Das et al.

BMC Public Health (2024) 24:3258 BMC Public Health

https://doi.org/10.1186/s12889-024-20672-w

RESEARCH Open Access

Ethnic foods of Northeast India: insight

into the light of food safety
Madhuchhanda Das1*, Anup Kumar Ojha1, Pallab Sarmah2, Dimpu Gogoi2, Karma G. Dolma3, Tapan Majumdar4,
Suranjana Chaliha Hazarika5, Dilem Modi6, Goutam Chowdhury7, Chaitali Konwar8, Reema Nath8,
Samaresh Das9 and Thandavarayan Ramamurthy7

Abstract
Background Traditional and fermented foods are widely consumed by the ethnic population of Northeast India.
These foods are not only very nutritious, easily available, and reasonably priced, but also boost immunity and pro-
tect from various seasonal infections and have been reported through several investigations. However, pathogens
transmitted by these foods have never been reported. The process of preparation and preservation of fermented
traditional foods involves various steps that can prompt contamination risks. Using the Indian Council of Medical
Research (ICMR)-FoodNet surveillance data, we report the profile of enteric bacteria and mycotoxin-producing fungal
pathogens identified in traditional and fermented food items and their importance in public health.
Methods Food samples were collected from rural areas of Assam, Arunachal Pradesh, Tripura, and Sikkim. Bacterial
and fungal pathogens were tested as per the standard operating procedure at respective ICMR-FoodNet labora-
tories and MycoNet laboratory at Assam. Samples were collected under six broad categories: milk products, edible
insects, non-vegetarian, legumes/cereals, veggies, and alcoholic beverages. Data compilation was done centrally
through a digital data portal. Quality assurance was done by the ICMR-National Institute for Research in Bacterial
Infections (NIRBI), Kolkata.
Result A total of 1227 samples were collected, among which 78 samples (6.8%) were positive for enteric pathogens,
with Bacillus cereus being the most prevalent one (n = 59). Furthermore, 71 fungal isolates were detected from differ-
ent food categories. The most common mycotoxin-producing fungal genera include Aspergillus [A. fumigatus (n = 7)],
Rhizopus [R. arrhizus (n = 13)], and Penicillium (n = 2).
Conclusion Traditional foods have immense social, and cultural value and popularity among locals. However,
processing, fermentation, and preservation of these foods without any preservatives and refrigerators, increases
the possibility of contamination and growth by pathogenic organisms. It is crucial to understand the contamina-
tion risk involved during preparation so that the safety of these traditional foods can be ensured and local delicacies
can be relished without any fear of foodborne infections and outbreaks, particularly when consumed by masses
during festivals.
Keywords Ethnic foods, Enteric pathogens, Mycotoxin, Foodborne infections, Food safety

*Correspondence:
Madhuchhanda Das
[email protected]; [email protected]
Full list of author information is available at the end of the article

© The Author(s) 2024. Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0
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Das et al. BMC Public Health (2024) 24:3258 Page 2 of 14

Introduction regions. In this work, we are reporting surveillance data

The Northeast region of India is very unique, considering of foodborne bacterial and mycotoxin-producing fungal
its geographical location and bio diversity, rich natural pathogens in different edible investigated ethnic and fer-
resources, multi-cultural tribal and non-tribal commu- mented food items of Northeast India, which have the
nities, and their traditional food habits and practices. potential to cause foodborne outbreaks and several direct
Most of these Indian states have their boundaries with impacts on public health. To the best of our knowledge,
five other countries (Bangladesh, Bhutan, China, Myan- this is the first report on foodborne bacterial and fungal
mar, and Nepal). Hence, culture of people and their food pathogens in traditional foods of Northeast India.
habits are influenced by their neighboring countries [1–
3]. Many ethnic communities still use their traditional
knowledge from their ancestors to prepare fermented Methods
and processed food from natural ingredients or consume The ICMR Task Force project has been conducting a
seasonal invertebrates. Fermented foods are the typical foodborne pathogen surveillance study since 2020 in
characteristic of Northeastern states. Soybeans, bam- Northeast India (Fig. 1). The present study was con-
boo shoots, local vegetables, meat, fish, and alcoholic ducted from October 2023 to March 2024 with state-
beverages are fermented traditionally to prepare more specific food items from different categories including
palatable and tangy food at home. Rice is fermented to alcoholic beverages, edible insects/small animals, non-
prepare beer which is very popular among tribal popula- veg, soybean/legumes/cereals, vegetables, and milk prod-
tion. Silkworm, snails and edible insects are also a local ucts (Table 1). Each food items were tested for enteric
delicacy, which not only provides protein and miner- pathogens (Table 2) and mycotoxin-producing fungi.
als but also provides food source for local tribes [4–8]. These specific food items were collected from Assam
Some insects are also used as a traditional oral medicine (Dibrugarh and Guwahati), Tripura, Arunachal Pradesh,
to cure gastritis, fever, cough, asthma, arthritis, rheuma- and Sikkim (Fig. 1). Data was collected in a centralized
tism, and diabetes [9, 10]. The cost of traditional foods is digital data platform and maintained by the Centre for
low and some of it may contain natural preservatives that Development of Advanced Computing (C-DAC), Kol-
can be active for a few days to months. Some of such per- kata, the data management partner of this study. Data
ishable foods are perineal, and some are prepared dur- validation was done by site Project Investigators (PIs)
ing festivals/seasons. Most of the fermented foods and and external quality assurance was made by the ICMR-
alcoholic beverages is made at the household level. Gen- National Institute for Research in Bacterial Infections
erally, these foods are not cooked well, consumed fresh (NIRBI) Kolkata, and Internal Quality assurance was
right after the preparation, and also stored for a long time done by ICMR-Regional Medical Research Centre
without refrigeration. Most of these foods could be con- (RMRC), Dibrugarh, site coordinator of the project.
taminated during preparation due to the lack of hygiene
practices and food safety awareness among the commu- Sample collection
nities. Consumption of uncleaned insects, like scarab Initially, a field survey was conducted to prepare a list of
beetle may cause cardiac malfunction, kidney diseases, locally available traditional foods. Based on one month
and gut inflammation as they produce different allergens of field survey data, a final list of common and state-spe-
like phytate, oxalate, saponins, and alkaloids [10]. These cific traditional food items was finalized (Table 1; Fig. 2),
foods have not been investigated from a food safety point which was approved by the Technical Review Committee
of view. Although a plethora of nonpathogenic microor- (TRC). Samples were collected from tribal household and
ganisms are reported from these traditional fermented local vendors. In the field, each investigating team was
food items, the pathogenicity of these microbes in the assisted by an epidemiologist, a social worker, and a local
human gut has not been studied well [11]. These unap- guide. Verbal consent was taken from the Gram Prad-
proved insect-based foods are not commercially available han (village head), before interacting with villagers/local
and are prepared at the household level. They are sold in communities. The entire process of food preparation was
local shops, food stalls, and small markets, which are out observed by the investigating team. Careful inspection of
of reach to food safety officials. food hygiene was also observed and documented using a
Most of these foods contain a lot of unknown/unre- standardized Case Report Form (CRF) (Fig S1). The sam-
ported microbes, and have the potential to cause food- ples collected in the study were divided into six broad
borne diseases and outbreaks [12, 13]. Hence, it is categories namely- alcoholic beverages, edible insects/
important to establish the safety of traditional foods, small animals, non-veg, soybean/legumes/cereals, veg-
which are the local delicacies, used frequently and thus etables, and milk products. Each of these categories was
have constant demand in different Northeast Indian further subcategorized into different groups.
Das et al. BMC Public Health (2024) 24:3258 Page 3 of 14

