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Review

The Role of Early Life Microbiota Composition in the Development of Allergic Diseases

by
Maimaiti Tuniyazi
,
Shuang Li
,
Xiaoyu Hu
,
Yunhe Fu
* and
Naisheng Zhang
*
Department of Clinical Veterinary Medicine, College of Veterinary Medicine, Jilin University, Changchun 130062, China
*
Authors to whom correspondence should be addressed.
Microorganisms 2022, 10(6), 1190; https://doi.org/10.3390/microorganisms10061190
Submission received: 12 May 2022 / Revised: 2 June 2022 / Accepted: 7 June 2022 / Published: 9 June 2022
(This article belongs to the Section Medical Microbiology)
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Abstract

:
Allergic diseases are becoming a major healthcare issue in many developed nations, where living environment and lifestyle are most predominantly distinct. Such differences include urbanized, industrialized living environments, overused hygiene products, antibiotics, stationary lifestyle, and fast-food-based diets, which tend to reduce microbial diversity and lead to impaired immune protection, which further increase the development of allergic diseases. At the same time, studies have also shown that modulating a microbiocidal community can ameliorate allergic symptoms. Therefore, in this paper, we aimed to review recent findings on the potential role of human microbiota in the gastrointestinal tract, surface of skin, and respiratory tract in the development of allergic diseases. Furthermore, we addressed a potential therapeutic or even preventive strategy for such allergic diseases by modulating human microbial composition.

1. Introduction

In recent decades, allergic diseases such as asthma, atopic dermatitis (AD), and food allergy (FA) have become a major healthcare issue in many Western countries and developed nations around the world [1,2]. Studies have identified that genetic and environmental factors are the main causes of allergic diseases [3,4]; the topic, however, needs more exploration.
Allergy is positively related to the degree of development of human society, where living environment and lifestyle are most predominantly distinct [5,6]. Such changes include urbanized and industrialized living environments with overused hygiene products and antibiotics, coupled with stationary lifestyles and fast-food-based diets. All such factors result in reduced microbial diversity in early life [7], which, according to ecosystem theory, leads to impaired immune protection and to slow recovery of normal microbial communities [8].
Human microbiota has become an increasingly popular area of study due to its role in host physical and mental health and metabolism [9,10]; it comprises of bacteria, viruses, fungi, protozoa, and archaea. Although human microbiota can be found in the oral and nasal cavity, on surfaces of the skin, and in the respiratory and reproductive tracts [11], it primarily colonizes the gastrointestinal tract. Accumulating evidence indicates that human microbiota plays an important role in the development and prevention of allergic diseases [12]. Commensal microbial communities in the gastrointestinal tract and other organs have shown to modulate both innate and acquired immune responses via various axes, including the gut–lung axis and the gut–skin axis. Recent studies showed that numerous environmental factors can affect microbiota colonization, composition, and metabolic activity in early life, and modify the host functions digestion and nutrient absorption for host energy production and immune modulation and protection [13,14,15,16]. Naturally, early life microbiota colonization with healthy microbiota with proper diversity and abundance is a critical factor in the later development of immune protection in infants. In contrast, dysbiosis of the microbial community is associated with greater disease susceptibility and immune-related disorders later in life, including allergic diseases [12,17,18].
Bacteria, previously, were considered as pathogens; however, it is evident that they have a crucial role in host physiology [19]. Recent advances in culture-independent DNA-sequencing technology (i.e., 16S rRNA sequencing) and data analysis methods have revealed that every part of the human body is colonized with different microbial species, which play a complex role in the pathogenesis of FA [20], AD [21], and asthma [22]. In this paper, we aimed to review recent findings on the potential role of the human microbial community in the gastrointestinal tract, the surface of the skin, and the respiratory tract in the development of allergic diseases. Furthermore, we addressed a potential therapeutic or even preventive strategy for such allergic diseases by modulating human microbial composition.

2. Maternal Influencing Factors for the Development of Allergic Diseases in Infants

Numerous studies have shown that microorganism colonization begins in mammals during birth, and its composition can be influenced by several prenatal and postnatal environmental and host-related factors that have vital roles in the development of a healthy immune system. Among such factors (Figure 1), delivery methods (vaginal or cesarean section delivery) [23,24,25], feeding choices (breast or bottle feed) [26], antibiotic or probiotic use [27,28], and other processes of early gut microbiota modulation by vaginal fluid or fecal microbiota transplantation (FMT) [29,30,31] can dramatically change the gut microbiota composition and modulate the infant’s immune development and tolerance to different antigens. Delivery mode determines the colonization of early life microbiota in infants. For example, babies born by cesarean section lack commensal microbial communities that can be found in vaginal-born infants [32]. Instead, such delivery approaches result in colonization of pathogenic bacteria such as Enterococcus, Enterobacter, and Klebsiella species that are typically found in the hospital environment [33]. Although such a microbial gap is mainly closed after 6 to 9 months of breastfeeding (except for Bacteroides, which remain absent or at a very low level in most cesarean-section infants), cesarean-section delivery can increase the susceptibility of respiratory infectious disease in the first year of life, which is determined by the first week of microbial colonization [34].
Only naturally born infants have gut microbiota similar to their mother’s vaginal microbial community; infants born by cesarean section have gut microbiota similar to their mother’s skin microbiota instead [48]. For example, at an early age, infants have microbiota that are similar to their mother’s vaginal microbial community which mainly consist of Lactobacillus species, suggesting that the infants might have obtained a certain part of their microbiota from the birth canal during birth [49]. However, it has also been reported that Lactobacillus and Streptococci are found in high numbers in a mother’s milk [50], indicating breastfeeding has a significant impact on an infant’s gut microbial composition. Weaning (breastmilk) plays a role as an additional inoculum of the infant gut [51], which not only has microbes but also enriches bacterial species such as Bifidobacterium (utilizing nutrients in breastmilk). These bacteria, as the first arrivals in the infant intestinal tract, consume all the oxygen and create a suitable anaerobic condition for further colonization by other species that are characteristic in the healthy adult gut microbial community. Microbial communities in babies that are born vaginally and fed with breast milk are termed as having relatively healthier microbiomes with the highest abundance of Bifidobacteria and the lowest number of opportunistic pathogenic bacteria such as Clostridium difficile and Escherichia coli [50,52,53,54,55].
Early life antibiotic use both in pregnancy and the postnatal stage influences the establishment of normal infant gut microbiota and increases the development of allergic diseases [56,57]. Infants from mothers exposed to antibiotics during delivery showed decreased microbial diversity compared to non-exposed infants. The microbiota of infants exposed to antibiotics was characterized by a decreased abundance of Bacteroidetes and Bifidobacteria, with a concurrent increase of Proteobacteria, which were most pronounced in terms of vaginally born infants. Furthermore, antibiotics administered during pregnancy and labor have been associated with an elevated risk of AD [58] and asthma [59,60].
Probiotics, vaginal, and/or fecal microbiota transplantation are three major methods to modulate early life gut microbiota in infants and result in favorable outcomes, especially in the preventive effect on disease development that may occur later in life [30,31,61]. However, it is worth mentioning that such microbial modulation therapies are a time-sensitive issue. According to previous reports [62,63], the period of the first 1000 days of an infant’s life, beginning from conception to 2 years of age, is a vital window of opportunity for microbiota modulation. The infant gut microbiota becomes more mature and individual both in functions and compositions after this period. Later in life, gut microbiota are mostly influenced by factors including antibiotic or probiotic, dietary change, and FMT, and all of them can alter immune responses, thereby changing the host’s ability to defend against diseases including allergic, infectious, and autoimmune disorders.

3. Non-Maternal Influencing Factors for the Development of Allergic Diseases in Infants

The infant’s gut microbiota is relatively much less populated compared to adults [64], and its initial composition greatly affects the host in terms of whether the host could develop proper immune responses to protect from various diseases later in life (Figure 2). A study involving 14,572 children [65], among whom 10,220 received at least one antibiotic treatment during the first 2 years of life, showed that early antibiotic exposure was associated with an increase risk of childhood asthma, allergic rhinitis, atopic dermatitis, celiac disease, overweight, obesity, and attention deficit hyperactivity disorder. Although such links are also influenced by the quantity, type, and timing of antibiotic exposure, any disruptions of gut microbiota result in increased susceptibility to various disorders. Germ-free experimental animals are best for studying the role of gut microbiota. Such studies have proved that there is a codependent relationship between gut microbiota and immune system development [66,67,68,69,70,71,72,73,74,75,76].
In human studies, in terms of allergic diseases, gut microbiota showed a vital role in the establishment of adaptive and innate immunity protection. For example, compared to healthy infants, babies with lower IgG responses to specific clusters of microbiota antigens are closely related to the development of allergic diseases including asthma, AD, and FD [12,85,86]. Studies have shown that infants with high risk of AD are associated with lower abundance of Proteobacteria with increased toll-like receptor (TLR)-4-induced innate inflammatory responses, while depletion of Ruminococcaceae is associated with increased TLR-2-induced innate inflammatory responses [87,88,89]. In recent years, the role of gut microbiota in asthma has become a popular area of study. Indeed, infants that are at a greater rate of developing asthma have lower abundance of some gut bacterial taxa such as Faecalibacterium and Bifidobacterium [90,91]. Similarly, food allergy in early age is also closely related to reduced gut microbial abundance [12]. Such studies suggest that modulating gut microbiota to a normal composition with proper abundance and function may be a novel method for promoting regulatory tolerogenic immune responses.

