The Impact of Daily Kimchi Consumption: A Pilot Study

Background: Kimchi, a traditional fermented Korean food, contains prebiotics and probiotics, which have demonstrated ability to impact irregular gastrointestinal (GI) symptoms. Objective: To evaluate the impact of daily kimchi consumption on GI symptoms, sensory characteristics and consumer acceptability of kimchi, and the microbial content in homemade and commercial kimchi. Design: Dietary intervention study incorporating an experimental design. Participants consumed 75g (½ cup) of kimchi twice a day for 14 days. Instruments included 3-day food records, a modified Gastrointestinal Symptom Rating Scale (GSRS), stool diaries using the Bristol Stool Scale (BSS), and a 7-point Hedonic scale (for sensory analysis and consumer acceptability). Lactic Acid Bacteria (LAB) were enumerated via plating methods. Participants/Setting: Participants (n=20) experiencing irregular GI symptoms were recruited from a Mountain West university community during fall 2017. Main Outcome Measures: Main outcomes included GI symptoms, tracking of bowel movements, pre and post response to consumer acceptability, and LAB levels in homemade and commercial kimchi. Analysis: Analysis included: 1) repeated measures ANOVA (p<0.05) for the GSRS and BSS with post-hoc testing for mean comparison between symptoms, 2) paired T-tests to assess mean differences in consumer acceptability and nutrient intake, and 3) culture-based microbial analysis with surface plating methods to determine bacterial counts. Results: Participants reported a significant decrease in abdominal pain, heartburn, acid regurgitation, abdominal rumbling and distention, and eructation and gas production. Consumer acceptability and sensory characteristics questionnaires showed a majority of participants ‘liked’ kimchi and were willing to consume kimchi in the future. Bacterial analysis showed homemade kimchi had a lower concentration of LAB compared to commercial kimchi. Conclusions: Kimchi is a nutrient dense probiotic source, acceptable among consumers in the study, with potential to impact irregular GI symptoms. Understanding consumer perception of kimchi provides valuable insight to when kimchi may be suggested as a method of probiotic and prebiotic intake.


Introduction
Fermentation has ancient roots in a variety of cultures. Kimchi, a fermented mixture of cabbage, salt, red peppers, radishes, and a variety of spices, has been a staple to Korean culture for over 4,000 years. [1,2] Lactic acid producing bacteria (LAB) produced during fermentation have been identified as factors that help maintain and improve gastrointestinal (GI) health. [3][4][5] Irregular GI symptoms affect 14.1% of the total U.S population. [6] The effects of irregular GI symptoms are associated with a severe decrease in quality of life, and a substantial financial burden on society. [6] The dysbiosis of the microbiome and resulting irregular GI symptoms may be induced by a wide variety of circumstances that include consumption of a Westernized diet which is typically high in fat and refined carbohydrates and low in dietary fibre. [7] Supplementation of probiotics may mitigate dysbiosis of the microbiome. [8] Probiotics amounts confer a health benefit on the host. [9] Research on the use of probiotics to alleviate dietary related GI disorders has shown potential. [3,4,10] With current research demonstrating positive effects with supplementation of LAB, [4,10] and the consumption of a variety of probiotics to maximize diversity and discourage the growth of harmful bacteria, [11] kimchi could provide a viable source of beneficial probiotics.
The bacteria promoted during kimchi fermentation have been demonstrated to act safely and effectively as probiotics. [12] Kimchi also contains prebiotics, such as inulin, a major food source for the growth of probiotic bacteria. Increased efficacy of probiotic supplementation has been demonstrated when prebiotics are present, lending credibility to claims that consumption of kimchi could positively affect the microbiome and improve irregular GI symptoms. [3,11] However, there is a paucity of literature addressing fermented foods in the Western diet and potential impact on the microbiome and GI symptoms. This pilot study examined 1) the impact of habitual consumption of kimchi on irregular GI symptoms and bowel form, 2) consumer acceptability and sensory characteristics of kimchi and 3) the microbial content in homemade and commercial kimchi.

