Abstract
The popularity of fermented foods and beverages is due to their enhanced shelf-life, safety, functionality, sensory, and nutritional properties. The latter includes the presence of bioactive molecules, vitamins, and other constituents with increased availability due to the process of fermentation. Many fermented foods also contain live microorganisms that may improve gastrointestinal health and provide other health benefits, including lowering the risk of type two diabetes and cardiovascular diseases. The number of organisms in fermented foods can vary significantly, depending on how products were manufactured and processed, as well as conditions and duration of storage. In this review, we surveyed published studies in which lactic acid and other relevant bacteria were enumerated from the most commonly consumed fermented foods, including cultured dairy products, cheese, fermented sausage, fermented vegetables, soy-fermented foods, and fermented cereal products. Most of the reported data were based on retail food samples, rather than experimentally produced products made on a laboratory scale. Results indicated that many of these fermented foods contained 105−7 lactic acid bacteria per mL or gram, although there was considerable variation based on geographical region and sampling time. In general, cultured dairy products consistently contained higher levels, up to 109/mL or g. Although few specific recommendations and claim legislations for what constitutes a relevant dose exist, the findings from this survey revealed that many fermented foods are a good source of live lactic acid bacteria, including species that reportedly provide human health benefits.
Introduction
Fermentation has long been used to preserve and enhance the shelf-life, flavor, texture, and functional properties of food (Hutkins, ). More recently, the consumption of fermented foods containing live microorganisms has emerged as an important dietary strategy for improving human health (Marco et al.,
). In general, lactic acid bacteria (LAB) from several genera, including Lactobacillus, Streptococcus, and Leuconostoc are predominant in fermented foods, but other bacteria as well as yeast and fungi also contribute to food fermentations. Commercially-produced fermented foods also frequently serve as carriers for probiotic bacteria. Despite this interest and the potential public health benefits of these foods, there is still considerable confusion about which fermented foods actually contain live microorganisms, as well as understanding the role of these microbes on the gut microbiome (Slashinski et al.,
).
Nonetheless, yogurt and other cultured dairy products are generally perceived by consumers as good sources of live and health-promoting organisms (Panahi et al.,
). Moreover, in a survey of 335 adults, yogurt was the main food associated with probiotic bacteria (Stanczak and Heuberger,
). However, the actual concept of fermentation is evidently not so familiar—a survey of 233 college students attending Brescia University College in London, Ontario revealed that nearly two-thirds were unfamiliar with the term “fermented dairy products,” and about the same percent were unsure that several cultured dairy products were fermented (Hekmat and Koba, ).
That a particular food or beverage is produced by fermentation does not necessarily indicate that it contains live microorganisms. Bread, beer, wine, and distilled alcoholic beverages require yeasts for fermentation, but the production organisms are either inactivated by heat (in the case of bread and some beers) or are physically removed by filtration or other means (in the case of wine and beer). Moreover, many fermented foods are heat-treated after fermentation to enhance food safety or to extend shelf-life. Thus, fermented sausages are often cooked after fermentation, and soy sauce and sauerkraut and other fermented vegetables are made shelf-stable by thermal processing. Some products, such as many of the commercial pickles and olives, are not fermented at all, but rather are placed into brines containing salt and organic acids. Even non-thermally processed fermented foods may yet contain low levels of live or viable organisms simply due to inhospitable environmental conditions that reduce microbial populations over time. It is important to note, however, that the absence of live microbes in the final product does not preclude a positive functional role. For example, food fermentation microbes may produce vitamins or other bioactive molecules in situ or inactivate anti-nutritional factors and yet be absent at the time of consumption.
Labeling live microbes in fermented foods and beverages
Yogurt, kefir, and other cultured dairy product manufacturers have long promoted the presence of live cultures. Indeed, the “live and active” seal was created by the National Yogurt Association (NYA), for yogurt products in the United States containing at least 100 million cells or cfu per gram at the time of manufacture (Frye and Kilara, ). According to the NYA, the “live and active” seal refers only to yogurt cultures, and specifically to the two species that comprise such cultures, Streptococcus thermophilus and Lactobacillus delbrueckii subsp. bulgaricus. However, frozen yogurt, kefir and other cultured dairy products also claim the presence of live and active cultures, even though the microorganisms may be different than those found in yogurt. In the U.S., there is no regulatory requirement to state microbial levels, thus these label declarations are strictly voluntary.
In contrast, in other regions, the number of live microbes present in yogurt and other cultured dairy products must satisfy regulatory requirements. For example, according to the CODEX standards for fermented milk products, the minimum number of starter culture bacteria in yogurt is 107 cfu per g (CODEX STAN 243-2003). If other organisms are indicated on the label, they must be present at 106 cfu per g. Nonetheless, in Europe, to make a claim for yogurt containing live cultures for improving lactose digestion, the European Food Safety Agency requires a minimum of 108 cfu per g of live bacteria (EFSA Panel on Dietetic Products, Nutrition and Allergies, ). In contrast, in Australia and New Zealand, a minimum of only 106 cfu per g is required (Commonwealth of Australia Gazette, ).
For many years, cultured dairy products were the only fermented foods that included label declarations regarding the presence of live microorganisms. Label declarations on sauerkraut or kimchi or miso, had, until recently, been rare. The popularity of artisan-style fermented foods (Johnson, ) and interest in their health properties (Marco et al.,
) has led more manufacturers to inform consumers, via food labels, that their products contain live microorganisms. In some cases, the species in these types of foods have been identified and then compared to label claims (Yeung et al.,
; Scourboutakos et al.,
). However, to our knowledge, data on the actual levels of live microorganisms in most fermented retail products has not readily been reported or summarized in an organized form. Therefore, consumers, despite their interest in probiotics and functional fermented foods (Linares et al., ), have had little access to this useful information.
Survey design
The purpose of this study, therefore, was to survey the scientific literature and identify published papers in which the number of live microorganisms in a range of fermented foods was reported. Included were so-called western-fermented foods such as yogurt, cheese, and sausage, as well as soy-based and cereal-based fermented foods that are widely consumed in other regions (Tamang et al.,
). We then organized and summarized the quantitative data from those reports. Our interest was focused on those reports in which foods were obtained from retail locations or were made under manufacturing conditions. Thus, reports describing results from experimentally-produced fermented foods on a laboratory or pilot scale were excluded, in part because they do not reflect commercial processing, distribution, and storage conditions as do retail products. A large number of the reports in the literature in which levels of microbes in fermented foods were described were of this sort. In addition, many reports have analyzed the importance of microbial food safety and hygienic conditions of fermented food products and have reported the presence of spoilage microorganisms or food pathogens. However, the organisms responsible for fermentation and that are commonly present in the finished products were the focus of this current study.
Search criteria
Scientific articles were chosen that satisfied specific parameters relevant to our stated goals. Specifically, our database search (Google Scholar, WorldCat, Scopus, and PubMed) focused on those studies that enumerated microorganisms exclusively in fermented food products. Keywords for these searches included, but were not limited to, the type of fermented food analyzed and, “commercially produced,” “commercial product,” “enumerated,” “lactic acid bacteria,” “microbial characterization,” “probiotic,” and “culture.” Food products that served only as vehicles for delivery of probiotic microorganisms were not included. Thus, studies that reported counts for frozen yogurt were included, but studies on ice cream containing probiotic microorganisms were not. In general, results were only included for commercial products, bought at retail locations, or those experimentally-produced under industrial manufacturing conditions. Thus, strictly experimental products (e.g., made in a laboratory or under small experimental-scale conditions) were not considered. The only exceptions were for products for which little or no data from retail or industrially manufactured sources was available. In those cases, lab- or pilot-scale-produced products were included, provided they were made using traditional manufacturing methods. No restrictions for date, location, or language were applied.
