Effect of Consumption of Animal Products on the Gut Microbiome Composition and Gut Health (2024)

Meat products

The gut microbiome is significantly influenced by diet. In particular, meatproduct consumption affected gut microbiota composition (Table 1). Animal-based diets affect gut microbiotadifferently than plant-based diets (Muegge etal., 2011; Walker et al.,2011; Wu et al., 2011). Dependingon the type of diet, the gut microbiota can change even in a short time, such as3 days. There was no change in alpha-diversity for either animal- or plant-baseddiet, but the animal-based diet significantly improved beta-diversity (David et al., 2014). Another study found nosignificant differences in either the alpha-or beta-diversity of the gutmicrobiota between the animal- and plant-based diets, but did affect thecomposition of the gut microbiota (Kohnert etal., 2021). The meat-rich diet increased Roseburia,Faecalibacterium, and Blautia more thanthe strict vegan diet (Kohnert et al.,2021). High animal protein intake and low carbohydrates also affectedthe reduction of Bacteroides spp. while reducing the abundanceof the butyrate producer Roseburia/Eubacteriumrectale (Russell et al.,2011).

Meat is a major component of an animal-based diet. Meat is classified as follows:red meat (beef and pork), white meat (chicken and fish), and processed meat.Recent epidemiological studies have reported higher mortality risks and certainchronic diseases in groups that consume more red and processed meat (Al-Shaar et al., 2020; Petermann-Rocha et al., 2021). Moreover, the WHO classifiedred meat as group 2A, a probable carcinogen (Bouvard et al., 2015). In a review of more than 800 epidemiologicalstudies, >10 studies found a 17% increased risk of colorectalcancer (CRC) for every 100 g increase in red meat intake. Nevertheless, researchon the effect of meat product consumption on the gut microbiome remains unclear,and evidence on the effect on health is insufficient.

Consumption of red meat affects the gut microbiome. Consuming 200 g of red meatdaily significantly reduced Clostridium sp. (Foerster et al., 2014). However, findingson the health effect of Clostridium sp. are inconsistentbecause the changes that occur at the species level are very distinct. Inaddition, consuming 380 g of beef for 4 weeks affected the reduction ofdiarrheal disease-related Bacteroidesfragilis and the increase of intestinal movement regulatorBifidobacterium adolescentis (Hentges et al., 1977). Meanwhile, there are studiescomparing the effects of red and white meat consumption on the gut microbiome. Abeef-based diet increased the relative abundance ofLachnospira, the Lachnospiraceae NK4A136group, and Ruminococcus 2, whereas the chicken-based diet didnot show significant changes (Zhao et al.,2022). After consuming a beef-based diet, Akkermansiamuciniphila was reduced and blood cell counts were elevated,altering markers associated with inflammation. Replacing the beef-based dietwith a chicken-based diet reduced inflammation-related monocytes and basophils.This appears to be related to the chicken-based diet’s suppression ofBacteroides ovatus, a factor in generating immunoglobulinA. In an intervention study in which pork or chicken was consumed, both groupsaltered the gut microbiota in a similar pattern, with reductions in theBacteroidetes phylum, Bacteroidaceae, andChristencellaceae families (Dhakal et al., 2022). However, in a cross-sectional study observingpork and chicken eaters, high Bacteroidetes levels were foundin the chicken eaters, and differences were observed at the species level (Shi et al., 2021).

It is well-recognized that meat consumption is harmful to persons with diseases.Red meat may increase the gut microbiota’s production of uremic toxinssuch as trimethylamine (TMA) n-oxide (TMAO), indoxyl sulfate, and p-cresylsulfate. These uremic toxins are linked to a higher risk of cardiovascular death(Mafra et al., 2018). In addition,red meat, unlike white meat, is associated with CRC (Sasso and Latella, 2018). This is mainly because of thered-colored heme iron found in large quantities in the muscle myoglobin of redmeat. Heme iron causes direct harm, such as causing cytotoxic damage to colonicepithelial cells, and indirect harm by inducing alterations of the gutmicrobiota (Ijssennagger et al., 2012). Ared meat diet rich in heme iron increases Streptococcusbovis, Fusobacterium,Clostridium, and Helicobacterpylori, which are related to colorectal carcinogenesis (Sasso and Latella, 2018). However, it isunclear whether the increase or decrease in the gut microbiome caused by certainsubstances, such as toxins and heme iron, contributes to diseases.

