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Kimchi fermentation and characteristics of the related lactic acid bacteria

Mheen, Tae Ick

Korea Institute of Science and TechnologyInformation

Ⅰ. Introduction

Kimchi is a Korean fermented vegetable food that are salted, blended with

various ingredients and fermented for a certain period of time at ambient

temperature. The characteristics of kimchi differ depending on the varieties of

kimchi. The varieties are due to the raw materials used, processing methods,

seasons, localities and functional properties of kimchi. More than 200 kinds of

kimchi are available in Korea, but kimchi can be classified as two major groups,

ordinary and mul-kimchi. Ordinary kimchi without added water includes

baechu kimchi (diced Chinese cabbage), tongbaechu kimchi (whole Chinese

cabbage), yeolmoo kimchi (young oriental radish) and kakdugi (cubed radish

kimchi). Mul-kimchi includes baik kimchi (baechu kimchi with water), dongchimi

(whole radish kimchi with water) and nabak kimchi (cut radish and Chinese

cabbage). 1)

The raw materials used for kimchi preparation are divided into three groups,

major, sub-ingredients (spices) and optional ingredients. A recipe for the

simplest kimchi may include cabbage 100 g, garlic 2 g, red pepper powder 2 g,

green onion 2 g, ginger 0.5 g, with optimum salt content of 2-3%.2)

The optimum pH for the best taste of kimchi is 4.2-4.5 and the optimum

acidity is 0.6-0.8% as lactic acid. The best taste is attained after 2-3 days of

fermentation at 20℃ with 2-3% salt. Kimchi has a unique sour, sweet,

carbonated taste and usually is served cold. Also, kimchi contains a lot of live

lactic acid bacteria (LAB). In this respect, kimchi differs from western

sauerkraut and Japanese asatsuke, and the former is only acidic in taste and

served warm, and latter is not a fermented product and has few live LAB.

Total amount of kimchi production is estimated to 1,500,000 M/T in 2000 and

one fourth of total consumption of kimchi was commercially produced in the

same year. According to a national survey, an adult consumes 50-100 g/day of

kimchi in summer and 150-200 g/day in winter.2)

During the last 50 years, many genus and species of bacteria, yeasts, and

fungi has been isolated and reported from kimchi samples, but it was confirmed

that major microorganisms responsible for kimchi fermentation are LAB and

yeasts are known to be role for softening of kimchi texture and off-flavor. The

major genus and species of LAB isolated and identified from kimchis are

Leuconostoc mesenteroides, Leuconostoc dextranicum, Leuconostoc citreum,

Lactobacillus brevis, Lactobacillus fermentum, Lactobacillus plantarum, Pediococcus

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pentosaceus, and Streptococcus faeculis.1-3)

The sugars in raw materials are converted to lactic acid, acetic acid, carbon

dioxide and ethanol by hetero fermentative LAB during kimchi ripening, and

these acids and carbon dioxide are responsible for the fresh and carbonated

taste of kimchi. However, after a certain period of time, excessive lactic acids are

formed and off flavors are developed due to the growth of homo fermentative

LAB and yeasts. 1,2)

The total number of kimchi microorganisms reaches its maximum level

(1x108-9 cells/ml) at optimum-ripening time and after then number of

microorganisms decrease slowly and again increase and maintains 2nd

maximum level (1x106-7 cells/ml) as kimchi fermentation carried. In the kimchi

fermentation system, it seems clear that hetero fermentative LAB producing

organic acids and carbon dioxide from sugars are major species in the early

stage of fermentation, and homo fermentative LAB producing excessive lactic

acid are major species in the late stage of fermentation.2)

It was also confirmed that low salt concentration and low temperature (eg,

2% and 10o C) favor growth of hetero fermentative LAB, while high salt

concentration and high temperature (eg, 3.5% and 30oC) favor growth of homo

fermentative LAB. Therefore, salt concentration and temperature are the most

important key factors for controlling kimchi fermentation.2)

Besides the two key factors for controlling kimchi fermentation, many other

factors such as raw materials used, processing methods, addition of natural

preservatives and starters affecting kimchi fermentation and preservation has

been reported in previous reviews and books.1-6)

In this article, the factors affecting kimchi fermentation, microbial and

chemical changes during kimchi fermentation, and some characteristics of LAB

from kimchi will be reviewed.

Ⅱ. Factors affectingon kimchi fermentation

Kimchi fermentation occurs mainly by the microorganisms naturally present

in the raw materials that contain numerous microflora including LAB. Various

LAB may initiate fermentation, but hetero fermentative type LAB increased

rapidly with organic acids accumulation and homo fermentative type LAB

increased thereafter. Numerous chemical, physical, and biological factors may

contribute directly to the growth of microorganisms and the extent of

fermentation.

The important factors that affect kimchi fermentation are microorganisms,

temperature,salt concentration, fermentable carbohydrates, other available

nutrients, or any inhibitory compounds in raw materials used, as well as

oxygen and pH. In this chapter, the salts, temperature, raw materials, natural

preservatives and selected starter cultures related to the kimchi fermentation

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will be discussed in detail.

1. Salts

Salt is one of the key factors for controlling the kimchi fermentation and

preservation of good quality of kimchi at various temperatures. There are more

than 200 kinds of kimchi available in Korea.However, salt concentrations of

those kimchi are all different depending on the makers. A flow-chart for

processing baechu kimchi is shown in Fig. 1.

Prior to kimchi preparation the major raw materials such as Chinese

cabbages and radishes may be salted with either salt solution or dry salt and

washed with clean water. This treatment is the most important step for

fermentation and maintenance of kimchi quality. It was reported that the

optimum salt concentration of kimchi is about 2.0-3.0%, while acceptable level is

individually determined by housewive's experiences.2) Therefore, it is necessary

to optimize the salting condition. Of two types of salting methods, direct

addition method is widely used conventionally at household level, but this

method has the disadvantage of difficulty in control of the final salt content of

kimchi. Brine method is more preferable for the commercial production of

kimchi. Satisfactory quality of kimchi could be obtained when cabbages are

salted for 3-6 hours using 15% salt solution. 2,7)

Salting is carried out over a wide range of time from 3 to 15 hr depending on

the salt concentration, temperature, varieties, and cutting way and size of

cabbages. For baechukimchi, the final salt concentration is adjusted to 2.0 - 3.0%

of the overall ingredients, and this concentration is the best for optimum

fermentation. This concentration is maintained during fermentation and

preservation. If the salt concentration is below the optimum concentration,

fermentation proceeds too fast and frequently causes quick acidification and

softening. On the other hand, color and flavors are not acceptable when the salt

concentration is over 6%.2) 　Depending on the salting time, free sugars and

amino acids were reduced in raw cabbages and texture, chemical and physical

properties, and total microflora have been changed during salting.7-10)

Generally, salting reduces the moisture content (10-12%), relative volume,

and weight, as well as theinternal void space of the cabbage. These changes

affect the physical properties of the vegetable, especially the flexibility and

firmness of the tissue, which give a typical textural property to the final

product.As a result of brining, the total microorganisms, such as aerobic counts

in salted cabbage are reduced (11-87%) and LAB are increased (3-4 times), and

reducing sugars also decreased (7-17%) .7,11 )

Washing conditions in salted cabbage on the quality of kimchi is also

important for the retention of quality of characteristics.12) Chinese cabbage

treated with1000 ppm solution of grapefruit seed extracts or citric acid at 10oC

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showed a retarded increase in titratable acidity and decrease in pH and

reducing sugar content.12), and kimchi made from Chinese cabbage soaked in a

heated 10% salt solution at 40oC has improved quality and shelf-life of kimchi.13)

Fig. 2 shows the effect of salt concentration and temperature on acid

production during kimchi fermentation. Total acid was more at lower salt

content (2.25%) than high concentration of salt at any temperature tested. At the

lower salt content, maximum acidity was reached in a shorter period. At 30oC

and 2.25-3.5% salt content, acidity of kimchi was maintained in the same pattern

throughout. The acidity of 1.55% was reached in 5 days and maintained at 1.6%

thereafter, but at 5.0 and 7.0% salt content, acidity reached 1.4 and 1.1% after 5

and 6 days, respectively.

