Lupine Publishers | Scholarly Journal of Food and Nutrition
Abstract
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.
Keywords:Kimchi; gastrointestinal; consumer acceptability; fermented
foods; bacterial content; probiotics
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. [3-5] 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 are live microorganisms which when
administered in adequate 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 (7=strongly agree, 1=strongly
disagree) for five statements: ‘I enjoy consuming fermented foods as part of my
regular diet’, ‘I am aware of different types of fermented foods and how to
prepare them’, ‘I am interested in learning more [5] about the different types
of fermented foods’, ‘I am willing to eat kimchi in the future’, and ‘I plan on
consuming kimchi regularly’. [17] Participants recorded a three-day food diary
(including two weekdays and one weekend day) during each week of the study.
Training on tracking dietary intake, portion sizes, and guidance to continue
with regular diet patterns was provided by the lead researcher and a registered
dietitian prior to the initiation of the study.
Food records were examined at the exit
interview with discrepancies in portion sizes or unclear entries clarified to
increase accuracy. Diaries were utilized to compare and contrast oral dietary
intake during the study period and to promote adherence to the kimchi
intervention and avoidance of other fermented foods. Threeday food records were
analyzed with dietary analysis software (ESHA Food Processor Nutrition Analysis
Software, ESHA Products, Salem, OR 2018).
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. Repeated measures ANOVA was used to assess
significant changes in symptoms reported on the GSRS with post-hoc testing
(Least Significant Difference, LSD) for mean comparison between symptoms.
Frequency of slow, normal, and fast bowel movements reported on the BSS diaries
were compared between the first and second week to identify improvement or
changes in typical bowel formation and analyzed using repeated measures ANOVA.
Posthoc testing using LSD determined differences between categories. Consumer
acceptability pre- and post-intervention was analyzed using a paired T-test.
Mean intake of key nutrients including macronutrients, dietary fibre, and
sodium were compared from week 1 to week 2 of the study using paired T-test
analysis. All statistics were performed using SPSS 24.0 (IBS SPSS Statistics
for Windows, Version 24.0. Armonk, NY: IBM Corp 2016). The statistical
significance was defined as p< 0.05 for all estimates.
Results
Forty individuals were screened with
twenty-one individuals meeting inclusion criteria. One participant was lost to
attrition on day 6 of the intervention. The GSRS and BSS were collected from
individuals who completed the study. Consumer acceptability and sensory [7]
characteristics included all twenty-one participants. Participant demographics
are displayed in Table 1. Study compliance was assessed using food records or
feedback at the exit interview. Gastrointestinal symptoms on the GSRS were
grouped into six major categories (Table 2). Symptoms in categories 1, 3, and 4
were improved (p< 0.01) with kimchi consumption. Normal distribution was
confirmed upon analysis using repeated measures ANOVA. Kimchi consumption had
no measurable effect on typical stool form. The frequency of slow and normal
bowel movements increased slightly, but not significantly (p=0.673).
Table 3 contains a complete
breakdown of sensory characteristics. More than half (57.1%) of the study
population ‘liked’ the kimchi, and an additional 9.5% “extremely liked” it.
Aroma and appearance had the highest occurrence of ‘neither dislike nor like’
with 28.6% reporting for each. Minor changes in consumer acceptability were
seen over the two-week period. The only statement to demonstrate a significant
increase was ‘I enjoy consuming fermented foods as part of my regular diet’
(p=0.007). Comparison of average intake of calories, fat, protein,
carbohydrates (CHO), dietary fibre, and sodium (Na) are presented in Table 4.
Sodium data for one substantial outlier was excluded from the analysis. No
significant differences between week 1 and 2 were detected for any of the
selected nutrients.
Consumption of ½ cup kimchi twice a
day and no additional fermented food intake was confirmed via the food diaries
or verbally at the exit interview microbial counts of LAB were determined for
both commercial and homemade kimchi. Commercial kimchi found LAB content when
plated on MRS agar to be approximately 5.31 log CFU/g. Commercial kimchi plated
on MRS with the addition of X-gal found content to be approximately 5.26 log
CFU/g. Based on results obtained from plating on X-gal supplemented media, no
detectable levels of Leuconostoc spp. were discernible. Homemade kimchi
plated on MRS and MRS + X-gal, presented slightly lower concentrations of 4.21
log CFU/g and 4.26 log CFU/g respectively with no Leuconostoc spp.
detected.