Data reporting
For most products, quantitative data relied on cultural methods using well-established types of differential, selective, and general purpose media, as well as appropriate incubation conditions. LAB were the main group described, although other bacterial groups were occasionally reported. Some studies reported single microbial counts, whereas other reported ranges. Although papers reported counts either as log or as actual values, all of the data described in this review are shown as logs. For some products, values were estimated from graphs or figures. When products were held for shelf-life or aging studies, the counts from multiple times points are shown. Otherwise, single time-point data was reported. The region or origin of product manufacture was also noted.
General survey results
Approximately 400 published studies were reviewed in which fermented foods were characterized for the presence of live microorganisms. However, about three-fourths were excluded and not used in our results. Several excluded studies focused on development of selective methods for distinguishing between different species of LAB, determining ratios (e.g., cocci-to-rods in yogurt), or for enumerating only probiotics organisms. Although most studies reported data based on traditional plating methods, many of the more recent studies reported abundance data (i.e., 16S rRNA-based community sequencing). Because the latter 16S-based methods also detect non-viable cells, these studies were excluded unless total counts were also reported. Ultimately, more than 140 studies were included in our survey. Although the literature from which the results were assembled covers a 50 year period and a range of different regions and methodologies, the results are remarkably consistent. As summarized below, nine groups of fermented foods were reviewed in this survey. These included yogurt and other cultured dairy products, cheese, fermented meats, fermented vegetables, traditional fermented Asian products, fermented cereals, beer, and fermented tea (Kombucha).
Yogurt and other cultured dairy products
Studies were conducted for retail or commercially manufactured yogurts and other cultured dairy products obtained in the U.S., Australia, Spain, France, Norway, Greece, Argentina, and South Africa (Table
). All of the yogurts examined contained the yogurt culture organisms, S. thermophilus and L. delbrueckii subsp. bulgaricus, at levels ranging from < 104 to 109 cfu/g or ml. In general, counts for S. thermophilus were somewhat higher than for L. delbrueckii subsp. bulgaricus. In several studies, other microorganisms, including Bifidobacterium spp. and Lactobacillus spp., were also enumerated. Levels of the latter ranged from undetectable (< 10 cfu/g) to 108 cfu/g. The addition of these probiotic bacteria did not appear to have any effect on levels of the yogurt culture organisms. Although most studies reported counts at only a single time point, other studies reported initial counts as well as at a second time point, usually considered end-of-shelf-life. In such cases, counts were generally similar at both time points (>106 cfu/g), provided samples were stored at refrigeration temperatures (Hamann and Marth, ).
Table 1
RegionTypeSourceAnalyzed microorganismsInitial Count (log cfu/mL or g)Final Count (log cfu/mL or g)AgeCP
ReferencesArgentinaFull and reduced fat yogurtRetailS. thermophilus8.87–9.46–Within shelf life6Vinderola and Reinheimer,
L. bulgaricus
5.58–7.95–Bifidobacteria
2.60–8.71–L. acidophilus
4.62–8.39–L. casei
8.02–8.33–Set, skimmed set, drinking, and set with “dulce de leche” yogurt
Industrially manufacturedTotal LAB7.54–8.62–Within shelf life25Birollo et al., S. thermophilus7.72–8.58–L. bulgaricus7.29–7.38–AustraliaFull and reduced fat yogurt
Commercially ManufacturedStreptococci9.15–9.68.79–9.15After manufacture and by expiration4Micanel et al.,
L. bulgaricus9.088.36L. acidophilus6.66–8.086.38–8.04Bifidobacteria5.817.54Skim milk and regular yogurt
Did not specifyL. casei–3.41–7.49Did not specify2Ravula and Shah,
Variety of flavored, natural, and skinny yogurt
RetailS. thermophilus8.62–9.17–After purchase5Tharmaraj and Shah,
L. bulgaricus4.92–7.68–L. rhamnosus7.36–7.72–L. casei4.01–5.53–B. lactis6.36–7.4–L. acidophilus5.23–7.83–Variety of flavored yogurts
RetailL. acidophilus< 2–8.34< 2–8After purchase (around 20–30 days before expiration) and at expiration26 CP from 14 companiesShah et al.,
Bifidobacteria< 2–6.86< 2–6.18L. casei5.65–8.18< 2–8.08Yogurt
Did not specifyL. acidophilus–6.56–18Talwalkar and Kailasapathy,
Bifidobacteria–6.54L. casei–6.38Yogurt
Obtained from manufacturerL. acidophilus4–8.5NVO−7.7After manufacture and 30 days5Shah et al.,
B. bifidum3.3–7NVO−2.5ChinaYogurtRetailS. thermophilus + Lactobacillus–4.0–8.18End of shelf life31Dong et al., EnglandYogurt
RetailBifidobacteria–4.9–7.62Does not specify8Iwana et al., GreeceiGreek type yogurtObtained from manufacturerS. thermophilus9.18.550 days (product shelf life)1Alexopoulos et al., L. delbrueckii subsp. bulgaricus8.87.9ItalyPlain stirred style yogurtRetailS. thermophilus7.71–8.9–10 days after manufacture11De Noni et al., L. bulgaricus5.48–8.41–Sweetened stirred style yogurtRetailS. thermophilus8.3–9.59–10 days after manufacture11De Noni et al., L. bulgaricus< 4–8.18–South AfricaLow fat, fruit flavorediObtained from manufacturerS. thermophilus8.7–9.57.9−9.5Directly after production, and at expiration date3Lourens-Hattingh and Viljoen,
L. bulgaricus7–8.65.5–7L. acidophilus7–8.74.9–7B. bifidum2–5.22.2–4.9United StatesCustard style yogurt—plain and flavorediRetailTotal LAB9.1–15 days after manufacture2 CP from 1 manufacturerHamann and Marth, S. thermophilus9.1–L. bulgaricus8.1–Dannon, Breyers, Yoplait, YoBaby, Wal-Mart, and Kroger varietiesRetailLactobacillus–7.68–8.98before expiration10Dunlap et al., Flavored yogurtRetailL. bulgaricus5.2–8.876.15–8.690 and 4 weeks after purchase58 CP/7 brandsIbrahim and Carr, S. thermophilus7.51–8.947.9–8.99Bifidobacteria< 1–4.7NVO
Plain nonfat yogurtRetailS. thermophilus8.14–9.83–After manufacture3Laye et al., L. bulgaricus9.04–9.33–Stirred style yogurt–flavorediRetailTotal LAB8.6–6 days after manufacture1Hamann and Marth, S. thermophilus8.6–L. bulgaricus7.3–YogurtRetailTotal LAB-7.2–8.1At expiration date2Shin et al.,
Bifidobacteria–6.5–7.1Organisms in commercial yogurt products by region.
*
CP, commercial products.
**
NVO, No viable organisms.
a
Only viable in 4 of 6 CP.
b
Only viable in 3 of 6 CP.
c
Reported as average on duplicate agar plates.
d
L. delbrueckii spp. bulgaricus—reported in only one product. L. acidophilus −1 of 4 CP had NVO. Bifidobacteria−1 of 4 CP had NVO and 1 product had no detectable counts at initial enumeration (week 0).1
e
Lower end of range are microbial counts for skim milk yogurt and higher end are for regular yogurt. Both products claimed to contain L. casei.
f
S. thermophilus —Seen in 5 of 5 CP, “yogurt culture” claimed in all 5 CP. L. bulgaricus—Seen in 2 of 5 CP, “yogurt culture” claimed in all 5 CP. L. rhamnous—Claimed in 2 of 5 CP. L. casei—Claimed in 2 of 5 CP. B. lactis—Claimed in 4 of 5 CP. L. acidophilus—Claimed in 4 of 5 CP.
g
L. acidophilus—Claimed in 24 CP. Bifidobacteria—Claimed in 18 CP. L. casei—Claimed in 8 CP.
h
L. acidophilus—9 of 18 CP. Bifidobacteria-−8 of 18 CP. L. casei—6 of 18 CP.
i
Interpreted from graph.
j
L. acidophilus—2 of 5 CP had NVO. B. bifidum—4 of 5 CP had NVO.
k
Observed in 5 of 8 CP, claimed in all products.