Recently, to examine the quality of mul-kimchi, the temperature (4, 15, and

25oC for 10 days) and salt concentration (0, 0.2, 0.5, 1.0, 1.5, 2.0, 2.5, and 3.0%) in

water was conducted, and found that the pH was lowest and acidity was

highest in the mul-kimchi containing 1.0% salt.14)

Effect of salt concentration on dongchimi (ponytail Chinese radish kimchi)

fermentation was also studied15) Diced Chinese radishes were fermented at 4oC

with salt concentration of 1.5- 6.3%. The pH level reduced during the

fermentation, while the total acid content of dongchimi increased and the salt

concentration of dongchimi liquid decreased. Equilibrium for salt concentration

between dongchimi liquid and solid radish was achieved after fermentation of

15-22 days.

2. Temperature

The most important factor affecting kimchi fermentation is temperature,

since the kimchi fermentation occurs mainly by the microorganisms naturally

present in raw materials. Kimchi is now available in all year round but the

quality of kimchi differs depending on localities and seasons. Ambient

temperature is applied for making kimchi at household level. Kimchi

fermentation and over-acidification occurs simultaneously at ambient

temperature.

Fig. 3 shows the changes of pH and total acids during kimchi fermentation at

various temperatures. Ripening time of kimchi depending on fermentation

temperature, accordingly the changes in pH and acidity, showed notable

differences. At 20oC, pH dropped sharply with increasing acidity, but pH and

acidity at 10oC changed more slowly compare with high temperature tested.

Maximum total acid produced in kimchi at 20oC and 15oC is 1.6%, but it never

exceeds total acidity of 1.2% at 10oC. As a result of panel test, it was evaluated

that the pH and acidity of optimum ripening period of kimchi were 4.2 and

0.6% (as lactic acid), respectively.16)

The optimum-ripening time and the edible period of kimchi varied

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depending upon the fermentation temperature and salt content as shown in

Table 1. At 30oC, the optimum-ripening period was 1 day and the edible period

was also 1-2 days. But at lower temperature, the optimum ripening time and the

edible period were longer than those of at higher temperature. At 5oC and

above 5.0% salt content, kimchi was ripened very slowly and at 7.0% salt

content it was not ripened even after 180 days fermentation．16)

Chemical changes, LAB and yeast counts in kimchi prepared by commercial

manufacturer in large scale were monitored at different fermentation

temperature．17) It has been confirmed that the optimum pH of kimchi was

around 4.2 and reached within 2 days at 25oC, 3 days at 15oC, and 23 days at 5oC

fermentation, respectively．17)

In order to investigate the fermentation characteristics of kimchi which was

made at

12oC and fermented at 17oC and 4oC, the pH, total acid, total microorganisms,

LAB, dissolved carbon dioxide content, reducing sugars and temperature at the

center of a kimchi jar were studied．The pH and the total acid content of

kimchi that was fermented at 17oC for 4 days were almost the same as those of

kimchi fermented at 4 oC for 48 days. The total cell counts of microorganisms

and LAB in kimchis which were fermented at 17oC for 2 days and 4oC for 9 days

were 1.5x 109 and 6.3x108 cells/ml, and 2.0x108 and 8.7x107 cell/ml, respectivel

y． The results showed that it took 23 and 35 hr, respectively, to reach the

temperature of 17oC and 4oCat the center of a jar during bulk fermentation of

kimchi from the fermentation of initial temperature of 12oC．18)

The effects of fermentation temperature (0-15oC) and salt concentration (1.5,

2.75, 4.0%) on fermentation parameters of kimchi were also analyzed by

response surface methodology． pH decreased and acidity increased with

increasing fermentation time, reduction and incremental rates were increased

as temperature increased and salt concentration decreased. The optimum pH

of 4.2 was achieved within 14-24 days at 5-15oC, but at 5oC, pH was still >4.2

after 24 days. Maximum edible acidity (0.75%) was reached within 8 days at

15oC, but at 0oC, acidity was only 0.35-0.43% after 24 days of fermentation.

Edible periodsfor kimchi, based on the acidity range 0.4-0.75%, were 4, 10, and

18 days for the fermentation at 15, 10, and 5o C, respectively, with 2.75% NaCl．19)

Differences in quality characteristics such as pH, acidity, reducing sugar

content, microbial counts and sensory properties between whole Chinese

cabbage kimchi (pogi kimchi) and sliced Chinese cabbage kimchi (mat kimchi)

were examined during the fermentation at 20 oC for 10 days and 5 oC for 50

days. Pogikimchi showed delayed fermentation of approximately 2 days at 20 oC

and 10 days at 5 o

C than mat kimchi. Ordor, color and flavor scores of kimchi

were higher in the samples fermented at 20 oC than those fermented at 5 oC,also

there were no great differences between sensory properties of pogi and mat

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kimchi. Gas composition of the packages containing the kimchi fermented at 20

oC showed increased CO2 concentration and decreased O2concentration after 3

days for both kimchi varieties.20)

The effect of fermentation temperature on the sensory, physicochemical and

microbiological properties of kakdugi(cubed radish kimchi) and on free sugar,

organic acid and volatile compound levels in kakdugi during fermentation was

also investigated． 21-22) After the initial fermentation for 12, 24 and 36 hr at 20

oC, kakdugi was fermented for 57 days at either 4 oC, 10 oC or 20 oC, respectively.

The pH was decreased to the range of 4.1~4.3 from the initial pH 5.8, and

total acidity was increased 2~4times than that of in the initial period (0.24%).

The number of LAB was remarkably increased in palatable period and was

gradually decreased thereafter.21)

Free sugar levels decreased at each temperature during fermentation (with

the exception of mannitol, levels of which increased) although decreases were

less marked in samples fermented at 4 oC. Of the organic acids tested, lactic acid

production was the most pronounced, increasing substantially with time and

temperature. In contrast malic acid, which was the most abundant organic acid

initially, decreased in concentration during fermentation, and this decrease was

most pronounced at higher temperature.

Levels of the volatile compound, methyl allyl sulfide, were initially very low,

but increased dramatically up to approximately 45 days after which levels

decreased. The increase corresponded to the increased aroma in sensory

evaluations. These results suggest that fermentation at 4oC, following an initial

fermentation at 20 oC for 36 hr, is suitable for the production of good quality

kakdugi with high free sugar and organic acid contents.22)

Recently, the characteristics of natural lactic acid fermentation of radish juice

were investigated at different salt concentration (0-2%) and temperature

(10-30oC) with aview of low salt kimchi (a kind of water kimchi). It was found

that LAB isolated from radish juice fermented at 2% salt concentration was

mainly Leu. mesenteroides, Lac. plantarum and Lac. brevis.Growth rate of LAB

increased with increasing temperature at 1% salt concentration and LAB were

still active at 10oC. The time to reach pH 4.0 during the fermentation of juice

containing 1% salt was 11~13 days at 10oC and 2~3 days at 30oC.23)

3. Raw materials

Kimchi, a fermented vegetable food with various sub-ingredients (spices),

has been the most popular side dish that is served with cooked rice for

hundreds of years in Korea. In total, there are about 200 kinds of kimchi, whose

raw materials are mainly Chinese cabbages and radishes. Dried red pepper

powder, garlic, green onion and ginger are the widely used seasonings. The

types and amounts of seasonings used in kimchi vary greatly between

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manufacturers and processors. Therefore, the quality and species of major

ingredients may significantly affect fermentation and the product characteristics

of kimchi.

