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Traditional Indian fermented foods: A rich source of lactic acid bacteria

Article  in  International Journal of Food Sciences and Nutrition · November 2012


DOI: 10.3109/09637486.2012.746288 · Source: PubMed

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International Journal of Food Sciences and Nutrition,
2012; Early Online: 1–14

Traditional Indian fermented foods: a rich source of lactic acid bacteria

R. SATISH KUMAR, P. KANMANI, N. YUVARAJ, K. A. PAARI, V. PATTUKUMAR, & V. ARUL

Department of Biotechnology, Pondicherry University, Puducherry-605014, India

Abstract
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This review describes the diversity of Indian fermented food and its significance as a potential source of lactic acid bacteria
(LAB). Fermented foods consumed in India are categorized based upon their base material. Fermented foods such as dahi,
gundruk, sinki, iniziangsang, iromba, fermented rai, kanjika and handua were reported to have significant medicinal properties.
Some fermented products such as koozh, dahi and kanjika are consumed unknowingly as, probiotic drinks, by local people.
There are very few reports regarding isolation of LAB from Indian fermented foods available in the past; however, due to
growing consciousness about potential health benefits of LAB, we now have scores of reports in this field. There is an abundant
opportunity available for food microbiologists to explore the Indian fermented foods for the isolation of new LAB strains for
their potential role in probiotic research.

Keywords: fermented foods, probiotics, lactic acid bacteria, traditional foods


For personal use only.

Introduction
Traditional fermented foods are popularly consumed it up to 3.5 (Steinkraus 1983). Traditional uses of
and form an integral part of our diet since early history. many LAB as fermentation agents for foods are
It can be prepared in the household or in cottage considered to be safe for the general population.
industry using relatively simple techniques and Lactic acid bacterial genera consist of Lactobacillus,
equipments (Aidoo et al. 2006). Fermentation was Lactococcus, Enterococcus, Streptococcus, Pediococcus,
evolved as a preservation or prevention technique and Leuconostoc, Weisiella, etc.
during lean periods to counter spoilage of food India is traditionally rich in fermented foods. In the
products. It is one of the oldest and most economical Indian sub-continent, fermented food using local
methods for producing and preserving foods. In food crops and other biological resources are very
addition to preservation, fermented foods can also common. But the nature of the products and base
have added benefits of enhancing flavour, increased material varies from region to region (Sekar and
digestibility, and improving nutritional and pharma- Mariappan 2007). Fermented foods such as idli and
cological values (Jeyaram et al. 2009). Lactic acid dahi were described as early as 700 BC. At present,
bacteria (LAB) perform an essential role in the there are hundreds of fermented foods with different
preservation and production of wholesome fermented base materials and preparation methodology. Each
foods. Homo-fermentative and hetero-fermentative fermented food is associated with a unique group of
LAB are generally fastidious on artificial media, but microbiota, which increases the level of proteins,
they grow readily in most food substrates and lower the vitamins, essential amino acids and fatty acids.
pH rapidly to a point where other competing However, fermented foods are still produced tra-
organisms are no longer able to grow. Leuconostocs ditionally by spontaneous fermentation and only
and Lactococcus generally lower the pH to 4.0 – 4.5 limited knowledge has been obtained regarding the
and some of the Lactobacilli and Pediococci lower microbiota of these products (Jeyaram et al. 2009).

Correspondence: V. Arul Associate Professor, Department of Biotechnology, Pondicherry University, Puducherry-605014, India.
Tel: þ 91-413-2654429 ext. 429. Fax: þ 91-413-2656742. E-mail: [email protected]

ISSN 0963-7486 print/ISSN 1465-3478 online q 2012 Informa UK, Ltd.


DOI: 10.3109/09637486.2012.746288
2 R. Satish kumar et al.

Literature survey was undertaken to enumerate the preparation of Kallappam, fermented toddy is added
indigenous fermented foods reported so far. The main to the batter as an additional source of LAB. The
objective of our study was to focus on the indigenous fermented batter is prepared into either as steamed
fermented foods that are explored and unexplored for cakes (idli) or as pan cakes (dosa, appam) before it
LAB. Since LAB isolated from fermented foods are gets too soured. Idli is a natural fermented food,
becoming globally important for the use as human both bacteria and yeasts are generally introduced by
probiotics, new isolates may pave a way for intense the ingredients. Leuconostoc mesenteroides is the most
research in the medical application. Furthermore, commonly encountered bacterium (Nout and Sarkar
large proportions of fermented foods are unexplored 1999). Dhokla is similar to idli except that the dal
for their microbiota, hence these can be exploited in used is Bengal gram (Cicer arietinum). LAB
future to isolate useful probiotic strains. contributes lactic acid and acetoin, imparting sour
Fermented foods are categorized as follows: taste and a pleasant flavour (Aidoo et al. 2006).
(i) cereal-based (with/without pulses) fermented Koozhu is the Tamil name for porridge made from
foods, (ii) cereal/pulse and buttermilk-based fermen- millet. Finger millet, a traditional South Indian
ted food, (iii) cereal-based fermented sweets and weaning food, is also consumed in the fermented
snacks, (iv) milk-based fermented foods, (v) vegetable, form, as koozhu in rural and urban households
bamboo shoot (BS) and unripe fruits-based fermented (Antony et al. 1998). Koozhu is made from
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foods, (vi) meat-based fermented foods and (vii) pulse Kezhvaragu or Cumbu flour and broken rice (called
(legume)-based fermented foods. noyee in Tamil) in a mud pot. Koozhu is consumed
as a breakfast and during festival time by the rural
population. Koozhu is easily digested and it cools the
Cereal-based (with/without pulses) fermented foods
body; therefore, during summer street vendors sell it
Cereal-based fermented foods are considered as as a cool drink in South India. Fermented rice or
staple foods in their respective regions. Most of the Pazhaiya soru is prepared by adding water to cooked
foods such as idli, dosa, dhokla, koozhu, nan, parotta, rice and by incubating the mixture overnight, and
ambali, pazhaiya soru are consumed on the daily basis finally adding buttermilk and salt and directly
For personal use only.