In addition to fresh yogurt, frozen yogurt was also examined for bacteria. Results from several studies indicates that when these products were assessed for the relevant yogurt LAB, levels were generally similar to fresh yogurt, with counts ranging from 104 to 109 cfu/g. The stability of lactic cultures in frozen yogurt during long-term storage at freezer temperature (-23 C) has also been studied (Lopez et al., ). In general, LAB (S. thermophilus and L. delbrueckii subsp. bulgaricus) survived beyond the designated shelf-life period (1 year), with less than a 0.5 log reduction for most samples.
The number and type of live microorganisms in other cultured dairy products have also been reported (Table
). These include kefir, cultured buttermilk and simply “fermented milk.” As for other cultured dairy products, populations of LAB were in the 105–109 cfu/g range.
Table 2
Dairy productRegionSourceAnalyzed microorganismsInitial Count (log cfu/mL or g)Final Count (log cfu/mL or g)AgeCP
ReferencesAmasiSouth AfricaRetailLAB5.1–6.29–Did not specify5Moyane and Jideani,
Total bacteria count3.62–4.96–Cultured ButtermilkEthiopia
Dairy farms and processing unitsLactococci6.07–9.25–Does not specify16Gebreselassie et al., Lactobacilli6.07–8.61–IndiaRestaurantTotal viable count6–Does not specify1Jayashree et al., United StatesRetailTotal bacteria count7.3–8.646.08–7.24After purchase and 7 days after8Vasavada and White,
Fermented MilkArgentinaRetailS. thermophilus9.11–9.49–Within shelf life2Vinderola and Reinheimer,
L. acidophilus4.62–6.60–SpainCommercially ManufacturedS. thermophilus8.428.37After manufacture and at shelf life (24 days)50Medina and Jordano,
L. bulgaricus7.716.87Bifidobacteria6.876.62Spain
RetailS. thermophilus9730 days10Gueimonde et al., Lactobacillus7–7.35.1–6.8Bifidobacteria5.6–7.54.1–7.6SpainRetailS. thermophilus9.27–Within shelf life (28 days)1García-Cayuela et al., L. bulgaricus7.64–L. acidophilus6.65–L. casei6.79–B. lactis8.2–Frozen YogurtFranceObtained from manufacturer
S. thermophilus8.19–5 weeks after manufacture1Lopez et al., SpainObtained from manufacturerS. thermophilus7.57–7.58–1 week after manufacture2Lopez et al., L. bulgaricus4.29–6.79–United StatesVariety of flavors soft/hard from retail and the manufacturer
Total bacteria< 5.52–8.81–Does not specify34Kosikowski, Vanilla flavors from retail
LAB6.11–9.32–Does not specify10Schmidt et al.,
Variety of flavors from retailTotal viable bacteria2.30–8.53–Within shelf life19Tieszen and Baer,
KefirGreece
RetailYeast5–15 days before expiration9Kalamaki and Angelidis, KoreaManufactured with commercial grainLAB9.62–After fermentation–
Kim et al., Acetic acid bacteria9.52–Yeast7.67–Norway
Obtained from TINE Meieret dairy companyLeuconostoc7.16.3After production and at expiration5Grønnevik et al., Lactobacillus8.16.4Lactococcus8.15.8Yeast3.33.9TurkeyRetailLactobacillus6.51–8.01–Does not specify4Kesmen and Kacmaz, Lactococcus7.53–8.30–United States
Manufactured with commercial starter cultureLactobacillus9.15–After fermentation–
OBrien et al.,
Lactococcus9–Yeast7.2–Organisms in commercial cultured dairy products separated by product.
*
CP, Commercial Products.
a
Analyzed sour cream buttermilk and sour milk buttermilk.
b
Interpreted from graph.
c
No significant decrease in S. thermophilus over time. L. bulgaricus was absent in this CP.
d
Only 23 CP of 34 CP had viable organisms.
e
NVO in 6 CPs (< 1 log).
f
Only viable counts seen in 8 of the 9 CPs.
g
Lab-scale fermentation with commercial kefir grain/starter
h
Presumptive (95:5 ratio) for lactobacillus and lactococcus.
i
Reported as average from triplicate agar plates.
Cheese
Although considerable microbiological data for cheese exists, most of these reports are concerned with microorganisms having public health or cheese quality implications. Still, levels of lactic acid and related bacteria were reported for more than 30 types of cheese from 18 countries including the United States, Italy, France, Germany, Mexico, Ireland, and South Africa (Table
). Many papers reported the microorganisms as mesophilic streptococci, lactococci, and lactobacilli or as thermophilic streptococci and lactobacilli. Others reported total microorganisms and total LAB. For most products, only one time period was recorded (usually the most aged sample). Microbial counts ranged from undetectable (< 103 cfu/g) to 109 cfu/g, with the highest levels found in Tilsit cheese (typically aged 2–4 months). In contrast, Grana Padano aged 1 year, Parmesan aged greater than 1 year, and Swiss Gruyere aged greater than 1 year all showed no detectable microorganisms (< 103 cfu/g). As noted for other products, the methods used by the investigators may have influenced the reported data. Thus, enumeration of selected organisms (e.g., S. thermophilus) was only possible if the appropriate medium and growth conditions were used.
Table 3
CheeseRegion (Type)SourceAnalyzed microorganismsCount (log CFU/g)AgeCP
ReferencesAfuega'l PituSpainTraditionally manufacturedTotal viable bacteria count8.0660 days2Cuesta et al., Lactococci6.77Leuconostocs6.76Lactobacilli8.01Armada
SpainTraditionally manufacturedAerobic Mesophiles4.39–8.1416 weeks2Tornadijo et al.,
Lactococci4.17–6.38Lactobacilli4.19–8.09Leuconostocs3.38–7.58AsiagoItaly (Asiago Allevo)Commercial sampleMeso. streptococci5.73–10 months1Gatti et al., Therm. streptococci8.9Meso. lactobacilli4.5Therm. lactobacilli7.2Blue Cheese
United StatesRetailTotal plate count7.32Within shelf life1Genigeorgis et al., BrieItalyCommercial samplesMeso. streptococci5.31–2 months1Gatti et al., Therm. streptococci<3Meso. lactobacillin.d.
Therm. lactobacilli<3South Africa
Commercially manufacturedLAB7–8.88 weeks8Viljoen et al.,
BurgosSpainRetailLAB4.6–8.8Time of purchase36Garcia et al., CabralesSpainObtained from manufacturersAerobic mesophiles7.45–8.3690 days2Flórez et al., Lactococci7.44–8.12Lactobacilli5.85–7.15Leuconostoc spp.5.40–6.14Obtained from manufacturersc, dTotal viable count6.8–7.9120 days2Nuñez,
Streptococci3.5–5.9Leuconostocs3–3.8Lactobacilli3.2–6.5Yeast+Molds4.1–7.2Camembert
South AfricaCommercially manufacturedLAB7.6–8.58 weeks8Viljoen et al.,
CheddarIrelandCommercially manufacturedL. paracasei839 weeks3Fitzsimons et al., Ireland
Obtained from manufacturerNSLAB
1.70–6.908 weeks8Jordan and Cogan, NSLAB6.1552 weeks2U.S.