The important raw materials of kimchi are divided into three groups such as

the majorraw materials, sub-ingredients (spices) or fermented fishery products,

and optional (minor) ingredients.

As seen in Table 2, baechu (Chinese cabbages) are the most common majorraw

materials for preparing kimchi and radishes are other raw materials for kakdugi

(cubed radish kimchi) and dongchimi (whole radish kimchi with water)

preparation. Cabbages, whole radish, cucumber, mustard leaves, green onion,

and leeks that are available in various seasons and localities are the raw

materials for making special kimchi in Korea.

The sub-ingredientsinclude garlic, hot pepper powder, green onion, ginger

and fermented fishery products such as shrimp and anchovy. The optional

(minor) raw materials include leek, parsley,glue plant, mustard leaves, pear,

chest nut, oyster, frozen pollack, starches, monosodium glutamate (MSG),

andsweetener. One of the important criteria for making good taste of kimchi is

the selection of good quality of raw materials, and the next is the good

formulation of kimchi ingredients and seasonings.

Table 3 shows the basic ingredients for making baechu kimchi, kakdugi,

dongchimi, and other mul-kimchi (water-kimch, but the simplest kimchi recipe

includes salted cabbages 100 g, hot pepper powder 2 g, garlic 1.5 g, green onion

2 g, ginger 0.5 g and final salt concentration of 2-3%.16)

Generally softer texture and higher sugar content of vegetables are more

desirablefor making good quality and taste of kimchi than harder texture and

lower sugar content. However, harden texture ofvegetables are more favorable

for long-term preservation without softening.2)

Among the many kind of kimchi, baechu kimchi has been consumed for a long

time as a traditional fermented vegetable food in Korea. The ingredients

involved in baechu kimchi preparation, such as red pepper, garlic, ginger, green

onion, leek, fermented shrimp or anchovy, sugar, etc., affect the kimchi

fermentation rate differing with kinds and amounts of ingredients. Effects of

raw materials and ingredients on kimchi fermentation have been extensively

studied.25,29-32)

Besides the temperature and salt concentration, types of kimchi are also the

factors for controlling kimchi fermentation. Therefore, three main types of

Chinese cabbage kimchi, baechu kimchi and tongbaechu kimchi (semi-solid types

of the cabbage kimchi prepared with a large amount of hot pepper powder and

a small amount of water) and baek kimchi (a liquidtype of kimchi prepared with

a small amount of hot pepper powder and a large amount of water), were

selected as models to compare fermentation characteristics of kimchi. In this

result, the amount of hot pepper powder and water are believed to be the

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primary (or external) and the secondary (or internal) factors, respectively, those

affect and control kimchi fermentation.33)

The difference of qualitative characteristics between whole Chinese cabbage

kimchi (pogi kimchi) and sliced Chinese cabbage kimchi (mat kimchi) was

examined during the fermentation at 20oC and 5oC. Pogi kimchi showed a

delayed fermentation about 2 days at 20oC and 10 days at 5oC.20)

The growth of microorganisms could be controlled by theappropriate

addition of raw materials. Among the sub-ingredients, radishes,34) hot pepper

powder,29-32) fermented anchovy and shrimp,35-38) starches,35,39) reducing

sugar,31,40) soluble solids,41) and protein sources42) have been probed their

accelerated effect on kimchi fermentation, but garlic and leek has showed

delayed effect,29-31,43,44)and green onion and ginger had controversial effect on

kimchi fermentation.30-32) On the other hand, mustard or leaf mustard,45) and

extracts of leek44) were known to delay the fermentation period of kimchi.

Additionof dried methanol extracts of radish stimulated the growth of LAB,

especially Lac. fermentum, Lac. leichmannii, Lac. sake, and Lac. brevis.34)

The composition of pigments in hot pepper consists of 40 different

carotenoids with capsanthin and capsorubin as a major carotenoid and

carotenes as provitamin A. The average amount of hot pepper added to kimchi

was found to be 2.24% with frequency of use of 97.3%. In spite of the fact that

hot pepper was reported to promote the fermentation of kimchi, it did not show

any significant increase in sour taste and did not affect sweet, salty, palatable

and crispy tastes.31)

Garlic is used most frequently as a sub-ingredient (100%) in kimchi. Since

ground garlic is used in kimchi-making, alliin is changed to allicin with an

intensive taste. This allicin takes part in the desirable fermentation of kimchi by

inhibiting the growth of various unnecessary microorganisms derived from

sub-ingredients in the initial fermentation period and to delay the fermentation

of kimchi. Garlic improves storage capacity by prolonging fermentation period

by LAB and is beneficial to less acidification.29,30,32,43,46)With fermentation of

kimchi, the intensive hot taste of garlic was slowly changed to the harmonized

taste and flavor.31)

Green onion and leek contain various allyl sulfides, carotenes and vitamin C.

The frequency of use in the general cabbage kimchi was 72.8% for green onion

and 32.4% for leek, which both are much lower compared with that of 97.3% for

hot pepper and 100% for garlic. The amounts of green onion and leek used for

kimchi making are still high, ie, 0.6-0.9% for green onion and 2.0-6.0% for

leek.Recently, it has been reported that leek could retard the fermentation of

kimchi because of its antimicrobial activity.44)

Ginger contains unique components like citral and linalol, and hot taste

components such as gingerone and shogaol. Ginger caused a delay in

fermentation and there were no significant differences in the sour, sweet, salty,

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hot, palatable, unpleasant and overall tastes, acidic odor and color between the

kimchi fermented with and without ginger.30,31)

Fermented anchovy and shrimp contain a lot of proteins and amino acids,

and have their own unique taste and flavor. Therefore, those sub-ingredients

would affectnot only the nutritional balance but also the improvement of the

sensory quality of kimchi. These fermented fish products and other protein

sources such as skim milk, soy protein isolate, beef extract, and fish protein

produced high lactic acid and promoted the growth of LAB.37,38,42)

The frequency of addition of starch and sugar in kimchi making was 27%

with a concentration of 0.4-3.0%, and sugar was used for sweet and harmonized

tastes. However, since starch and sugar are utilized as a carbon source

byvarious microorganisms present in kimchi, they are expected to affect the

kimchi fermentation and sensory quality. In the results, starch and sugar

promote the fermentation of kimchi and contribute greatly to harmony of tastes

by reducing the hot and overall tastes, and acidic and garlic odors.31,39)

Yulmoo, a young radish, is a vegetable that has been a major raw material of

kimchi just as much as Chinese cabbage. Compared with Chinese cabbage,

yulmoois chiefly cultivated in summer and thus is cheaper during this season.

Yulmoo kimchi is also different from baechu kimchi in that it requires less

seasoning. Owing to the use of various seasonings like red pepper powder and

fermented fish products, Chinese cabbage kimchi is more expensive and at the

same time more prone to turn sour than yulmoo kimchi in summer. Therefore,

yulmookimchi would not only taste better but also be economical during

summer. To evaluate the effect of starch on yulmookimchi fermentation wheat

flour was used as starch source and compared with glutinous rice. It was found

that both wheat flour and glutinous rice flour hastened the fermentation of

yulmoo kimchi.39)

4. Natural preservatives

The groups of LAB involved in kimchi fermentation continuously produce

organic acids after theoptimum ripening, and cause changes in the composition

of kimchi. These changes are called the over-ripening or acid-deteriorationof

kimchi, which is often observed in summer kimchi and in winter kimchi stored

for an extended period. The over ripening ofkimchi is the most serious problem

in the storage of kimchi. Since the over-ripening of kimchi is mainly due to

activities of lactic acid-forming LAB, the best way to overcome it is to control

the growth of LABwithout destroying the quality of kimchi.