by the local population. Cereals such as rice (Oryza consumed (Sekar and Mariappan 2007). It is an
sativum), ragi flour (Eleusine coracana), wheat flour early morning diet for farmers prior to going to the
(Triticum spp.), barley flour (Hordeum vulgare), and field. Predominant microbiota isolated from these
pulses such as black gram dhal, red gram, green gram foods include: Weissella paramesenteroides, Lactobacillus
dhals are predominantly used in the preparation. fermentum, L. plantarum, Enterococcus faecalis,
These cereals and legumes are cultivated in India Pediococcus acidilactici, P. cerevisiae, L. mesenteroides
since the Indus valley civilization (9000 –5500 BC) (Table I). L. plantarum AS1 isolated from South
period (Samanta et al. 2011) and they are commonly Indian fermented food Kallappam successfully pre-
used as ingredients in the preparation of significant vented colonization of entero-virulent bacterium
number of foods. These cereals and legumes are Vibrio parahaemolyticus in HT-29 cell line (Satish
considered as effective substrates for the production et al. 2011) and colorectal cancer in male Wistar rats
of probiotic-incorporated functional food, as they can (Satish et al. 2012). LAB isolated from dosa inhibited
be used as a source of non-digestible carbohydrates, pathogens such as Bacillus cereus, Staphylococcus
which stimulate the growth of Lactobacilli and aureus, Listeria monocytogenes, Pseudomonas aerugi-
Bifidobacteria. They contain water-soluble fibres such nosa, V. parahaemolyticus and Aeromonas hydrophila
as b-glucan, arabinoxylan, galacto-oligosaccharides through their antibacterial protein bacteriocin
and fructo-oligosaccharides, which are digested by (Pal et al. 2005). Still, there is a large proportion
selective groups of LAB (Swennen et al. 2006). of foods in this category which are unexplored for
Cereals and legumes are fermented by several groups microbiota.
of bacteria in the large intestine, yielding a variety of
fermentation products, particularly short-chain fatty
Cereal/pulses and buttermilk-based fermented foods
acids (SCFAs). The resulting SCFA is known to
provide an acidic environment in the large intestine, Buttermilk is an additional source of LAB in this
which stimulates the proliferation of lactic microbiota type of fermented foods. Although there are very few
(Macfarlane et al. 2006; Roopashri and Vardaraj dishes reported in this category, these foods are
2009). very popularly consumed in most parts of India.
In the preparation of fermented foods such as idli, W. paramesenteroides isolated from Mor kuzhambhu
dosa, adai dosa, kallappam, ambali and dhokla, the showed antibacterial activities towards food borne
batter is prepared from the basic ingredients pathogens Salmonella typhi and L. monocytogenes
(Table I), and this batter is left overnight at room (Satish et al. 2010). Blandino et al. (2003) reported
temperature for fermentation, occasionally sodium non-LAB Bacillus sp., Micrococcus sp. in rabdi.
bicarbonate is added to provide anaerobic conditions Himachal Pradesh fermented foods Kulu and Kadi
for the growth of yeast and LAB. During the are still unexplored for its microbiota (Table II).
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For personal use only.

Table I. Cereal-based (with/without pulses) fermented foods.

Fermented food Usual composition/ingredients Place of origin/usage LAB isolated Refs

Koozhu E. coracana (ragi) flour, boiled rice, non-fat yoghurt Tamil Nadu W. paramesenteroides, L. fermentum Satish et al. (2010)
Pazhaiya soru Rice, curd and salt Tamil Nadu E. faecalis, P. Acidilactici Ramakrishnan (1977, 1979)
Idli Rice, black gram dhal, table salt, fenugreek seeds South India L. mesenteroides, E. faecalis, P. cerevisiae Mukherjee et al. (1965), Steinkraus
et al. (1967)
Dosa Rice, black gram dhal (either raw or parboiled rice), South India L. mesenteroides, E. faecalis Labana and Kawatra (1986), Chavan
table salt and Kadam (1989), Steinkraus (1996)
Adai dosa Boiled rice, Bengal gram, red gram, black gram, South India Pediococcus sp., Streptococcus sp., Chavan and Kadam (1989)
green gram Leuconostoc sp.
Kallappam Boiled or raw rice, coconut toddy South India L. fermentum, L. plantarum Satish et al. (2010)
Dhokla Bengal gram dhal, rice and leafy vegetables South India L. fermentum, L. mesenteroides, E. faecalis Ramakrishnan et al. (1976), Blandino
et al. (2003), Roy et al. (2007)
Ambali Ragi (Millet) flour and rice India L. fermentum, L. mesenteroides, E. faecalis Ramakrishnan (1977, 1979)
Nan Wheat flour, sugar, salt and backslop North India Not reported Sandhu et al. (1986)
Siddhu or khobli Wheat flour, opium seeds/walnut/black gram and Himachal Pradesh Not reported Thakur et al. (2004)
starter material Malera
Chilra or lwar Wheat/barley, buckwheat flour and starter material Himachal Pradesh Not reported Thakur et al. (2004)
Treh
Marchu Wheat flour and starter material malera Himachal Pradesh Not reported Thakur et al. (2004)
Pinni or bagpinni Barley flour and buttermilk or Chhang Himachal Pradesh Not reported Thakur et al. (2004)
Parotta Wheat flour, sugar, egg, salt South India Not reported Indrani and Rao (2003)
Sez Rice (Oryza sativa) and the starter balam Himachal Pradesh Not reported Kanwar et al. (2007)
Chakuli Par-boiled rice and black gram, jackfruit or palmyra Orissa Not reported Roy et al. (2007)
palm fruit
Enduri pitha, Par-boiled rice and black gram Orissa Not reported Roy et al. (2007)
munha pitha
Jhan chang Barley and the starter material Phab Himachal Pradesh Not reported Kanwar et al. (2007)
Babru Rice, salt and spices Himachal Pradesh Not reported Kanwar et al. (2007)
Taotjo Roasted wheat meal or glutinous rice and soybeans East India Not reported Blandino et al. (2003)
Traditional Indian fermented foods
3
4 R. Satish kumar et al.