Meanwhile, in inflammatory bowel disease (IBD)-induced mouse experiments,high-dose red meat induced intestinal microbial imbalance and reduced therelative abundances ofLachnospiraceae_NK4A136_group,Faecalibaculum, Blautia, andDubosiella (Li et al.,2021). This results from a study that contradicts the previoushealthy human study in which beef intake increasedLachnospiraceae_NK4A136_group.Lachnospiraceae_NK4A136_group is abutyrate-producing bacteria that protects the intestinal mucosal and reducesinflammation (Li et al., 2021; Zhao et al., 2022).

Taken together, red, white, and processed meats are all observed to havedifferent effects on the gut microbiome. However, there are currentlyinsufficient studies that compile adequate information to determine consistentchanges in the gut microbiome. In addition, like other food consumption,excessive meat consumption has also been linked in studies to the emergence ofdisease, albeit the exact mechanisms related to alterations in the gutmicrobiome are unknown.

Processed meat products

The WHO classified processed meats as group 1 carcinogens (Bouvard et al., 2015). The consumption of processed meat isknown to increase the incidence of CRC. N-nitroso compounds, such as nitratesused as preservatives in processed meat, are considered the leading cause ofCRC. Moreover, certain microorganisms in the gut can reduce nitrate to nitritethrough metabolic processes (González-Soltero et al., 2020). However, a diet containingprocessed meat and an intake of nitrate-rich water did not show significantchanges in the fecal microbiome (Sinha et al.,2021).

One human study confirmed the correlation between fried meat intake and gutmicrobiota. A randomized controlled trial was conducted for 4 weeks, and the gutmicrobiota of 59 participants in the group treated with fried meat and 58participants in the control group with restricted fried meat intake werecompared. In the gut microbiome of the fried meat intake group,Lachnospiraceae and Flavonifractordecreased, and Dialister, Dorea, andVeillonella increased (Gaoet al., 2021).

There are two studies in rats on the correlation between consuming sausage andthe modulation of gut microbiota. In one study, rats were fed for 4 weeks on oneof three diets: inulin-fortified pork sausage, control pork sausage, or standardchow diet. Rats in the inulin-fortified pork sausage group had increasedabundances of Actinobacteria, unclassifiedLachnospiraceae, Erysipelotrichaceae, Bifidobacterium, andBacteroides uniformis. In addition, unlike conventionalsausages, the sausage fortified with inulin showed similar effects to thegeneral dietary fiber intake, such as increasing short-chain fatty acid (SCFA)and Bifidobacteria (Thøgersen et al., 2018). In a subsequent study, rats were fedfor 4 weeks on one of four diets: control sausage, sausage with added inulin andcalcium, sausage with added inulin, and sausage with added calcium. In the gutmicrobiota of the two groups of rats fed the calcium-rich sausage andcalcium-added inulin-fortified sausage, Firmicutes increased,and Bacteroidetes decreased at the phylum level. At the genuslevel, Ruminococcaceae and Staphylococcus wereincreased in both groups, and in particular, Bifidobacteriawere increased in the intestinal microflora of rats in the group fed sausagescalcium-rich and fortified with inulin (Thøgersen et al., 2020).

Acorn-fed Iberian ham is a traditional cured meat product. A study was conductedon changes in gut microbiota caused by an acorn-fed ham diet using rats as anexperimental model. The acorn-fed ham diet had a lower carbohydrate content andhigher protein content than that of the control diet, resulting in increasedproteolytic metabolism-related Bacteroidetes andProteobacteria and decreased saccharolyticmetabolism-related Firmicutes at the phylum level. In addition,Dorea, Phascolarctobacterium, orButyricimonas, which are highly related to ulcerativecolitis disease, were decreased at the genus level (Fernández et al., 2020).

In conclusion, consumption of different types of processed meats can causechanges in the gut microbiome. However, processed meat consumption was notassociated with adverse changes in the gut microbiome, such as an increase inpathogenic bacteria or dysbiosis. These results show that there is no clearcausal link between processed meat consumption and adverse health effects ofchanges in the gut microbiome.