4. The Role of Lung and Gut Microbiota in Asthma

Asthma is one of the most serious allergic diseases both in children and adults in the developed world, currently affecting 300 million people—a number that is increasing every year [22]. Its connection to the gut microbiota was established years ago, and studies have indicated that early-life antibiotic exposure, diet, formula feeding, cesarean section, and an industrialized living environment that are directly involved in altering gut microbiota could aggravate asthma. Especially in the first year of life, when the maturation of gut microbiota occurs, any disruptions during this period of development may cause asthma and other immunological diseases [92,93,94,95,96,97,98,99,100,101,102,103,104,105]. According to a previous study [90], gut microbiota of neonates is closely related to development of allergic diseases; the lowest relative abundance of Bifidobacteria, Akkermansia, and Faecalibacterium genera and higher relative abundance of Candia and Rhodotorula fungi have the highest risk of developing atopy and asthma. Therefore, such data suggest that the complex and dynamic nature of the gut microbiota may be an important factor in the development of asthma symptoms.
In addition to gut microbiota, mounting evidence suggests that the lung microbiota is also involved in the onset of respiratory diseases, especially in early life [106,107,108,109]. This connection is supported by not only preclinical trials but also case-controlled animal experiments [110,111,112].
Healthy lungs are predominantly colonized with commensal bacterial phylum such as Bacteroides and Prevotella spp. [113,114]. Similar to gut microbiota, lung microbiota has a critical period of 2 weeks, during which it promotes the transient expression of programmed death ligand 1 (PDL1) in dendritic cells, which is vital for the Treg-mediated attenuation of allergic airway responses [115]. Exposing children to a diverse microbial environment is important for establishing a healthy immune response. Studies have shown that children who grow up in farms [82,103,116], where they have much more contact with microorganisms compared to urban environments, have a lower rate of developing allergic diseases. Studies have also indicated that early life respiratory tract colonization with certain bacteria, such as Streptococcus, Moraxella, or Haemophilus, increase the severity of lower respiratory viral infection in the first year of life, and the risk of developing asthma symptoms later in life [117].
Asthma is not a single disease. It is a result of a complex interaction which involves two major elements: the mother and the baby (Figure 3). Each of them has an individual or combined contribution to the development of asthma. On the other hand, such complexity also creates more opportunity for treating and preventing asthma during pregnancy and early life by various approaches. For example, antibiotic use during pregnancy increases asthma susceptibility in children; however, the severity of asthma may depend on the dose, type, and timing of their usage [35,39,65,118,119,120]. Such human studies are also proven in animal experiments [121]. Therefore, careful use of antibiotics during pregnancy could alleviate asthma symptoms in the offspring. After delivery, during the window of opportunity, modulating gut microbiota via different methods, including probiotic supplement [121,122,123,124], fecal, or vaginal microbiota transplantation [31,125,126], can ameliorate asthma in children. From the standpoint of exposing infants to diverse microbial communities, raising children in a farming environment, a big family, or with pets could also increase tolerance of allergens, thereby decreasing allergic diseases including asthma.
At the same time, the most direct approach may be supplementing short chain fatty acid (SCFA), which can promote the maturation of dendritic cells in bone marrow, leading to mature cells with reduced ability to instigate Th2 responses in the lung and to induce IgA production by mucosal B cells [130]. SCFAs, especially butyrate acid produced by dietary fiber in the presence of Faecalibacterium prausnitzii [131], have an anti-inflammatory role and can promote epithelial barrier permeability.

5. The Role of Skin and Gut Microbiota in Atopic Dermatitis

AD, a chronic inflammatory skin disease, is also a major issue we are facing in modern times; it affects 15–30% of children and 10% of adults [132]. Its pathogenesis remains obscure [133], but it is considered to be a result of a complex combination of the immune response, the impaired barrier function, and microbiota elements. Among those factors, skin and gut microbiota seem to be more directly related to the development of AD (Figure 4). Studies showed that changes in skin microbiota immune modulation are due to disturbances in epidermal barrier function [134]. Skin microbiota composition is mainly influenced by age, gender, ethnicity, climate, ultraviolet exposure, and lifestyle [135]. Healthy skin surface is colonized with commensal bacterial species [136], such as Lipophilic Propionibacterium species, Staphylococcus and Corynebacterium species.
AD is a complex skin disorder resulting from epidermal barrier dysfunction, altered innate/adaptive immune responses and impaired skin microbial biodiversity [143]. Indeed, healthy skin microbiota protects the surface from various diseases including acute and chronic AD. When the skin microbiota loses microbial diversity [137], with the predominance of the Staphylococcus aureus over Staphylococcus epidermidis, AD occurs. Studies also showed that skin microbiota diversity is also related to AD and the risk of allergic sensitization to common allergens [144].
Similar to gut and lung microbiota, the composition of skin microbiota at an early age is also related to AD. For instance, a study showed that 2-month-old babies with lower abundance of Staphylococci species on their skin had a lower risk of developing AD at 1 year [145]. This is due to early life colonization of the skin by Staphylococci epidermidis being associated with the induction of specific Tregs that modulate activation of host immune responses locally [146].
Interestingly, unlike other allergic diseases, AD is not or is poorly associated with cesarean delivery [147,148,149]. Such data further indicate the role of skin microbiota in the development of AD. Studies showed that, in the hospital environment, especially in the operating room, bacteria such as Staphylococcus and Corynebacterium predominate [150], which are healthy skin microbiota. Therefore, first connecting with healthy skin microbiota could act as a shield for resisting colonization by bacteria that may induce AD. Based on such results, skin microbiota modulation via probiotics or healthy skin microbiota may provide us a novel therapeutic approach for alleviating AD symptoms [151].
Recent studies indicated that gut microbiota is associated with immune modulation as a factor of AD development [152,153]. Data showed that the severity of AD is closely related to the abundance of certain bacteria. For example, a study indicated that, compared to healthy controls, people with AD have a lower density of Bifidobacterium in their intestinal tract [139]. However, the count and percentage of Bifidobacterium is different according to the stage of AD. Early gut microbiota colonization is associated with various diseases, including AD. For example, Clostridium difficile is related to the development of AD, while lower abundance of Bacteroidetes at 1 month of age is associated with AD at 2 years of age [154,155,156]. A recent study showed that, compared to healthy school children, the gut of patients with AD was significantly less abundant in some bacterial species, namely Lachnobacterium and Faecalibacterium [127]. Such studies highlight the possibility of preventing and treating AD by modulating gut microbiota. Indeed, evidence has suggested that oral supplementation of Lactobacillus and Bifidobacterium strains could reduce the risk of AD in infants by regulating T cell-mediated responses [157]. FMT, as the most direct approach of modulating gut microbiota, is reported to be associated with suppression of AD-induced allergic responses by restoration of gut microbiota and immunological balance both in human and animal studies [158,159].