Discussions
An emerging number of clinical
studies have evaluated the use of probiotics to improve GI disorder. The
majority of these studies place emphasis on encapsulated probiotic supplements
or probiotic enriched fermented milks/yogurts containing a mixture of LAB and
Bifidobacterium spp. A number of these studies have demonstrated subjective
improvement with regards 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 studies. [3,21,22]
Stool form was not significantly affected which was corroborated with
non-significant changes on participants’ BSS. Previous studies have found that
probiotic supplementation has little effect on typical stool forms. [4,22]
Despite a recent rise in popularity of functional fermented foods, little is
reported on consumer acceptability, sensory characteristics, and preference for
kimchi. A previous study by Jang et al, evaluating the acceptability of kimchi
presented similar findings to the current study in that there was an overall
liking and perception of kimchi.25 Jang et al. found that in general, U.S.
panelists gave overall liking scores of 6-7 on a 9-point hedonic scale.
The author described this as the
liking of kimchi to be ‘slightly, to moderately pleasant.’ It should be noted
that the higher liking of kimchi could have been related to participant’s
preconceived notion about fermented foods and kimchi in general. It is
plausible that some of the participants were attracted to the study due to the
opportunity to incorporate kimchi into their regular diet. Food diaries
provided insight about the typical diet of participants and allowed for
comparison of key nutrients between each week. No significant changes in
dietary intake of key nutrients was detected. Caloric intake is based on
individual needs, so there are no set averages to assess participant caloric
intake. According to the Institute of Medicine, Acceptable Macronutrient
Distribution Range (AMDR), 20-35% of kcals should come from fat. [26] For the
average 2278 kcal consumed by participants in this study, fat intake was 106 g
which provided 41.8% of total kcal, [12] above AMDR recommendations.
The AMDR for protein is 10-35% of
kcals. Participant protein intake was 90 g which provided 15.8% of total kcal, meeting
the AMDR recommendation. Finally, the AMDR for CHO is 45-65% of kcals. Average
CHO intake was 245g which provided 43.0% of kcal, just under the minimum
recommendation. Diet, particularly dietary fibre, is a major component that
influences GI function and microbiota. [27] Current recommendations for dietary
fibre per day are 38g for men and 25g for women under age 50.26 Participant
dietary fibre intake ranged from 13 g to 45 g with an average intake of 25g.
The mean dietary fibre intake of all individuals 2 years and older in the U.S.
population is 16g per day. [28] Kimchi contributed an additional 4g of dietary
fibre per day per participant which contributed to dietary fibre intake higher
than the national average.
Sodium consumption among participants
was well above the 1,500 mg/day recommendation for both men and women, [29]
with an average intake of 4,414mg. It was also above the average daily sodium
intake (3,400 mg) for individuals over 2 years of age. [30] Consumption of
kimchi contributed to this high average intake, as it added 1,400 mg of sodium
per day. Kimchi has been evaluated for the impact an individual’s health.
[24,31- 33] However, limited literature elucidates the potential for kimchi to
act as a safe and effective probiotic source. [12,24,34] In the current study,
bacterial evaluation denoted that the commercial kimchi had LAB concentrations
of approximately 5. [31] log CFU/g, which is lower than the suggested
concentrations found within traditional fermented kimchi (8log CFU/g) [35] and
what is described on the commercial product packing (8.16 log CFU/g). Bacterial
concentrations in kimchi are influenced by a variety of factors, specifically
variations in raw materials such as vegetable type, harvesting area, season,
and supplemental ingredients. [18] Furthermore, LAB has been described as
comprising 68.7-98.1% of total bacteria present in kimchi. [35] This study was
also not able to detect presence of 13 Leuconostoc spp. which are major
contributors to the fermentation process.
The reasoning behind the lack of Leuconostoc
spp. remains unclear. Leuconostoc spp. have been seen to predominate in
the earlier stages of fermentation,18,36 thus microbial succession could be a
reason. However, some strains such as, Le. gasicomitatum, have been seen to
increase in later stages of fermentation, [37] which should be detectable by
the plating methods utilized in our study due to their β-galactosidase
activity.38 Despite the unclear reasoning for the lack of detectable Leuconostoc
spp., this may prove to be advantageous for classifying kimchi as a probiotic
rich food. Leuconostoc spp. have demonstrated low survival rates when
passing through the GI tract31 which is vital for the classification as a
probiotic. However, Lactococcus and Lactobacillus spp. have been
validated to act as efficient probiotic bacteria. [24] While the microbial
analysis followed previous literature for developing laboratory protocols
[18,19] the study was limited to analysing presence of LAB, not total microbial
content, thus estimations cannot be extrapolated to all commercial products.
More so, while this study demonstrated improved symptoms, participants were
aware of the intent of the study which could have induced the placebo effect.
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
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