Table II. Cereal/pulse and buttermilk-based fermented food.

Fermented food Usual composition/ingredients Place of origin/usage LAB isolated Refs

Rabdi (rabadi) Flour of barley, pearl millet, corn Rajasthan Bacillus sp., Micrococcus sp. Blandino et al. (2003)
or soybean and country buttermilk
Kulu Wheat flour, buttermilk Himachal Pradesh Not reported Savitri and Bhalla (2007)
Kadi/kadu/kheeru Buttermilk/dahi and gram flour Himachal Pradesh Not reported Savitri and Bhalla (2007)
Mor kuzhambhu Buttermilk, gram flour, vegetables, spices Tamil Nadu Weissella paramesentroides Satish et al. (2010)

Cereal-based fermented sweets and snacks (Prashant et al. 2009, Thapa 2002). Chhurpi has a
white, soft with a mild to strong flavoured taste and is
These foods are consumed mostly during festival times
consumed as curry mix with wild edible ferns
and other special occasions. Wheat, rice and barley
(Diplazium spp.), pickels and condiments along with
flours are predominantly used cereals. Sugar or salt is
boiled rice in meals (Tamang et al. 2000). Average per
added compulsorily in the fermented foods mentioned
capita consumption of Chhurpi is 6.9 g/day in
in this category (Table III), in jilebi and selroti sugar
Darjeeling hills, and 9.9 g/day in Sikkim (Yonzan and
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as high as 25% is added (Tamang et al. 1988; Yonzan


Tamang 1998). In a ripened Chhurpi, LAB were . 7.5
and Tamang 2009). These foods select only those
logCFU/g. All LAB strains except L. mesenteroides
microbes which can survive low water activity.
BFE1637 showed high degree of hydrophobicity. This
Fermented sweets and snacks are popularly consumed
is a significant property of LAB that assists in
throughout India, consequently many reports are
colonization of epithelial cells. Enzymes such as
available for this category but only few reports are
peptidases and esterase-lipases of LAB strains may
available on microbiota isolation. Barring jilebi and
play an important role in the improvement of cheese
bhataru, none of the foods are explored. L. fermentum,
quality. Similarly, Chhu (Sheden) is a strong flavoured
L. buchneri, L. plantarum, L. acidophilus, L. mesenter-
traditional cheese-like product in Sikkim, Darjeeling
oides, Lactococcus lactis, Streptococcus lactis and
For personal use only.

hills, Arunachal Pradesh and Ladakh (Table IV). It is


E. faecalis are reported LAB species isolated from
consumed as curry by cooking it in butter along with
this class of fermented foods (Table III).
onions, tomatoes and chillies and is mixed with beef or
yak meat. Dewan and Tamang (2007b) explored the
microbiota present in Chhu. LAB were predominantly
Milk-based fermented foods
present at 8.1 – 8.8 logCFU/g. They isolated 120
Milk and milk-based products are consumed most strains of LAB. All strains showed high degree of
popularly due to their nutritive value. For the same hydrophobicity and did not produce any biogenic
reason milk is easily curdled by pathogenic microor- amines, which indicates the strains could be used as a
ganisms, hence fermentation of milk using LAB is starter culture. They had coagulation and acidification
preferred for prevention of nutrient quality. LAB property. Shyow is a thick gel curd like product,
convert milk sugar lactose into lactic acid and selective prepared from yak milk (Table IV). Mohi is buttermilk,
strains produce antibacterial substance bacteriocin to prepared by churning dahi (Table IV). It is consumed
suppress milk curdling bacteria. Most of the foods in as a refreshing beverage. Somar is a soft paste, strong
this category are prepared by simply adding LAB to flavoured with bitter taste and is consumed as
milk of either cow, buffalo or yak and allowed to soup along with cooked rice or finger-millets by the
ferment. One such fermented food is dahi, its Sherpas of Sikkim (Table IV). Philu is a typical
description is found in texts as old as 700 BC. Dahi indigenous cream-like milk product obtained from
or curd is most popular and commonly used cow milk or yak milk and is mostly eaten as a cooked
traditional Indian fermented product. Dahi differs paste delicacy with boiled rice by the Sikkimese
from yogurt in its use of mixed starters of mesophilic (Dewan and Tamang 2007a). LAB isolated from
lactococci. A principal flavour-inducing metabolite is Shyow, Mohi, Somar and Philu were characterized by
diacetyl, which is appreciated more by people of South Dewan and Tamang (2007a). LAB strains produced
Asian origin compared to the acetaldehyde flavour in various enzymes such as esterase, phosphatase,
yogurt (Yadav et al. 2007b). leucine-arylamidase, b-galactosidase and peptidase.
Yak milk is processed into a number of dairy These bacterial strains inhibited pathogens such as
products such as fermented milk (Kurut), cheese Enterobacter agglomerans, Enterobacter cloacae and
(Chhurpi), Chhur churpen, Churkham, Chhu, Philuk, Klebsiella pneumoniae. LAB strains did not produce
Shyow and Maa (Table IV). The chemical composition any undesirable biogenic amines. Some of the LAB
of yak cheese is around 68.2% of total solid, 49.4% of strains showed high degree of relative hydrophobicity
butterfat on a dry matter basis and 1.37% of salt. It is (. 75%), as judged by bacterial adherence to
largely consumed in the Himalayan highland and its hydrocarbon, indicating their hydrophobic nature.
industrial production has not yet been standardized Khadi is a delicacy of Gujarat (Table IV). This
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For personal use only.

Table III. Cereal-based fermented sweets and snacks.