Fig. 1 Geographical map showing the regions selected for the collection of ethnic food samples. Each state (Sikkim, Assam, Tripura & Arunachal
Pradesh) consists of 4 districts for collecting the samples. Sikkim-Gangtok, Mangan, Soreng, and Namchi; Assam-Kamrup Rural, Kamrup Metro,
Dhemaji, & Dibrugarh; Tripura- North Tripura, South Tripura, West Tripura, & Dhalai; Arunachal Pradesh- Namsai, Lower Dibang Valley, East Siang, &
Papum Pare

The alcoholic beverages were mainly based on rice and products like cheese and buttermilk were included in the
millet. A locally made wine called ‘Guras ko rakshi’ is pre- study (Table 1). Images of some of the collected samples
pared from the Rhododendron plant was also collected. are shown in Fig. 2. A range of ethnic food samples were
Edible insects comprised of silkworm, cricket, locust, tested to identify fungal pathogens, including Xajor pitha,
snail, grasshopper, and stink bug (Tari) were collected. Til pitha, Tel pitha, Mua dry fish, Sela dry fish, Dorikona
Samples from the non-veg categories were fish and meat- dry fish, Shingara dry fish, Goroi dry fish, Puthi dry fish,
based. The meat-based items were the meat from beef, Panitenga, Xukotimas, Pitha guri, Rice wine, Bamboo
pork, hen, chicken, and squirrels. Samples collected from shoot, Khar, Kesa pitha, Bet gaj, and Sunga mas (Table 1).
cereals/seed-based food include soybean, rice, and millet.
A variety of fermented vegetables or herbs-based foods Sample transport & processing
such as bamboo shoots, local vegetables (like banana Collected samples were, transported to the laboratories,
flowers, chilies, nettle leaves, betel nut, cane culms, red and processed as per the Standard Operating proce-
cherry, mustered leaves/shoots, etc.), cotton flower, wood dure (SOP) [14]. All the centers used the listed standard
potato stem, elephant foot yam, and mushroom were col- strains in this SOP as reference bacteria. Briefly, the sam-
lected from vegetable samples. Milk-based fermented ples were homogenized and incubated in enrichment
Das et al. BMC Public Health (2024) 24:3258 Page 4 of 14

Table 1 Different state-specific food items collected from 4 northeastern states in India. ND, not determined
S.No Sample Category Food Item (Local name) State Item Content Sample form

1 Alcoholic Beverages Xaj/xai mod Assam Rice wine ND

Xajor pitha Assam Rice wine starter ND
Mirung Apong Arunachal Pradesh Millet and Yeast Distilled
Nogin Apong Arunachal Pradesh Cooked rice and Yeast Distilled
Guras ko rakshi Sikkim Rhododendron wine Fermented
Gowra Tripura Rice water Fermented
Chuwak Tripura Rice wine Fermented
Chuwan/Muli Tripura Rice Ball and herbs Dried
Ghad Tripura Cooked rice and Rice ball Cooked
with herbs
Chaang Sikkim Millet alcoholic brew Fermented
Tongba Sikkim Rice and millet alcoholic brew Fermented
Apong Assam Rice Beer Fermented
2 Edible Insect/small animals Polu Assam Silkworm Raw / Cooked
Uisiringa Assam Cricket insect Raw / Cooked
Foring Assam Locust insect Raw / Cooked
Takom Arunachal Pradesh Grasshopper is either boiled Cooked
or fried
Eri Tapum Arunachal Pradesh Silkworm is boiled Cooked
Tari Arunachal Pradesh Tari is boiled. Cooked
Kakambuk Tripura Snail with Vegetable Cooked
Panihamuk Assam Freshwater snail Raw / Cooked
3 Non-Veg Xukan Mas Assam Sun dried fish / dried fish Dried
above fireplace
Xukan Mas Assam Fish marinated with herbs Fermented
and kept in bamboo hollows.
Xukoti Assam Hukoti is a special fish dish Dried
prepared from dried small fish
like (puthi maas) pounded
with arum stem and dried
and stored in bamboo tubes
Shidol Arunachal Pradesh Fish is dried and fermented Dried / Fermented
Ngosan Arunachal Pradesh Fish is sundried or dried Dried
over fireplace
Sukakomaccha Sikkim Sun dried local fish Dried / Fermented
Sidra Sikkim Sun dried local fish Dried / Fermented
Sukuti Sikkim Sun dried local fish Dried / Fermented
Nappi Tripura Dry Fish Fermented
Mosdeng (Bharta) Tripura Smoked Dry fish with vegetable Smoked
Bermabutui Tripura Cooked Vegetable with dry fish Cooked
Gudok Tripura Cooked Vegetable with dry fish Cooked
Awandru Tripura Cooked Vegetable with rice flour Cooked
Chakhwi Tripura Cooked Vegetable with baking Cooked
soda
Aasannam Tasum Arunachal Pradesh Shrimp is sundried Dried
Dinsan Arunachal Pradesh Meat of beef/pork/mithun Smoked
is smoked.
Aasannam Aaki Arunachal Pradesh Intestine of beef/pork/mithun Dried
is dried over fireplace.
Das et al. BMC Public Health (2024) 24:3258 Page 5 of 14

Table 1 (continued)
S.No Sample Category Food Item (Local name) State Item Content Sample form