Meat protein

Proteins can show different changes in the composition of the intestinalmicrobiota depending on the type, such as plant and animal origin. Animalfood-originated protein is a great source of nutrients and can affect thecomposition of the gut microbiome (Lang et al.,2018). However, no human study has directly tested the effect of meatprotein intake on the modulation of the gut microbiome; however, there have beenanimal studies.

In one study using a rat model, the effect of various dietary proteins, such asplant (soy), dairy (casein), red meat (beef and pork), and white meat (chickenand fish) proteins, on the composition of gut microbiota was assessed (Zhu et al., 2015). At the phylum level,the group fed white meat protein had a higher abundance ofFirmicutes but lower Bacteroidetes thanthe other groups. Conversely, the chicken protein-fed group had a higherabundance of Actinobacteria, and the rats fed beef protein hada higher abundance of Proteobacteria. At the genus level,Ruminococcaceae and Lactobacillaceae wereabundant in the group fed red meat protein, andLactobacillaceae were more abundant in the group fed whitemeat protein. Consumption of meat protein reduced serumlipopolysaccharide-binding protein (LBP) compared to soy protein. Typically, thepresence of LBP in the blood is regarded as a biomarker of an inflammatoryreaction. This may be related to the composition of the gut microbiome.Bacteroidetes are major lipopolysaccharide (LPS)-producingbacteria, which are reduced by consuming meat proteins. Therefore, casein andmeat protein intake may help maintain gut microbiome balance and reduce antigenload and inflammatory response. In addition, when comparing each group, meatproteins, mainly white meat proteins, contained moreLactobacillus than non-meat proteins (casein, soy).Lactobacillus is well known as representative probioticbacteria. In other words, the recommended level of meat protein intake couldhelp the growth of beneficial intestinal bacteria such asLactobacillus (Zhu et al.,2015).

White meat-originated protein consumption has been linked to alterations in thegut microbiome in two rat model studies. Zhu et al. compared the feces of4-week-old and 64-week-old rats fed a chicken protein diet. The results showedthat the gut microbiome composition differed significantly between young andmiddle-aged mice. At the phylum level, Firmicutes decreased formiddle-aged rats but increased for young rats. However, the level ofBacteroidetes increased for middle-aged rats and decreasedfor young rats. At the genus level, the relative abundance of the beneficialbacterium Lactobacillus increased by chicken protein in theyoung group. In contrast, it had the opposite effect in the middle-aged group(Zhu et al., 2016a). In anotherstudy, the relative abundance of Lactobacillus was higher inthe chicken protein group than in the casein control group; it also showed thehighest levels of organic acids, including lactate, which can promote the growthof Lactobacillus (Zhu et al.,2017).

A. muciniphila is considered a next-generation probioticbacteria (Ross, 2022). It playssignificant roles in lipid metabolism and enhances intestinal immune function toprevent obesity, IBD, and diabetes (Rodrigues etal., 2022). In a study that compared the effects of soy and chickenprotein-based diet intake on the composition of intestinal microbiota using agerm-free mice model, compared to a soy protein-based diet, a chickenprotein-based diet helped the growth of A. muciniphila andmaintained mucus barrier function and intestinal homeostasis (Zhao et al., 2019b).

Overall, red meat proteins can modulate the alteration of the gut microbiome in adirection that reduces LPS-producing bacteria. White meat protein may helpmaintain gut homeostasis by increasing Lactobacillus orA. muciniphila levels. However, numerous perspectives onthe gut microbiota of meat protein consumption have been reported in priorresearch. Therefore, more research is required to provide clear scientificevidence.