Screening of natural preservatives such as edible plants, herbs and spices,

antimicrobial agents and related compounds to inhibit kimchi fermentation

were studied extensively.47) Among 42 oriental medicinal plants tested, Baicall

skullcap (Scutellaria baicalensis), and Assam indigo (Cimicifuga foetida) were very

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effective for preserving kimchi. Among 32 herbs and spices tested, peppermint

(Mentha piperita L.), cinnamon (Cinnamomum verum Presl), lemon balm (Melissa

officinalis L.), clove (Eugenia caryophyllate Thunb.), hop (Humulus lupulus L.),

rosemary (Rosmarinus officinalis L.), sage (Salivia officinalis L.), horse radish

(Moringa oleifera Lam.) and thyme (Thymus vulgaris L.) showed high

antimicrobial activity against microorganisms in kimchi. Clove was themost

effective microbial inhibitor, when added to fresh kimchi. However, sensory

test was not good for evaluation of the effect of herbs and spices, since their

highly specific flavors affected the taste of kimchi. Among 28 fruits, vegetables

and related plants tested, leaves of pine tree (Pinus rigida), persimmon

(Diospyros kaki) and oak leaves (Quercus glauca) also demonstrated a significant

bactericidal effect. In addition, of 21 natural preservatives added individuallyto

fresh kimchi, only nisin and caffeic acid were able to inhibit fermentation.47)

The changes of pH and acidity of baechu kimchi and mul kimchi were

remarkably inhibited by adding the tea catechins at the level of 2 mg/g fresh

baechu, results suggesting that the tea catechins can be successfully used for the

extension of shelf-life of kimchi.48)

Studies were carried out to investigate the effects of Lithospermum

erythrorhizon, Glycyrrhiza uralensis (LG) with and without dipping of salted

Chinesecabbage in 1% chitosan solution (LGDC) on fermentation of kimchi at

10oC during25 days. The sour taste of LG and LGDC added kimchi was

changed more slowly than that of control during fermentation of kimchi. The

shelf-life of LGDC added kimchi was extended over 10 days compared with

control.49)

By the addition of 1% mixed extracts of Lithospermum erythrorhizon and

Scutellaria baicalensis and 1% crab shell treated with ozone to kimchi, color,

flavor, and sourness were slightly inferior, while texture and overall

acceptability were found to be the same or slightly superior compared with

untreated kimchis.50)

It was also found that the kimchi containing 2% of ozone treated crab shell

powders showed both strong neutralization action for 0-25 days and buffer

action after 25 days during fermentation at 10 oC.51)

Addition of 500 ppm grape fruit seed extract showed the highest pH during

fermentation at 20oC and lowest titratable acidity compared with control

kimchi. The total microbial counts were higher than LAB counts right after the

preparation of kimchi,but they were similar after three days. However, sensory

evaluation of 3 day old kimchi samples showed a significant difference (P<0.05)

between the control and the treatment in odor, color and taste, except for the

one with 50 ppm.52)

Recently, fermentation characteristics of mustard leaf kimchi added with

green tea and pumpkin powder has been studied and found that the sensory

scores of flavor, aroma and overall acceptability were highest in the kimchi with

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0.3% pumpkin powder and 0.2% green tea powder.53)

The effect of chitosan (0.5%) on properties of kimchi was studied during the

fermentation at 20 oC for 8 days. It was confirmed that chitosan reduced the

total number of microorganisms and levels of Leuconostoc sp. and Lac. plantarum

in kimchi, and the lower mol. wt. chitosan fraction had the greatest effect on

levels of Leuconostocsp. Also, chitosan reduced the intensity of sour and stale

flavor notes in kimchi, and the content of reducing sugar in control kimchi

samples was lower than in those containing chitosan for the first 6 days of

fermentation at 20oC. Malic acid content was lower and lactic and acetic acid

contents were higher for control kimchi than in those with chitosan for the first

4 days of fermentation. Control kimchi contained more succinic acid than those

with chitosan for the first 2 days of fermentation.54-55) Leuconostoc sp. and Lac.

plantarum were higher in the control than in the kimchis containing chitosan

dissolved in 0.3% acetic acid and 0.05% sodium benzoate.55) It is also found that

addition of chitosan to kimchis influences pectic substance levels and improves

their textural properties.56)

Two % ginseng in kimchi had the best overall preservative and quality, and

promoted the growth of Lac. plantarumand Lac. fermentum and inhibitedthe

growth of Leu. mesenteroides and Ped. cerevisiae.57)

One or two % of omija (Schizandra chinensis, a fruit of maximowiczia

typica)extracts had strong growth inhibitory properties against isolated LAB

were shown by fumaric and itaconic acid among various organic acids of

Schizandra chinensis.58) The growth of Sac. cerevisiae and Lac. casei in the culture

media containing 1.0 and 1.5% of methanol extracts of kukija (Lycii fructus, a

fruit of the Chinese matrimony vine) were increased, where as that of E. coli was

somewhat decreased.59)

Addition of sap from pine needles (Pinus densiflora) delayed kimchi

fermentation by slowing down the decrease in pH and inhibiting the growth of

Lactobacillus sp.60)

Water extract of pine needles had more inhibitory effects against Lac.

plantarumthan against Leu. mesenteroides,and the vascularity of kimchi tissue of

control kimchi was degraded more than that of water extracts of pine needles

added kimchi.61,62)

It was found that mustard oil (200 ppm) had antimicrobial effect on the major

LAB of kimchi such as Lac. plantarum, Lac. brevis, Leu. mesenteroides and Ped.

cerevisiae, and mustard and mustard oil could control the shelf life after 15 days

storage at 15oC.63)

The extract of bamboo leaves had a wide range of antimicrobial activity

against Brettanomyces custersii, Klebsiella oxytoca, Pichia membranaefaciens which

cause kimchi softening.64)

Recently, the effects of Sepiae os, cuttlefish

born,65)enoki mushroom (Flammulina velutipes),66) Monascus koji,67) and

boiled-dried fusiforme, a kind of seaweed 68) on the fermentation and quality of

- 12 -

kimchi have been studied.

5. Starters

Qualities of kimchi can be controlled bydesirable microorganisms,and

various fermentation conditionssuch as temperature, salt concentration, and

nutrients in raw materials.

The major preparation procedure for kimchi includes lactic acid fermentation

by the addition of various kinds of vegetables, spices, edible salt to Chinese

cabbage and radishes. Kimchi is generally acknowledged to be more nutritious

than other vegetable foods such as sauerkraut, pickles, and Japanese tsukemono

or asatsuke. In addition,it is also known that the fermentation processes of

kimchi involve more complex biochemical and microbiological processes

compared with other fermented vegetable foods.2,16,69)

During the entire stage of natural fermentation of kimchi, lactic

acid-producing bacteria are major population, and after prolonged

fermentation, various and excess organic acids are produced by the LAB

species. Those excess organic acid productions in kimchi fermentation are called

the acidification of kimchi. After that stage, other microorganisms including

yeasts grow on the surface of kimchi, and that growth causes the softening of

the texture of the ingredients.70) Therefore, generally, it can be defined that the

edible good taste of kimchi is obtained before the texture softening and the

acidification.

A hetero fermentative type of LAB, Leuconostoc mesenteroides, is a major

bacterial population of kimchi from the initial to the middle stage of

fermentation. During those stages, hetero fermentative type LAB produce

various metabolites such as lactic acid, acetic acid, ethanol, carbon dioxide,

mannitol, and dextran which are associated with the taste of kimchi, and the

number of LAB reaches the highest during the optimum- ripening period.

However,the total number of Leu. mesenteroidesdecreases sharply when the pH

of kimchi is decreased to 4.0. On the other hand, a homo fermentative type LAB,

Lac. plantarum, whichhas a strong pH tolerance under high organic acid

concentrations, has been continuously increased in their number during kimchi

fermentation to the last stage.It has been reported that the acidification of

kimchi is mainly caused by Lac. plantarum.16)

As already mentioned, kimchi fermentation and ripening are carried out by

the microorganisms present in raw materials. Sugars in raw materials are

converted to lactic and acetic acid, carbon dioxide,ethanol and mannitol by the

LAB growing at 1-3% salt concentration.