Aaki Arunachal Pradesh Intestine of beef/pork/mithun Cooked

is boiled.
Aadin Arunachal Pradesh Meat of beef/pork/mithun. Cooked
Lipo Arunachal Pradesh Wild squirrel meat is smoked Smoked
over a fireplace.
Kebung akki Arunachal Pradesh Rat intestine is either boiled Cooked
or fried.
Pasing Arunachal Pradesh Wild pheasant meat is boiled. Cooked
Luktir Arunachal Pradesh Meat of chicken/pork/beef Pickled
is dried and made into pickle.
Yekki Arunachal Pradesh Minced meat is stuffed Cooked
inside the intestine and boiled.
Lang satchu Sikkim Smoked beef meat Smoked
Chempo Sikkim Beef liver with sauce Cooked and Fermented
Gyuma Sikkim Beef meat chunks prepared Cooked
in fresh beef blood, semolina
flour with spice stuffed in a beef
intestine
Wachipa Sikkim Burnt feather of hen cooked Cooked
with rice, chicken meat and veg-
etable
Soyabeans / Legumes / Cereals Ronyang Arunachal Pradesh Soybean is fermented Fermented
Kinema Sikkim Fermented soybean Fermented
Joha chiwda Assam Pressed or flattened rice Raw
Kola saul Assam Black rice Raw / Cooked
Bora saul Assam Sticky Rice Raw / Cooked
Rajmah Assam Redbean seed Raw / Cooked
Kesa mithoi Assam Rice soaked in water and pow- ND
dered and balls are made
with milk, sugar etc.
Pithaguri Assam Powdered rice grains ND
Bora Chaul Assam Sticky Rice ND
Ghila pitha Assam Rice flour, jaggery, semolina, Cooked
salt, oil.
Til pitha Assam Rice powder, jaggery, black Cooked
sesame seeds
Mirik Arunachal Pradesh Millet grain is grinded Powdered
into a powdered form.
Ammin Arunachal Pradesh Rice grain is grinded into a pow- Powdered
dered form.
Aapin Arunachal Pradesh Rice is boiled or steamed Cooked
Dheroh Sikkim Millet rice and porridge Cooked
Khuri Sikkim Buckwheat rolls Cooked
Kentsong Sikkim Roasted maize Roasted
Kodo ko roti Sikkim Millet chapati Cooked
Zhero Sikkim Deep fried rice flour Cooked
Selroti Sikkim Rice flour bread with spices Cooked
Khabjay Sikkim Deep fried rice flour cookies Cooked
Laphing Sikkim Steamed rice /pulses flour Cooked
gluten
5 Vegetables Khorisa Assam Assam Khorisa/Bamboo Shoots/ Fermented
Khorisa
Eyup Arunachal Pradesh Bamboo shoot is sundried. Dried
Eting Arunachal Pradesh Raw bamboo shoot. Raw
Das et al. BMC Public Health (2024) 24:3258 Page 6 of 14

Table 1 (continued)
S.No Sample Category Food Item (Local name) State Item Content Sample form

Ekung Arunachal Pradesh Bamboo shoot is fermented. Fermented

Tassey Arunachal Pradesh Stem extract. Cooked
Pila Arunachal Pradesh Pila is fermented Fermented
Tama Sikkim Bamboo shoots Fermented
Muya Kwran Tripura Sun Dried bamboo shoot Dried
for long storage
Kolakhar Assam Burnt ash of banana plant/peel Fermented
Panitenga/Kahudi(Tangy fer- Assam Chinese mustard seeds with khar Fermented
mented mustard chutney) and fermented
Betelnut Assam Betelnut Fermented
Kharoli/Behua Assam Fermented mustard seeds Fermented
chutney
Betgaj Assam Cane culms ND
Dhekia (Fern) Assam Fern ND
Khar Assam Burnt ash of banana plant/peel ND
Kolmou Assam Leafy veg Raw
Singhara Assam Fruit Raw
Ditey Arunachal Pradesh Spices are sundried. Dried
Marsang Arunachal Pradesh Vegetable is boiled. Cooked
Gudruk Arunachal Pradesh Mustard leaves/shoots and rad- Cooked
ish is cooked together.
Tenga Pat Arunachal Pradesh Green leafy vegetable is fer- Fermented
mented
Engye Arunachal Pradesh The leaves are boiled. Cooked
Sitir Arunachal Pradesh Chillies are sundried and grinded Dried
into powdered form.
Paksum Arunachal Pradesh Banana flower can be Cooked
either boiled or fried.
Tapar Arunachal Pradesh Mushroom is either boiled Cooked
or fried.
Namsung Tong Arunachal Pradesh Algae is fermented. Fermented
Tagyok Arunachal Pradesh Algae is boiled. Cooked
Sisnu Sikkim Nettles leaves curry Cooked
Ningro Sikkim Wild fern vegetable curry Cooked
Lapsi Sikkim Hog plum pickle Pickled
Nakima Sikkim Tupistra nutans vegetable/pickle Pickled / Cooked
Thotne Sikkim Polygonum molle vegetable Pickled
curry/pickle
Philingo Sikkim Niger seed pickle Pickled / Powdered
Gundruk Sikkim Dried mustard leaves Fermented/Cooked
Sinki Sikkim Dried mustard shoots and radish Fermented/Cooked
Dalle Khursani Sikkim Red cherry pepper pickle Fermented / Pickled
Cotton Flower/ Borchuk Bubar Tripura Sun Dried Dried
Tha Bosok Tripura Sun Dried (wood potato stem) Dried
Batima/Elephant foot yam Tripura Smashed and boiled with bak- Boiled
ing soda
6 Milk Products Churpi Arunachal Pradesh Buttermilk is boiled and the solid Cooked
mass is obtained.
Churpi Sikkim Cottage cheese Uncooked/Cooked
Philu Sikkim Cheese with butter curry Cooked
Suja/Pheuja Sikkim Butter tea Cooked and Fermented
Das et al. BMC Public Health (2024) 24:3258 Page 7 of 14