Dairy products

Investigations have examined how dairy products, including milk, yogurt, andcheese, affect the gut microbiome (Table2). Two studies reported the effects of the quantity of dairyproducts on the gut microbiota. Swarte et al.(2020) divided 46 healthy overweight adults into high-dairy diet(HDD) and a low-dairy diet (LDD) groups for 6 weeks. HDD showed relativelyhigher Streptococcus, Leuconostoc, andLactococcus abundances and lowerFaecalibacterium and Bilophila abundances.At the species level, the abundances of Streptococcusthermophilus and Leuconostoc mesenteroides wereincreased; however, Faecalibacterium prausnitzii andClostridium aldenense were decreased. Predicted metabolicpathways were also studied; however, there were no significant changes by HDD(Swarte et al., 2020). Alternatively,a randomized controlled trial was performed in one human study for 24 weeks;however, there was no significant change in gut microbiota composition ordiversity according to the difference in dairy intake (Bendtsen et al., 2018).

Another human study analyzed the correlation between consuming whole milk and gutmicrobiota. In the 3-month randomized, double-blind study, 24 of 64 maleparticipants received 500 mL of bovine milk daily. Then, the relative abundanceof members in the phylum Proteobacteria significantlyincreased. At the genus level, Lactobacillus andRoseburia tended to increase, whereasPrevotella decreased (Fernandez-Raudales et al., 2012).

There was more research on yogurt intake and gut microbiota change than on otherdairy products. First, three cross-sectional studies were identified from eachcohort study performed in France, Spain, and the United Kingdom. Thirty healthyadults who consumed at least 200–400 g of yogurt daily had significantlylower Enterobacteriaceae levels than those who did not consumeyogurt daily. Although there was no difference in the intestinal SCFAconcentration between the groups, β-galactosidase activity wassignificantly increased in the yogurt intake group (Alvaro et al., 2007). In another study, annual dietaryfermented food intake was investigated by a food frequency questionnaire (FFQ)from 130 people. Natural yogurt consumers showed significantly higher fecallevels of Akkermansia, and sweetened yogurt consumers displayedsignificantly lower fecal levels of Bacteroides. Additionally,cheese consumers presented significantly higher levels of the major fecal SCFAs(acetate, propionate, and butyrate; González et al., 2019). According to another FFQ survey from4,117 participants, >73% consumed 125 g of yogurt at least onceweekly and had higher abundances of Bifidobacterium animalissubsp. Lactis and S. thermophilus (Le Roy et al., 2022).

In a study of 36 healthy adult women who consumed fermented milk for 4 weeks, nosignificant changes in gut microbiota were found (Tillisch et al., 2013). Similarly, six healthy adults whoconsumed yogurt for 6 weeks showed no significant changes in gut microbiotacomposition or diversity (Lisko et al.,2017). However, unlike these two studies, most studies found thatconsuming fermented dairy products affected gut microbiota, particularlyLactobacillus and Bifidobacterium.Fermented milk intake was associated with increased intestinalLactobacillus (particularly Lactobacillusacidophilus) and Bifidobacterium (Link-Amster et al., 1994). It was alsoconfirmed that the intestinal Bifidobacterium increased, whileRoseburia decreased after consuming fermented milk (Volokh et al., 2019). In addition, threerandomized, double-blind studies found that yogurt intake affected the increasein intestinal Lactobacillus spp. Specifically, consuming 400 gof yogurt daily for 2 weeks was associated with increased intestinalLactobacillus delbrueckii spp. bulgaricusand Streptococcus salivarius spp. thermophiles(Burton et al., 2017). One studyfound that yogurt consumption increased Lactobacillus paracaseiand Lactobacillus rhamnosus but did not affect alpha- orbeta-diversity (Alvarez et al., 2020). Theincreased L. rhamnosus in this study has been shown to improvethe immune response in another study (Kang etal., 2021a). García-Albiach etal. (2008) reported that yogurt consumption increased the intestinaldensity of lactic acid bacteria (LAB) and the pathogen Clostridiumperfringens (García-Albiachet al., 2008). Similarly, fermented milk intake increasedFirmicutes and decreased Bacteroidetes atthe phylum level (Unno et al., 2015).