As seen in Table 4, many LAB were isolated from kimchi, and among them,

Lac. plantarum, Lac. brevis, Lac. acidophillus, Lac. bavaricus, Lac. homohiochii, Ped.

cerevisiae, Leu. mesenteroides, Leu. dextranicum, and Leu. paramesenteoides have

- 13 -

beentried as kimchi starters to improve the quality and shelf-life extension of

kimchi.71-76)

The combination ofvarious strains such as Leu. mesenteroides, Lac. brevis, Lac.

plantarum and Ped. cerevisiae which were isolated from kimchi could be used as

starters for kimchi fermentation. These starters increase the fermentation rate,

and mixed strains are more effective than a single strain to produce better

organoleptic quality of kimchi.71)

Generally,kimchi fermentation has been carried out relatively at low

temperature, and psychrotrophic LAB were isolated and characterized from

kimchi fermented at 5oC. 24,75) Therefore,psychrotrophic LAB isolated from

kimchi fermented at low temperature were studied as starters for their effect on

kimchi fermentation. The results indicated that the fermentation period could

be shortened by using the LAB starters which isolated from low temperature

kimchi. Among the LAB used as kimchi starters, it was confirmed that

Leuconostoc species were more effective than any other Lactobacillus species

tested for kimchi fermentation.76)

Because the acid production from the hetero fermentative type LAB is lower

than that of the homo fermentative type LAB, the addition of an acid-tolerant

mutant strain of Leu. mesenteroides as starter of a kimchi fermentation may

inhibit the rapid pH decease and lactic acid production during kimchi

fermentation. Therefore, a mutant strain, Leu. mesenteroides M-10 which could

grow in low pH (3.0) at 10oC and produce more CO2 than wild type was

mutagenized to be improved as akimchi starter. With respect to total

acceptability, the kimchisprepared using the mutant strain M-10 were better

than the other strains, and use of the mutant strain extended the

optimum-ripening period of kimchi by two fold compare with that of control.

This report suggested that a mutant strain of Leu. mesenteroideswhich has more

stable growth ability in acidic conditions was able to extend the edible period of

kimchi.77)

Psychrotrophic yeast, Saccharomyces fermentati YK-19 that showed better

growth at 10oC than at 25oC in the medium containing 0.3% lactic acid and 0.6%

acetic acid,was isolated from kimchi and used as a kimchi starter in order to

prevent over-acidification of kimchi.78) The addition of Sac. fermentati YK-19

prolonged the period of optimum fermentation (at pH 4.2 and 0.6-0.8 acidity) by

>63%. The lactic acid content increased rapidly in control samples, followed by

the kimchi with Sacharomyces sp. Yk-17 and Sac.fermentati YK-19 as starters. The

growth of Lactobacillus species was inhibited by the addition of yeast starter,

particularly by Sac. fermentati YK-19. Furthermore, sensory scores such as acidic

and moldy flavor were reduced by starter addition, while flavor scores for

freshness were increased.79)

Leu. paramesenteroidesP-100, a psychrotrophic mutant which grow well at pH

4.0, and 10oC, and in organic mixture (lactic acid:acetic acid;1:2) was improved

- 14 -

from wild type Leu. paramesenteroides Pw. A wild strain Pw and a mutant strain

P-100 were inoculated as starters and the total acceptability of the kimchi were

evaluated.80,81) Kimchi added with mutant strain had better tastethan that of

control kimchi by sensory test and the optimal pH range of kimchi extended up

to about 2.2-2.5 times. In the kimchi added with Leu. paramesenteroides P-100 ,

the succinic acid content was higher than that of others, and the total number of

Lac. plantarumwas reduced about 2.5 fold with respect to control kimchi.80)

The effects of the addition of Leu. mesenteroides M-100, an acid-tolerant mutant

improved from wild type strain Leu. mesenteroides Mw,82) and Sac. fermentati

YK-19, an acid-utilizing and aromatic flavor-producing yeast, were tested for

the retardation of acidification and the prolongation of the edible period of

kimchi. The addition of Leu. mesenteroidesM-100 to kimchi preparation may

induce the prolonged acidification of kimchi because of its low production of

lactic acid and increased growth in comparison with Lac. plantarum. Also Sac.

fermentati YK-19 may lengthen the edible period of kimchi by reducing the

content oflactic acid and acetic acid in the later period of kimchi fermentation,

and the good flavor in the starter-added kimchi group may be due to the

various compounds, carbon dioxide, and succinic acid produced by Leu.

mesenteroides M-100 and Sac. fermentati YK-19.83)

Recently, the effects of the addition of mutant strains of Leu. mesenteroides and

Leu. paramesenteroides which have increased adipic acid resistance compared

with wild type species on shelf life of kimchi were evaluated.84) The addition of

a combination of both mutants was more effective than that of single strain in

extending shelf-life of kimchi. The optimum inoculation was 0.005% of a 1:10

mixture of Leu. mesenteroides: Leu. paramesenteroides according to the results from

acidification tests and sensory analysis.84)

To extend the storage period and inhibit contamination of E. coli, conditions

for kimchi brining in lactic acid solution and effect of the halophilic

Lactobacilllus HL-48 starter were investigated. The results showed that the pH

value of the starter inoculated kimchi was 4.2 after 18 hr fermentation at 25oC,

while the pH of the starter non-inoculated kimchi was 3.3 at the same

condition.85)

Ⅲ. Microbial and chemical changes during kimchi fermentation

1. Microbial changes

The number and species of major microorganisms in kimchi fermentation

vary widely, and are influenced by raw materials and other ingredients.

However, the growth, activity, and role of the microorganisms participating in

the fermentation are influenced more by environmental conditions, especially

by temperature and salt concentration.

- 15 -

Generally, total LAB was highly distributed throughout the whole

fermentation period. However, they were slightly declined as the acidity

increased. The growth pattern of the major LAB during fermentation at 20 to 30

oC is that the number of Leuconostoc species increase initially, and then at pH 4.0

to 4.5 they decrease rapidly with an increase in the number of Lactobacillus

species. However, at 5 to 15 oC, the times for the increase and decrease of LAB

are delayed.16,69)

The total counts at the optimum-ripening time were 1x10 8-9 cells/ml and

Leuconostoc spp. appeared maximum levels at this time, and after then total

counts decreased and increased again by little. Lactobacillus and Pediococcus

appeared maximum level at this period (1x106-7 cells/ml).16,69) The number of

Leu. mesenteroides reached its maximum value at the optimum-ripening stage of

kimchi and decreased when kimchi became acidic. At the same fermentation

temperature, the total number of Leu. mesenteroides was higher at lower salt

content than at higher one. The maximum number reached after 1 day at 30oC, 3

days at 20oC, 6 days at 14oC, and 27 days at 5oC. It is very interesting to note that

the number of Leu. mesenteroidesreached maximum with the corresponding

increase in the total viable count. Lac. brevisgrew better at higher temperature

and lower salt content at over-ripening period of kimchi. Ped. cerevisiae was

dominant at higher salt content (5-7%) and also appeared generally at

over-ripening stage of kimchi. Lac. plantarum appeared at the time when the Leu.

mesenteroides decreased in number and after the appearance of Lac. brevis and

Ped. cerevisiae. The population of Lac. plantarum was dominant at the

over-ripening and acid-deteriorated stage of kimchi. Lac. brevis, Ped. cerevisiae,

and Lac. plantarum were not detected at any levels of salt contents at 5oC. Str.

faeculis appeared rarely at all temperature and salt contents but its number was

negligible.16)

Film-forming yeasts appear on the surfaces of the kimchi preserved for long

term period, and they produce polygalacturonase and contribute to softening

the texture of kimchi by degrading of pectic substances.70)