Methods
During fall 2017, healthy participants (n=20) aged 18-40 years, experiencing irregular GI symptoms, but without history of malabsorptive or inflammatory bowel disease were recruited for a dietary intervention. Exclusion criteria included one or more of the following: diagnosed hypertension (due to high sodium content of kimchi), antibiotic use within past 3 months, current consumption of fermented products, excessive alcohol consumption (>3 drinks/day) (due to potential impact on GI microbiome) [13] and suppressed immune function (due to presence of live bacteria in kimchi). A sample size of 20 was estimated to provide an effect size of 0.8. [14] After initial phone screening to confirm eligibility, written, informed consent was obtained. The study was approved by the Institutional Review Board at the University of Wyoming. For this pilot intervention, participants consumed 75 grams (~½ cup) of kimchi twice a day for 14 days. Gastrointestinal symptoms were assessed at initiation, day 7, and day 14 using the Gastrointestinal Symptom Rating Scale (GSRS) [18] to evaluate the presence and severity of common symptoms associated with food intake.
The GSRS measures abdominal pain, heartburn, acid reflux, nausea and vomiting, borborygmus (stomach rumbling), abdominal distention, eructation (belching), gas production, decreased or increased passage of stools, hard or loose stools, urgent need to defecate, and satisfaction of bowel movement. The GSRS was modified from initial scale (0-3) to allow for consistency with other study questionnaires and each symptom was rated using a 7-point Likert Scale, where 1=no discomfort/presence of symptom and 7=severe discomfort/high frequency. Participants were asked to evaluate each bowel movement over the 14-days using the BSS (a common clinical tool used to evaluate GI transit time). [16] The BSS is a visual scale that depicts 7 types of common bowel forms, ranging from watery diarrhea with no solids (type 7) to constipation depicted as hard, separate lumps (type 1). Bowel formation of 1 or 2 was categorized as slow, 3 or 4 was normal, and 5-7 was fast.
The total number of slow, normal, and fast were represented as a percentage of total bowel movements during the week.
Sensory characteristics and overall palatability were assessed by a 7-point Hedonic scale (7=extremely like, 1=extremely dislike) to rate appearance, flavour, texture, aroma, mouthfeel, and overall acceptability. Consumer acceptability and feasibility of including kimchi in their typical diet was assessed using a 7-point Likert scale

Bacterial Analysis
Culture-based microbial analysis of the fermented kimchi was conducted to enumerate LAB. Three major genera are known to predominate within traditionally fermented kimchi; Leuconostoc, Lactobacillus, and Weissella. [18] Bacterial enumeration was conducted using surface plating on de Man, Rogosa, and Sharpe (MRS) agar (Thermo Fischer Scientific). X-gal (5Bromo-4-Chloro-

3-Indolyl β-D-Galactopyranoside) additive was purchased through
Millipore Sigma, previously Sigma-Aldrich, St. Louis, MO. Ten grams of kimchi from the commercial product and homemade kimchi (prepared by a culinary-trained researcher in a controlled campus teaching kitchen) were resuspended in 100ml of sterile saline (0.85% saline) solution in a WhirlPak® (Nasco, Fort Atkinson WI).
The samples were mixed by hand for five minutes followed by serial dilutions using saline dilution blanks.
MRS agar or MRS agar supplemented with X-gal were utilized for surface plating. The supplementation with X-gal (chromogenic substrate for β6 galactosidase) provided additional differential discrimination for Leuconstoc spp. 19 Leuconostoc spp. are known to synthesize β-galactosidase enzyme, thus colonies precipitate a blue color upon plating. MRS is commonly used to isolate and enumerate LAB.20Incubation was performed inside an anaerobic chamber containing anaerobic sachets (Thermo Scientific Oxoid anaerogen 2.5L Sachet) at 37˚ C for 72 hrs. Plating was performed in triplicates and counts were averaged to estimate kimchi microbial load as log10 CFU/g.

Statistical Analysis
Descriptive statistics were performed on all variables.     Table 4. Sodium data for one substantial outlier was excluded from the analysis. No significant differences between week 1 and 2

Results
were detected for any of the selected nutrients.  to GI symptoms such as belching-abdominal fullness, bloating after meals, difficulty with defecation, and stomach gurgling. [3,21,22] Further research has demonstrated increased efficacy of probiotic supplementation when combined with prebiotic food sources such as inulin compared to probiotics alone. [3,23] Little research is available on the potential of fermented foods to act as beneficial probiotic sources.
Microbiological evaluation of kimchi has demonstrated the presence of a wide variety of LAB with the ability to act safely as probiotics. [12,24] However, limited information is [11] available for the use of kimchi to improve GI symptoms. Studies of probiotic supplementation generally emphasize high concentrations of bacteria and a wide variety of probiotic strains to maximize alleviation of symptoms. [11] In the current study, significant subjective improvement for abdominal pain, heart burn, acid regurgitation, abdominal rumbling and distention, and belching and gas production was observed, which is consistent with other

Conclusions & Recommendations
Kimchi allows for inclusion of a nutrient dense vegetable source that has potential to impact GI health. Importantly, kimchi may provide a feasible and palatable method of supplementing probiotics within the diet and provides health professionals with an additional option to recommend to patients or clients. Further exploration of the impact of kimchi consumption would be beneficial in corroborating the evidence found within this study.