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Review Article | Open Access

Roles of fermented plant-, dairy- and meat-based foods in the modulation of allergic responses

Muhamad Hafiz Abd Rahima(), Nur Hazlin Hazrin-Chongb, Hanis Hazeera Harithc, Wan Abd Al Qadr Imad Wan-Mohtard, Rashidah Sukora,e
Faculty of Food Science and Technology, Universiti Putra Malaysia, 43400 Serdang, Selangor, Malaysia
Department of Biological Sciences and Biotechnology, Faculty of Science and Technology, Universiti Kebangsaan Malaysia, 43600 Bangi, Selangor, Malaysia
Faculty of Medicine and Health Sciences, Universiti Putra Malaysia, 43400 Serdang, Selangor, Malaysia
Functional Omics and Bioprocess Development Laboratory, Institute of Biological Sciences, Faculty of Science, Universiti Malaya, 50603 Kuala Lumpur, Malaysia
Laboratory of Food Safety and Food Integrity, Institute of Tropical Agriculture and Food Security, Universiti Putra Malaysia, 43400 Serdang, Selangor, Malaysia
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Abstract

This review attempts to delineate the effects and roles of fermented foods on allergic responses (AR), specifically from milk, plant, and meat sources. Evidence for AR alleviation and aggravation were noted for many different fermented food groups. Positive outcomes on AR through fermented foods could be linked to microbial hydrolysis of food allergens, improvement in gut microbiota robustness, and modulation of the immune system that promotes a balance between T helper 1 (Th1) and Th2 cells. Studies on plant-based, non-protein rich fermented foods tend to show more favourable results compared to those on meat-based or protein-rich group. The usage of specific and known starter cultures are helpful in alleviating AR, as in the case for many yogurt, Kefir or Dahi products. Sufficient fermentation time was also deemed important, exemplified in studies that showed inefficient AR reduction through consumption of fresh cheese. However, formation of new allergens through fermentation of certain meat-based foods, or by using specific fermenting microbes (e.g. Penicillium sp.), is possible. Thus, combination of starter cultures and food substrates must be considered in preventing or eliminating AR from intake of these foods. This review may aid consumers to make informed decision during the consumption of fermented food.

Keywords

AllergyFermented foodMilk-based allergensPlant-based allergensAnimal-based allergens

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Food Science and Human Wellness
Volume 12 Issue 3,
May 2023
Pages 691-701
DOI: 10.1016/j.fshw.2022.09.002
Cite this article:
Rahim MHA, Hazrin-Chong NH, Harith HH, et al. Roles of fermented plant-, dairy- and meat-based foods in the modulation of allergic responses. Food Science and Human Wellness, 2023, 12(3): 691-701. https://doi.org/10.1016/j.fshw.2022.09.002
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The roles of different fermented milks in AR.