Traditionally manufactured with commercial starter cultureLactobacillus5.1180 days–Madkor et al.,
Colby
United StatesRetailTotal plate count7.6Within shelf life1Genigeorgis et al., ComteFrance
Obtained from manufacturerLb. paracasei6.28–7.59168–280 days4Depouilly et al., Lb. rhamnosus5.37–6.9Switzerland
Commercially manufacturedThermophilic streptococci6.7524 weeks3Bouton et al., Thermophilic lactobacilli7Facultative heterofermentative lactobacilli7.5Propionibacteria7.75DanboDenmarkIndustrially manufacturedLactococcus5.766 weeks1Gori et al., Lactobacillus5.82–5.87EdamEgypt (Edam-like cheese)
Manufactured with commercial starter cultureTotal viable bacteria count7.7615 weeks1Ayana and El-Deeb, ItalyCommercial samplesMeso. streptococci2.91–2 months1Gatti et al., Therm. streptococci4.3Meso. lactobacilli5.8Therm. lactobacilli5.3FetaGreeceObtained from manufacturer
LAB6.160 days1Alexopoulos et al., Retail
Lactobacillus5.95–7.19>60 days4Rantsiou et al.,
Lactococcus4.18– < 5Iran (Probiotic feta)Commercially manufacturedLactobacillus acidophilus6.7Did not specify1Mohammadmoradi et al.,
Bifidobacterium lactis6.7FontinaItalyCommercial sampleMeso. streptococci8.33–10 months1Gatti et al., Therm. streptococci8.3Meso. lactobacilli4.6Therm. lactobacilli8.6Italy (Fontal)Commercial samplesMeso. streptococci<31–2 months1Gatti et al., Therm. streptococci5.2Meso. lactobacilli<3Therm. lactobacilli4.4Galotyri
GreeceRetailTotal viable count8.03Time of purchase1Samelis and Kakouri,
Lactobacilli7.55Lactococci8.11GorgonzolaItalyCommercial sampleMeso. streptococci3.53–10 months1Gatti et al., Therm. streptococci7.4Meso. lactobacilli3.1Therm. lactobacilli6.4Obtained from manufacturer
Total mesophilic bacteria7.36–7.5686 days1Gobbetti et al., S. thermophilus7.85–7.92Lb. delbrueckii subsp. bulgaricus3.67–5.77Mesophilic lactobacilli5.57–5.69Lactococci7.73–7.87Mold6.81–7.44GoudaBelgium
Commercially manufacturedTotal microflora count5.842 days1Messens et al.,
LAB7.1Lactococcus lactis6.1Belgium (Bellie)
Commercial starter cultureEnterococcus6.45–6.9012 weeks1Van Hoorde et al.,
Lactobacillus6.3–7.3Lactococcus7.2–7.7Leuconostoc7.4–7.6Belgium (Dulses)
Commercial starter cultureEnterococcus6.40–6.5512 weeks1Van Hoorde et al.,
Lactobacillus6.90–7.20Lactococcus7.50–7.70Leuconostoc7.60–7.90South AfricaCommercially manufacturedLactobacillus8.9632 days1Welthagen and Viljoen,
Lactococcus9.1Total plate count9.04Gubbeen
Germany
Traditionally manufactured with commercial starter cultureTotal bacterial count7.316 days1Mounier et al.,
Grana PadanoItaly
Commercially manufacturedLactobacillus4.94–6.229 months1Monfredini et al.,
Lactococcus3.15–6.05ItalyCommercial samplesMeso. streptococci<3>1 year3Gatti et al., Therm. streptococci<3Meso. lactobacilli<3Therm. lactobacilli<3ItalyCommercial samplesMeso. streptococci<33 days ripened1Gatti et al., Therm. streptococci<3Meso. lactobacilli4.4Therm. lactobacilli7ItalyfObtained from manufacturerLactobacillus4.5313 months6Santarelli et al.,
Total viable count7.11HavartiDenmark (Pasteurized milk havarti)Traditionally manufacturedLactococcus5.6912 weeks1Gori et al., Lactobacillus3.65–5.54Denmark (Raw milk Havarti)Traditionally manufacturedLactococcus7.5612 weeks1Gori et al., Lactobacillus6.45–7.75LivarotFranceRetailTotal bacteria count8.58Does not specify1Mounier et al.,
Yeast6.38Limburger
United StatesRetailTotal plate count7.98Within shelf life1Genigeorgis et al., ManchegoSpainRetailLAB4.6–10.03Time of purchase36Garcia et al., Manufactured with commercial starter culture
Lactococcus5.9150 days1Poveda et al.,
Lactobacillus5.5Monterey Jack
United StatesRetailTotal plate count>6.0–8.62Within shelf life4Genigeorgis et al., MozzarellaItalyCommercial SamplesMeso. streptococci6.3< 20 days1Gatti et al., Therm. streptococci7.6Meso. lactobacilli4.3Therm. lactobacilli<3Italy (Buffalo milk)RetailLAB4.82Within expiration date18Pisano et al.,
Italy (Mozzarella Bufala)Commercial samplesMeso. streptococci5.6< 20 days1Gatti et al., Therm. streptococci5.6Meso. lactobacilli4.8Italy (Mozzarella Bufala Campana)Local marketsLAB4.0–7.8Within shelf life3Devirgiliis et al., Italy (Cow milk)Commercially manufactured with commercial starterTherm. lactobacilli4.615 days1De Angelis et al., Meso. lactobacilli4.81Streptococcus7.85Enterococcus3.87Italy (Cow milk)RetailLAB7.08Within expiration date14Pisano et al.,
Muenster
United StatesRetailTotal plate count4.53Within shelf life1Genigeorgis et al., ParmesanItaly (Parmigiano Reggiano)Obtained from manufacturerLAB7.52150 days15Coppola R. et al., Italy (Parmigiano Reggiano)Commercially manufacturedLAB6.182 months1Gatti et al., LAB2.324 monthsItaly (Parmigiano Reggiano)Commercial samplesMeso. streptococci<3>1 year1Gatti et al., Therm. streptococci<3Meso. lactobacilli<3Therm. lactobacilli<3Puzzone di Moena
ItalyTraditionally manufacturedLactobacillus7.1–7.73 months2Franciosi et al., Lactococcus7.5–7.7Pecorino RomanoItalyCommercial sampleMeso. streptococci3.53–10 months1Gatti et al., Therm. streptococci5.5Meso. lactobacilli3.7Therm. lactobacilli3ProvoloneItaly (Piquant provolone)Commercial sampleMeso. streptococci2.5–3.43–10 months2Gatti et al., Therm. streptococci5.4–8.3Meso. lactobacilli2.8– < 3Therm. lactobacilli5.5–7.2Italy (Sweet provolone)Commercial sampleMeso. streptococci< 3–4.33–10 months2Gatti et al., Therm. streptococci4.5–7.1Meso. lactobacilli<3Therm. lactobacilli< 3–7.1Queso Fresco
MexicoObtained from manufacturerMesophilic streptococci6.85–9.07Within 5 days of manufacturer6Renye et al.,
Thermophilic streptococci5.04–9.02Mesophilic lactobacilli7.13–8.99Thermophilic lactobacilli5.01–9.01Leuconostoc5.86–9.23Enterococcus5.05–7.91Serrano
BrazilRetailLactococcus8.60–9.10Within shelf life10Delamare et al., Lactobacillus7.95–9.10StiltonUnited Kingdom
RetailMesophilic LAB8.87Within shelf life16Ercolini et al., Lactobacillus7.76Mesophilic streptococci8.97Mesophilic, anaerobic LAB8.85United Kingdom (blue-veined raw milk cheese)
Obtained from manufacturerLAB6.90–7.41After aging (12 weeks)1Yunita and Dodd,
Lactobacillus4.85–6.18Lactococcus7.83–8.65Swissc, rFranceTraditionally manufacturedPropionibacteria7.5–7.624 weeks2Demarigny et al., Facultatively heterofermentative Lactobacillus7.4–7.9Thermophilic streptococci3.0–5.6Thermophilic lactobacilli2.6–5.9Swiss GruyereItalyCommercial sampleMesophilic streptococci<3>1 year1Gatti et al., Thermophilic streptococci<3Mesophilic lactobacilli<3Thermophilic lactobacilli<3TilsitAustriaObtained from manufacturerTotal bacterial count8.4–9.721 days13Eliskases-Lechner and Ginzinger, Organisms in commercial cheese separated by product.