The number of fungal flora during kimchi fermentation decreased in number

at higher temperature (30oC), but the total number of fungi decreased and

remained constant at temperature below 20oC. However, yeast population

during kimchi fermentation showed typical changes depending upon the

temperature and salt concentration. Total number was not changed at 20-30oC,

but it showed gentle curve of initial increase to slow decrease in the later phase

at lower temperature (14-5oC).16)

The typical changes of major LAB during kimchi fermentation at 20oC are

shown in Fig. 4. The patterns of microbial changes in each lactic acid bacterial

group, Leuconostocs, Lactobacilli, and Streptococci, were similar at different

fermentation temperature, and the microbial changes accelerated by increasing

the temperature. Among them, Leuconostocs showed higher number at high

- 16 -

temperature than the others. The numbers of Leuconostocs and Streptococci

increased the beginning but they rapidly decreased after the optimum-ripening

period. Pediococci increased their number after Streptococci, but they rapidly

disappeared later.69)

The strains of Leuconotocs, Streptococci, Pediococci and Lactobacilli were

identified as Leu. mensenteroides subsp. mesenteroides, Str. faecalis, Str. faecium,

Ped. pentosaceus, Lac. plantarum, Lac. sake and Lac. brevis. Among the LAB

isolated, Lac. brevis and Lac. plantarum appeared mainly at the beginning and

around the over-ripening period of fermentation, respectively.69)

Kimchi fermentation is dominated by Lactobacillus spp. at 25 oC and

Leuconostoc spp. at 5 oC.86) The levels of Streptococcus and Pediococcus species are

lower than those of Leuconostoc and Lactobacillusspecies and decrease

considerably at lower temperature. Like Leuconostoc species, Streptococcus and

Pediococcus species increase initially, and then decrease rapidly after the

optimum-ripening period during the fermentation. Lac. sake and Lac. brevis also

are included among the Lctobacillus species. The Lac. sake especially is isolated

from an early stage and is not able to survive under pH 4.0 at the later stages.

Lac. brevis are also isolated at early stages, but smaller numbers are only found

in the later stages. Lac. plantarumis isolated from all the stages during the

fermentation period, but especially at the later stages after the

optimum-ripening period.69,86)

Lactobacillus sp. and Leuconostoc sp. were the main bacteria isolated from

optimum-

ripened kakdugi(53 and 43%, respectively) as well as from over-ripened

kakdugi. (63 and 37%, respectively). Leuconostoc mesenteroides subsp.

paramesenteroides was the dominant strain among the LAB from kakdugi. The

isolates from optimum-ripened kakdugi required more amino acids for growth

compared to those fromover-ripened samples, while no difference was

observed with respect to vitamins. The physiological characteristics of the

isolates, such as amino acid and vitamin requirements, were different from

those of 9 type strains of various Leuconostoc spp.26)

Recently, 88 strains of LAB were isolated from dongchimi, and the

predominant strains were identified as Leu. mesenteroides subsp. mesenteroides at

the initial stage of fermentation (on the 5th day), Lc. lactis subsp. lactis at the

middle stage (30th day), and Lac. curvatus and Lc. lactis subsp. lactis at the final

stage (50th day). The 88 strains of isolates were classified into 15 groups

according to the fermentation properties, of which, 6 groups of Leu.

mesenteroides, 3 groups of Lac. curvatus, 2 groups of Lac. cellobiosus, and each of 1

group of Leu. citreum, Lc. lactis. subsp. lactis Lac. acidophilus and Lac. delbrueckii

subsp. delbrueckii.87)

In the early 1960's, LAB such as Lac. brevis, Lac. plantarum, Leu. mesenteroides,

Ped. cerevisiae, and Str. faeculis were isolated from kimchi and it was reported

- 17 -

that the main microorganisms responsible for kimchi fermentation are Leu.

mesenteroides, Lac. brevis, Ped. cerevisiae, and Lac. plantarum which was just

thesame as in sauerkraut fermentation.88,89) However, kimchi is less acidic than

sauerkraut and the optimum acidity and pH of kimchi are 0.6-0.8% and 4.5-4.2,

respectively, while those of sauerkraut are 1.6-2.0% and 3.7-3.5. Also, sauerkraut

fermentation is completed after 20 days at 23oC with 2.25% salt content, whereas

kimchi fermentation is completed only within 3 days under similar

fermentation conditions. Therefore, it has been suggested that the main

microorganism in kimchi fermentation is Leu. mesenteroides rather than Lac.

plantarum and Lac. plantarum is a main acid-deteriorating organism in kimchi

fermentation unlike in sauerkraut where it constitutes main responsible

microorganism.16)

Recently, many new LAB were isolated and identified from various kimchis

using molecular techniques. However, the role of new LAB has not yet been

confirmed by testing as kimchi starters. New LAB from kimchi will be

discussed more in chapter IV-1.

2. Chemical changes

The chemical compositions of kimchi may be different basically depending

on the varieties of cabbage, kinds and amounts of minor ingredients such as

garlic, green onion, leek, hot pepper powder, ginger, and fermented anchovy or

shrimp. However, kimchi fermentation was carried out continuously by LAB

existing in the raw materials. The sugars in kimchi raw materials were

converted to organic acids, carbon dioxide, ethanol, and other flavoring

compounds by lactic acid fermentation.

Generally, the best quality of kimchi can be obtained at pH 4.2-4.5 and at the

time being maximum levels of carbon dioxide production. Acidity at the

optimum- ripening period is 0.6 -0.8% as lactic acid, and reaches 1.5% upon

over-ripening and becomes 1,5-2.0% at the stage of acid-deterioration of kimchi.

The optimum-ripening time and shelf-life of edible period were changed

depending on the salt content, fermentation temperature and time as seen in

previous Table 3.

In most cases, the kimchi fermentation process has several stages based on

the changes of pH, acidity and reducing sugar content. The first stage has a

rapid decrease of pH, an increase of acidity and a decrease of reducing sugar.

The second stage shows a gradual decrease in pH, an increase in acidity, but a

rapid decrease of reducing sugar. The last stage has no or only gradual changes

in pH, acidity, and reducing sugars.16)

Generally, during the kimchi fermentation, pH and reducing sugars decrease

while total acids increase. The pH starts from 5.5-6.0, reaches 4.5-4.2 at optimum

- 18 -

ripening period, and drops further down upon over-ripening period. High

temperature and low salt content showed faster fermentation than low

temperature and high salt content.

Lactic, acetic, citric, malic, fumaric, succinic, oxalic, tartaric, malonic, maleic,

and glycolic acid were identified from kimchi samples. Among the organic

acids identified, lactic acid and acetic acid are the major acid that increased by

fermentation. However, the kimchi fermented at lower temperature (6-7oC)

contains more lactic and succinic acid, and less oxalic, malic, tartaric, malonic,

maleic and glycollic acid than the kimchithat fermented at higher temperature

(22-23oC), while no difference is noted in citric acid level.90) Higher salt

concentration brings about a lower acetic acid, and large amounts of acetic acid

and carbon dioxide make kimchi tasteful.16,91-93)

The production of carbon dioxide during kimchi fermentation was stimulated

by higher temperatures and was affected by seasonal factors. Kimchi made

from winter baechu (Chinese cabbage) produced much more fermentative gas

than that made from summer baechu. It was suggested that the changes in

carbon dioxide concentration could be used as a characteristic index for

indicating the fermentation course of packaged kimchi products.94)