ItemFermenting microoganismsSubject(s)Outcome(s)*RemarkReference(s)
ALISARR
Notes: *AL, allergens; ARR, Allergic response reduction; IS, immune system modulation. If the box(es) is empty, it indicates that the study did not report any findings on the area. ✓, positive; X, negative; O, mixed. Mixed means no clear indication it reduces or increases.
Fermented milkLactobacillus rhamnosus MTCC 5897OVA-induced infant mice✓✓Given to lactating mice to see the effect on mice infant[21]
UnidentifiedOVA-induced adult mice✓✓Improved respiratory allergy symptoms in mice[22,118]
L. acidophilus L-922,4-Dinitrofluorobenzene (DNFB)-induced mice✓✓The milk with heat-killed bacteria still improved AR[37]
Bifidobacterium lactis Bi-07 and L. acidophilus NCFMHealthy adults (n = 100)✓Increased fecal bacteria and improved intestinal health[119]
Bifidobacterium lactis CNCM I-2494Healthy women (n = 538)✓Improved GI-symptoms in healthy adult women[120]
UnidentifiedChildren with CMA (n = 57)✓Baked milk products are better than fermented milk on CMA children[121]
CheeseUnidentifiedChildren (n = 931)ODiversity of cheese consumption can contribute to better protection against certain AR[45]
UnidentifiedAllergic patient (n = 5)XCross-reactivity can happen between goat and sheep cheese[40]
UnidentifiedHereditary angioedema adults (n = 42)XAllergy may not be caused by IgE-mediated but food intolerance[19]
UnidentifiedOVA-sensitive children (n = 21)✓XCheese is responsible for allergenicity, but aging may hydrolyse allergens[38]
UnidentifiedChildren with AD and their mothers (n = 84)✓Turkish fermented foods benefit on infantile AD[46]
UnidentifiedChildren (n = 34)XHeat does not alter the allergenicity of cheese[39]
E. faecalis VB43In vitro molecular✓The strain capable of hydrolyzing allergenic proteins in milk[26]
UnidentifiedA 5-year-old girlOInduced tolerance to cow\'s milk does not necessarily protect the milk of other mammals[41]
UnidentifiedCaco-2 cells and rats✓Enzyme-modified cheese inhibited the permeation of allergens such as OVA[50]
YogurtUnidentifiedAllergic children (n = 34)OIgE-CMA children with GI syndrome tolerated yogurt well (100%), compared to children with IgE-CMA urticaria and anaphylaxis (7%)[48]
UnidentifiedBALB/c mice✓✓Yogurt involves in IS and regulated gut arginine and proline metabolism pathways involved in AR[51]
UnidentifiedChildren with CMA (n = 34)OTurkish yogurt was tolerated by half of the children[49]
L. delbrueckii ssp. bulgaricus OLL1073R-1Spleen cells in mice✓Enhanced IS via exopolysaccharide from L. delbrueckii ssp. bulgaricus[36]
UnidentifiedJapanese children (n = 1 550)OOnly protect against AD and food sensitization, but not other allergic diseases[52]
UnidentifiedAllergen-induced mice✓Yogurt produced better immune response than milk[122]
UnidentifiedPatients below 14 years (n = 40)OOnly partially protect against cow\'s milk products[123]
UnidentifiedAllergic conjunctivitis adults (n = 26)✓Alternative dietary treatment for allergic conjunctivitis due to the presence of nobiletin and β-lactoglobulin[53]
UnidentifiedInfants with eczema (n = 391) and atopic sensitization (n = 380)✓Reduction of eczema and food allergen sensitization with New Zealand yogurt[124]
B. animalis subsp. lactis LKM512Adult AD patients (n = 10)✓Improve fecal bacteria and SCFAs production[54]
L. acidophilus strain L-55Japanese adults✓Reduce the AR associated with Japanese cedar pollinosis[55]
L. plantarum L67Rat basophilic leukemia and splenocytes cells✓Improve IS by deactivation of certain signalling mechanism in Th cells[56]
DadihLactococcus lactis subsp. lactisBALB/c mice✓Modulation of IS in non-induced mice were used[59]
L. plantarum IS-10506BALB/c mice and AD-children (n = 22)✓✓Improved AD and supress AR in mice[60]
DahiDahi bacteria and L. acidophilus and Bifidobacterium bifidumWhey protein‐induced mouse✓Modulation of IS in the treatment group, but normal dahi (without starter culture) did not provide similar effects[61]
L. acidophilus, L. casei and Lactococcus lactis subsp. biovar diacetylactisOVA-induced AD mice✓Improved AR in the treated group but not in normal Dahi and milk[62]
KefirKazachstania turicensis CAU Y1706OVA-induced AD mice✓Improved gut microbiota[65]
L. Kefiranofaciens M1OVA-induced mice✓✓Heat-inactivated probiotic in Kefir improved asthma syndromes in mice[35,63]

A summary of previous literature on the AR of plant-based fermented foods.