*
CP, Commercial Products.
**
n.d., not determined.
***
NSLAB, non-starter LAB count.
a
Winter and summer cheese analyzed on surface and in center.
b
Did not support L. monocytogenes surface growth when enumerated.
c
Interpreted from graph.
d
Surface and interior of cheese was analyzed.
e
Lactobacillus count of control cheese (not adjunct culture added).
f
Lb. rhamnosus and Lb. paracasei were the only microorganisms enumerated in all 4 CP.
g
Average of CP.
h
The control from an Edam-like cheese experiment of goat's diet.
i
3 of 4 CP reported “not applicable” (< 5 log cfu/g).
jIndustrial Cheese with commercial starter cultures
k
Pressure treatment of 0.1 MPa.
l
Only licensed cheeses analyzed.
m
Measurement of bacterial growth on cheese surface.
n
Grana Trentino cheese; Measurements from middle section and core.
o
Winter and summer cheese at 30°C.
p
Raw and pasteurized milk cheese.
q
Reported as average of triplicate agar plates.
rRaw and microfiltered milk reported.
Fermented meats
Microbial counts for fermented sausages are shown in Table
. In general, samples were either obtained from retail, directly from manufacturers, or were produced via industrial conditions. Most samples were from the United States, Spain, Portugal, and Italy and were composed of pork and/or beef. The levels of microorganisms (LAB and total) ranged from undetectable (< 102 cfu/g) to 1010 cfu/g. Data were reported as either within the product shelf life or after ripening or maturation of the sausage. Counts of viable microorganisms in sausages from the United States were generally lower (< 107 cfu/g) compared to sausages from other countries. In particular, LAB levels were all < 106 cfu/g. In contrast, several of the European sausages contained high levels of LAB (>108 cfu/g.). European sausages were more often artisan sausages from smaller manufacturers, although similar microorganisms are used in comparison to sausages from the United States.
Table 4
CountryTypeSourceAnalyzed microorganismsCount (log CFU/g)AgeCPReferencesFranceDry fermented sausageObtained from manufacturerLAB6.50–7.74End of drying (9 weeks)1Chevallier et al., GreeceDry fermented sausageObtained from manufacturerLAB7.63–8.2028 days after formulation1Samelis et al.,
Commercially produced
LAB8.1–8.2End of curing period2Papamanoli et al.,
ItalyCiauscolo salamiCommercially produced
LAB7.5End of ripening (45 days)1Aquilanti et al., Yeast5.5Obtained from manufacturerTotal bacteria2.7–5.95End of ripening22Silvestri et al.,
LAB6.77–8.65Fermented Sausage, Friuli Venezia Giulia regionCommercially produced
Total bacteria6.1End of ripening (45 days)1Cocolin et al., LAB8.3Commercially produced
Total aerobic count6.62–9.11End of ripening (21 days)3Comi et al., LAB8.39–8.47Obtained from manufacturerTotal bacteria4.19–9.11End of maturation3Rantsiou et al.,
LAB8.34–8.78Salami bergamascoObtained from manufacturerTotal bacteria6–7.17After maturation of 60 days2Cocolin et al., LAB9–9.14Salami BrianzaLocal marketsMesophilic lactobacilli8.6After purchase1Di Cagno et al., Salami cremoneseObtained from manufacturerTotal bacteria5.17–6.69After maturation of 60 days5Capita et al., LAB7.54–9.38Salami MantovanoObtained from manufacturerTotal bacteria4.23–9.87After maturation of 60 days4Capita et al., LAB7.6–9.38Commercially produced
Lactobacilli8.01–8.73End of ripening (60 days)2Pisacane et al.,
Salami MilanoObtained from manufacturerLAB8.0End of ripening (60 days)1Rebecchi et al.,
Salami NapoliObtained from manufacturer
Mesophilic lactobacilli6.7End of ripening (30 days)1Coppola et al., Commercially produced
Mesophilic LAB5.5End of ripening (41 days)1Coppola S. et al., Salami PiacentinoLocal marketsMesophilic lactobacilli8.3After purchase1Di Cagno et al., Obtained from manufacturer
LAB8.02–8.84End of ripening (63 days)6Połka et al.,
Salami PiedmonteseCommercially producedLAB7.84End of ripening (45 days)1Greppi et al., Salami VarziLocal marketsMesophilic lactobacilli8.6After purchase1Di Cagno et al., Salsiccia Basilicata
Commercially producedLAB4–7.23End of ripening (40 days)10Parente et al.,
Yeast6–6.6Soppressata Basilicata
Commercially producedLAB8–8.4End of ripening (40 days)9Parente et al.,
Yeast5.2–7Soppressata Molisana
Commercially producedLAB8.4End of ripening (28 days)2Coppola et al., Spain and PortugalAlheirasRetailLAB5.9–10.5Within shelf life12Capita et al., ; Ferreira et al., AndrollaObtained from manufacturerTotal aerobic mesophilic bacteria7.81–9.52After 20–30 days of ripening20García Fontán et al., LAB8.78–9.36BotilloObtained from manufacturerTotal aerobic mesophilic bacteria7.63–9.37After 15–20 days of ripening15García Fontán et al., LAB8.34–9.56Chorizo OstrichRetailTotal bacteria7.3Within shelf life8Capita et al., LAB6.23Chorizo DeerRetailTotal bacteria5.46Within shelf life6LAB5.15Chorizo PorkRetailTotal bacteria8.25Within shelf life18LAB8.46Salchicón OstrichRetailTotal bacteria6.09Within shelf life22LAB5.61Salchicón DeerRetailTotal bacteria6.28Within shelf life8LAB6.26Salchicón PorkRetailTotal bacteria8.09Within shelf life19LAB7.5United StatesDry salamiRetailTotal bacteria3–6Does not specify11Acton and Dick, LAB3–5Genoa salamiRetailTotal bacteria3–7Does not specify8LAB2–6Lebanon bolognaRetailTotal bacteria7–8Does not specify5LAB< 3PepperoniRetailTotal bacteria4–7Does not specify14LAB2–6San Francisco dry salamiRetailTotal bacteria6–7Does not specify4LAB3–6Semidry salamiRetailTotal bacteria3–4Does not specify8LAB< 2Summer sausageRetailTotal bacteria3–4Does not specify19LAB4ThuringerRetailTotal bacteria3–7Does not specify13LAB5–6Organisms in commercial sausage products by region.
a
Interpreted from graph.
b
Three seasons were analyzed.
c
Crespone casings and Gentile casings were used.
d
Core and edge data reported.
e
With and without commercial starter cultures.