Fermented food Usual composition/ingredients Place of origin/usage LAB isolated Refs

Jilebi Wheat, sugar and curd South India L. fermentum, S. lactis, Ramakrishnan (1977), Prakash et al.
L. buchneri, E. faecalis (2004)
Gulgule Wheat flour and starter material Malera Himachal Pradesh Not reported Thakur et al. (2004)
Seera Wheat, sugar and ghee Himachal Pradesh Not reported Thakur et al. (2004)
Chhuchipatra pitha, Podo pitha Par-boiled rice, black gram, coconut, sugar Orissa Not reported Roy et al. (2007)
and curd
Bhaturu or indigenous bread Wheat and starter material Khameer/Malera Himachal Pradesh L. plantarum, L. acidophilus, Tamang (1998), Thakur et al. (2004),
L. mesenteroides, L. lactis Kanwar et al. (2007)
Kulcha Wheat and the starter Khameer/Malera Northern India Not reported Parveen and Hafiz (2003)
Chitou Par-boiled rice and black gram Orissa Not reported Roy et al. (2007)
Selroti Rice, banana, honey, ghee and spices Himachal Pradesh and Sikkim Not reported Tamang et al. 1988, Yonzan and
Tamang (2009)
Manna Wheat Himachal Pradesh Not reported Savitri and Bhalla (2007)
Kurdi Wheat North India Not reported
Thuktal Barley Himachal Pradesh Not reported Savitri and Bhalla (2007)
Aska, anarshe, aenkadu/askalu, patande Rice Himachal Pradesh Not reported Savitri and Bhalla (2007)
Torani Rice Orissa Not reported Thakur et al. (2004)
Aet, aktori, baari, babroo, bhatooru, chhura, Wheat flour Himachal Pradesh Not reported Blandino et al. (2003), Thakur et al.
mande/manna, malpude, tcung, shunali (2004), Savitri and Bhalla (2007)
Chhangpa, doo, khawalag, marpinni/ Roasted barley flour Himachal Pradesh Not reported Blandino et al. (2003), Thakur et al.
marjag, tchog, thuktal (2004), Savitri and Bhalla (2007)
Khatta Gram, walnut powder Himachal Pradesh Not reported Savitri and Bhalla (2007)
Mangjangkori Buck wheat bran Himachal Pradesh Not reported Thakur et al. (2004)
Tchhoso roti Kodra flour Himachal Pradesh Not reported Savitri and Bhalla (2007)
Tiskori Wheat bran Himachal Pradesh Not reported Savitri and Bhalla (2007)
Sang Wheat grains Himachal Pradesh Not reported Savitri and Bhalla (2007)
Traditional Indian fermented foods
5
6 R. Satish kumar et al.

(1996), Patil et al. (2010), Davies (1940),


fermented food is prepared from sour dahi (curd) or

Srinivasan and Banerjee (1946), Steinkraus

Tamang et al. (2000), Singh et al. (2007a),


buttermilk mixed with spices and dhal and warmed.

Tiwari and Mahanta (2007), Prashant


Tamang et al. 1988, Tamang (1998),
The sour curd is made from cow’s milk, inoculated
with a culture of curd and allowed to ferment for a day

Dewan and Tamang (2007b)


or even longer at room temperature. The sour curd

Dewan and Tamang (2007a)


Dewan and Tamang (2007a)
Dewan and Tamang (2007a)
Dewan and Tamang (2007a)
Dewan and Tamang (2007a)
Dewan and Tamang (2007a)

Sukumar and Ghosh (2010)


Tiwari and Mahanta (2007)
is either used directly for further processing or

Savitri and Bhalla (2007)


Dellaglio et al. (2005)
churned into buttermilk and then processed. This

Singh et al. (2007a)


food is often served with rice or the naan (Sukumar

et al. (2009)
and Ghosh 2010). LAB isolated from khadi exhibited
antibacterial activity against S. aureus, Escherichia coli
and P. aeruginosa and also showed basic probiotic
Refs

properties (Sukumar and Ghosh 2010).


LAB species isolated from fermented milk
products include Streptococcus cremoris, S. lactis,
S. thermophilus, Lactobacillus bulgaricus, L. acidophilus,
L. helveticus, L. cremoris, P. pentosaceous, P. acidilactici, W. cibara,

L. helveticus, L. cremoris, L. plantarum, L. curvatus,


W. paramesenteroides, L. fermentum, L. plantarum, Lactobacillus
S. cremoris, S. lactis, S.thermophilus, L. bulgaricus, L. acidophilus,

subsp. pseudoplantarum, L. alimentarius, L. kefir, L. hilgardii,

L. farciminis, L. brevis, L. alimentarius, L. lactis subsp. cremoris

L. fermentum, L. paracasei subsp. pseudoplantarum,


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L. alimentarius, L. lactis subsp. lactis, L. lactis subsp. cremoris

L. alimentarius, L. kefir, L. hilgardii, Enterococcus


faecium, L. mesenteroides, L. farciminis, L. brevis, L. lactis
L. plantarum, L. curvatus, L. fermentum, L. paracasei

L. bifermentans, L. paracasei subsp. pseudoplantarum


L. casei subsp. casei, L. bifermentans and E. faecium

subsp. cremoris, L. casei subsp. casei and L. bifermentans


(Table IV). Mitra et al. (2007) isolated L. lactis from dahi
E. faecium and L. mesenteroides, L. helveticus

which produced nisin-like (Nisin Z) bacteriocin that


inhibited important food pathogens L. monocytogenes
L. paracasei subsp. pseudoplantarum

and S. aureus.
Table IV. Milk-based fermented foods.

delbrueckii subsp. indicus

Vegetable, BS and unripe fruits-based fermented foods


For personal use only.

The lactic acid fermentation of vegetables, applied as a


preservation method for the production of finished
Pediococcus sp.
Not reported

Not reported

Not reported

Not reported
Not reported

and semi-finished products, is considered as an


LAB isolated

important technology because of its capability to


improve the nutritive value, palatability, acceptability,
microbial quality and shelf-life of the fermented
product (Kingston et al. 2010). Moreover, this is a
remarkable procedure to store the perishable vegetable
Place of origin/usage

in the absence of cold-storage or refrigeration, where


Himachal Pradesh,
Arunachal Pradesh

Arunachal Pradesh

Arunachal Pradesh

majority of rural people cannot afford canned or frozen


foods. Fermented vegetable-based foods have a
number of medically beneficial properties; they are
Gujarat
Sikkim
Sikkim
Sikkim
Sikkim
Sikkim
Sikkim
Sikkim
India

mentioned in a separate section below. Fermented BS


products are consumed as a traditional food by ethnic
people of North-eastern states of India (Tamang et al.
Yak milk is preferred for making this