6. The Role of (Oral and) Gut Microbiota in Food Allergy

It is obvious that oral and gut microbiomes are closely related to food allergies (Figure 5). The oral mucosa is the first entity to come into contact with antigens and is the beginning of a continuous gastrointestinal ecosystem that contains local antigen-presenting cells and lymphoid cells, and is associated with organizing lymphoid structures [160]. As studies evidence by subclinical immunotherapies [161], antigen exposure and presentation by oral immune cells modulate systemic immune tolerance. The oral cavity is colonized by a complex microbial community that is directly connected to the gut microbiota both in early life and during pathogenic reaction [162,163]. The composition of the oral microbiota is influenced by birth mode and parents. Data showed that the composition of oral microbiota has distinct colonization patterns between cesarean section and vaginally delivered infants with vaginally born babies having a higher number of taxa [164]. In addition, a recent study found that during the first 18 months of life the oral microbiota of infants was influenced by their parents and shared commensal and disease-related bacteria [165]. This may be why breastfeeding and exposure to diverse microbial environments such as farms and big homes are important for decreasing the incidence of allergic diseases in infants [166,167]. At the same time, a study showed that residential microbial communities favor the crosstalk between innate myeloid and lymphoid cells that contributes to immune homeostasis in the gut and the development of oral tolerances to oral antigens [168].
From the perspective of gut microbiota, a previous study indicated that infants with cow’s milk allergy (CMA) had relatively higher abundant bacterial taxa, particularly anaerobics, compared to healthy controls after 6 months of milk formula feeding [172]. More precisely, according to this study, gut microbiota of infants with CMA had higher concentrations of Lactobacilli and lower concentrations of Enterobacteria and Bifidobacteria. Infants whose CMA was resolved by 8 years of age had an enhanced Clostridia and Firmicutes rate in their gut [173]. The gut microbiota of children with egg allergy had a greater abundance of certain genera compared to healthy ones, namely Lachnospiraceae and Ruminococcaceae [174]. A recent study involving 14 children with food allergy and 87 children with food allergen sensitization found that Dorea, Haemophilus, Dialister, and Clostridium genera were reduced in healthy participants, while the genera Citrobacter, Lactococcus, Oscillospira, and Dorea were reduced in participants with food allergy [175]. Furthermore, data have shown that, compared to healthy controls, the gut microbiota of peanut or tree nut allergy patients had a decreased richness and increased concentration of Bacteroides species [176].
Germ-free mice are ideal for studying gut microbiota-related human diseases. Indeed, the role of gut microbiota in the development of CMA has been proven to be prominent. A study showed that germ-free mice were protected from developing susceptibility to CMA if colonized with gut microbiota from healthy infants [177]. Furthermore, transferring specific bacterial strains, Bifidobacterium or Clostridium, to mice was shown to reduce the risk of food sensitization by inducing mucosal Treg [178]. A study also showed that Clostridia can stimulate innate lymphoid cells to produce IL-22, which contributes to straightening the epithelial barrier and decreasing the permeability of the intestine to dietary proteins [179]. Some functional effects of Clostridia in food allergy may also exert, via their fermentation metabolites such as butyrate, an SCFA that is known for its role in immunoregulatory and tolerogenic properties [180,181,182,183,184,185]. In addition, butyrate is the only SCFA produced exclusively by gut microbial fermentation, while others are influenced by host metabolism [186]. Recent findings support the hypothesis that butyrate might contribute to the development of immune oral tolerance and the prevention and treatment of food allergies [187,188,189].
Previous human and animal studies established the association between oral and gut microbiota and food allergy. Although the mechanisms involved are complex and dynamic, they underline the possibility of preventing and treating food allergy by microbial modulation. For example, a study showed that, compared to non-supplemented hypoallergenic milk formula, supplementation with hydrolyzed casein formula containing the probiotic Lactobacillus rhamnosus GG promoted CMA resolution at 12, 24, and 36 months [190], which was found to enrich butyrate-producing bacterial strains [180]. Using an amino-acid-based formula that contained a specific synbiotics, a combination of prebiotic blend of fructooligosaccharides and the probiotic strain Bifidobacterium breve M-16V has been shown to modulate the gut microbiota and its metabolic activities in infants with non-IgE-mediated CMA [191,192,193]. In addition, a study indicated that oral supplementation with Lactobacillus rhamnosus GG could enhance the efficacy of oral immunotherapy in inducing peanut tolerance and immune changes in children with peanut allergy [194]. However, this was an uncontrolled study; future studies including a control group are needed to further determine such results.
Fecal microbiota transplantation is another potential therapeutic approach for food allergy. Studies showed that re-establishing the gut microbiota of patients can ameliorate the allergic symptoms by increasing microbiota diversity in FMT trials [195,196]. Dysbiosis of gut microbiota leads to development of food allergy [173]; then, restoration of immune homeostasis and reconstruction of the impaired gut microbiota barrier by FMT may be able to promote the development of oral tolerance [195].

7. Conclusions

Microbiota during pregnancy and an infant’s early life are both crucial for the development of a healthy immune system and disease protection. Inappropriate or insufficient microbiota, either in mothers or infants, can have various harmful effects on immune health, contributing to the development of allergic diseases. Although recent studies have deepened our understanding of the relationships between maternal and infant microbiota and the immune system with respect to allergic diseases, the mechanisms involved at molecular levels remain unelucidated. Indeed, allergic disease is not a single disease but rather a result of complex microbial and immune interactions involving both the mother and the infant. Such complexity gives us opportunities for intervention and modulation both during pregnancy and early infant life to decrease allergic symptoms. Therefore, understanding the mechanisms involved is of utmost importance for developing effective and safe prevention strategies for allergic diseases.

Author Contributions

Conceptualization: Y.F., N.Z.; Supervision: Y.F., N.Z.; Visualization: M.T.; Writing—Original draft: M.T.; Writing—Review & editing: X.H., S.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Conflicts of Interest

None of the authors have a financial interest in any of the products, devices, or materials mentioned in this manuscript. The authors declare that they have no conflicts of interest.