Table 2 List of enteric pathogens screened from ethnic food samples

S. No Food items Pathogens screened

1 Milk based food products Listeria monocytogenes

Bacillus cereus
Yersinia enterocolitica
Campylobacter jejuni
Diarrhoeagenic Escherichia coli (DEC) [ETEC, EPEC, EAEC, EIEC, STEC and DAEC]
Staphylococcus aureus
Salmonella spp.
Shigella spp.
2 Raw pork, beef, mutton, poultry meat, bush Diarrhoeagenic Escherichia coli (DEC) [ETEC, EPEC, EAEC, EIEC, STEC and DAEC]
meat/Edible insects Bacillus cereus
Staphylococcus aureus
Salmonella spp.
Shigella spp.
Yersinia enterocolitica,
Clostridium perfringens
Listeria monocytogenes
Campylobacter spp.
3 Fish Pathogenic Vibrio parahaemolyticus
Vibrio cholerae serogroups O1 and O139
Diarrhoeagenic Escherichia coli (DEC) [ETEC, EPEC, EAEC, EIEC, STEC and DAEC]
Salmonella spp.
Bacillus cereus
Staphylococcus aureus
Listeria monocytogenes
Clostridium botulinum
Clostridium perfringens
Campylobacter jejuni
4 Vegetables based foods (cereals/pulses/ Salmonella spp.
regional herbs/bamboo shoots, etc. Shigella spp.
Bacillus cereus
Diarrhoeagenic Escherichia coli (DEC) [ETEC, EPEC, EAEC, EIEC, STEC and DAEC]
Vibrio cholerae serogroups O1 and O139
Salmonella spp.
Listeria monocytogenes
5 Alcoholic beverages Listeria monocytogenes
Yersinia enterocolitica
Bacillus cereus
Campylobacter jejuni
Diarrhoeagenic Escherichia coli (DEC) [ETEC, EPEC, EAEC, EIEC, STEC and DAEC]
Staphylococcus aureus
Salmonella spp.
Shigella spp.

broth before putting it into the specific agar medium for samples were also tested for the presence of mycotoxin-
isolation of the bacterial pathogens i.e. DEC, Salmonella, producing fungi, at Assam Medical College, which is
Shigella-MAC agar, SMAC agar; Staphylococcus-Baired the advanced mycology diagnostic and research center
Parker agar; Salmonella and Shigella spp -XLD agar, HE (AMDRC) of ICMR (MycoNet center). The fungal iso-
agar; Vibrio- TCBS agar; Listeria monocytogenes-PAL- lates were detected using both conventional (Micro-
CAM agar; B cereus-MYP. Food samples were tested for scopic culture identification) and molecular approaches
enteric bacteria in ICMR-FoodNet centers at ICMR- (MALDI-TOF/PCR) [15–19]. Isolated bacterial and fun-
RMRC, Dibrugarh, Gauhati Medical College and Hos- gal isolates were tested for their antimicrobial resistance
pital (GMCH), Guwahati, Agartala Medical College, (AMR) following the standard guidelines [20, 21]. For the
Tripura, Sikkim Manipal Institute of Medical Sciences, determination AMR, disc diffusion method was used to
Sikkim, Bakin Pertin General Hospital (BPGH), Pasighat, test bacterial isolates whereas, for fungal isolates, micro
Arunachal Pradesh. For the identification, biochemi- broth dilution method was employed for the evaluation
cal and molecular (PCR) approaches were used to con- of minimum inhibitory concentration (MIC). The antimi-
firm the enteric pathogenic species using the SOP made crobials tested both for bacterial and fungal isolates are
for this study [14] (Table S1 & Fig S2). In addition, food given in Table S2.
Das et al. BMC Public Health (2024) 24:3258 Page 8 of 14

Fig. 2 Ethnic Indian foods from Northeast region: a Kesa mithoi- soaked and powdered rice ball in milk and sugar b Pila- fermented bamboo
shoots, c Tangpok – dried fermented leaves, d Okonglok – river stone algae, e Khar – raw papaya mixed with filtered water created from sun-dried
banana peels, f Tashi – palm tree extract based food, g Eyup – sundried bamboo shoots, h Perin – raw soybean-based food, i Bamboo shoot achar
– fermented bamboo shoots pickle, j Khorisa – fermented bamboo shoots, k Ekung – fermented bamboo shoots, l Panitenga - fermented mustard
seeds chutney, m Xukoti - dried small fish pounded with arum stem stored in bamboo tubes, n Sunga mas – pork meat based food popular
in Assam, o Dried prawns, p Xukan mas - fish marinated with herbs and kept in bamboo hollows for fermentation, q Silk worm, r Tari – belong
to genus Coridius (Hemiptera: Dinidoridae) and consumed in boiled form in Arunachal Pradesh, s Pani xamuk – freshwater edible snail consumed
raw/cooked, t Amruli poruwar tup - red ant eggs consumed as a traditional cuisine by people of Assam

Data management and analysis maximum positivity rate (4.8%) was recorded for B.
A secured web platform (https://​w ww.​icmrf​oodnet.​in/) cereus. This suggests that, out of all the collected sam-
was designed to collate data centrally from all the cent- ples, B. cereus was the most common enteric pathogen.
ers. A digital Case Report Form (eCRF) was designed The efficacy of several antimicrobials against the iso-
with a drop-down menu to minimize data entry errors. lated enteric pathogens was assessed by antimicrobial
For confirmation, a double data entry method was susceptibility testing (AST). The AST’s results are dis-
followed. Data validation was done by the principal played in Table S3. Nearly 70% of tested isolates of B.
investigators. cereus were resistant to ampicillin and ceftazidime,
while > 90% of the isolates were sensitive to clindamycin,
Ethical approval erythromycin, gentamicin, rifampicin, and vancomycin.
This study was approved by the Institute Ethics Com- S. aureus, showed a high resistance (100%) to ceftriaxone,
mittee of the participating Institutes as well as the imipenem, and nalidixic acid. Salmonella was resistant
ICMR-Central Ethics Committee on Human Research (100%) to azithromycin, cefoxitin, ceftazidime, nalidixic
(ICMR-CECHR) (Reference Number: CECHR acid, and tetracycline. Listeria monocytogenes was resist-
003/2023). ant (100%) to nalidixic acid and rifampicin. Yersinia
showed high resistance (100%) to ampicillin, nalidixic
acid, and tetracycline.
Result A total of six different types of food samples were col-
We have collected a total of 1227 ethnic food items lected, and tested for mycotoxin-producing fungi. As
(Tables 1 and 3) from all four Northeast states. Among shown in Tables 4 and 71 different isolates of fungi were
them, 78 (6.8%) were positive for different enteric identified by microscopy. Confirmation of the indicated
pathogens. The pathogens from enteric bacteria were fungus species was obtained through microscopic exami-
mainly- Bacillus cereus (n = 59), Enteroaggregative nation (Fig. 3).
E. coli (EAEC) (n = 1), Staphylococcus aureus (n = 6), Aspergillus was the leading genus. Aspergillus fumiga-
Listeria monocytogenes (n = 9), Salmonella enterica tus (n = 7) and Rhizopus arrhizus (n = 13) were the most
(n = 1), Yersinia enterocolitica (n = 1), and Vibrio chol- commonly isolated species. Aspergillus niger (n = 2),
era (n = 1). The positivity rate (%) for enteric patho- Aspergillus flavus (n = 1), Mucor racemosus (n = 2), Lich-
gens from ethnic food samples is given in Table 3. A theimia corymbifera (n = 4), Penicillium spp. (n = 2), and
 Das et al. BMC Public Health
(2024) 24:3258