2009b). In India, BSs are harvested annually in Sikkim


Yak milk and cut fruits of crab apple
cheese although any other fresh

(26.2 tonnes), Meghalaya (435 tonnes) and Mizoram


Usual composition/ingredients

(426.8 tonnes). BSs are low in fat and cholesterol, but


very high in potassium, carbohydrates and dietary
Chhurpi and fresh milk

fibres. Many nutritious and active materials (vitamins


milk may be used

and amino acids) and antioxidants (flavones, phenols


Cow or yak milk
Yak or cow milk

Buttermilk/curd
Buttermilk/curd

and steroids) can be extracted from BSs (Choudhury


Cow/yak milk

et al. 2011). Fermented bamboo-based foods and their


(Thung)

Cow milk
Cow milk
Cow milk
Yak milk

health benefits were also discussed. LAB are the


Milk

dominant microorganisms in ethnic fermented veg-


etables and BS products (Tamang and Tamang 2009).
Pediococcus pentasaceous, L. cellubiosus, L. plantarum,
Chhurpi or durkha

L. fermentum, L. brevis, L. mesenteroides, L. lactis,


Fermented food

(dahi, thayir)

Philu or Philuk
Chhur chirpen

E. faecium and P. acidilactici are predominant LAB


or churapi

Churkham

species found in fermented vegetables (Table V).


Shyow

Somar

Khadi

Tamang et al. (2009b) determined the functional


Curd

Chhu

Gheu
Mohi

Maa
Jhol

properties of LAB isolated from ethnic fermented


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For personal use only.

Table V. Vegetable, BS and unripe fruits-based fermented foods.

Fermented food Usual composition/ingredients Place of origin/usage LAB isolated Refs

Gundruk Leaves of mustard/ Arunachal Pradesh P. pentasaceous, L. fermentum, L. casei, L. casei Dahal et al. (2005), Singh et al. (2007b),
radish/cauliflower subsp. pseudoplantarum, L. plantarum Tamang and Tamang (2009)
Sinki Radish root North-east India L. casei, L. brevis, L. plantarum, L. fallax, L. fermentum Tamang and Sarkar (1993), Singh et al.
(2007b)
Sauerkraut or Sauerkohi Cabbage India L. mesenteroides, L. plantarum Steinkraus (1996)
Anishi Yam Nagaland Not reported Tamang and Tamang (2009)
Soibum or soijim BSs Manipur, Nagaland L. plantarum, L. brevi, L. corniformis, L. delbrueckii, L. fallax, Tamang and Tamang (2009), Jayaram
L. lactis, L. mesenteroides, E. durans, S. lactis, Bacillus et al. (2009)
subtilis, B. licheniformis, B. coagulans
Soidon BSs Manipur Lactobacillus brevis, L. fallax, L. lactis, L. plantarum, Tamang and Tamang (2009), Jeyaram
Carnobacterium sp., E. faecium et al. (2010)
Kardi or handua BSs Orissa Not reported Panda and Padhy (2007)
Bamboo tenga BSs Arunachal Pradesh Not reported Tiwari and Mahanta (2007)
Hikhu BSs North-east India Not reported Singh et al. (2007b)
Hiring BSs North-east India L. plantarum, L. lactis Singh et al. (2007b), Tamang and
Tamang (2009)
Ekung BSs Manipur L. plantarum, L. brevis, L. casei, T. halophilus Singh et al. (2007b)
Eup BSs Arunachal Pradesh L. plantarum, L. fermentum Tamang and Tamang (2009)
Khorisa-tenga, ushoi, amil, BSs North-east India Not reported Choudhury et al. (2011)
Iromba
Lungseij BSs Meghalaya Not reported Murughar and Subbulakshmi (2006),
Singh et al. (2007b)
Mesu BSs Darjeeling hills and Sikkim L. plantarum, L. brevis, L. curvatus, Leuconostoc citreum, Tamang and Tamang 2009
Pediococcus pentosaceus
Khalpi Cucumber Sikkim L. brevis, L. plantarum Tamang (1998), Tamang and Tamang
(2010)
Rai (brassica juncea) seeds Mustard seeds North-east India Not reported Singh et al. (2007b)
Goyang Wild plant magane-saag Darjeeling hills and Sikkim L. plantarum, L. brevis, L. lactis, E. faecium, P. pentosaceus Tamang and Tamang (2009)
(Cardamine macrophylla
Willd.) leaves
Inziangsang Mustard leaves Nagaland, Manipur L. plantarum, L. brevis, P. acidilactici Tamang and Tamang (2009)
Kanji Carrot or beet root, rice, North India L. pentosus, L. paraplantarum, L. plantarum Reddy et al. (2007), Madhu et al. (2010),
mustard Kingston et al. (2010)
Traditional Indian fermented foods
7
8 R. Satish kumar et al.