References

  1. Bach, J.-F. The Effect of Infections on Susceptibility to Autoimmune and Allergic Diseases. N. Engl. J. Med. 2002, 347, 911–920. [Google Scholar] [CrossRef] [PubMed]
  2. Ren, J.; Xu, J.; Zhang, P.; Bao, Y. Prevalence and Risk Factors of Asthma in Preschool Children in Shanghai, China: A Cross-Sectional Study. Front. Pediatr. 2022, 9, 793452. [Google Scholar] [CrossRef] [PubMed]
  3. Portelli, M.A.; Hodge, E.; Sayers, I. Genetic risk factors for the development of allergic disease identified by genome-wide association. Clin. Exp. Allergy 2015, 45, 21–31. [Google Scholar] [CrossRef] [PubMed]
  4. Gilles, S.; Akdis, C.; Lauener, R.; Schmid-Grendelmeier, P.; Bieber, T.; Schäppi, G.; Traidl-Hoffmann, C. The role of environmental factors in allergy: A critical reappraisal. Exp. Dermatol. 2018, 27, 1193–1200. [Google Scholar] [CrossRef] [Green Version]
  5. Özdemir, A.; Can, D.; Günay, I.; Nacaroglu, T.; Karkiner, C.; Üstyol, A.; Kamalı, H.; Ayanoğlu, M.; Günay, T.; Dogan, D. Effect of industrialization on allergic diseases in school children. J. Turgut Ozal Med. Cent. 2018, 25, 232–235. [Google Scholar] [CrossRef]
  6. Fogarty, A.W. What have studies of non-industrialized countries told us about the cause of allergic disease? Clin. Exp. Allergy 2015, 45, 87–93. [Google Scholar] [CrossRef] [Green Version]
  7. Sbihi, H.; Boutin, R.C.; Cutler, C.; Suen, M.; Finlay, B.B.; Turvey, S.E. Thinking bigger: How early-life environmental exposures shape the gut microbiome and influence the development of asthma and allergic disease. Allergy 2019, 74, 2103–2115. [Google Scholar] [CrossRef] [Green Version]
  8. Coyte, K.Z.; Rao, C.; Rakoff-Nahoum, S.; Foster, K.R. Ecological rules for the assembly of microbiome communities. PLoS Biol. 2021, 19, e3001116. [Google Scholar] [CrossRef]
  9. Clemente, J.C.; Ursell, L.K.; Parfrey, L.W.; Knight, R. The Impact of the Gut Microbiota on Human Health: An Integrative View. Cell 2012, 148, 1258–1270. [Google Scholar] [CrossRef] [Green Version]
  10. Cryan, J.F.; Dinan, T.G. Mind-altering microorganisms: The impact of the gut microbiota on brain and behaviour. Nat. Rev. Neurosci. 2012, 13, 701–712. [Google Scholar] [CrossRef]
  11. Dekaboruah, E.; Suryavanshi, M.V.; Chettri, D.; Verma, A.K. Human microbiome: An academic update on human body site specific surveillance and its possible role. Arch. Microbiol. 2020, 202, 2147–2167. [Google Scholar] [CrossRef] [PubMed]
  12. Peroni, D.G.; Nuzzi, G.; Trambusti, I.; Di Cicco, M.E.; Comberiati, P. Microbiome Composition and Its Impact on the Development of Allergic Diseases. Front. Immunol. 2020, 11, 700. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  13. Sugahara, H.; Odamaki, T.; Hashikura, N.; Abe, F.; Xiao, J.-Z. Differences in folate production by bifidobacteria of different origins. Biosci. Microbiota Food Health 2015, 34, 87–93. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  14. Rowland, I.; Gibson, G.; Heinken, A.; Scott, K.; Swann, J.; Thiele, I.; Tuohy, K. Gut microbiota functions: Metabolism of nutrients and other food components. Eur. J. Nutr. 2018, 57, 1–24. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  15. Gomez de Agüero, M.; Ganal-Vonarburg, S.C.; Fuhrer, T.; Rupp, S.; Uchimura, Y.; Li, H.; Steinert, A.; Heikenwalder, M.; Hapfelmeier, S.; Sauer, U.; et al. The maternal microbiota drives early postnatal innate immune development. Science 2016, 351, 1296–1302. [Google Scholar] [CrossRef] [PubMed]
  16. Francino, M.P. Early Development of the Gut Microbiota and Immune Health. Pathogens 2014, 3, 769–790. [Google Scholar] [CrossRef] [Green Version]
  17. Tamburini, S.; Shen, N.; Wu, H.C.; Clemente, J.C. The microbiome in early life: Implications for health outcomes. Nat. Med. 2016, 22, 713–722. [Google Scholar] [CrossRef] [Green Version]
  18. Gensollen, T.; Blumberg, R.S. Correlation between early-life regulation of the immune system by microbiota and allergy development. J. Allergy Clin. Immunol. 2017, 139, 1084–1091. [Google Scholar] [CrossRef] [Green Version]
  19. Zheng, D.; Liwinski, T.; Elinav, E. Interaction between microbiota and immunity in health and disease. Cell Res. 2020, 30, 492–506. [Google Scholar] [CrossRef]
  20. Shu, S.-A.; Yuen, A.W.T.; Woo, E.; Chu, K.-H.; Kwan, H.-S.; Yang, G.-X.; Yang, Y.; Leung, P.S.C. Microbiota and Food Allergy. Clin. Rev. Allergy Immunol. 2019, 57, 83–97. [Google Scholar] [CrossRef]
  21. Kim, J.E.; Kim, H.S. Microbiome of the Skin and Gut in Atopic Dermatitis (AD): Understanding the Pathophysiology and Finding Novel Management Strategies. J. Clin. Med. Res. 2019, 8, 444. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  22. Barcik, W.; Boutin, R.C.T.; Sokolowska, M.; Finlay, B.B. The Role of Lung and Gut Microbiota in the Pathology of Asthma. Immunity 2020, 52, 241–255. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  23. Stokholm, J.; Thorsen, J.; Chawes, B.L.; Schjørring, S.; Krogfelt, K.A.; Bønnelykke, K.; Bisgaard, H. Cesarean section changes neonatal gut colonization. J. Allergy Clin. Immunol. 2016, 138, 881–889.e2. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  24. Shaterian, N.; Abdi, F.; Ghavidel, N.; Alidost, F. Role of cesarean section in the development of neonatal gut microbiota: A systematic review. Open Med. 2021, 16, 624–639. [Google Scholar] [CrossRef]
  25. Kim, G.; Bae, J.; Kim, M.J.; Kwon, H.; Park, G.; Kim, S.-J.; Choe, Y.H.; Kim, J.; Park, S.-H.; Choe, B.-H.; et al. Delayed Establishment of Gut Microbiota in Infants Delivered by Cesarean Section. Front. Microbiol. 2020, 11, 2099. [Google Scholar] [CrossRef]
  26. Ma, J.; Li, Z.; Zhang, W.; Zhang, C.; Zhang, Y.; Mei, H.; Zhuo, N.; Wang, H.; Wang, L.; Wu, D. Comparison of gut microbiota in exclusively breast-fed and formula-fed babies: A study of 91 term infants. Sci. Rep. 2020, 10, 15792. [Google Scholar] [CrossRef]
  27. Zhong, H.; Wang, X.-G.; Wang, J.; Chen, Y.-J.; Qin, H.-L.; Yang, R. Impact of probiotics supplement on the gut microbiota in neonates with antibiotic exposure: An open-label single-center randomized parallel controlled study. World J. Pediatr. 2021, 17, 385–393. [Google Scholar] [CrossRef]
  28. Yousuf, E.I.; Carvalho, M.; Dizzell, S.E.; Kim, S.; Gunn, E.; Twiss, J.; Giglia, L.; Stuart, C.; Hutton, E.K. Persistence of Suspected Probiotic Organisms in Preterm Infant Gut Microbiota Weeks After Probiotic Supplementation in the NICU. Front. Microbiol. 2020, 11, 574137. [Google Scholar] [CrossRef]
  29. Berardi, A.; Rossi, K.; Pizzi, C.; Baronciani, D.; Venturelli, C.; Ferrari, F.; Facchinetti, F. Absence of neonatal streptococcal colonization after planned cesarean section. Acta Obstet. Gynecol. Scand. 2006, 85, 1012–1013. [Google Scholar] [CrossRef]
  30. Wilson, B.C.; Butler, M.; Grigg, C.P.; Derraik, J.G.B.; Chiavaroli, V.; Walker, N.; Thampi, S.; Creagh, C.; Reynolds, A.J.; Vatanen, T.; et al. Oral administration of maternal vaginal microbes at birth to restore gut microbiome development in infants born by caesarean section: A pilot randomised placebo-controlled trial. eBioMedicine 2021, 69, 103443. [Google Scholar] [CrossRef]
  31. Korpela, K.; Helve, O.; Kolho, K.-L.; Saisto, T.; Skogberg, K.; Dikareva, E.; Stefanovic, V.; Salonen, A.; Andersson, S.; de Vos, W.M. Maternal Fecal Microbiota Transplantation in Cesarean-Born Infants Rapidly Restores Normal Gut Microbial Development: A Proof-of-Concept Study. Cell 2020, 183, 324–334.e5. [Google Scholar] [CrossRef] [PubMed]
  32. Biasucci, G.; Rubini, M.; Riboni, S.; Morelli, L.; Bessi, E.; Retetangos, C. Mode of delivery affects the bacterial community in the newborn gut. Early Hum. Dev. 2010, 86 (Suppl. 1), 13–15. [Google Scholar] [CrossRef] [PubMed]
  33. Shao, Y.; Forster, S.C.; Tsaliki, E.; Vervier, K.; Strang, A.; Simpson, N.; Kumar, N.; Stares, M.D.; Rodger, A.; Brocklehurst, P.; et al. Stunted microbiota and opportunistic pathogen colonization in caesarean-section birth. Nature 2019, 574, 117–121. [Google Scholar] [CrossRef] [PubMed]