Fermented vegetables
Microbial counts for fermented vegetables, including sauerkraut, olives, mustard pickles, pickles, and kimchi are summarized in Table
. Fermented cucumbers products were also considered (listed as pickles). Laboratory-manufactured products, using industrial or traditional practices, were included due to the lack of literature on fermented vegetables from retail sources.
Table 5
ProductRegion (Type)Source/Fermentation styleAnalyzed microorganismsCount (log cfu/mL or g)AgeReferencesKimchiTaiwan
SupermarketsAerobic bacteria1–7.2Within shelf lifeTsai et al.,
South KoreaIndustrially produced with a spontaneous fermentation
,
Leuconostoc citreum7.490 daysCho et al., Leuconostoc gasicomitatum8Weissella koreensis8Lactobacillus sakei7.4Retail (online and markets) with starter cultures and spontaneous fermentationsLAB7.14–9.235 days after purchaseKim et al., Obtained from commercial distributors
,
Total viable bacteria7.9–8.34 weeks of fermentationLee et al., LAB7.8–8.3Obtained from commercial distributors
,
Total viable bacteria7.94 weeks of fermentationLee M. et al., LAB7.8Mustard PicklesTaiwan
SupermarketsAerobic bacteria< 1.0–4.2Within shelf lifeKung et al., OlivesGreece (Conservolea naturally black olives)Laboratory manufactured with a spontaneous fermentationLAB count7.930 daysPanagou et al.,
Laboratory manufactured with a commercial starter cultureLAB count830 daysPanagou et al.,
Italy (Bella Di Cerignola -Debittered green table olives)
,
Commercially manufactured with a spontaneous fermentationLAB count5.590 daysDe Bellis et al., Italy (Nocellara del Belice–Spanish-style green olives)
Industrially manufactured with a spontaneous fermentationViable cell count6.58–7.40131 daysAponte et al., Lactobacillus7.21–7.35Lactic streptococci6.49–6.95Italy (Nocellara del Belice–green table olives)Obtained from commercial manufacturer with spontaneous fermentationLAB4.537–10 monthsRomeo et al.,
Portugal (Galega and Cordovil)
Laboratory manufactured with a spontaneous fermentationViable LAB count4.9150 daysSilva et al.,
Southern Spain (Spanish-style green olives)
Industrially manufactured with a spontaneous fermentationLactobacillus5.5120 daysRuiz-Barba and Jiménez-Díaz,
Lactic cocciNVO
120 daysIndustrially manufactured with commercial starter culture
Lactobacillus5.9120 daysRuiz-Barba and Jiménez-Díaz,
Lactic cocci4120 daysUnited States (Sicilian-style green olive–colossal Sevillano olives)
Commercially manufactured with a spontaneous fermentationLAB count7.4200 daysGolomb et al., PicklesIndia
,
Laboratory manufactured with a spontaneous fermentationLAB7.13 daysSingh and Ramesh,
United States
,
Laboratory manufactured with a pure culture fermentationP. cerevisiae8.26–8.77Did not specifyEtchells et al., L. plantarum8.72–8.96L. brevis7.79–8.45SauerkrautUnited States
Commercially manufactured with starter cultureLAB8.310 daysJohanningsmeier et al., Heterofermentative LAB2.7United States
Commercially manufactured with a spontaneous fermentationTotal microbial count760 daysLu et al.,
LAB7Croatia
Laboratory manufactured with a spontaneous fermentationTotal microbial count6.0442 daysBeganović et al., LAB3.7942 daysFinland
Large-scale manufacturing with a spontaneous fermentationLAB7.315 daysViander et al.,
Organisms in fermented vegetables separated by product.
*
NVO, No viable organisms.
a
20 commercial products.
b
Interpreted from graph.
c
Incubation of microorganisms were at 15°C.
d
Three seasons were analyzed.
e
19 out of 44 Chinese cabbage samples (88 total samples using other vegetables) were provided by commercial suppliers.
f
14 CP (Commercial Products).
g
Data from control set (no inoculation) with 8% NaCl.
h
Olive from both irrigated and not irrigated fields.
i
30 cucumber samples were used.
j
Individual fermentations of each microorganism.
k
Fermentations with 4% NaCl.
l
Fermentations with 1.2% NaCl.
Microbial counts for sauerkraut were generally reported as LAB with counts ranging from 103 to 108 cfu/g. Reported samples were for sauerkraut originating from the United States, Finland, and Croatia. Levels of LAB and Lactobacillus were reported for olives produced in Italy, Greece, Portugal, Spain, and the United States. These products contained 104 to 108 cfu/g and were between 30 and 200 days.
Other products for which quantitative data were reported included mustard pickles and kimchi from Taiwan and pickled cucumbers from China, India, and the United States. Microbial counts ranged from undetectable (< 101) to 108 cfu/g. For several of these products, levels of species (e.g., Lactobacillus plantarum, Lactobacillus brevis, and Pediococcus cerevisiae) were reported. Species of Leuconostoc, Weissella and Lactobacillus were also reported for Korean kimchi, where they were generally present between 107 and 108 cfu/g.
Traditional asian fermented products
Another group of fermented foods that contain lactic acid bacteria and other bacteria are those products traditionally manufactured in Asia and that rely on grain or legume substrates. One important difference in the fermentation of these food products compared to other fermented foods is the reliance on fungal enzymes to convert complex carbohydrates to simple sugars. Aerobic conditions are another unique characteristic used in various parts of the fermentation process. Data were collected for several products, including miso, tempeh, fish sauce, and fermented fish (Table
). Similar to the fermented vegetables, there were few reports on products from retail sources. Therefore, laboratory manufactured products made using industrial or traditional practices were included. In general, aerobic bacteria counts of miso ranged from 102 to 107 cfu/g. Similar bacterial counts were reported for fish sauce. LAB counts for tempeh and fermented fish were between 103 to 107 cfu/g with fermented fish being at the lower end of the range.
Table 6
ProductRegion (Type)SourceAnalyzed microorganismCount (log cfu/g)AgeReferencesFermented FishJapan (Funazushi—fermented sushi)Obtained from commercial manufacturerLAB3.48–5.43Does not specifyTsuda et al.,
Fish SauceMalaysia (anchovy)
Obtained from commercial manufacturerAerobic bacteria4.92–5.536–12 monthsZaman et al.,
MisoTaiwan
SupermarketsAerobic bacteria2.1–7.1Within shelf lifeKung et al., JapanLaboratory manufactured with a spontaneous fermentationAerobic bacteria4.315 weeksOnda et al.,
TempehNetherlandsLaboratory manufactured with industrial processes and a spontaneous fermentation
LAB7.01Does not specifyNout et al.,
Shops, production places, and restaurants
,
LAB3–924 h after purchaseSamson et al.,
Organisms present in traditional Asian fermented products separated by product.
a
5 CP.
b
27 CP (Commercial Products).
c
Measure of tempeh and not the soak.
d
81% of samples >107 CFU/g.
e
110 samples were analyzed.
Fermented cereals
Fermented porridges and gruels are widely consumed in many African countries. Here, studies were reported from Burkina Faso, Uganda, Ghana, Benin, Tanzania, and Mexico (Table
). These cereals were made using pearl millet, millet, sorghum, and maize as starting grains. In general, the cereals contained LAB and mesophilic aerobic bacteria with a range of 105 to 109 cfu/g.