vegetables (gundruk, sinki, khalpi and inziangsang) of because of its simplicity and low cost of processing.
the Himalayas. LAB strains showed strong acidifica- When fatty fishes are salted there is usually a certain
tion and coagulation activities. They showed anti- degree of fermentation involved. Fermentation of fish
microbial activity, particularly a strain L. plantarum is brought about by autocatalytic enzymes from fish
isolated from inziangsang, a fermented leafy vegetable and microorganisms in the presence of high-salt
product, was inhibitory towards S. aureus and concentration (Majumdar and Basu 2010). Hentak is
P. aeruginosa. LAB strains showed various enzymatic a ball-like paste prepared by fermentation of a mixture
activities such as alkaline phosphatase, esterase, of sun-dried fish (Esomus dandricus) powder and
esterase lipase, lipase, leucine arylamidase, valine petioles of aroid plants (Alocasia macrorhiza) in
arylamidase, cysteine-arylamidase, acid phosphatase, Manipur (Thapa et al. 2004). Tungtap is a fermented
napthol-AS-B1-phosphohydrolase, a-galactosidase, fish paste, commonly consumed by the Khasias tribes
b-galactosidase, a-glucosidase, b-glucosidase, of Meghalaya in the North-eastern state of India
N-acetyl-b-glucosaminidase and also degraded oligo- (Thapa et al. 2004). Dry fish (Danio spp.) is mixed
saccharides. Some strains of L. plantarum showed with salt, kept in an earthen pot and fermented for
more than 70% hydrophobicity and adherence to the 4 – 7 days. It is consumed as pickle. L. lactis
mucus secreting HT-29 MTX cells. Seventeen LAB subsp. cremoris, Lactococcus plantarum, E. faecium,
strains from kanji responded positively when screened Lactobacillus fructosus, L. amylophilus and L. corneformis
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for probiotic properties such as acid tolerance, subsp. torquens are predominant LAB species reported
bile salt tolerance, antimicrobial activity against in fermented fish (Table VI). Thapa et al. (2004)
food-borne pathogens (B. cereus, L. monocytogenes, studied significant characteristics of LAB isolated from
E. coli, S. aureus, Yersinia enterolytica), b-galactosidase Ngari, Hentak and Tungtap. LAB strains showed the
activity, antibiotic susceptibility and cholesterol presence of proteolytic enzymes, antibacterial effect
assimilation (Reddy et al. 2007). L. plantarum isolated and absence of biogenic amines (tyramine, cadaverine,
from ayurvedic medicinal food Kanji or Kanjika is a histidine and putrescine). All tested strains had more
potential source of Vitamin B12 (Madhu et al. 2010). than 30% hydrophobicity, among which Lactobacillus
During fermentation of radish taproot product fructosus HL1 showed 84.3% hydrophobicity.
For personal use only.

sinki, L. plantarum utilizes mannitol to remove the Hydrophobicity is an important property of LAB for
bitter flavour from the finished product (Tamang and adherence to epithelial cells. Lactobacillus sake,
Sarkar 1993). BS-based fermented foods contain L. curvatus, L. divergens, L. carnis, L. sanfrancisco,
Lactobacillus plantarum, L. brevi, L. corniformis, L. mesenteroides, E. faecium, L. plantarum, L. brevis and
L. delbrueckii, Leuconostoc fallax, L. lactis, L. mesenteroides, Pediococcus pentosaceous are reported in fermented
Enterococcus durans, S. lactis, L. casei, Tetragenococcus meat products of eastern Himalayas (Table VI). These
halophilus and L. fermentum as predominant LAB LAB showed inhibitory activity towards Klebsiella
species (Table V), they also showed functional pnemoniae which is a contaminant of stored meat, they
probiotic properties (Tamang et al. 2009b). During were also able to synthesize enzymes, important for
fermentation of BSs, L. lactis helps in reducing cyanogen the digestion of mixed substrates (Rai et al. 2010).
glycoside content that causes major diseases of nervous
system, goiter and miscarriage (Singh et al. 2007b).
Pulse-based fermented foods
A pulse is an annual leguminous crop yielding from
Meat-based fermented foods. Meat is highly susceptible 1 to 12 seeds of variable size, shape and colour within
to microbial spoilage. Drying, smoking and a pod (http://en.wikipedia.org/wiki/Pulse (legume)).
fermentation of meat are critical steps in the Black gram, soybean, Bengal gram, red gram and
traditional processing of meat (Oki et al. 2011). In green gram are most commonly used pulses in this
India, people of the North-eastern region ferment type of fermented foods. Soybean (Glycine max) is a
meat of yak, goat, pig, fish and crab for preservation summer leguminous crop, grown under rain-fed
for longer period. Kargyong is an ethnic sausage-like conditions in upland terraces as a sole crop as well as
fermented product prepared from yak, beef and pork. mixed crop with rice and maize up to an elevation
Three varieties of Kargyong are prepared and of 1500 m in North-east India; due to Mongolian
consumed: yak kargyong (prepared from yak meat), population, consumption of different recipes of
lang kargyong (prepared from beef) and faak kargyong soybean is a tradition. Food researchers have
(prepared from pork). Yak kargyong is a popular documented a number of soybean-based Indian
fermented sausage in Sikkim, Ladakh, Tibet, fermented foods (Tamang et al. 2009b). Fermented
Arunachal Pradesh and Bhutan in the Himalayas soybean food is an economical source of plant protein
(Rai et al. 2010). Fermented fish products are as compared to animal and milk products on the basis
important dietary components in the protein- of protein cost per kg, which is easily accessible to the
deficient South-East Asia. Preservation of fish by salt rural poor of the North-eastern region. Kinema is a
is an age-old technology. This method of preservation fermented food from whole soybean seeds. Its colour
still enjoys popularity in many developing countries is grey tan, has a sticky texture and is flavourful
Int J Food Sci Nutr Downloaded from informahealthcare.com by 210.212.230.197 on 11/27/12
For personal use only.

Table VI. Meat-based fermented foods.

Fermented food Usual composition/ingredients Place of origin/usage LAB isolated Refs