DescriptionSubject(s)Factors/Symptom(s)Conclusion(s)Reference(s)
Fermented sourdough for bowel-sensitive individualsHumansα-Amylase/trypsin inhibitors (ATIs) and FODMAPs, GI bowel-symptoms, inflammation markersSourdough baking decreased ATIs and FODMAPs in wheat but not better than yeast-fermented bread[95]
Lactobacillus-fermented soymilkSoymilk and BALB/c miceHistamine, mast cell protease-1 (mMCP-1), IgG, IgE, allergic-specific cytokines, and histomorphologyDegradation of allergens and reduction of anaphylactic symptoms[66]
Soybean tempeh with Rhizopus oligosporus, A. elegans, Neurospora crassa, and R. oryzaeTempeh and soy-sensitive individualGlycinin, b-conglycinin, trypsin inhibitor, oligosaccharides, antinutrients, IgE immunoreactivityAllergens and antinutrients were degraded, especially when R. oligosporus and A. elegans were being used[70]
Soybean fermented with Bacillus amyloliquefaciens (SFBA)AD-mouse modelMast cell, IgE, IL-4, IL-31, collagen fibre depositionSFBA reduces AR through regulation of NF-κB and mitogen-activated protein kinase (MAPK) but SFBA may reduce skin thickness[69]
Fermented soy protein isolate (B. subtilis, R. oryzae, S. cerevisiae, L. helveticus)Soy protein isolateGly m 5 (β-conglycinin)Reduction of allergenicity by L. helveticus but not S. cerevisiae and R. oryzae[67]
Douchi (fermented soybean)AD-like NC/Nga miceProtein kinase C (PKC), IL-4 substance P, iNOS and matrix metallopeptidase-9 (MMP-9)Partially alleviates AD-like skin lesions[125]
Germinated black soybean (L. pentosus SC65 and Pediococcus pentosaceus ON81A)DNFB-induced DTH mice and RAW 264.7 macrophage cellsCD4+ and CD8+ T cells and NK cells, DTH-related cytokineL. pentosus SC65 resulted in higher bioactive compounds and anti-inflammatory activity[126]
Natto (fermented soybeans)HumanIgE, basophils, poly-γ-glutamic acidHeightened allergic sensitivity and anaphylaxis episode due to the presence of poly-c-glutamic acid[72-74]
Soy sauce (fermented soybean and wheat)HumanHistamine and IgESoy sauce allergies may be caused by substances raised during fermentation[77]
L. paracasei CBA-L74 fermented rice flourHumansSCORing Atopic Dermatitis (SCORAD)100% SCORADs improvement can be seen at week 12[96]
Fermented plant product (fruits, roots grains, algae and sugar)JCP-mice modelSBP-specific immunoglobulin titers, the serum concentration of mast cell protease 1, and cytokine productionReduced sneezes but only mast cell protease 1 was suppressed[127]
Fermented dried Citrus unshiu peel extracts (B. subtilis)LPS-induced RAW264.7 macrophages and HaCaT cellsNO assay, tumour necrosis factor, IL-6, and prostaglandin E2 (PGE2)Reduced inflammation associated with skin dryness[128]
Pasteurized fermented citrus juice (L. plantarum YIT 0132)HumansNasal and stuffy nose symptoms score, Th1, Th2, IgE, eosinophil cationic proteinTreatment reduced AR-related symptoms by modulation of the immune response[129]
Fermented Morinda citrifolia (random probiotics)NC/Nga mice induced by 2,4-dinitrochlorobenzeneHistamine, thymic stromal lymphopoietin, Th-mediated cytokines and chemokines, skin barrier-related proteinsReduce AD skin lesions by improving Th1/Th2/Th17/Th22 balance and skin barrier function[130]
Fermented red ginseng (fecal microbiota)Cell culture, animals, and humansHydrophobic metabolites such as compound K and ginsenosideFermentation with gut microbiota enhances the anti-AR in vitro and in vivo[131,132]
Fermented grape marc (L. plantarum)OVA-induced BALB/c miceIgE, eosinophils, passive cutaneous anaphylaxisSignificant reduction of allergy factors in red (but not white) wine caused by an unidentified compound[100]
Sake lees (L. paracasei NPSRIk-4) and fermented milk (L. brevis NPSRIv-8)Murine model of AR and RBL2H3 rat basophilic leukemia cellsSneezing and basophilsReduced AR symptoms and degranulation of basophils[101]
Sesame fermented by Lentinula edodesSesame, HaCaT cellsAllergen proteins, Th-mediated cytokines, and chemokinesDegradation of Ses i allergen and inhibition of inflammatory mediators via NF-κB and signal transducer and activator of transcription 1 (STAT1) inhibition[97]
Kombucha from Coriolus versicolor and Lentinus edodesPeripheral blood mononuclear cell culturesTh-mediated cytokines, total polysaccharides, phenols and flavonoidsPolysaccharide extracts modulate Th1/Th2[98]
Fermented vegetables, fruits, legumes, seafood, and seaweedHumanAD (survey)High levels of consumption (> 92 times/month) of Korean fermented foods were associated with a lower prevalence of AD[85]
Kimchi and asthma relationshipHumanAsthma (survey)Intake of kimchi is significantly higher in individuals without asthma[83]
Kimchi (L. plantarum SY11 and L. plantarum SY12)RAW 264.7 (murine macrophage) and HT-29 (human colon adenocarcinoma)Digestion model, antimicrobial and NO assaysReduced Th2 cytokines, cyclooxygenase-2, tumor necrosis factor-α, and inducible nitric oxide synthase[84]
Human faecal microbiota (B. longum IM55) and kimchi (L. plantarum IM76)(OVA)-induced AR and microbiota disturbance miceOVA-induced allergic nasal symptoms, IgE, IL-4, IL-5, IL-10, mast cells, eosinophils, Th2 cells, regulatory T cellsImprove AR by enhancing Th1/Th2 and gut microbiota balance[86]
Canavalia gladiata (legume) extract fermented with A. oryzaeAD-induced NC/Nga miceAmino acids, scratching episodes, IgE, histamine, and Th1/Th2 cytokinesImprove AD symptoms by increasing amino acids content, arrest allergic symptoms, and modulate the immune system[99]
LAB-fermented buckwheat sproutsBuckwheat sproutNicotianamine (NA) and 200-hydroxynicotianamine (HNA), Indole-3-ethanolIncreased functional components and degradation or allergens[102]