Table 3 Total number of samples tested for enteric pathogens. Positivity rate for each enteric pathogen is given in parenthesis
States Sample Enteric Positivity Bacillus Enteroaggregative Staphylococcus Salmonella (n) Listeria Yersinia Vibrio cholera (n)
Tested Pathogens Rate (%) cereus E. coli aureus (n) monocytogenes enterocolitica
(n) (n) (n) (n)

Arunachal Pradesh 94 2 2.1 0 (0.0%) 1 (1.0%) 0 (0.0%) 0 (0.0%) 0 (0.0%) 0 (0.0%) 1 (1.0%)
Assam 567 9 1.58 7 (1.2%) 0 (0.0%) 2 (0.3%) 0 (0.0%) 0 (0.0%) 0 (0.0%) 0 (0.0%)
Sikkim 283 64 2.22 49 (17.31%) 0 (0.0%) 4 (1.4%) 1 (0.35%) 9 (3.18%) 1 (0.35%) 0 (0.0%)
Tripura 283 3 1.00 3 (1.0%) 0 (0.0%) 0 (0.0%) 0 (0.0%) 0 (0.0%) 0 (0.0%) 0 (0.0%)
Total 1227 78 6.80 59 (4.8%) 1 (0.08%) 6 (0.49%) 1 (0.08%) 9 (0.73%) 1 (0.08%) 1 (0.08%)
n = number of isolates
Page 9 of 14
Das et al. BMC Public Health (2024) 24:3258 Page 10 of 14

Table 4 Various fungal species identified in a variety of ethnic food samples

Fungal species Food samples Total
Bamboo shoots Cereals Fish Insects Small animals Vegetables Wine

Arthrinium phaeospermum 1 1
Aspergillus flavus 1 1
Aspergillus fumigatus 2 3 1 1 7
Aspergillus niger 1 1 2
Aspergillus versicolor 1 1
Lichtheimia corymbifera 2 1 1 4
Mucor circinelloides 1 1
Mucor racemosus 1 1 2
Mucor spp. 1 1 1 3
Penicillium spp. 2 2
Rhizomucor spp. 2 2
Rhizopus arrhizus 3 5 5 13
Rhizopus arrhizus complex 1 1
Rhizopus microsporus 1 2 3
Rhizopus microspores complex 1 1
Rhizopus homothallicus 2 2
Saccharomyces cerevisiae 2 1 8 11
Scopulariopsis brevicaulis 1 1
Syncephalastrum spp. 1 1
Yeast spp. 2 1 1 1 7 12
Total 71

Saccharomyces cerevisiae (n = 11) were the other fungi

that were identified in this study.
Results of antifungal susceptibility testing using MIC
microbroth dilution method are shown in Table S4. The
highest MIC (8 µg/ml) was detected in A. flavus and R.
arrhizus respectively against fluconazole and caspo-
fungin. This suggests that these fungi may be less suscep-
tible to the tested drugs.

Discussion
Most of the published literature revealed the awareness
of preparing traditional foods and their health benefit
as it comprises beneficial bacteria like Lactobacillus. A
review of the literature published by Chandra and Tiwari
(2022), reported the presence of non-pathogenic micro-
organisms like Lactic Acid Bacteria (LAB), Candida sp.,
Bacillus sp., and Saccharomyces cerevisiae in fermented
northeast food products [11]. As these foods are not
Fig. 3 Microscopic images of fungal species isolated from ethnic commercially available in the market, they are prepared
foods. a Aspergillus niger (black, radiate conidial head with septate
and hyaline hyphae); b Aspergillus fumigatus (smooth, light green
at the household level and sometimes sold in the local
conidia with septate and colorless hyphae); c Penicillium spp (septate markets in limited quantities. Hence, the collection and
hyphae bearing flask shaped phialides with single celled spores testing of these food items are challenging. Contamina-
of conidia); d Rhizopus arrhizus (aseptate and coenocytic hyphae tion of traditional foods by pathogens is not uncommon
bearing sporangium with asexual spores) [22–24]. Therefore, consumption of these contaminated
Das et al. BMC Public Health (2024) 24:3258 Page 11 of 14