Ngari Puntius sophore (Phoubu) Fish Manipur and Assam E. faecium, L. fructosus, L.amylophilus, L. plantarum Thapa et al. (2004), Jeyaram
et al. (2009)
Hentak Esomus danricus (Fish), petioles Manipur L. lactis subsp. cremoris, L. plantarum, E. faecium, L. fructosus, Thapa et al. (2004), Jeyaram
of A. macrorhiza L. amylophilus et al. (2009)
Tungtap Danio sp. (Fish) Maghalaya L. lactis subsp. cremoris, L. plantarum, E. faecium, L. fructosus, Thapa et al. (2004), Murugkar
L.corneformis subsp. torquens and Subbulakshmi (2006)
Fermented fish Puntias sophore (Trash fish). Manipur Not reported Murugkar and Subbulakshmi
(2006)
Lona ilish Hilsa, Tenualosa ilisha Fish North-eastern India Not reported Majumdar and Basu (2010)
Crab Crabs, Sesamum orientale L. North-eastern India Not reported Mao and Odyuo (2007)
(ground blacktil)
Utonggari Local fish (named ‘phobou’) Assam Not reported Singh et al. (2007b)
Lang kargyong Beef Eastern Himalayas L. sake, L. curvatus, L. divergens, L. carnis, L. sanfrancisco, L. mesenteroides, Rai et al. (2010)
E. faecium
Yak kargyong Meat of yak Eastern Himalayas L. plantarum, L. sake, L. casei, L. curvatus, L. carnis, L. divergens, Rai et al. (2010)
L. sanfrancisco, Leu. mesenteroides, E. faecium
Faak kargyong Pork Eastern Himalayas L. brevis, L. plantarum, L. carnis, Leu. mesenteroides Rai et al. (2010)
Kheuri Yak/beef meat Sikkim Not reported Rai et al. (2009)
Lang satchu Beef Sikkim L. casei, L. carnis, P. pentosaceous Rai et al. (2010)
Yak satchu Red meat of yak Sikkim E. faecium, P. pentosaceous Rai et al. (2010)
Suka Ko Masu Red meat of buffalo or goat Darjeeling hills and Sikkim L. plantarum, L. carnis, E. faecium Rai et al. (2010)
Chilu Yak/beef/lamb meat Sikkim Not reported Rai et al. (2009)
Chartayshya Red meat of goat Western Himalayas Enterococcus hirae, P. pentosaceous, Weissella cibaria Rai et al. (2009), Oki et al.
(2011)
Geema Red meat of goat Western Himalayas E. durans, E. hirae, L. mesenteroides, L. citreum, P. pentosaceous Oki et al. (2011)
Arjia Red meat of goat Western Himalayas E. hirae, E. faecalis, P. pentosaceous Oki et al. (2011)
Traditional Indian fermented foods
9
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For personal use only.

10

Table VII. Pulse-based fermented foods.

Fermented food Usual composition/ingredients Place of origin/usage LAB isolated Refs

Kinema Soybeans Darjeeling, Sikkim E. faecium Kiers et al. (2000), Sarkar et al. (2002), Tamang
(2003), Singh et al. (2007b)
Tungrymbai Soybeans Meghalaya E. faecium Dike and Odunfa (2003), Murughar and
Subblakshmi (2006), Tamang et al. (2009),
R. Satish kumar et al.

Sohliya et al. (2009)


Axone Soybeans North-eastern India Not reported Singh et al. (2007b), Mao and Odyuo (2007),
Tamang et al. (2009)
Bekang Soybeans Mizoram Not reported Singh et al. (2007b), Tamang et al. (2009)
Aagya, peron namsing, Yanni Soybeans Arunachal Pradesh Not reported Singh et al. (2007b)
perung, chukchoro, soybean
(libi) chhurpi
Bari Soybeans Sikkim Not reported Singh et al. (2007b)
Hawaizaar, hakhu mata/akhuni Soybeans Manipur Not reported Singh et al. (2007b)
Peruyyan Soybeans Arunachal Pradesh Not reported Tamang et al. (2009)
Wadi Black gram and oil Punjab, West Bengal L. mesenteroides, L. fermentum Batra and Millner (1974), Sandhu et al. (1986),
Sandhu and Soni (1989), Aidoo et al. (2006)
Papad Black gram, Bengal gram, lentil India Not reported Shurpalekar (1986), Aidoo et al. (2006),
(Lens culinaris) and red gram Roy et al. (2007)
or green gram
Wari Black bean and soybean Uttar Pradesh L. bulgaricus S. thermophilus Tewary and Muller (1989), Tewary and Muller
(1992), Kulkarni et al. (1997)
Masyaura Black gram or green gram, Darjeeling hills and Sikkim P. pentosaceous, P. acidilactici, Dahal et al. (2005), Dahal et al. (2003)
Colocosia tuber, ashgourd and Lactobacillus sp.
or radish
Bedvin roti Black gram, opium seeds Himachal Pradesh Not reported Thakur et al. (2004)
or walnut
Amriti Black gram West Bengal Not reported Steinkraus (1996)
Channa dal dhokla Channa dal, yoghurt, sugar South India Not reported
Khaman Bengal gram dhal South India Not reported Tamang (1998)
Ballae Black gram North India Not reported Roy et al. (2007)
Borhe Black gram Himachal Pradesh Not reported Thakur et al. (2004)
Sepubari Black gram Himachal Pradesh Not reported Thakur et al. (2004)
Teliye mah Black gram Himachal pradesh Not reported Thakur et al. (2004)
Aakhuni Soybean Manipur Not reported Tamang (1998)
Bekanthu Soybean Nagaland Not reported Tamang (1998)
Madrah Kidney beans Himachal Pradesh Not reported Thakur et al. (2004)
Traditional Indian fermented foods 11

(Singh et al. 2007b). During Kinema fermentation, gas trouble, and significantly improves digestion
S. aureus level was decreased as LAB count increased (Singh et al. 2007b).
(Nout et al. 1998). A remarkable increase in free Kanjika or kanji is a lactic fermented rice product. It
amino acids, mineral contents, vitamin-B complex and has been prescribed for a number of chronic diseases
antioxidant activity was reported during kinema by Indian ayurvedic practitioners (Reddy et al. 2007).
fermentation (Sarkar et al. 1997; Tamang and Nikkuni Carrot Kanji is considered to have high nutritional
1998; Tamang et al. 2009). Increase in carotene value and cooling and soothing properties (Sura et al.
and folic acid has been reported in tungrymbai 2001). Beetroot kanji is considered to have potential to
(Murungkar and Subbulakshmi 2006). The LAB prevent infection and malignant disease (Kingston
present in wadis are mainly responsible for acidifica- et al. 2010). Fermented BS juice has preservation
tion. The LAB bring about a significant increase in property similar to vinegar. Meat, fish or vegetables
soluble nitrogen, free amino acids, proteolytic activity are cooked with it to have longer shelf-life (Mao and
and B-vitamins including thiamine, riboflavin and Odyuo 2007). Handua or Kardi (Table V) is used as
cyanocobalamine (Sandhu and Soni 1989). The medicine against any digestive problems, particularly
reported LAB from pulse-based fermented foods against constipation. The Meitei community in North-
were E. faecium, L. mesenteroides, L. fermentum, eastern India use fermented BSs (Soibum) along with
L. bulgaricus, Streptococcus thermophilus, P. pentosaceous fermented fish against the plague disease (Singh et al.
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and P. acidilactici (Table VII). 2007b).