The changes of the content of organic acids, carbon dioxide, alcohols and

carbonyl compounds of the various kimchi which were made from cabbage

with green onion, garlic, ginger, and red pepper fermented at 12oC-16oC were

investigated. The identified nonvolatile organic acids were acetic, formic,

propionic, butyric, valeric, n-caproic and malic acid. The identified carbonyl

compounds were acetaldehyde and acetone. The content of lactic acid was

increased with fermentation, and higher in kimchis containing red pepper,

garlic and green onion. The content of acetic acid wasincreased with

fermentation, especially in the kimchi containing garlic. The content of carbon

dioxide was higher in the kimchi containing garlic. Alcohols identified in all

kimchis were only ethanol. Carbonyl compounds had no direct effect on

off-flavor of kimchi.92)

The production of free non-volatile and volatile organic acids in kimchi

during fermentations at 30, 20, and 5oC, were determined by gas

chromatography. The order in the amount of non volatile organic acid, soon

after preparation, was malic,citric, tartaric, pyroglutamic, oxalic, lactic, succinic,

and L-ketoglutaric acids. The major non volatile acids at the optimum ripening

time were malic, tartaric, citric and lactic acids, and as the temperature was

lowered, the amount of lactic, succinic, oxalic, pyroglutamic and fumaric acid

increased, while that of malic, and tartaric acids decreased. The order in the

amount of volatile acids at the beginning was acetic, butyric, propionic and

formic acids. Among these acids, acetic acid was significantly increased in its

amount during fermentation. The kimchi fermented at low temperature

produced more acetic acid than that fermented at high temperature.90,95)

- 19 -

Of 17 volatile flavor components tentatively identified from kimchi, ethanol

was the most abundant, and increased in fermented kimchi while the others

decreased with the time of fermentation.96) It was also found that the ratio of

volatile to non volatile acids found to be highest at the optimum-ripening time

of kimchi.16)

Vitamin B1, B2, B12, and niacin reachedthe highest levels -twice the original

content- at maturation. It was also found that kimchi had the most palatable

taste at this period and subsequently there was a sharp decrease in B vitamins

with a sudden development of acids. On the other hand, although both vitamin

C and carotene decrease during fermentation, their residual contents were still

significant.97)

Many kinds of free amino acids were identified from mustard leaf kimchi

samples, and it was found that major free amino acids were proline, glutamic

acid, alanine and histidine. It was also found that nucleic-acid related

compounds were hypoxanthine, inosine monophosphate (IMP), and guanine

monophosphate (GMP).98)

Major flavor components were identified as dimethyl disulfide, dimethyl

trisulfide, dipropyl disulfide, 1-butane-1-isothiocyanate, and diallyl disulfide

from kimchi fermented at 5oC by GC and GC-MS. The contents of organic acids

such as lactic and citric acid increased during fermentation. Free amino acids

were importantin kimchi flavor. Total concentration of free amino acids

increased from 316 to 600 mg/100g of kimchi on fermentation, and glutamic

acid, alanine, valine, leucine, lysine and arginine levels were high. Sensory

evaluation showed that kimchi flavor was closely related to the contents of

non volatile organic acids and free amino acids and pH.99)

In wooung kimchi, a specialty kimchi prepared form burdock (Arctium lappa

L), fermented at 15oC, it was found that the major volatile components were

identified as ethanol, hexanol, 2-hexanol, disulfidedi-2-prophenyl, zingiberene,

and beta-sesquiphellandrene. The relative amounts of hexanal, 1-hexanal and

ethanol decreased, while the relative amounts of acetic acid ethyl ester,

3-hydroxy-2-butanone and acetic acid increased gradually during

fermentation.100)

Aroma-active compounds in kimchi prepared with or without fish sauce

were analyzed. The most intense aroma compounds in kimchi included

dimethyl trisulfide, diallyl disulfide isomers, diallyl trisulfide, and methylallyl

disulfide. However, addition of fish sauce did not noticeably affect the aroma

profile of kimchi.101)

Recently, flavor compounds of dongchimi soup fermented at different

temperature and salt concentration were analyzed. In this study four organic

acids including acetic, lactic, malic, and succinic acid were identified. The flavor

compounds of dongchimisoup were composed of mainly dimethyl disulfide and

ethanol followed by 3-(methylthio)-1-propene. Acetic acid and dimethyl

- 20 -

trisulfide were also detected significantly. Dongchimi soup fermented at 4 oC

after prefermentation at 12 oC for 12 hr contained the largest amount of flavor

compounds.28)

The taste and flavor components have been identified from various kimchi

samples. However, the exact amounts of those compounds during kimchi

fermentation were not clearly analyzed. Further researches are needed to

improve the tastes and quality of kimchis.

Ⅳ. Characteristics of LAB from kimchis

1. Identification of kimchi microorganisms

Kimchi fermentation and ripening were carried out by the microorganisms

present in the raw materials. Sugars in the raw materials are converted by the

LAB surviving at 2~3%salt concentration to lactic, acetic acid, carbon dioxide,

ethanol and mannitol.

The qualityof kimchi depends on the composition of the LAB involved in

the fermentation process. Therefore, in order to study the ecology of kimchi

microorganisms, it is important to understand the components of the microbial

community and identification of the physiologically active microorganisms for

kimchi fermentation.

Isolation and identification of microorganisms have long been attempted in

kimchi, conventionally prepared and fermented with the mixture of salted

cabbage and spices such as sliced radish, red peppers, garlic, ginger, green

onions, and fermented fish sauces. Kimchi is a fermented food with the variety

of vegetables. Therefore, it is expected that various LAB propagate in its

habitat.

Since 1960, many aerobic bacteria, anaerobic bacteria including LAB, yeast,

and fungi were isolated and identified from kimchi and other vegetable

fermented products and were reported in Korea as seen in Table 5 and 6.

Seven genera of LAB include Lactobacillus, Leuconostoc, Weissella,

Pediococcus, Streptococcus, Lactococcus, and Enterococcus were isolated and

identified from kimchis as seen in Table 5. Among them, Lac. brevis, Lac.

plantarum, Leu.citreum, Leu. lactis, Leu. mesenteroides subsp. mesenteroides, Leu.

mesenteroides subsp. dextranicum, Weis. pramesenteroides, Str. faecium, and Ped.

pentosaceus have been commonly isolated.

Six genera of aerobic bacteria from kimchi were Achromobacter,

Flavobacterium, Pseudomonas, Aerococcus, Aeromonas, and Bacillus, and ten

genera of yeast from kimchi wereBretanomyces, Candida, Cryptococcus,

Citeromyces, Debaryomyces, Kluyveromyces, Pichia, Rhodotorula, Saccharomyces and

Torulopsis as seen in table 6. However, there is no clear evidence how those

aerobic bacteria and yeasts except Saccharomyces species have been involved

- 21 -

and affected kimchi fermentation.

Recently, Leu. mesenteroides, Lac. curvatus, Lac. cellobiosus, Leu. citreum,

Lactococcus lactis subsp. lactis, Lac. acidophilus and Lac. delbrueckii subsp.

delbrueckii were isolated from dongchimi made by traditional method.87) Also,

ethanol and low acid producing Weis. paramesenteroides P30 were isolated from

kakduki (cubed radish kimchi) and used as kimchi starter for reduced acid

production.111) Lac. plantarum and Lac. pentosus from low salt (0.2-1.0%)

mul-kimchi and Lac. plantarum, and Lac. brevis from medium salt (3.0%)

mul-kimchi were isolated and identified. Other identified LAB were Leu.

citreum, Leu. mesenteroides subsp. mesenteroides and dextranicum and Str. faecium

in mul-kimchi containing 0-3.0% salt, while Pediococcus sp. was not detected. As

gram-negative organisms, Aeromonas hydrophyla, Pseudomonas fluorescens,

Pseudomonas aureofaciens and yeast Candida pelliculosa, Cryptococcus laurentii were

identified in the mul-kimchi.27)