foods/drinks may be harmful to health, particularly for a presence of enteric bacteria in these items highlights
vulnerable rural population. the possibility of contamination during production,
As population of the Northeastern region is of differ- harvesting, and handling after harvest.
ent tribal communities and their common food practice Identification of enteric pathogens like B. cereus,
involves the fermentation of locally available vegetables, S. aureus, and Vibrio spp. indicates the risk of out-
fish, and other items which are abundantly available in breaks associated with consumption of traditional food
nature (the size of the population consuming these foods preparations. B. cereus is a foodborne pathogen caus-
are given in Table S5). Consumption of edible insects ing serious illness due to the production of emetic and
and other small animals are also being used as traditional diarrheal enterotoxin in the intestinal tract of the host.
remedy to cure gastritis, fever, cough, asthma, arthritis, The findings in this study are consistent with the pre-
rheumatism, and diabetes [9, 10]. Most of these tradi- vious reports from the Northeast region [22, 32–34].
tional food items are reported to have antioxidants, anti- Antimicrobial susceptibility testing indicated the pres-
inflammatory, anticancer, antimicrobial, and antibacterial ence of susceptible pathogens to most of the drugs.
inhibitors of the pancreatic lipase enzyme, insulin regu- These results indicate that illnesses caused by these
lators, and glycemic inhibitors [8, 25]. In addition, these pathogens can still be treated with efficient antimicro-
low-cost foods are very nutritious, can be fermented at bials. However, it is important to note that antimicrobi-
home using traditional methods without any preserva- als such as ampicillin and ceftazidime for B. cereus and
tives and can be stored without refrigeration [2, 3, 26– ceftriaxone, imipenem, and nalidixic acid for S. aureus
28]. However, as these foods contain diverse microbial might not be effective for the infections caused by the
communities, including probiotics as well as potentially respective pathogens. To prevent AMR, it is crucial to
the pathogens that may cause infections. From the food use some of these antimicrobials judiciously [35] Since
safety point of view, it is important to investigate the the number of other pathogens are less in number, it is
safety of these foods. Also, it is important to determine difficult to ascertain their AMR trends.
the contaminating source comprising raw foods and Mycotoxin in foods is due to the presence/growth of
other components, processing methods, etc. It has been different species of toxin-producing fungi. Mycotoxins
recognized that scarab insect consumption can cause gut in humans induce chronic but acute infections [36].
inflammation, neurological disorders, cardiac malfunc- Direct consumption of toxigenic fungi contaminated
tions, kidney stones, and allergies [10]. foods can affect humans and animals. In 2004, 125 peo-
The results of our investigation provide a crucial insight ple died and nearly 200 others required medical treat-
into the safety aspects of traditional foods in North- ment after eating maize contaminated with aflatoxin in
east India. The identification of pathogens in a variety Kenya [37]. Aflatoxin, produced by the molds, Aspergil-
of food items highlights the importance of the constant lus flavus and A. parasiticus, and A. nomius. Aflatoxins
surveillance and comprehensive food safety protocols are mutagenic, teratogenic, carcinogenic, and immuno-
to safeguard public health. The alcoholic drinks were suppressive agents in animals and possibly in humans
also contaminated, which were thought to go through [38–40].
a fermentation process that generally inhibits bacterial Patulin toxin is produced by Penicillium, Aspergillus,
growth. In addition, concerns about food handling pro- and Byssochlamys growing on fruits including apples,
cedures, storage conditions, and hygiene requirements in pears, grapes and other fruits. Ochratoxin A (OTA) toxin
processing facilities are highlighted due to the presence is produced by Penicillium, and Aspergillus ochraceus.
of enteric bacteria, mostly in fish and meat products. A OTA is associated with hepatic and nephrotoxin that
potential risk to consumer health from these products has been linked to tumors in the human urinary tract.
could be due to cross-contamination during processing Citrinin produced by Penicillium and Aspergillus and is
or insufficient cooking/drying temperatures. also a potent nephrotoxin. Ergot produced by Claviceps
Identification of enteric bacteria in soybean products affecting the central nervous system [41, 42]. Fusarium
broadens the scope of the analysis. Soybean is an impor- toxins are produced by over 50 species of Fusarium.
tant component in many traditional meals around the Rhizopus microsporus can produce two types of myco-
world and it is frequently used for its nutritional values toxins; rhizoxins and rhizonins. In this study, we have
and adaptability in ethnic cuisines. Pathogens found in identified mycotoxigenic Aspergillus, and Rhizopus in
soy-based foods emphasize the significance of source different food items and they have the potential to exert
control and the application of good sterilization tech- health hazards. Saccharomyces cerevisiae was also identi-
niques in processing and farming environments [29–31]. fied in various food products, which is known for its anti-
The most common ingredient in different ethnic mycotoxin additives (AMA) to neutralize mycotoxin and
cuisines is vegetables, especially bamboo shoots. The have beneficial effects [43].
Das et al. BMC Public Health (2024) 24:3258 Page 12 of 14

Numerous fungal species linked to ethnic food sam- need for constant surveillance and implementation of
ples were found in the current investigation, which raises food safety protocols in the region. In this regard, we
questions about possible mycotoxin contamination. have already taken the initiative to create a network
Notably, A. niger (n = 2) and A. flavus (n = 1) are identi- with State Health Authorities (STA), and Integrated
fied in ethnic food samples. These species are known to Disease Surveillance Programme (IDSP) in the region
produce aflatoxins, a type of highly carcinogenic toxin and established a chain of regional centers to conduct
[12, 44]. Rhizopus microsporus (n = 3) can produce two surveillance, testing, outbreak investigation, and aware-
types of mycotoxins; rhizoxins and rhizonins has been ness programmes in this area to ensure public health
reported from fermented foods earlier [45]. These results safety. The most common pathogens found in the study
indicate the possibility of mycotoxin contamination in are B. cereus, Listeria monocytogenes, S. aureus, Asper-
ethnic foods. The wide variety of fungus species detected gillus, and Rhizopus arrhizus, which might contrib-
in this study highlights the need for appropriate handling ute to sporadic/outbreak infection in this region and
and storage procedures to prevent the growth of toxi- need to be monitored constantly. As communities are
genic fungi in these food products. unequivocally attached to traditional foods, any public
For sanitary standards in India, the Food Safety and health intervention must be approached with caution
Standards Authority of India (FSSAI) has developed considering the cultural sensitivity, and deeply held
extensive microbiological criteria that apply to a variety beliefs. Adequate sanitary practices can be made such
of food items. These standards are intended to guarantee as using cleaned raw material, proper cooking, avoid
food safety and quality by establishing thresholds for cer- longer storage without preservatives, proper storage
tain pathogens and contaminants. FSSAI sets maximum and processing of the food to avoid contamination. The
permissible limits for the foodborne pathogens in certain risk can be reduced by creating awareness about food
food products (https://​gfrs.​fssai.​gov.​in/​2023/​files/​docs/1-​ safety in the community. Knowledge and health guide-
Micro​biolo​gical%​20cri​teria%​20for%​20foo​dstuf​f s-​2005-​ lines based on scientific evidence would be the game
2073-​08-​03-​2020.​pdf ). These guidelines and standards changers for the country.
are followed strictly for the foods produced commer-
cially. However, for ethnic foods, no such standards are Supplementary Information
reported except that the norms and standards have been The online version contains supplementary material available at https://​doi.​
traditionally developed by the people over the time and org/​10.​1186/​s12889-​024-​20672-w.
applied to the ethnic food in India. Natural methods
Supplementary Material 1.
such as exposure to the sun which removes the mois-
ture thereby reducing water activity can prevent the food
Acknowledgements
from spoilage. The water activity of the food can also be
The authors acknowledge the Indian Council of Medical Research (ICMR),
lowered by using salt, treating food with honey [46]. Delhi, for providing financial assistance for the study.