Consumption of fermented dairy products also inhibits pathogens in pathologicalconditions. In 38 H. pylori-infected children, when 200 mL ofyogurt was consumed daily for 4 weeks, the representative pathogenEscherichia coli decreased, and the beneficial bacteriaBifidobacterium spp. increased (Yang and Sheu, 2012). Additionally, fermented milkconsumption decreased Bilophila wadsworthia levels in patientswith IBD, which is a strain known to cause IBD by inducing barrier collapse byproducing hydrogen sulfide. Meanwhile, the intake of fermented milk increasedintestinal SCFA concentration and significantly increased the level ofbutyrate-producing bacteria. Among SCFAs, butyrate is particularly helpful instrengthening the gut barrier (Veiga et al.,2014). Kefir intake significantly increased the abundance ofLactobacillus in the gut microbiota of patients with IBD(Yılmaz et al., 2019).Another study showed that ingestion of kefir increased the relative abundance ofActinobacteria but had no significant effect onBacteroidetes, Proteobacteria, orVerrucomicrobia (Bellikci-Koyu et al., 2019).

Cheese is a high-protein-containing dairy product, a densely nutrient-rich solidfood, unlike raw milk or yogurt. Four studies reported the effect of cheeseconsumption on gut microbiota. When 13 female adults consumed 30 g of Bryndzacheese daily for 4 weeks, there was no change in alpha-diversity; however, therelative abundance of LAB (Lactobacillales,Streptococcaceae, Lactococcus, andStreptococcus) significantly increased. Additionally, SCFAproducers such as Phascolarctobacterium andButyricimonas increased significantly in Bryndza cheeseconsumers (Hric et al., 2021). A humanpilot study of Parmesan cheese consumption for 7 days showed thatBifidobacterium mongoliense strains from cheese couldtransiently colonize the human gut (Milani etal., 2019). In two studies of Camembert cheese intake affecting gutmicrobiota, higher Enterococcus faecalis, L.lactis, and L. mesenteroides levels were found infecal samples (Firmesse et al., 2007;Firmesse et al., 2008).

In conclusion, intake and types of dairy products are important gutmicrobiome-changing factors. A higher dairy product intake increases theintestinal Lactobacillus and Bifidobacteriumlevels. In H. pylori infection or IBD condition, consumingfermented dairy products may help hosts suppress the pathogen proliferation.Most reported studies have confirmed that consuming dairy products can improvehost health by increasing the number of beneficial bacteria in the gut.

Dairy protein

Numerous studies are underway to determine why consuming dairy products altersthe gut microbiome. Dairy nutrients have been the subject of several studies(Ha et al., 2021; Lim et al., 2020). It is also used toenhance the quality of other foods (Kang et al.,2021b). Several studies have examined how dairy proteins affect thegut microbiome. The gut microbiome of rats changed according to the intake ofmilk protein. When 14% or 53% of whole milk protein was fed torats, there were changes in microbiota composition, such as a decrease in genecopy numbers in Clostridium coccoides and Clostridiumleptum groups in the high protein group compared to that in thenormal protein group (Liu et al., 2014).However, studies on casein or whey proteins have been increasing. Casein andwhey proteins are known as the main proteins in milk. In particular, caseinconstitutes approximately 80% of the total protein in milk, while wheyprotein accounts for approximately 20% (Davoodi et al., 2016).

One study fed casein to mice for 2 weeks. The abundance ofBacteroidetes at the phylum level significantly increasedin the casein-treated group, while Lachnospiraceae andRuminococcaceae decreased at the family level, andParabacteroides and Bacteroides increasedat the genus level (Kim et al., 2016).Other studies have also shown that the gut microbiome changes when high caseinconcentrations are ingested. When the rats were fed diets containing either19.4% or 52% casein for 24 weeks, the gut microbiota of the groupsfed high casein concentrations were altered. At the phylum level, there was arelative expansion of Actinobacteria and a relative contractionof Saccaribacteria. At the genus level, there was an expansionof Bifidobacterium, Bacteroides,Parabacteroides, and Oscillospira (Snelson et al., 2021). Alternatively,another study reported that changes in the gut microbiota caused by a highcasein intake could be detrimental to intestinal health. This is because therelative abundance of pathogens in the colon increased in the 54%high-concentration casein intake (HCD) group compared to that in the normalintake (20% casein; NCD) group.Escherichia/Shigella,Enterococcus, Streptococcus, andsulfate-reducing bacteria increased >2–5 times in the HCD groupcompared to the NCD group. In contrast, Ruminococcus,Akkermansia, and F.prausnitzii, which are generally regarded as beneficialbacteria in the large intestine, were reduced (Mu et al., 2016). In another study, the number of E.coli increased in the HCD group, whereas bacteria that protectintestinal epithelium (A.muciniphila, Bifidobacterium),propionate-producing bacteria (Prevotella), butyrate-producingbacteria (Roseburia/Eubacteriumrectale), and acetate producing bacteria(Ruminococcusbromii), were reduced (Mu etal., 2017). However, studies remain insufficient to suggest thatchanges in the gut microbiota caused by a high casein intake may be detrimentalto gut health.