  34. Reyman, M.; van Houten, M.A.; van Baarle, D.; Bosch, A.A.T.M.; Man, W.H.; Chu, M.L.J.N.; Arp, K.; Watson, R.L.; Sanders, E.A.M.; Fuentes, S.; et al. Impact of delivery mode-associated gut microbiota dynamics on health in the first year of life. Nat. Commun. 2019, 10, 4997. [Google Scholar] [CrossRef] [Green Version]
  35. Wu, P.; Feldman, A.S.; Rosas-Salazar, C.; James, K.; Escobar, G.; Gebretsadik, T.; Li, S.X.; Carroll, K.N.; Walsh, E.; Mitchel, E.; et al. Relative Importance and Additive Effects of Maternal and Infant Risk Factors on Childhood Asthma. PLoS ONE 2016, 11, e0151705. [Google Scholar] [CrossRef]
  36. Xu, B.; Pekkanen, J.; Jarvelin, M.R.; Olsen, P.; Hartikainen, A.L. Maternal infections in pregnancy and the development of asthma among offspring. Int. J. Epidemiol. 1999, 28, 723–727. [Google Scholar] [CrossRef] [Green Version]
  37. Sly, P.D. Maternal Asthma, Pregnancy Complications, and Offspring Wheeze. Untangling the Web. Am. J. Respir. Crit. Care Med. 2019, 199, 1–2. [Google Scholar] [CrossRef]
  38. Blaser, M.J.; Bello, M.G.D. Maternal antibiotic use and risk of asthma in offspring. Lancet Respir. Med. 2014, 2, e16. [Google Scholar] [CrossRef]
  39. Loewen, K.; Monchka, B.; Mahmud, S.M.; Azad, M.B.; Jong, G. Prenatal antibiotic exposure and childhood asthma: A population-based study. Eur. Respir. J. 2018, 52, 1702070. [Google Scholar] [CrossRef]
  40. Gray, L.E.K.; O’Hely, M.; Ranganathan, S.; Sly, P.D.; Vuillermin, P. The Maternal Diet, Gut Bacteria, and Bacterial Metabolites during Pregnancy Influence Offspring Asthma. Front. Immunol. 2017, 8, 365. [Google Scholar] [CrossRef] [Green Version]
  41. Viljoen, K.; Segurado, R.; O’Brien, J.; Murrin, C.; Mehegan, J.; Kelleher, C.C. Pregnancy diet and offspring asthma risk over a 10-year period: The Lifeways Cross Generation Cohort Study, Ireland. BMJ Open 2018, 8, e017013. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  42. Polloni, L.; Ferruzza, E.; Ronconi, L.; Lazzarotto, F.; Toniolo, A.; Bonaguro, R.; Muraro, A. Perinatal stress and food allergy: A preliminary study on maternal reports. Psychol. Health Med. 2015, 20, 732–741. [Google Scholar] [CrossRef] [PubMed]
  43. Mägi, C.-A.O.; Bäcklund, A.B.; Carlsen, K.L.; Almqvist, C.; Carlsen, K.-H.; Granum, B.; Haugen, G.; Hilde, K.; Carlsen, O.C.L.; Jonassen, C.M.; et al. Allergic disease and risk of stress in pregnant women: A PreventADALL study. ERJ Open Res. 2020, 6, 00175-2020. [Google Scholar] [CrossRef]
  44. Dioun, A.F.; Harris, S.K.; Hibberd, P.L. Is maternal age at delivery related to childhood food allergy? Pediatr. Allergy Immunol. 2003, 14, 307–311. [Google Scholar] [CrossRef]
  45. Saito, K.; Yokoyama, T.; Miyake, Y.; Sasaki, S.; Tanaka, K.; Ohya, Y.; Hirota, Y. Maternal meat and fat consumption during pregnancy and suspected atopic eczema in Japanese infants aged 3-4 months: The Osaka Maternal and Child Health Study. Pediatr. Allergy Immunol. 2010, 21, 38–46. [Google Scholar] [CrossRef]
  46. Sestito, S.; D’Auria, E.; Baldassarre, M.E.; Salvatore, S.; Tallarico, V.; Stefanelli, E.; Tarsitano, F.; Concolino, D.; Pensabene, L. The Role of Prebiotics and Probiotics in Prevention of Allergic Diseases in Infants. Front. Pediatr. 2020, 8, 583946. [Google Scholar] [CrossRef]
  47. Schäfer, S.; Liu, A.; Campbell, D.; Nanan, R. Analysis of maternal and perinatal determinants of allergic sensitization in childhood. Allergy Asthma Clin. Immunol. 2020, 16, 71. [Google Scholar] [CrossRef]
  48. Dominguez-Bello, M.G.; Costello, E.K.; Contreras, M.; Magris, M.; Hidalgo, G.; Fierer, N.; Knight, R. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc. Natl. Acad. Sci. USA 2010, 107, 11971–11975. [Google Scholar] [CrossRef] [Green Version]
  49. Mueller, N.T.; Bakacs, E.; Combellick, J.; Grigoryan, Z.; Dominguez-Bello, M.G. The infant microbiome development: Mom matters. Trends Mol. Med. 2015, 21, 109–117. [Google Scholar] [CrossRef] [Green Version]
  50. Simpson, M.R.; Avershina, E.; Storrø, O.; Johnsen, R.; Rudi, K.; Øien, T. Breastfeeding-associated microbiota in human milk following supplementation with Lactobacillus rhamnosus GG, Lactobacillus acidophilus La-5, and Bifidobacterium animalis ssp. lactis Bb-12. J. Dairy Sci. 2018, 101, 889–899. [Google Scholar] [CrossRef]
  51. Ferretti, P.; Pasolli, E.; Tett, A.; Asnicar, F.; Gorfer, V.; Fedi, S.; Armanini, F.; Truong, D.T.; Manara, S.; Zolfo, M.; et al. Mother-to-Infant Microbial Transmission from Different Body Sites Shapes the Developing Infant Gut Microbiome. Cell Host Microbe 2018, 24, 133–145.e5. [Google Scholar] [CrossRef] [PubMed]
  52. Niu, J.; Xu, L.; Qian, Y.; Sun, Z.; Yu, D.; Huang, J.; Zhou, X.; Wang, Y.; Zhang, T.; Ren, R.; et al. Evolution of the Gut Microbiome in Early Childhood: A Cross-Sectional Study of Chinese Children. Front. Microbiol. 2020, 11, 439. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  53. Vandenplas, Y.; Carnielli, V.P.; Ksiazyk, J.; Luna, M.S.; Migacheva, N.; Mosselmans, J.M.; Picaud, J.C.; Possner, M.; Singhal, A.; Wabitsch, M. Factors affecting early-life intestinal microbiota development. Nutrition 2020, 78, 110812. [Google Scholar] [CrossRef] [PubMed]
  54. Hoyen, C. Factors Influencing the Composition of the Intestinal Microbiota in Early Infancy. Yearb. Neonatal Périnat. Med. 2007, 2007, 202–203. [Google Scholar] [CrossRef]
  55. Penders, J.; Thijs, C.; Vink, C.; Stelma, F.F.; Snijders, B.; Kummeling, I.; Van den Brandt, P.A.; Stobberingh, E.E. Factors Influencing the Composition of the Intestinal Microbiota in Early Infancy. Pediatrics 2006, 118, 511–521. [Google Scholar] [CrossRef] [Green Version]
  56. Dierikx, T.H.; Visser, D.H.; Benninga, M.A.; van Kaam, A.H.L.C.; de Boer, N.K.H.; de Vries, R.; Van Limbergen, J.; de Meij, T.G.J. The influence of prenatal and intrapartum antibiotics on intestinal microbiota colonisation in infants: A systematic review. J. Infect. 2020, 81, 190–204. [Google Scholar] [CrossRef]
  57. Milliken, S.; Allen, R.M.; Lamont, R.F. The role of antimicrobial treatment during pregnancy on the neonatal gut microbiome and the development of atopy, asthma, allergy and obesity in childhood. Expert Opin. Drug Saf. 2019, 18, 173–185. [Google Scholar] [CrossRef]
  58. Panduru, M.; Epure, A.M.; Cimpoca, B.; Cozma, C.; Giuca, B.A.; Pop, A.; Pop, G.; Simon, L.G.; Robu, M.; Panduru, N.M. Antibiotics administration during last trimester of pregnancy is associated with atopic dermatitis—A cross-sectional study. Rom. J. Intern. Med. 2020, 58, 99–107. [Google Scholar] [CrossRef]
  59. Stensballe, L.G.; Simonsen, J.; Jensen, S.M.; Bønnelykke, K.; Bisgaard, H. Use of Antibiotics during Pregnancy Increases the Risk of Asthma in Early Childhood. J. Pediatr. 2013, 162, 832–838.e3. [Google Scholar] [CrossRef]
  60. Geng, M.; Tang, Y.; Liu, K.; Huang, K.; Yan, S.; Ding, P.; Zhang, J.; Wang, B.; Wang, S.; Li, S.; et al. Prenatal low-dose antibiotic exposure and children allergic diseases at 4 years of age: A prospective birth cohort study. Ecotoxicol. Environ. Saf. 2021, 225, 112736. [Google Scholar] [CrossRef]
  61. Junca, H.; Pieper, D.H.; Medina, E. The emerging potential of microbiome transplantation on human health interventions. Comput. Struct. Biotechnol. J. 2022, 20, 615–627. [Google Scholar] [CrossRef] [PubMed]
  62. Grier, A.; McDavid, A.; Wang, B.; Qiu, X.; Java, J.; Bandyopadhyay, S.; Yang, H.; Holden-Wiltse, J.; Kessler, H.A.; Gill, A.L.; et al. Neonatal gut and respiratory microbiota: Coordinated development through time and space. Microbiome 2018, 6, 193. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  63. Robertson, R.C.; Manges, A.R.; Finlay, B.B.; Prendergast, A.J. The Human Microbiome and Child Growth—First 1000 Days and Beyond. Trends Microbiol. 2019, 27, 131–147. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  64. Yang, I.; Corwin, E.J.; Brennan, P.A.; Jordan, S.; Murphy, J.R.; Dunlop, A. The Infant Microbiome: Implications for Infant Health and Neurocognitive Development. Nurs. Res. 2016, 65, 76–88. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  65. Aversa, Z.; Atkinson, E.J.; Schafer, M.J.; Theiler, R.N.; Rocca, W.A.; Blaser, M.J.; LeBrasseur, N.K. Association of Infant Antibiotic Exposure with Childhood Health Outcomes. Mayo Clin. Proc. 2021, 96, 66–77. [Google Scholar] [CrossRef]