Ngari-dry fish of Puntus breed Phutunis or Eromus
dandricus is mixed with Iromba (fermented BSs) and
Traditional health benefits of fermented foods on
this dish called Yongchak Iromba is considered as an
the Indian population
appetizer and is well known to the old age women of
Indian fermented foods are consumed by the local the Meitei community (Singh et al. 2007b). Hentak
population not just as a diet but as traditional medicine (Table VI) is consumed as curry as well as condiment
too. Many of the foods were observed to have with boiled rice. Sometimes, it is given to the mothers
beneficial effect during ailment by the local people during confinement and patients during convalescence
For personal use only.

and they are used as a special diet or medicine for ages. (Sarojnalini and Singh 1988). Most of the claims are
Fermented food idli is easily digested and often used as based on traditional belief, hence there is a scope to
food for infant and invalids. It is a prescribed diet in conduct experiment-based research to prove these
the hospitals for patients undergoing treatment claims.
(Steinkraus 1996). Koozhu is included in the daily
diet of rural and agricultural workers and is claimed to
Proportion of fermented foods unexplored for LAB
be a nourishing health food (Antony and Chandra
1997). There is an increase in thiamine, riboflavin and Cereal-based (with/without pulses), cereal-based
niacin contents during its fermentation (Aliya and sweets and snacks, and pulse-based fermented foods
Geervani 1981; Rajyalakshmi and Geervani 1990). are largely unexplored with 62%, 95% and 83%,
Koozhu is given to children at weaning age respectively, out of the total fermented foods reported
(Mbithi-Munikya et al. 2002). Fermented milk dahi in each category. Almost 50% of the reported
can be used to cure intestinal disease such as diarrhea fermented foods in cereal/pulse and buttermilk-
(Agarwal and Bhasin 2002); intake of dahi has based, and vegetable, BSs and unripe fruit-based
anti-cholesteremic (Sinha and Sinha 2000), anti- fermented foods categories are explored. Most of
carcinogenic (Arvind et al. 2010), anti-diabetic (Yadav the fermented foods in milk-based and meat-based
et al. 2007a), angiotensin-converting enzyme inhibition fermented food categories have been explored, but
effect (Harun-ur-Rashid et al. 2007) and anti-atopic opportunities are available to explore rest of the
dermatitis effect (Watanabe et al. 2009). The above fermented foods and already isolated LAB strains for
properties are validated by in vivo experiments. various probiotic applications. Hence, there is abun-
Certain fermented vegetable products (gundruk, dant prospects for food-based researchers to explore
sinki and iniziangsang) are said to be good appetizers, and employ Indian fermented foods for probiotic
and the ethnic people use these foods for remedies applications.
from indigestion (Tamang and Tamang 2009). Bhutia
women use gundruk soup and give it to breast-feeding
Conclusion
mothers to improve milk efficiency. It is considered as
a tonic for old age people (Singh et al. 2007b). Indian fermented foods are diverse due to diversity in
Fermented radish root pieces are called sinki. It is India’s culture and food habit. These foods are very
very effective in curing diarrhea and stomach pain, rich in LAB. Some of the LAB reported in these
and is consumed mostly during lean period. Iromba fermented foods are demonstrated to confer a
is prepared from tree bean (Perkia roxburgii) and beneficial effect to the host, in another sense they
is considered an appetizer (Singh et al. 2007b). possess probiotic properties. Consumption of some of
Fermented rai helps in curing stomach pain and the fermented foods has medicinal properties such as
12 R. Satish kumar et al.

appetizing, relief from diarrhoea, constipation, Dewan S, Tamang JP. 2007b. Microbial and analytical character-
stomach pain and gas trouble; it also prevents plaque, ization of Chhu-A traditional fermented milk product of the
Sikkim Himalayas. J Sci Ind Res 65:747– 752.
infection and malignant diseases. Besides, they have
Dike EN, Odunfa SA. 2003. Microbiological and biochemical
cooling and soothing effect when consumed during evaluation of a fermented soybean product soyadawadawa. J
summer. There is a possibility that these beneficial Food Sci Technol 40:606–610.
effects could be contributed by LAB present in these Harun-ur-Rashid M, Togo K, Useda M, Miyamoto T. 2007.
fermented foods. Hence, there is a need to isolate more Probiotic characteristics of lactic acid bacteria isolated from
LAB and to perform extensive studies on their traditional fermented milk ‘Dahi’ in Bangladesh. Pakistan J Nutr
6:647–652.
probiotic properties.
Indrani D, Rao GV. 2003. Influence of surfactants on rheological
characteristics of dough and quality of parotta. Int J Food Sci
Technol 38:47–54.
Acknowledgements Jeyaram K, Romi W, Anand ST, Ranjita DA, Soni DS. 2010.
Bacterial species associated with traditional starter cultures used
Financial support from the Department of Biotech- for fermented bamboo shoot production in Manipur state of
nology (DBT), India, is gratefully acknowledged. India. Int J Food Microbiol 143:1–8.
R. Satish Kumar was supported by an Indian Council Jeyaram K, Singh A, Romi W, Devi AR, Singh WM, Dayanithi H,
et al. 2009. Traditional fermented foods of Manipur. Indian J
of Medical Research (ICMR) fellowship.
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Tradit Knowl 8(1):115–121.


Declaration of interest: The authors report no Kanwar SS, Gupta MK, Katoch C, Kumar R, Kanwar P. 2007.
Traditional fermented foods of Lahaul and Spiti area of
conflicts of interest. The authors alone are responsible
Himachal Pradesh. Indian J Tradit Knowl 6(1):42–45.
for the content and writing of the paper. Kiers JL, Van Lacken AEA, Rombouts FM, Nout MJR. 2000.
In vitro digestability of bacillus fermented soybean. Int J Food
Microbiol 60(2– 3):163–169.
Kingston JJ, Radhika M, Roshini PT, Raksha MA, Murali HS,
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