Conversely, casein is a non-meat protein that changes gut microbiota close to soyprotein, and there was no difference in alpha- and beta-diversity between humangroups consuming casein or soy protein (Beaumontet al., 2017). In animal experiments, casein intake was similar tothe gut bacteria composition of soy protein-treated groups rather than chicken,beef, and fish protein-treated groups. One study showed that casein consumptionwas related to the relative abundance of Lachnospiraceae (Zhu et al., 2016b). Similar to this study,rats fed with soy protein and casein had similar gut bacterial profiles at thefamily level that was characteristic of Lachnospiraceae (Zhu et al., 2015). Members of theLachnospiraceae family are known to protect the gut againsthuman colon cancer by producing butyrate. Additionally, the lower relativeabundance of Lactobacillus is associated with casein intake(Rist et al., 2014; Zhu et al., 2015; Zhu et al., 2016b).

Whey protein affects gut microbiota composition differently compared to casein.When high-fat diet mice were treated with casein or whey protein, differences inbeta-diversity were observed between groups (Boscaini et al., 2019). Another study showed a significantly higherproportion of Streptococcaceae at the family level in the groupfed a diet containing casein as the primary protein source (Boscaini et al., 2019; Boscaini et al., 2020; Nilaweera et al., 2017). In addition, highproportions of Lactobacillus andBifidobacterium were mainly observed in the group thatconsumed whey protein (Boscaini et al.,2019; Boscaini et al., 2020;Boudry et al., 2013; McAllan et al., 2014; Schaafsma et al., 2021; Sprong et al., 2010). The combination ofLactobacillus and Bifidobacterium has beenmentioned in one study as a potential candidate strain to be used for immuneenhancement, thus an increase in the proportion ofLactobacillus and Bifidobacterium in thegut microbiome could potentially associated with immune enhancing effects (Yu et al., 2022). In two studies byBoscaini et al. comparing casein and whey protein, at the family level, therelative abundance of Streptococcaceae was higher in the caseingroup, and the relative abundance of Lactobacillaceae washigher in the whey protein group. At the genus level, the relative abundance ofLactococcus was higher in the casein group, and therelative abundances of Parabacteroides,Lactobacillus, and Bifidobacterium werehigher in the whey protein group (Boscaini etal., 2019; Boscaini et al.,2020). In a study by Nilaweera et al.(2017) casein intake increased the proportion ofEnterobacteriaceae and Streptococcaceaecompared to the whey protein intake group (Nilaweera et al., 2017). Compared to casein, cheese whey proteinincreased fecal Lactobacilli andBifidobacteria counts in a colitis-induced rat model (Sprong et al., 2010), and a lactoperoxidaseand lactoferrin-enriched whey protein isolate increasedLactobacillaceae/Lactobacillus anddecreased Clostridiaceae/Clostridium inhigh-fat diet-fed mice (McAllan et al.,2014). In a human study to examine sleep quality and stress, those ona whey protein-based diet had significantly increased relative abundances ofBifidobacterium compared to the casein intake group (Schaafsma et al., 2021). Whey peptideextracts with a molecular weight of <1 kDa increasedLactobacillus spp. and Bifidobacteriumspp. (Boudry et al., 2013).

In conclusion, a long-term high-protein diet causes gut microbiota imbalance andincreases intestinal permeability. However, normal levels of casein intakeconstitute a gut microbiome that regulates the Lachnospiraceaefamily similarly to soy protein. Changes in the gut microbiome by whey proteinintake increased beneficial bacteria such as Lactobacillus andBifidobacterium, similar to the changes in the intake ofdairy products.