  66. Moreau, M.C.; Ducluzeau, R.; Guy-Grand, D.; Muller, M.C. Increase in the Population of Duodenal Immunoglobulin A Plasmocytes in Axenic Mice Associated with Different Living or Dead Bacterial Strains of Intestinal Origin. Infect. Immun. 1978, 21, 532–539. [Google Scholar] [CrossRef] [Green Version]
  67. Franchi, L.; Warner, N.; Viani, K.; Nuñez, G. Function of Nod-like receptors in microbial recognition and host defense. Immunol. Rev. 2009, 227, 106–128. [Google Scholar] [CrossRef] [Green Version]
  68. Baba, N.; Samson, S.; Bourdet-Sicard, R.; Rubio, M.; Sarfati, M. Commensal bacteria trigger a full dendritic cell maturation program that promotes the expansion of non-Tr1 suppressor T cells. J. Leukoc. Biol. 2008, 84, 468–476. [Google Scholar] [CrossRef]
  69. Fulde, M.; Hornef, M.W. Maturation of the enteric mucosal innate immune system during the postnatal period. Immunol. Rev. 2014, 260, 21–34. [Google Scholar] [CrossRef]
  70. Wesemann, D.R.; Portuguese, A.J.; Meyers, R.M.; Gallagher, M.P.; Cluff-Jones, K.; Magee, J.M.; Panchakshari, R.A.; Rodig, S.J.; Kepler, T.B.; Alt, F.W. Microbial colonization influences early B-lineage development in the gut lamina propria. Nature 2013, 501, 112–115. [Google Scholar] [CrossRef]
  71. Inman, C.F.; Laycock, G.M.; Mitchard, L.; Harley, R.; Warwick, J.; Burt, R.; Van Diemen, P.M.; Stevens, M.; Bailey, M. Neonatal Colonisation Expands a Specific Intestinal Antigen-Presenting Cell Subset Prior to CD4 T-Cell Expansion, without Altering T-Cell Repertoire. PLoS ONE 2012, 7, e33707. [Google Scholar] [CrossRef] [PubMed]
  72. Okogbule-Wonodi, A.C.; Li, G.; Anand, B.; Luzina, I.G.; Atamas, S.P.; Blanchard, T. Human foetal intestinal fibroblasts are hyper-responsive to lipopolysaccharide stimulation. Dig. Liver Dis. 2012, 44, 18–23. [Google Scholar] [CrossRef] [PubMed]
  73. Sansonetti, P.J. To be or not to be a pathogen: That is the mucosally relevant question. Mucosal Immunol. 2011, 4, 8–14. [Google Scholar] [CrossRef] [PubMed]
  74. Manicassamy, S.; Reizis, B.; Ravindran, R.; Nakaya, H.; Salazar-Gonzalez, R.M.; Wang, Y.-C.; Pulendran, B. Activation of beta-catenin in dendritic cells regulates immunity versus tolerance in the intestine. Science 2010, 329, 849–853. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  75. Franchi, L.; Kamada, N.; Nakamura, Y.; Burberry, A.; Kuffa, P.; Suzuki, S.; Shaw, M.H.; Kim, Y.-G.; Núñez, G. NLRC4-driven production of IL-1β discriminates between pathogenic and commensal bacteria and promotes host intestinal defense. Nat. Immunol. 2012, 13, 449–456. [Google Scholar] [CrossRef] [PubMed]
  76. Round, J.L.; Mazmanian, S.K. The gut microbiota shapes intestinal immune responses during health and disease. Nat. Rev. Immunol. 2009, 9, 313–323. [Google Scholar] [CrossRef]
  77. Ni, J.; Friedman, H.; Boyd, B.C.; McGurn, A.; Babinski, P.; Markossian, T.; Dugas, L.R. Early antibiotic exposure and development of asthma and allergic rhinitis in childhood. BMC Pediatr. 2019, 19, 225. [Google Scholar] [CrossRef]
  78. Zhang, J.; Ma, C.; Yang, A.; Zhang, R.; Gong, J.; Mo, F. Is preterm birth associated with asthma among children from birth to 17 years old? A study based on 2011-2012 US National Survey of Children’s Health. Ital. J. Pediatr. 2018, 44, 151. [Google Scholar] [CrossRef] [Green Version]
  79. El-Heneidy, A.; Abdel-Rahman, M.E.; Mihala, G.; Ross, L.J.; Comans, T.A. Milk Other Than Breast Milk and the Development of Asthma in Children 3 Years of Age. A Birth Cohort Study (2006–2011). Nutrients 2018, 10, 1798. [Google Scholar] [CrossRef] [Green Version]
  80. Roduit, C.; Scholtens, S.; De Jongste, J.C.; Wijga, A.H.; Gerritsen, J.; Postma, D.S.; Brunekreef, B.; Hoekstra, M.O.; Aalberse, R.; Smit, H.A. Asthma at 8 years of age in children born by caesarean section. Thorax 2009, 64, 107–113. [Google Scholar] [CrossRef] [Green Version]
  81. Goldberg, S.; Israeli, E.; Schwartz, S.; Shochat, T.; Izbicki, G.; Toker-Maimon, O.; Klement, E.; Picard, E. Asthma prevalence, family size, and birth order. Chest 2007, 131, 1747–1752. [Google Scholar] [CrossRef] [PubMed]
  82. Andersén, H.; Ilmarinen, P.; Honkamäki, J.; Tuomisto, L.E.; Hisinger-Mölkänen, H.; Backman, H.; Lundbäck, B.; Rönmark, E.; Lehtimäki, L.; Sovijärvi, A.; et al. Influence of Childhood Exposure to a Farming Environment on Age at Asthma Diagnosis in a Population-Based Study. J. Asthma Allergy 2021, 14, 1081–1091. [Google Scholar] [CrossRef] [PubMed]
  83. Wooldridge, A.L.; McMillan, M.; Kaur, M.; Giles, L.C.; Marshall, H.S.; Gatford, K.L. Relationship between birth weight or fetal growth rate and postnatal allergy: A systematic review. J. Allergy Clin. Immunol. 2019, 144, 1703–1713. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  84. Mathias, J.M.G.; Zhang, H.; Karmaus, W.; Soto-Ramirez, N.; Shen, Y. Mixed Infant Feeding—Direct Breastfeeding, Pumping and Feeding, and Formula Food Poses a Risk for Food Allergy in Early Childhood. J. Allergy Clin. Immunol. 2017, 139, AB385. [Google Scholar] [CrossRef] [Green Version]
  85. Christmann, B.S.; Abrahamsson, T.R.; Bernstein, C.N.; Duck, L.W.; Mannon, P.J.; Berg, G.; Björkstén, B.; Jenmalm, M.C.; Elson, C.O. Human seroreactivity to gut microbiota antigens. J. Allergy Clin. Immunol. 2015, 136, 1378–1386.e5. [Google Scholar] [CrossRef] [Green Version]
  86. Tanaka, M.; Nakayama, J. Development of the gut microbiota in infancy and its impact on health in later life. Allergol. Int. 2017, 66, 515–522. [Google Scholar] [CrossRef]
  87. West, C.E.; Rydén, P.; Lundin, D.; Engstrand, L.; Tulic, M.K.; Prescott, S.L. Gut microbiome and innate immune response patterns in IgE-associated eczema. Clin. Exp. Allergy 2015, 45, 1419–1429. [Google Scholar] [CrossRef] [Green Version]
  88. Yiu, J.H.C.; Dorweiler, B.; Woo, C.W. Interaction between gut microbiota and toll-like receptor: From immunity to metabolism. J. Mol. Med. 2017, 95, 13–20. [Google Scholar] [CrossRef] [Green Version]
  89. Sun, L.; Liu, W.; Zhang, L.-J. The Role of Toll-Like Receptors in Skin Host Defense, Psoriasis, and Atopic Dermatitis. J. Immunol. Res. 2019, 2019, 1824624. [Google Scholar] [CrossRef]
  90. Fujimura, K.E.; Sitarik, A.R.; Havstad, S.; Lin, D.L.; LeVan, S.; Fadrosh, D.; Panzer, A.R.; LaMere, B.; Rackaityte, E.; Lukacs, N.W.; et al. Neonatal gut microbiota associates with childhood multisensitized atopy and T cell differentiation. Nat. Med. 2016, 22, 1187–1191. [Google Scholar] [CrossRef] [Green Version]
  91. Stokholm, J.; Blaser, M.J.; Thorsen, J.; Rasmussen, M.A.; Waage, J.; Vinding, R.K.; Schoos, A.-M.M.; Kunøe, A.; Fink, N.R.; Chawes, B.L.; et al. Maturation of the gut microbiome and risk of asthma in childhood. Nat. Commun. 2018, 9, 141. [Google Scholar] [CrossRef] [PubMed]
  92. Cho, I.; Blaser, M.J. The human microbiome: At the interface of health and disease. Nat. Rev. Genet. 2012, 13, 260–270. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  93. Prescott, S.L. Early-life environmental determinants of allergic diseases and the wider pandemic of inflammatory noncommunicable diseases. J. Allergy Clin. Immunol. 2013, 131, 23–30. [Google Scholar] [CrossRef] [PubMed]
  94. Bäckhed, F.; Roswall, J.; Peng, Y.; Feng, Q.; Jia, H.; Kovatcheva-Datchary, P.; Li, Y.; Xia, Y.; Xie, H.; Zhong, H.; et al. Dynamics and Stabilization of the Human Gut Microbiome during the First Year of Life. Cell Host Microbe 2015, 17, 852. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  95. Yatsunenko, T.; Rey, F.E.; Manary, M.J.; Trehan, I.; Dominguez-Bello, M.G.; Contreras, M.; Magris, M.; Hidalgo, G.; Baldassano, R.N.; Anokhin, A.P.; et al. Human gut microbiome viewed across age and geography. Nature 2012, 486, 222–227. [Google Scholar] [CrossRef] [PubMed]
  96. Subramanian, S.; Huq, S.; Yatsunenko, T.; Haque, R.; Mahfuz, M.; Alam, M.A.; Benezra, A.; DeStefano, J.; Meier, M.F.; Muegge, B.D.; et al. Persistent gut microbiota immaturity in malnourished Bangladeshi children. Nature 2014, 510, 417–421. [Google Scholar] [CrossRef] [PubMed]