Clinical trial details

Conclusion Not applicable.
Food safety is a neglected public health issue but is one
Authors’ contributions
of the important components of a disease-free world. MD: Conceptualization, prepared original draft manuscript, review, and edit-
Although it is difficult to ensure contamination-free ing, project administration, investigation, resources., AKO: prepared detailed
foods in the complex food chain, systematic surveil- manuscript, review, and editing., PS, DG, KGD, TM, SCH, and DM: provide
data, review., GC: review and editing., CK: provided fungal data, review., SD:
lance of food and waterborne pathogens and their route provided table and figures and data analysis, review., RN: provided fungal data,
of transmission can help in generating and implement- review., TRM: review and editing.
ing food safety policies and reduce the transmission
Funding
of infection to humans. Recent initiatives of Sustain- This work was supported by the Indian Council of Medical Research, New
able Development Goals (SDG) 2030 and Global 20 Delhi. Grant ID: ER/FBS/PHASE-II/2023/DR/MD.
(G20) ensures global food safety and protection human
Data availability
health. In a country like India where many communi- All data underlying the results are available as part of the article and no addi-
ties have unique food practices, and prepare traditional tional source data are required.
foods during different festivals around the year and
believe that these foods give protection from various Declarations
diseases. Through this surveillance study, we identi-
Ethics approval and consent to participate
fied the presence of bacterial and fungal pathogens Ethical clearance from the ICMR-Central Ethics Committee on Human
in the traditional food items in North-East India that Research (CECHR) was obtained (Reference Number: CECHR 003/2023).
impose a health risk to consumers and highlight the
Das et al. BMC Public Health (2024) 24:3258 Page 13 of 14

Additionally, the informed consent to participate was obtained from all of the 15. Sekse C, Holst-Jensen A, Dobrindt U, Johannessen GS, Li W, Spilsberg B,
participants in the study. et al. High throughput sequencing for detection of foodborne patho-
gens. Front Microbiol. 2017;8:2029.
Consent for publication 16. Bader O. Fungal species identification by MALDI-ToF mass spectrometry.
Not applicable. Methods in Molecular Biology. Humana Press Inc.; 2017. pp. 323–37.
17. Rolland N, Girard V, Monnin V, Arend S, Perrin G, Ballan D, et al. Identifica-
Competing interests tion of Food Spoilage Fungi using MALDI-TOF MS: spectral database
The authors declare no competing interests. development and application to Species Complex. J Fungi. 2024;10:456.
18. Quéro L, Girard V, Pawtowski A, Tréguer S, Weill A, Arend S, et al. Develop-
Author details ment and application of MALDI-TOF MS for identification of food spoilage
1
Division of Development Research, Department of Health Research (Ministry fungi. Food Microbiol. 2019;81:76–88.
of Health & Family Welfare), Indian Council of Medical Research, Ansari Nagar 19. Priyanka SR, Venkataramana M, Balakrishna K, Murali HS, Batra HV.
East, New Delhi 110029, India. 2 ICMR-RMRC, Dibrugarh, Assam, India. 3 Depart- Development and evaluation of a multiplex PCR assay for simultaneous
ment of Microbiology, Sikkim Manipal Institute of Medical Sciences, Sikkim detection of major mycotoxigenic fungi from cereals. J Food Sci Technol.
Manipal University, Gangtok, Sikkim, India. 4 AGMC, Agartala, Tripura, India. 2015;52:486–92.
5
GMCH, Guwahati, Assam, India. 6 BPGH, Pasighat, Arunachal Pradesh, India. 20. Lewis JSII. M100: *Performance standards for antimicrobial susceptibility
7
ICMR-NIRBI, Kolkata, India. 8 AMCH, Dibrugarh, Assam, India. 9 CDAC, Kolkata, testing. USA: Clinical and Laboratory Standards Institute (CLSI); 2023.
India. 21. PROCOP GW. M59 epidemiological cutoff values for antifungal suscepti-
bility testing. USA: CLSI; 2020.
Received: 10 August 2024 Accepted: 8 November 2024 22. Keisam S, Tuikhar N, Ahmed G, Jeyaram K. Toxigenic and pathogenic
potential of enteric bacterial pathogens prevalent in the traditional
fermented foods marketed in the Northeast region of India. Int J Food
Microbiol. 2019;296:21–30.
23. Jeyaram K, Romi W, Singh TA, Devi AR, Devi SS. Bacterial species associ-
References ated with traditional starter cultures used for fermented bamboo shoot
1. Haokip T. Looking East: India’s Northeast. Manorama Year Book; 2024. p. production in Manipur state of India. Int J Food Microbiol. 2010;143:1–8.
96–104. 24. Jeyaram K, Mohendro Singh W, Premarani T, Devi AR, Chanu KS, Talukdar
2. Das G, Patra JK, Singdevsachan SK, Gouda S, Shin HS. Diversity of NC, et al. Molecular identification of dominant microflora associated
traditional and fermented foods of the seven sister states of India and with hawaijar - A traditional fermented soybean (Glycine max (L.)) food of
their nutritional and nutraceutical potential: a review. Front Life Sci. Manipur, India. Int J Food Microbiol. 2008;122:259–68.
2016;9:292–312. 25. Aiello D, Barbera M, Bongiorno D, Cammarata M, Censi V, Indelicato S,
3. Basumatary Z, Saha S, Chaudhuri S, Ray S, Kumar Nayak P, Sen Maiti S, et al. Edible insects an alternative nutritional source of bioactive com-
et al. Ethnic fermented foods and beverages of north-eastern India: a pounds: a review. Molecules. 2023;28(2):699.
comprehensive review section A-Research paper ethnic fermented foods 26. Singh HB, Yaipharembi N, Huidrom E, Devi CA. Traditional knowledge,
and beverages of north-eastern India: a comprehensive review. 2023. beliefs, and practices Associated with ethnic people of Manipur, North
4. Thangjam R, Ningthoujam K, Kadam V, Sorokhaibam M. A review on East India in Conservation of Biodiversity. Traditional ecological knowl-
edible insects and their utilization in Northeastern Himalaya. J Entomol edge of Resource Management in Asia. Springer International Publishing;
Zool Stud. 2020;8. 2023. pp. 61–76.
5. Sharma A, Kumar Gupta RK, Sharma P, Attri K, Sharma Scholar A, 27. Tamang JP. Ethno-microbiology of ethnic Indian fermented foods and
et al. Silkworm as an edible insect: a review. The Pharma Innov J. alcoholic beverages. J Appl Microbiol. 2022;133:145–61.
2022;11(2):1667–74. 28. Tamang JP. Dietary culture and antiquity of the himalayan fermented
6. Srivastava SK, Babu N, Pandey H. Traditional insect bioprospecting-As foods and alcoholic fermented beverages. J Ethnic Foods. 2022;9:30.
human food and medicine. Indian J Tradit Knowl. 2009;8(4):485–94. 29. Bahuguna A, Kumar V, Bodkhe G, Ramalingam S, Lim SM, Joe AR et al.
7. Rumpold BA, Schlüter OK. Nutritional composition and safety aspects of Safety Analysis of Korean Cottage Industries’ Doenjang, a traditional fer-
edible insects. Mol Nutr Food Res. 2013;57:802–23. mented soybean product: a special reference to Biogenic Amines. Foods.
8. Devi WD, Bonysana R, Kapesa K, Mukherjee PK, Rajashekar Y. Edible 2023;12.
insects: as traditional medicine for human wellness. Future Foods. 30. Chin XH, Elhalis H, Chow Y, Liu SQ. Enhancing food safety in soybean fer-
2023;7:100219. mentation through strategic implementation of starter cultures. Heliyon.
9. Mason JB, Black R, Booth SL, Brentano A, Broadbent B, Connolly P, et al. 2024;10.
Fostering strategies to expand the consumption of edible insects: the 31. Kim M, Kim YS. Detection of foodborne pathogens and analysis of
value of a tripartite coalition between academia, industry, and govern- aflatoxin levels in home-made Doenjang samples. Prev Nutr Food Sci.
ment. Curr Dev Nutr. 2018;2(8):nzy056. 2012;17:172–6.
10. Siddiqui SA, Ampofo KA, Dery EK, Eddy-Doh AM, Castro-Muñoz R, Push- 32. Deka P, Mehetre GT, Lalnunmawii E, Upadhyaya K, Singh G, Hashem A,
palatha M, et al. Scarabaeidae as human food – a comprehensive review. et al. Metagenomic analysis of bacterial diversity in traditional fermented
J Insects Food Feed. 2023;2:699–732. foods reveals food-specific dominance of specific bacterial taxa. Fermen-
11. Chandra Nath P, Tiwari A. Comparative studies on the ethnic fermented tation. 2021;7(3):167.
food products and its preservation methods with special focus of North- 33. Dey TK, Lindahl JF, Sanjukta R, Arun Prince Milton A, Das S, Kannan P, et al.
East India. J Ecol Nat Resour. 2022;6(4):16000319. Characterization of lactic acid bacteria and pathogens isolated from
12. Pandey AK, Samota MK, Kumar A, Silva AS, Dubey NK. Fungal mycotoxins traditionally fermented foods, in relation to food safety and antimicrobial
in food commodities: present status and future concerns. Front Sustain- resistance in tribal hill areas of Northeast India. J Food Qual. 2023;2023:12.
able Food Syst. 2023;7:1162595. 34. Patel P, Butani K, Kumar A, Singh S, Prajapati BG. Effects of fermented food
13. Skowron K, Budzyńska A, Grudlewska-Buda K, Wiktorczyk-Kapischke N, consumption on non-communicable diseases. Foods. 2023;12(4):687.
Andrzejewska M, Wałecka-Zacharska E, et al. Two faces of fermented 35. Gemeda BA, Assefa A, Jaleta MB, Amenu K, Wieland B. Antimicrobial
foods—the benefits and threats of its consumption. Front Microbiol. resistance in Ethiopia: a systematic review and meta-analysis of preva-
2022;13:845166. lence in foods, food handlers, animals, and the environment. One Health.
14. Karunasagar I, Ramamurthy T, Das M, Devi U, Baruah P, Panda S, et al. 2021;13:100286.
Standard operating procedures ICMR foodborne pathogen survey and 36. Omotayo OP, Omotayo AO, Mwanza M, Babalola OO. Prevalence of
research network (North-East India). https://​www.​icmrf​oodnet.​in/​static/​ mycotoxins and their consequences on human health. Toxicol Res.
assets/​files/​ICMR_​Stand​ardOp​erati​ngPro​cedur​es.​pdf. Accessed 1 Nov 2019;35:1–7.
2024. 37. Lewis L, Onsongo M, Njapau H, Schurz-Rogers H, Luber G, Kieszak S,
et al. Aflatoxin contamination of commercial maize products during an
Das et al. BMC Public Health (2024) 24:3258 Page 14 of 14