Lactic acid bacteria are widely distributed in Korean traditional fermented

food such as kimchi. Also many LAB have been isolated from kimchi,

particularly, the genera Lactobacillus, Leuconostoc, Weissella and Pediococcus are

known to play an important role in kimchi fermentation.69,89,111)Traditional

identification methods based on physiological phenotypes are labor intensive

and time consuming. Until recently, the identification of the LAB isolated from

kimchi has mostly depended on traditional phenotypic analyses. However, this

type of identification method using biochemical and morphological

characteristics is limited in its discrimination and accuracy.108) Therefore, studies

on their systematic taxonomy have been reported.104,106,118,119)Accordingly, the

effective study of kimchi fermentation requires the development of rapid and

accurate LAB identification methods, such as genotypic approach using modern

molecular typing and identification tools.103,109,120)

Recently, LAB in kimchi were identified and differentiated rapidly by using

the Biolog system. Leuconostoc and Lactobacillus are reported as the main genera

associated with kimchi fermentation.118,106). The former genus was generally

found at less than 15oC and wascomprised of isolated strains such as Leuconostoc

mesenteroides subsp. mesenteroides, Leu. citreum, Leu. gelidum, and Leu.

kimchi.107,112) All species of the genus Leuconostocisolated from kimchi have been

found to produce slime from sucrose so far, which is a dextran, and dextran

producing Leuconostoc lactis from sucrose media was also isolated from

kimchi.108)

Until 90's most taxonomic studies on isolates from kimchi have been based on

phenotypic characteristics, but after 90's a polyphasic approach including

phenotypic, chemotaxonomic, and molecular methods is applied to determine

the taxonomic position of kimchi microorganisms. Recently, novel strains such

as Leuconostoc kimchi,112) Lactobacillus kimchi,113) Weissella koreensis,114) and

Weissella kimchi117) from kimchi have been reported. However, further studies

- 22 -

are needed to understand the real role of those new strains on kimchi

fermentation.

Aerobic yeasts and molds appear on the surface of the upper layer and on

improperly covered vegetables at the later fermentation stages. Undesirable

kimchi with an off-flavors and softened texture is positively due to the

excessiveaerobic growth of moulds and film-forming yeasts. Particularly the

film-forming yeasts appeared in long term stored kimchi at low temperature

produce a polygalacturonase which degrade pectin to make kimchi's texture

soft.70) However, yeast appearing in low temperature (below 15℃) fermented

kimchi has a certain role in kimchi's flavor and odor.79)

2. LAB producing bacteriocins from kimchi

Kimchi is prepared with various kinds of vegetables, spices and other

ingredients and becomes palatable through proper fermentation. Kimchi

fermentation initiated by various microorganisms present in the raw materials,

but the fermentation is gradually dominated by LAB.1,5) The LAB play an

important role in the taste of kimchi, as in dairy products such as cheese and

fermented milk. The strains belonging to the genera Leuconostoc, Lactobacillus,

Streptococcus, Pediococcus and Lactococcus in kimchi have been reported1,16,24,104)

Accordingly, kimchi has been one of the important sources of LAB in Korea for

a long time. Generally, the LAB are known to have the potential to inhibit the

growth of microorganisms, especially pathogenic and spoilage bacteria. The

antimicrobial activity of LAB is known to be due to the produced organic acids,

hydrogen peroxide, diacetyl and bacteriocins. Many LAB have been isolated

from kimchi in Korea and some of them have been shown to have antimicrobial

activity and other useful properties121-123)

The LAB have long been known to produce antimicrobial proteins called

bacteriocins. Certain bacteriocins inhibit various food-born pathogens,

including Bacillus cereus, Clostridium perfringens, Listeria monocytogenes, and

Staphylococcus aureus. This suggests that bacteriocin-producing LAB may be

useful in biocontrol of kimchi either by applying the culture directly or by

adding the produced bacteriocin as a natural preservative. From this point of

view, there are many reports on the isolation of bacteriocin-producing LAB

from various kimchi samples.

As seen in Table 7, bacteriocins are produced by the genera of Pediococcus,

Lactobacllus, Leuconostoc, and Lactococcus in kimchis.

The LAB isolated from kimchi have antimicrobial activity against E. coli,

Staphylococcus aureus, Bacillus cereus and other microorganisms. Major LAB

responsibile for this activity are Pediococcus pentosaceus, Leuconostoc spp., Lac.

plantarum and Lactococcus lactis. The properties of the inhibitory substances

from these bacteria have been determined and purified. These bacteria could

- 23 -

produce adverse circumstances for the growth of other microorganisms.124,125)

Due to the antibacterial activity of nisin against wide range of gram- positive

bacteria and its stabilityunder acidic conditions, nisin have been studied on its

effectiveness in preventing over-acidification of kimchi. It has been reported

that nisin added kimchi showed a slower rate of acid production.47)However,

controversial result was found that the use of nisin to prevent over acidification

of kimchi was not effective because of the nisin inactivation by vegetable

components and the presence of nisin-resistant LAB on kimchi.125-127)

Ⅴ. Conclusion

Kimchi is characteristic in its palatability giving sour, sweet and carbonated

taste with medium texture in tissue of kimchi. In this respect kimchi differs

greatly from sauerkraut that is popular in the West. The optimum acidity, pH

and salt content of kimchi are 0.6% (as lactic acid), 4.5 and 2.0-2.5%,

respectively. Kimchi fermented at low temperature (7-14℃) was more tasty

than that at higher temperature (20-30℃).

The total number of kimchi microorganisms reaches its maximum level

(1x108-9 cells/ml) at optimum-ripening time, and after then the number of LAB

decreases slowly and maintains its 2nd maximum level (1x106-7 cells/ml).

Many aerobic and anaerobic bacteria, especially LAB were isolated and

identified from kimchi. However, in kimchi fermentation system, it seems clear

that hetero fermentative LAB producing organic acids, carbon dioxide, and

dextrans from sugars are major species in the early stage and optimum

fermentation period. Homo fermentative LAB producing excessive lactic acid is

a major species in the final stage of fermentation. The total aerobic bacteria and

fungi decreased and the yeasts somewhat increased and slowly decreased in

number at lower temperatures (10-14℃).

Carbon dioxide and organic acids such as lactic, acetic, succinic and citric

acids were detected during kimchi fermentation. Vitamin B1, B2, B12, and

niacin increased two fold at optimum ripening period and decreased during

over-ripening, while vitamin C and carotenoid decreased. It was also found

that the ratio of volatile to nonvolatile acids and carbon dioxide reached

maximum at optimum-ripening period of kimchi.

Kimchi fermentation is complex and is due mainly to certain LAB and yeasts

naturally present in raw materials. Several physicochemical and biological

factors such as salt and sugar concentration, temperature, raw materials, natural

preservatives and starter culture influence the quality of kimchi. Among the

many factors affecting kimchi fermentation, salt content and temperature are

the most important, and the next is the quality of raw materials and

microorganisms specially hetero fermentative LAB.

Many homo and hetero fermentative LAB, such as genus Lactobacillus,

- 24 -

Leuconostoc, Weissella, Lactococcus, Streptococcus and Pediococcus were isolated

and identified from various kimchi samples, but genus Leuconostoc, Weissella

and other LAB producing organic acids, carbon dioxide and bacteriocins are the

most important microorganisms for the controlled fermentation of kimchi.

However, further studies are need to understand the real mechanism of those

LAB on kimchi fermentation and improved classification techniques using

modern taxonomies such as polyphasic and molecular methods are necessary to

understand kimchi microorganisms.

After optimum ripening is reached, kimchi fermentation may continue until

the product has acidic taste and softenedtexture, which cause the acid

deterioration. So far the preservation of kimchi under refrigeration at around

5oC is known to be the best way for long-term preservation up to 6 months.

Finally, further researches are needed to develop the technology necessary for

the controlled fermentation using starters and long-term preservation of

commercial kimchi.

And also, further studies are needed to fully understand the mechanisms of

action and to gain a complete knowledge, even though systematic research is

difficult because of the complexity of kimchi.

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