  97. Bokulich, N.A.; Chung, J.; Battaglia, T.; Henderson, N.; Jay, M.; Li, H.; Lieber, A.D.; Wu, F.; Perez-Perez, G.I.; Chen, Y.; et al. Antibiotics, birth mode, and diet shape microbiome maturation during early life. Sci. Transl. Med. 2016, 8, 343ra82. [Google Scholar] [CrossRef] [Green Version]
  98. Gensollen, T.; Iyer, S.S.; Kasper, D.L.; Blumberg, R.S. How colonization by microbiota in early life shapes the immune system. Science 2016, 352, 539–544. [Google Scholar] [CrossRef] [Green Version]
  99. Geervliet, M. A Window of Opportunity: Modulation of the Porcine Gut Microbiota and Immune System by Feed Additives in Early Life. Ph.D. Thesis, Wageningen University, Wageningen, The Netherlands, 2021. [Google Scholar] [CrossRef]
  100. Cox, L.M.; Yamanishi, S.; Sohn, J.; Alekseyenko, A.V.; Leung, J.M.; Cho, I.; Kim, S.G.; Li, H.; Gao, Z.; Mahana, D.; et al. Altering the Intestinal Microbiota during a Critical Developmental Window Has Lasting Metabolic Consequences. Cell 2014, 158, 705–721. [Google Scholar] [CrossRef] [Green Version]
  101. Bisgaard, H.; Li, N.; Bonnelykke, K.; Chawes, B.L.K.; Skov, T.; Paludan-Müller, G.; Stokholm, J.; Smith, B.; Krogfelt, K.A. Reduced diversity of the intestinal microbiota during infancy is associated with increased risk of allergic disease at school age. J. Allergy Clin. Immunol. 2011, 128, 646–652.e5. [Google Scholar] [CrossRef]
  102. Nowak-Wegrzyn, A. Allergy Development and the Intestinal Microflora During the First Year of Life. Pediatrics 2002, 110, 431. [Google Scholar] [CrossRef]
  103. Ege, M.J.; Mayer, M.; Normand, A.-C.; Genuneit, J.; Cookson, W.O.C.M.; Braun-Fahrländer, C.; Heederik, D.; Piarroux, R.; von Mutius, E. GABRIELA Transregio 22 Study Group. Exposure to environmental microorganisms and childhood asthma. N. Engl. J. Med. 2011, 364, 701–709. [Google Scholar] [CrossRef] [PubMed]
  104. Penders, J.; Gerhold, K.; Thijs, C.; Zimmermann, K.; Wahn, U.; Lau, S.; Hamelmann, E. New insights into the hygiene hypothesis in allergic diseases: Mediation of sibling and birth mode effects by the gut microbiota. Gut Microbes 2014, 5, 239–244. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  105. Arrieta, M.-C.; Stiemsma, L.T.; Dimitriu, P.A.; Thorson, L.; Russell, S.; Yurist-Doutsch, S.; Kuzeljevic, B.; Gold, M.J.; Britton, H.M.; Lefebvre, D.L.; et al. Early infancy microbial and metabolic alterations affect risk of childhood asthma. Sci. Transl. Med. 2015, 7, 307ra152. [Google Scholar] [CrossRef]
  106. Smart, B.A. Childhood Asthma After Bacterial Colonization of the Airway in Neonates. Pediatrics 2008, 122, S206–S207. [Google Scholar] [CrossRef] [Green Version]
  107. Mansbach, J.M.; Luna, P.N.; Shaw, C.A.; Hasegawa, K.; Petrosino, J.F.; Piedra, P.A.; Sullivan, A.F.; Espinola, J.A.; Stewart, C.; Camargo, C.A., Jr. Increased Moraxella and Streptococcus species abundance after severe bronchiolitis is associated with recurrent wheezing. J. Allergy Clin. Immunol. 2020, 145, 518–527.e8. [Google Scholar] [CrossRef] [Green Version]
  108. Thorsen, J.; Rasmussen, M.A.; Waage, J.; Mortensen, M.; Brejnrod, A.; Bønnelykke, K.; Chawes, B.L.; Brix, S.; Sørensen, S.J.; Stokholm, J.; et al. Infant airway microbiota and topical immune perturbations in the origins of childhood asthma. Nat. Commun. 2019, 10, 5001. [Google Scholar] [CrossRef] [Green Version]
  109. Ranucci, G.; Buccigrossi, V.; De Freitas, M.B.; Guarino, A.; Giannattasio, A. Early-Life Intestine Microbiota and Lung Health in Children. J. Immunol. Res. 2017, 2017, 8450496. [Google Scholar] [CrossRef]
  110. Hammad, H.; Chieppa, M.; Perros, F.; Willart, M.A.; Germain, R.N.; Lambrecht, B.N. House dust mite allergen induces asthma via Toll-like receptor 4 triggering of airway structural cells. Nat. Med. 2009, 15, 410–416. [Google Scholar] [CrossRef] [Green Version]
  111. Schuijs, M.J.; Willart, M.A.; Vergote, K.; Gras, D.; Deswarte, K.; Ege, M.J.; Madeira, F.B.; Beyaert, R.; van Loo, G.; Bracher, F.; et al. Farm dust and endotoxin protect against allergy through A20 induction in lung epithelial cells. Science 2015, 349, 1106–1110. [Google Scholar] [CrossRef]
  112. Le Noci, V.; Guglielmetti, S.; Tagliabue, E.; Sfondrini, L.; Arioli, S.; Camisaschi, C.; Bianchi, F.; Sommariva, M.; Storti, C.; Triulzi, T.; et al. Modulation of pulmonary microbiota by antibiotic or probiotic aerosol therapy: A strategy to promote immunosurveillance against lung metastases. Cell Rep. 2018, 24, 3528–3538. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  113. Hilty, M.; Burke, C.; Pedro, H.; Cardenas, P.; Bush, A.; Bossley, C.; Davies, J.; Ervine, A.; Poulter, L.; Pachter, L.; et al. Disordered microbial communities in asthmatic airways. PLoS ONE 2010, 5, e8578. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  114. Di Cicco, M.; Pistello, M.; Jacinto, T.; Ragazzo, V.; Piras, M.; Freer, G.; Pifferi, M.; Peroni, D. Does lung microbiome play a causal or casual role in asthma? Pediatr. Pulmonol. 2018, 53, 1340–1345. [Google Scholar] [CrossRef] [PubMed]
  115. Gollwitzer, E.S.; Saglani, S.; Trompette, A.; Yadava, K.; Sherburn, R.; McCoy, K.D.; Nicod, L.P.; Lloyd, C.M.; Marsland, B.J. Lung microbiota promotes tolerance to allergens in neonates via PD-L1. Nat. Med. 2014, 20, 642–647. [Google Scholar] [CrossRef] [PubMed]
  116. Genuneit, J. Exposure to farming environments in childhood and asthma and wheeze in rural populations: A systematic review with meta-analysis. Pediatr. Allergy Immunol. 2012, 23, 509–518. [Google Scholar] [CrossRef]
  117. Teo, S.M.; Mok, D.; Pham, K.; Kusel, M.; Serralha, M.; Troy, N.; Holt, B.J.; Hales, B.J.; Walker, M.L.; Hollams, E.; et al. The Infant Nasopharyngeal Microbiome Impacts Severity of Lower Respiratory Infection and Risk of Asthma Development. Cell Host Microbe 2015, 17, 704–715. [Google Scholar] [CrossRef] [Green Version]
  118. Mulder, B.; Pouwels, K.B.; Schuiling-Veninga, C.C.M.; Bos, H.J.; De Vries, T.W.; Jick, S.S.; Hak, E. Antibiotic use during pregnancy and asthma in preschool children: The influence of confounding. Clin. Exp. Allergy 2016, 46, 1214–1226. [Google Scholar] [CrossRef]
  119. Zhao, D.; Su, H.; Cheng, J.; Wang, X.; Xie, M.; Li, K.; Wen, L.; Yang, H. Prenatal antibiotic use and risk of childhood wheeze/asthma: A meta-analysis. Pediatr. Allergy Immunol. 2015, 26, 756–764. [Google Scholar] [CrossRef]
  120. Yoshida, S.; Ide, K.; Takeuchi, M.; Kawakami, K. Prenatal and early-life antibiotic use and risk of childhood asthma: A retrospective cohort study. Pediatr. Allergy Immunol. 2018, 29, 490–495. [Google Scholar] [CrossRef]
  121. Alhasan, M.M.; Cait, A.M.; Heimesaat, M.M.; Blaut, M.; Klopfleisch, R.; Wedel, A.; Conlon, T.M.; Yildirim, A.; Sodemann, E.B.; Mohn, W.W.; et al. Antibiotic use during pregnancy increases offspring asthma severity in a dose-dependent manner. Allergy 2020, 75, 1979–1990. [Google Scholar] [CrossRef] [Green Version]
  122. Durack, J.; Kimes, N.E.; Lin, D.L.; Rauch, M.; Mckean, M.; McCauley, K.; Panzer, A.R.; Mar, J.S.; Cabana, M.D.; Lynch, S.V. Delayed gut microbiota development in high-risk for asthma infants is temporarily modifiable by Lactobacillus supplementation. Nat. Commun. 2018, 9, 707. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  123. Durack, J.; Kimes, N.E.; Lin, D.; Mckean, M.; Rauch, M.; Cabana, M.D.; Lynch, S. Early-life Lactobacillus rhamnosus GG Supplementation of High-risk for Asthma Infants Reprograms Gut Microbiota Development and promotes regulatory T-cells. J. Allergy Clin. Immunol. 2017, 139, AB15. [Google Scholar] [CrossRef] [Green Version]
  124. Calder, P. Faculty of 1000 evaluation for Effects of early prebiotic and probiotic supplementation on development of gut microbiota and fussing and crying in preterm infants: A randomized, double-blind, placebo-controlled trial. F1000Prime Rep. 2013, 6, 793482506. [Google Scholar] [CrossRef]
  125. Dominguez-Bello, M.G.; De Jesus-Laboy, K.M.; Shen, N.; Cox, L.M.; Amir, A.; Gonzalez, A.; Bokulich, N.A.; Song, S.J.; Hoashi, M.; Rivera-Vinas, J.I.; et al. Partial restoration of the microbiota of cesarean-born infants via vaginal microbial transfer. Nat. Med. 2016, 22, 250–253. [Google Scholar] [CrossRef] [PubMed]