Egg products

We summarized previous studies on the impact of egg products and their proteinson the composition and function of the gut microbiome (Table 3). Eggs have different effects on the gut microbiomedepending on the species and processing method. There are studies on hen eggwhite (HEW), duck egg white (DEW), and preserved duck egg white (PEW) using ratsas experimental models. Akkermansia andPeptostreptococcaceae were relatively high in abundance inthe HEW and DEW groups, respectively. In the PEW group, the intestinal microberichness was significantly lower than that of other groups, and in particular,compared to DEW, Proteobacteria abundance was relatively low.Egg consumption effects on gut microbes may differ depending on the egg type andprocessing method (Yu et al., 2020).

In a study comparing the effects of duck eggs and preserved duck egg intake onchanges in gut microbial composition using rats as experimental models, theingestion of preserved duck eggs increased the α-diversity of gutmicrobes compared to the duck egg group. There was no significant difference atthe phylum level; however,Firmicutes/Bacteroidetes were decreased.At the genus level, Veillonella,Phascolarctobacterium, Alpinimonas,Coprococcus 3, Coprococcus 2,Gelria, and unclassified Methylocystaceae,which were not found in the duck egg group, were found (Meng et al., 2020).

Egg yolk is a food ingredient commonly used in various processed foods. A studyusing the mouse as an experimental model found that Firmicutesand Epsilonbacteraeota were relatively decreased at the phylumlevel when egg yolk was fed. In addition, Lachnospiraceae andRuminococcaceae were significantly reduced at the familylevel, and Erysipelotrichaceae was significantly increased. Atthe genus level, Parasutterella andCoprostanoligenes showed a relatively high abundance (f*ckunaga et al., 2020).Parasutterella has been defined as a core component of thehuman and mouse gut microbiota and has been correlated with bile acidmaintenance and cholesterol metabolism (Ju etal., 2019). Coprostanoligenes is a bacteria that caninfluence host cholesterol levels. Therefore, these results indicate that eggyolk consumption can induce changes in gut microbiota related to cholesterolmetabolism (Kenny et al., 2020).

In a study on the change in gut microbes by comparing the gut microbes of obeseand lean rats and treating the obese rats with egg white hydrolyzed with pepsin(EWH), the gut microbe composition of obese and lean rats showed significantdifferences at the phylum and genus levels. However, in the gut microbiomecomposition of obese rats fed EWH,Lactobacillus/Enterococcus andC.leptum were similar to those of lean rats. Conversely, thechange in the microbial composition observed after ingestion of EWH did not showthe final weight loss effect in obese rats. Thus, this study suggests that,although consumption of EWH can induce changes in gut microbiota composition, itmay have difficulty elucidating the direct link between changes in gutmicrobiota composition and its effects on metabolism and health (Requena et al., 2017).

Unlike consuming only eggs compared to consuming eggs with prebiotic fibertogether, the results of cecal microbiota were changed in 111 species’abundance. The abundances of Actinobacteria,Deinococcus-Thermus, Deferribacteres, andVerrucomicrobia were relatively higher than that of thecontrol, and the abundance of Firmicutes species was relativelyless than that of the control group. These changes in bacterial composition arecorrelated with the production of plasma metabolites, such as plasma butyricacid, propionic acid, and other metabolites derived from carbohydrate, protein,and fat metabolism, in an obese male rat model (Avirineni et al., 2022).

Choline contained in eggs can produce TMA by enzyme reaction of intestinalmicrobes, and TMA can be converted into harmful substances which may triggermetabolic diseases such as TMAO (Salzano et al.,2022). In patients with metabolic syndrome, intestinal microbiota andtheir correlation to metabolites were the subject of a study on the impact ofegg consumption. It was found that there was no significant effect on microbialdiversity or abundance of taxa (Thomas et al.,2022). Phosphatidylcholine and choline bitartrate are two differentforms of choline. Phosphatidylcholine is a type of choline derived from soybeanand egg yolk. Choline bitartrate is a type of choline produced through chemicalsynthesis (Smolders et al., 2019). Therewas no significant difference between the baseline group, the group withphosphatidylcholine provided by eggs, and the group with choline bitartratesupplement. There was no significant correlation in the correlation analysisbetween intestinal microflora and TMAO. These results suggest that cholinesupplied from eggs may not be a major influencer on TMAO production (Thomas et al., 2022).

