customers, increasing the chances of ingredients becoming contaminated.

By purchasing ingredients stored in exposed environments from a Mala restaurant and performing a bacterial cultivation experiment with them, all ingredients were confirmed to be contaminated with a various bacteria including E. coli. Of the ingredients, tofu, starch noodles and bean sprouts were found with the most amount of E. coli, and a total of 9 bacteria species were found in the various ingredients. Among those, the four most found bacteria, C. geocarposphaerae, E. americana, P. extremaustratis, and V, boronicumulans, were identified through genetic analysis; It is known that C. geocarposphaerae and E. americana of these bacteria are known to be found in human clinical samples (Holmes et al., 2013; Grimont et al., 1983) and all 4 species were able to proliferate at human body temperature, confirming a high risk of human infection (Kangale et al., 2021; Grimont et al., 1983; López et al., 2009; Miwa et al., 2008). C. geocarposphaerae and E. americana was found not only in vegetables like bean sprouts, lotus root and spinach, but also in lamb, showing that human infection is possible regardless of ingredient type. Of the 6 types of spices, Star anise and Sichuan pepper best suppressed the multiplication of bacteria such as E. coli and slowed the spoilage of ingredients. The most effective concentration of Star anise and Sichuan pepper to be added to the ingredients was 2%. Zhu et al. (2011) also found that Sichuan pepper essential oil had antibacterial activity in the range of 1.25 to 1.25-1.25 mg/mL with minimum inhibitory concentration (MIC) and minimum bactericidal concentration (MBC) against 5 bacteria strains including E. coli, respectively. It has been suggested that it can be used as an antimicrobial agent in the food industry (Rui-Xue, 2011). Star anise is also known to have many potentials, such as antiviral, antioxidant, antibacterial, antifungal and more (Patra et al., 2020).

In conclusion, Mala food ingredients can be contaminated with various bacteria in the open environment but based on the water amount in the containers used for holding and storing the ingredients, adding 2% of Star anise and Sichuan pepper can prevent the proliferation of bacteria and spoilage of ingredients. There is a unique culture in China where the ingredients are displayed at restaurant entrances to emphasize the freshness of ingredients and for customers to select them for their dishes. However, openly displaying ingredients can make them susceptible to various contaminants. Of the various spices used for Chinese cuisine, a lot of them have antibacterial effects, so future research could explore further methods to use them in ingredient handling and storage without having the spices’ unique colors and scents embedded.

• Practical Application: When food ingredients are displayed in Chinese Mala restaurants, Star anise or Sichuan peppers can protect the ingredients from microbial contamination.

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Publication Dates

• Publication in this collection
  14 Mar 2022
• Date of issue
  2022

History

• Received
  10 Nov 2021
• Accepted
  06 Dec 2021