Table 7
Product (Region)SourceAnalyzed microorganismsCount (log CFU/g)GrainCPReferencesBen-saalga (Burkina Faso)Obtained from manufacturerTotal aerobic mesophiles7.1Pearl millet12Tou et al.,
LAB7Yeast5.5Bushera (Uganda)MarketsLAB8.1–8.4Millet5Muyanja et al.,
LAB8.4Sorghum5LAB8.9–9Millet and Sorghum5Fura (Ghana)Obtained from manufacturerLAB6.6–8Does not specify8Owusu-Kwarteng et al.,
Koko Sour Water (Ghana)
Obtained from manufacturerLAB8Does not specify3Lei and Jakobsen, Mawè (Benin)Market and manufacturerTotal aerobic mesophiles8.8Does not specify30Hounhouigan et al., LAB8.9Yeast6.4–6.9Pozol (Mexico)
MarketTotal bacteria9.5Does not specify1Omar and Ampe,
LAB9Togwa (Tanzania)
Obtained from manufacturerLAB9Sorghum, maize, millet, and maize36Mugula et al.,
Yeast7Organisms in commercial fermented cereals from Africa and Mexico.
a
Koko is porridge that have been heat treated. Koko sour water is the edible untreated water byproduct.
b
Interpreted from graph. Measured outside and inside of sample in triplicate.
c
Samples were obtained from manufacturer before fermentation.
Beer
Several sour beer products from Belgium, such as lambic and gueuze, were included in the survey (Table
). LAB counts were reported for these products, ranging from 102 to 105 cfu/g. The age of the products reported in the table refers to the longest time the beer was left to age. This maximum aging time was found to range from 40 days to 5 years across the different products.
Table 8
ProductRegionSourceAnalyzed microorganismsCount (log CFU/g)AgeReferencesGueuzeBelgiumObtained from a traditional breweryLAB5.25–5.312 yearsSpitaels et al.,
LAB3.87–3.884 yearsLAB3.49–3.965 yearsLambicBelgiumObtained from a traditional brewery
LAB3.08–4.2624 monthsSpitaels et al.,
Obtained from industrial breweryLAB4.33–4.3812 monthsSpitaels et al.,
Obtained from two breweries
LAB2.3–2.7540 daysMartens et al.,
Organisms in commercial sour beer products.
a
Incubated at 28°C aerobically or 20°C anaerobically on MRS agar.
b
Interpreted from graph.
Fermented tea (kombucha)
Kombucha is a fermented beverage made from sweetened tea to which a specialized culture is added. The latter is comprised of a symbiotic culture of bacteria and yeast or SCOBY, normally within a cellulose-type membrane. Bacteria commonly found in kombucha include the acetic acid bacteria belonging to the genera, Acetobacter, Gluconacetobacter, and Gluconobacter, as well as LAB. Most of the yeasts associated with kombucha are species of Saccharomyces, although other yeast genera may also be present (Teoh et al.,
; Coton et al., ). While this product is now widely consumed, and manufacturers promote the presence of live microorganisms on product labels, there are few published data on the levels of microbes present in retail products. One recent study reported both bacterial and yeast counts for two kombucha products that were produced under industrial manufacturing conditions (Coton et al., ). In general, acetic acid bacteria levels ranged from 106 to 107 cfu/mL at the end of the fermentation, and similar counts were reported for LAB and total aerobic bacteria. Total yeast counts of about 107 cfu/mL were also reported.
Discussion
Food-associated microbes travel and interact in the gut
The human gastrointestinal tract is home to more than 1012 microbes. This diverse ecosystem provides protection against pathogens, extracts nutrients from dietary components, and modulates the immune system (Lozupone et al.,
). The gut microbiota is also very stable, although several factors, including exposure to antibiotics, stress, and disease can disrupt this community, leading to dysbiosis (Sommer et al.,
). The ability of diet and dietary components to modulate the gastrointestinal microbiota, redress dysbiosis, and enhance human health is now well- established (David et al., ; Graf et al., ; Sonnenburg and Bäckhed,
).
Among the food components known to influence the composition of the microbiota are fermentable fibers and prebiotics that enrich for particular members of the gut microbiota. Another route by which the gastrointestinal microbiota may be modulated is via consumption of probiotics—live microbes consumed at a dose sufficient to provide beneficial effects (Hill et al., ). Probiotics, however, are temporary members of the microbiome and rarely persist more than a few days (Tannock,
; Derrien and van Hylckama Vlieg, ; Zhang et al.,
).
Perhaps the easiest and most common way to introduce potentially beneficial microbes to the gastrointestinal tract is via consumption of microbe-containing foods, and fermented foods and beverages, in particular. Like many probiotics, many microbes associated with fermented foods may also have the capacity to survive digestion, reach the gastrointestinal tract, and ultimately provide similar health benefits (Marco et al.,
). When consumed regularly, these fermentation-associated microbes form what some researchers have called the “transient microbiome” (Derrien and van Hylckama Vlieg, ).
In general, the microorganisms present in fermented foods and beverages originate via one of two ways. For so-called natural or spontaneous fermented foods, the microorganisms are autochthonous and are naturally present in the raw material or manufacturing environment. To survive fermentation and processing, the LAB, yeasts, and any other microorganisms present in the finished product must manage a range of selective and competitive pressures, including salt, organic acids, ethanol, anaerobiosis, and low pH. Many of the fermented foods reviewed in this survey, including fermented cereals, sauerkraut, kimchi, and other fermented vegetables, and fermented soy-based products are made by natural fermentation. In addition, many wines and even some fermented sausages and beers are made in this manner.
Other fermented foods rely on the addition of a starter cultures. Cultured dairy products, cheese, and fermented sausages are commonly made using starter cultures. When cultures are used, their selection is based on the performance characteristics specific to the product. In addition, the incubation temperature during fermentation and the nutrient content are usually well-suited to the needs of the microorganisms. In many cases, the culture is added at such high inoculum levels, there would be little competition from other organisms. Collectively, most food fermentation microorganisms are well-adapted to the food environment.
In contrast, once the organisms present in fermented foods are consumed, they become foreign or allochthonous to the gastrointestinal tract. In most cases, they lack the physiological and biochemical resources to compete in this ecological niche. If they survive transit, they do not become stable members of this community (Zhang et al.,
). Nonetheless, the presence of food fermentation-associated microorganisms in the GI tract, even if they are just “passing through,” is now well-documented (Lee et al., ; Walter et al.,
; Dal Bello et al., ; David et al., ; Derrien and van Hylckama Vlieg, ; Zhang et al.,
; Lisko et al., ).
Evidence of health benefits associated with fermented foods
The evidence for the potential health benefits of fermented foods is based on numerous epidemiological as well as clinical reports (reviewed in Marco and Golomb,
; Kok and Hutkins, ). In general, epidemiological studies have shown that consumption of fermented foods is associated with improvements of health status or reductions in disease risk. For example, yogurt-rich diets were associated with a reduced risk of metabolic syndrome in older Mediterranean adults (Babio et al., ). A similar finding was reported in another large cohort study that showed cultured milk consumption reduced the risk of bladder cancer (Larsson et al., ). Yogurt consumption has also been associated with reduced weight gain (Mozaffarian et al.,
). Epidemiological data also suggests that consumption of other fermented foods may be correlated to beneficial health outcomes. Consumption of kimchi and other fermented vegetables, for example, correlated with reduced incidence of asthma and atopic dermatitis in Korean adults (Park and Bae,
; Kim et al., ). Reduced risks of type 2 diabetes and high blood pressure among Japanese adults was associated with consumption of fermented soybean foods rich in phytoestrogens and bioactive peptides (Kwon et al., ; Nozue et al.,
). In contrast, the large European Prospective Investigation into Cancer and Nutrition cohort study from the Netherlands reported no association between fermented foods consumption and overall mortality (Praagman et al.,
).