Whole egg consumption increased plasma choline and betaine in overweightpostmenopausal women with mild hypercholesterolemia; however, it did notincrease plasma TMAO or alter gut microbiota composition, such asPrevotella, Anaeroplasma,Clostridium, and Peptostreptococcaceae,which are associated with TMAO concentrations (Zhu et al., 2020). In addition, whole egg consumption is believed tocause an increase in cholesterol and thereby induce cardiovascular disease.However, consuming two eggs daily for 2 weeks without changing their usual dietin people at low risk of developing metabolic diseases did not cause any changesin the gut microbiota. However, it rather positively modulated the functions ofthe gut microbiota, improving vascular health and intestinal function (Liu et al., 2022a).

Egg protein

Egg protein refers to the protein found in eggs, which is a complete proteincontaining all essential amino acids needed by the human body (Puglisi and Fernandez, 2022). One of theegg protein-derived peptides, Isoleucine-Arginine-Tryptophan (lle-Arg-Trp; IRW)and Isoleucine-Glutamine-Tryptophan (lle-Gln-Trp; IQW), reduce tumor necrosisfactor (TNF)-induced inflammatory responses and oxidative stress in endothelialcells (Majumder et al., 2013). In onestudy, consumption of the egg protein transferrin-derived peptides IRW and IQWincreased the ACE and Shannon index but decreased the Simpson index in obesemice induced by a high-fat diet. In addition, administration of IRW and IQWreduced the relative abundances of Firmicutes andParabacteroides, and IRW increased the abundance ofBacteroides, known as the major microorganisms that exhibitanti-obesity effects in the intestine. This study showed that ingesting eggprotein-derived peptides alleviates high-fat diet-induced obesity byreprogramming the gut microbiome (Liu et al.,2022b).

Egg yolks and egg whites have different nutritional compositions. Compared to eggyolk, egg white has a relatively low percentage of fat and proteins. In adextran sulfate sodium (DSS)-induced colitis mouse model study, 200 mg/kg bw ofegg white peptide ingestion decreased Ruminiclostridium andsignificantly increased Lactobacillus andCandidatus_Saccharimonas in the gutmicrobiome compared to the DSS group. In the correlation analysis,Lactobacillus andCandidatus_Saccharimonassignificantly reduced pro-inflammatory cytokines such as interleukin(IL)-1β and TNF-α. This indicates that the ingestion of egg whitepeptides can alleviate colonic inflammation by increasing the relative abundanceof beneficial bacteria and reducing pro-inflammatory cytokines (Ge et al., 2021). Ovotransferrin (OVT) isan egg white protein well known to have a wide range of biological activities,such as anti-inflammatory, antioxidant, and immunomodulatory functions (Lee et al., 2021). In a clinical study, adiet with OVT positively affected gut health by increasing the proportion ofAkkermansia, which promotes host immune regulation andintestinal epithelial cell integrity at the genus level of the gut microbiota(Zhang et al., 2020).

Conversely, in a study comparing the cecum microbiota of rats ingesting soy,milk, meat, fish, and egg proteins, along with oligosaccharides,Erysipelotrichaceae, Ruminococcaceae, andLachnospiraceae were the most abundant families in eggprotein and cellulose-fed rats. Erysipelotrichaceae,Bifidobacteriaceae, and Lachnospiraceaewere the most abundant families in egg protein and raffinose-fed rats,respectively (Sivixay et al., 2021).Erysipelotrichaceae, which was most abundantly increasedthrough the consumption of egg protein and prebiotics, is a characteristicbacterium that is decreased in patients with atopic dermatitis and increased inpatients with remission of the disease. For example,Erysipelatrichaceae_ UCG-003 is a potentialprobiotic used in a probiotic formula along with other beneficial bacteria andprebiotics (Wang et al., 2022). Theseresults indicate that the growth of Erysipelotrichaceae, whichcan have a positive effect on atopic dermatitis, can be promoted by egg protein(Sivixay et al., 2021).

The authors declare no potential conflicts of interest.

This article does not require IRB/IACUC approval because there are no human andanimal participants.

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