outbreak of acute aflatoxicosis in eastern and central Kenya. Environ

Health Perspect. 2005;113:1763–7.
38. Hussein HS, Brasel JM. Toxicity, metabolism, and impact of mycotoxins on
humans and animals. 2001;167(2):101–34.
39. Sarma UP, Bhetaria PJ, Devi P, Varma A. Aflatoxins: implications on Health.
Indian J Clin Biochem. 2017;32:124–33.
40. Marchese S, Polo A, Ariano A, Velotto S, Costantini S, Severino L. Aflatoxin
B1 and M1: biological properties and their involvement in cancer devel-
opment. Toxins. 2018;10(6):214.
41. Mahato DK, Kamle M, Sharma B, Pandhi S, Devi S, Dhawan K, et al. Patulin
in food: a mycotoxin concern for human health and its management
strategies. Toxicon. 2021;198:12–23.
42. Bacha SAS, Li Y, Nie J, Xu G, Han L, Farooq S. Comprehensive review on
patulin and Alternaria toxins in fruit and derived products. Front Plant Sci.
2023;14:1139757.
43. Moebus VF, Pinto LD, Köptcke FB, Keller KM, Aronovich M, Keller LA.
In vitro mycotoxin decontamination by Saccharomyces cerevisiae strains
isolated from bovine forage. Fermentation. 2023;9(7):585.
44. Tian F, Woo SY, Lee SY, Park SB, Im JH, Chun HS. Mycotoxins in soybean-
based foods fermented with filamentous fungi: occurrence and preven-
tive strategies. Compr Rev Food Sci Food Saf. 2022;21:5131–52.
45. Jennessen J, Nielsen KF, Houbraken J, Lyhne EK, Schnorer J, Frisvad JC,
et al. Secondary metabolite and mycotoxin production by the Rhizopus
microsporus group. J Agric Food Chem. 2005;53:1833–40.
46. Lelieveld H, Keener L, Martín-Belloso O, Braun S, McMahon H, Astley S,
et al. Science-based harmonization of regulations for the safety of tradi-
tional and ethnic foods. Regulating safety of traditional and ethnic foods.
Elsevier Inc.; 2016. p. 481–5.

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