Although many human clinical studies have assessed the effects of probiotic-containing fermented foods on health biomarkers, fewer randomized controlled trials (RCT) have considered fermented foods alone. Nonetheless, several reports provide evidence that fermented foods, such as kimchi, fermented soy products, and yogurt, can improve relevant biomarkers. For example, kimchi consumption improved fasting blood glucose and other metabolic syndrome symptoms in overweight and obese adults (Kim et al., ), and similar improvements were observed in healthy adults (Choi et al., ). Consumption of a fermented soybean paste also improved plasma triglyceride levels in obese adults (Lee Y. et al., ). Perhaps the strongest evidence is for yogurt and improved lactose tolerance, due to in vivo expression and release of β-galactosidase by the yogurt culture microbes, S. thermophilus and L. delbrueckii subsp. bulgaricus (Kolars et al., ; Martini et al.,
; Pelletier et al.,
; Savaiano,
). This is the only approved health claim approved by the European Food Safety Authority (EFSA Panel on Dietetic Products, Nutrition and Allergies, ).
As noted previously, some fermented foods could impart health benefits even in the absence of live microorganisms in the finished products. For example, in sour dough bread manufacture, LAB may express phytase enzymes that degrade phytates and therefore enhance mineral absorption (Nuobariene et al.,
). In the manufacture of red wine, ethanol produced early in the fermentation enhances extraction of polyphenolic compounds from the grape skins. Fermented foods may also contain vitamins and other bioactive molecules produced in situ from microbial metabolism that are not present in the original food. Recently, Saubade et al. (
) noted that folic acid deficiency is a global health problem and suggested that fermented foods could be a food-based alternative for delivering folic acid to at-risk populations. Although some LAB are able to produce modest levels of folate (Leblanc et al., ), amounts produced in foods may be too low to be reach required levels (Saubade et al.,
). Thus, selection of over-producing strains, as well as combining strains with non-LAB may be necessary to enhance production of this vitamin in foods.
If present, fermentation-derived microorganisms, despite their transient nature, may yet have the potential to influence gut microbiota diversity, structure, and function (Zhang et al.,
). Notably, they may also affect health due to their ability to out-compete pathogens for resources, produce short chain fatty acids from available carbohydrates, secrete anti-microbial agents, contribute to immune homeostasis, and produce vitamins, in situ (Derrien and van Hylckama Vlieg, ).
The number of fermentation-associated microbes depends on region and product age
In this survey, we reviewed the literature for studies that included quantitative data on microorganisms present in commercial fermented food products. To our knowledge, this is the first time that there has been a compilation of the hundreds of previous studies that enumerated microbes in fermented foods from retail samples or commercial products. In general, most of the products for which data were available contained at least 106 cells/mL or g. However, there was considerable variation depending on product age and region, and several relevant bacterial species or groups were present at less than that amount.
Although regular consumption of yogurt is often included in dietary guidelines (Smug et al.,
), recommendations for other fermented foods rarely exist (Chilton et al., ). Likewise, to our knowledge, there are few guidelines for what constitutes a minimum dose of live microorganisms. The one exception is the yogurt health claim for “improved lactose tolerance” that was approved in 2010 by the European Food Safety Authority (EFSA Panel on Dietetic Products, Nutrition and Allergies, ). The claim states that yogurt should contain at least 108 cfu live starter microorganisms per gram- the same count the NYA requires for the “live and active” seal, as noted above.
Even in the absence of a seal or stamp, many commercial yogurt products, as well as kefir, fermented vegetables, and miso, also provide numerical information on their labels. Recently, Derrien and van Hylckama Vlieg () suggested that consumption of 1010 cells would be necessary to induce an effect on the microbiota and host health. This could be achieved by consuming 100 g of fermented food containing 108 cells/g.
According to the results reported in this survey, many commercial fermented food products would be close to meeting this requirement (Figure
). However, several caveats are relevant. First, there was a wide range of reported microbial counts (over several logs) within the various product groups. Some products also reported total LAB, whereas other reported specific genera or species or as thermophilic or mesophilic. Second, for most products, enumeration relied on standard cultural methods for LAB (including medium and incubation conditions), which may have under-estimated more fastidious species. This can be attributed to the high stress conditions of fermented products that can occasionally lead to injured microorganisms that are viable but not culturable.
Figure 1
Finally, the age or time at which the products were analyzed also varied considerably. In general, “fresher” products had higher numbers. These would include yogurt and cultured dairy products, as well as kimchi, sauerkraut, and other fermented vegetables. The counts from the cheeses also varied widely, with the longer aged cheeses (e.g., Parmesan, Grana) consistently having the lowest counts.
Recommendation of fermented foods as part of dietary guidelines
In many cultures, fermented foods containing live microorganisms are consumed on a regular or even daily basis (Hutkins, ). Based on the data reported in this survey, consumption of fermented foods would not only provide important macronutrients, they could also deliver large numbers of potentially beneficial microorganisms to the gastrointestinal tract. For example, if Korean kimchi contains 108 lactic acid bacteria per g (Table
), and given per capita consumption of kimchi is estimated at 100 g per person per day, then the daily consumption of live microbes from kimchi alone would be 1010. Likewise, in the Netherlands, where yogurt consumption is also around 100 g per day, similar levels of microbes (i.e., 1010 cfu per day) would be ingested. These are the doses noted above that can influence the gut microbiota and provide a potential health benefit (Derrien and van Hylckama Vlieg, ).
Recently, the concept of “shared core benefits” was introduced to explain how and why phylogenetically related organisms could deliver similar health benefits (Sanders et al.,
). Thus, although the microbes in fermented foods cannot, by definition, be considered probiotic, many of them are evolutionarily highly related to probiotic organisms, and they often share the same molecular mechanisms responsible for health-promoting properties in probiotic organisms. The application of various omic approaches to understand functional properties of fermentation-derived microbes will also likely reveal new attributes relevant to the health benefits these microbes may provide (Macori and Cotter,
).
In part, this is why several prominent groups have recommended that health care professionals should promote fermented foods containing live microbes as part of public health policy (Ebner et al., ; Sanders et al.,
; Chilton et al., ; Bell et al., ; Hill et al., ). In particular, including fermented foods in dietary guidelines for specific populations has also been recommended. For example, Bell et al. () recently suggested fermented foods should be introduced to children early in life and incorporated into their everyday meal plans. In addition, regular consumption of fermented foods could be especially important for low income, resource-challenged communities that are disproportionally susceptible to gastrointestinal infections (Kort et al., ).
Statements
Author contributions
SR, CK, and RH each contributed 30% to data collection. MH contributed 10% to data collection. SR, CK, and RH wrote the manuscript.
Acknowledgments
This project was funded by the National Dairy Council and facilitated by the International Scientific Association for Probiotics and Prebiotics. We thank Mary Ellen Sanders for her helpful comments.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
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Keywords
fermented foods, live microbes, lactic acid bacteria, health benefits, probiotics
Citation
Rezac S, Kok CR, Heermann M and Hutkins R (2018) Fermented Foods as a Dietary Source of Live Organisms. Front. Microbiol. 9:1785. doi:
Received
13 May 2018
Accepted
17 July 2018
Published
24 August 2018
Volume
9 - 2018
Edited by
Jyoti Prakash Tamang, Sikkim University, India
Reviewed by
Victor Ladero, Consejo Superior de Investigaciones Científicas (CSIC), Spain; Baltasar Mayo, Consejo Superior de Investigaciones Científicas (CSIC), Spain; Fernanda Mozzi, CERELA-CONICET, Argentina
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*Correspondence: Robert Hutkins
This article was submitted to Food Microbiology, a section of the journal Frontiers in Microbiology
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