  126. Cunnington, A.J.; Sim, K.; Deierl, A.; Kroll, J.S.; Brannigan, E.; Darby, J. “Vaginal seeding” of infants born by caesarean section. BMJ 2016, 352, i227. [Google Scholar] [CrossRef] [Green Version]
  127. Galazzo, G.; van Best, N.; Bervoets, L.; Dapaah, I.O.; Savelkoul, P.H.; Hornef, M.W.; Lau, S.; Hamelmann, E.; Penders, J.; Hutton, E.K.; et al. Development of the Microbiota and Associations with Birth Mode, Diet, and Atopic Disorders in a Longitudinal Analysis of Stool Samples, Collected from Infancy Through Early Childhood. Gastroenterology 2020, 158, 1584–1596. [Google Scholar] [CrossRef]
  128. Abrahamsson, T.R.; Jakobsson, H.E.; Andersson, A.F.; Björkstén, B.; Engstrand, L.; Jenmalm, M.C. Low gut microbiota diversity in early infancy precedes asthma at school age. Clin. Exp. Allergy 2014, 44, 842–850. [Google Scholar] [CrossRef] [Green Version]
  129. Gao, Y.; Nanan, R.; Macia, L.; Tan, J.; Sominsky, L.; Quinn, T.P.; O’Hely, M.; Ponsonby, A.-L.; Tang, M.L.K.; Collier, F.; et al. The maternal gut microbiome during pregnancy and offspring allergy and asthma. J. Allergy Clin. Immunol. 2021, 148, 669–678. [Google Scholar] [CrossRef]
  130. Trompette, A.; Gollwitzer, E.S.; Yadava, K.; Sichelstiel, A.K.; Sprenger, N.; Ngom-Bru, C.; Blanchard, C.; Junt, T.; Nicod, L.P.; Harris, N.L.; et al. Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nat. Med. 2014, 20, 159–166. [Google Scholar] [CrossRef]
  131. Canani, R.B.; Costanzo, M.D.; Leone, L.; Pedata, M.; Meli, R.; Calignano, A. Potential beneficial effects of butyrate in intestinal and extraintestinal diseases. World J. Gastroenterol. 2011, 17, 1519–1528. [Google Scholar] [CrossRef]
  132. Udkoff, J.; Waldman, A.; Ahluwalia, J.; Borok, J.; Eichenfield, L.F. Current and emerging topical therapies for atopic dermatitis. Clin. Dermatol. 2017, 35, 375–382. [Google Scholar] [CrossRef] [PubMed]
  133. Brunner, P.M.; Leung, D.Y.M.; Guttman-Yassky, E. Immunologic, microbial, and epithelial interactions in atopic dermatitis. Ann. Allergy Asthma Immunol. 2018, 120, 34–41. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  134. Wollina, U. Microbiome in atopic dermatitis. Clin. Cosmet. Investig. Dermatol. 2017, 10, 51–56. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  135. Tong, J.; Li, H.Y. The human skin microbiome. In The Human Skin Microbiome; CABI: Wallingford, UK, 2014; pp. 72–89. [Google Scholar] [CrossRef]
  136. Grice, E.A.; Segre, J.A. The skin microbiome. Nat. Rev. Microbiol. 2011, 9, 244–253. [Google Scholar] [CrossRef]
  137. Baurecht, H.; Rühlemann, M.C.; Rodríguez, E.; Thielking, F.; Harder, I.; Erkens, A.-S.; Stölzl, D.; Ellinghaus, E.; Hotze, M.; Lieb, W.; et al. Epidermal lipid composition, barrier integrity, and eczematous inflammation are associated with skin microbiome configuration. J. Allergy Clin. Immunol. 2018, 141, 1668–1676.e16. [Google Scholar] [CrossRef] [Green Version]
  138. Geoghegan, J.A.; Irvine, A.D.; Foster, T.J. Staphylococcus aureus and Atopic Dermatitis: A Complex and Evolving Relationship. Trends Microbiol. 2018, 26, 484–497. [Google Scholar] [CrossRef]
  139. Watanabe, S.; Narisawa, Y.; Arase, S.; Okamatsu, H.; Ikenaga, T.; Tajiri, Y.; Kumemura, M. Differences in fecal microflora between patients with atopic dermatitis and healthy control subjects. J. Allergy Clin. Immunol. 2003, 111, 587–591. [Google Scholar] [CrossRef]
  140. Gołębiewski, M.; Łoś-Rycharska, E.; Sikora, M.; Grzybowski, T.; Gorzkiewicz, M.; Krogulska, A. Mother’s Milk Microbiome Shaping Fecal and Skin Microbiota in Infants with Food Allergy and Atopic Dermatitis: A Pilot Analysis. Nutrients 2021, 13, 3600. [Google Scholar] [CrossRef]
  141. Park, Y.M.; Lee, S.Y.; Kang, M.J.; Kim, B.S.; Lee, M.J.; Jung, S.S.; Yoon, J.S.; Cho, H.J.; Lee, E.; Yang, S.I.; et al. Imbalance of Gut, and Determines the Natural Course of Atopic Dermatitis in Infant. Allergy Asthma Immunol. Res. 2020, 12, 322–337. [Google Scholar] [CrossRef]
  142. Cukrowska, B.; Bierła, J.B.; Zakrzewska, M.; Klukowski, M.; Maciorkowska, E. The Relationship between the Infant Gut Microbiota and Allergy. The Role of Bifidobacterium breve and Prebiotic Oligosaccharides in the Activation of Anti-Allergic Mechanisms in Early Life. Nutrients 2020, 12, 946. [Google Scholar] [CrossRef] [Green Version]
  143. Huang, Y.J.; Marsland, B.J.; Bunyavanich, S.; O’Mahony, L.; Leung, D.Y.M.; Muraro, A.; Fleisher, T.A. The microbiome in allergic disease: Current understanding and future opportunities-2017 PRACTALL document of the American Academy of Allergy, Asthma & Immunology and the European Academy of Allergy and Clinical Immunology. J. Allergy Clin. Immunol. 2017, 139, 1099–1110. [Google Scholar] [PubMed] [Green Version]
  144. Malhotra, N.; Yoon, J.; Leyva-Castillo, J.M.; Galand, C.; Archer, N.; Miller, L.S.; Geha, R.S. IL-22 derived from γδ T cells restricts Staphylococcus aureus infection of mechanically injured skin. J. Allergy Clin. Immunol. 2016, 138, 1098–1107.e3. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  145. Kennedy, E.A.; Connolly, J.; Hourihane, J.O.; Fallon, P.G.; McLean, W.H.I.; Murray, D.; Jo, J.-H.; Segre, J.A.; Kong, H.H.; Irvine, A.D. Skin microbiome before development of atopic dermatitis: Early colonization with commensal staphylococci at 2 months is associated with a lower risk of atopic dermatitis at 1 year. J. Allergy Clin. Immunol. 2017, 139, 166–172. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  146. Salava, A.; Lauerma, A. Role of the skin microbiome in atopic dermatitis. Clin. Transl. Allergy 2014, 4, 33. [Google Scholar] [CrossRef] [Green Version]
  147. Laubereau, B.; Filipiak-Pittroff, B.; von Berg, A.; Grübl, A.; Reinhardt, D.; Wichmann, H.E.; Koletzko, S.; GINI Study Group. Caesarean section and gastrointestinal symptoms, atopic dermatitis, and sensitisation during the first year of life. Arch. Dis. Child 2004, 89, 993–997. [Google Scholar] [CrossRef] [Green Version]
  148. Richards, M.; Ferber, J.; Chen, H.; Swor, E.; Quesenberry, C.P.; Li, D.-K.; Darrow, L.A. Caesarean delivery and the risk of atopic dermatitis in children. Clin. Exp. Allergy 2020, 50, 805–814. [Google Scholar] [CrossRef]
  149. Lasley, M.V. Caesarean Delivery and the Risk of Atopic Dermatitis in Children. Pediatrics 2021, 148, S5–S6. [Google Scholar] [CrossRef]
  150. Shin, H.; Pei, Z.; Martinez, K.A., 2nd; Rivera-Vinas, J.I.; Mendez, K.; Cavallin, H.; Dominguez-Bello, M.G. The first microbial environment of infants born by C-section: The operating room microbes. Microbiome 2015, 3, 59. [Google Scholar] [CrossRef] [Green Version]
  151. Hendricks, A.J.; Mills, B.W.; Shi, V.Y. Skin bacterial transplant in atopic dermatitis: Knowns, unknowns and emerging trends. J. Dermatol. Sci. 2019, 95, 56–61. [Google Scholar] [CrossRef] [Green Version]
  152. Craig, J.M. Atopic dermatitis and the intestinal microbiota in humans and dogs. Vet. Med. Sci. 2016, 2, 95–105. [Google Scholar] [CrossRef]
  153. Zuo, W.; Sun, C. The Role of the Intestinal Microbiota in Atopic Dermatitis. Int. J. Dermatol. Venereol. 2021. ahead of print. [Google Scholar] [CrossRef]
  154. Penders, J.; Thijs, C.; van den Brandt, P.A.; Kummeling, I.; Snijders, B.; Stelma, F.; Adams, H.; van Ree, R.; Stobberingh, E.E. Gut microbiota composition and development of atopic manifestations in infancy: The KOALA Birth Cohort Study. Gut 2007, 56, 661–667. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  155. Abrahamsson, T.R.; Jakobsson, H.E.; Andersson, A.F.; Björkstén, B.; Engstrand, L.; Jenmalm, M.C. Low diversity of the gut microbiota in infants with atopic eczema. J. Allergy Clin. Immunol. 2012, 129, 434–440.e2. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  156. Forno, E.; Onderdonk, A.; McCracken, J.; Litonjua, A.; Laskey, D.; Delaney, M.; Dubois, A.; Gold, D.R.; Ryan, L.; Weiss, S.; et al. Diversity of the Gut Microbiota and Eczema in Infants. Am. J. Respir. Crit. Care Med. 2009, 179, A5981. [Google Scholar] [CrossRef]
  157. Rø, A.D.B.; Rø, T.B.; Storrø, O.; Johnsen, R.; Videm, V.; Øien, T.; Simpson, M.R. Reduced Th22 cell proportion and prevention of atopic dermatitis in infants following maternal probiotic supplementation. Clin. Exp. Allergy 2017, 47, 1014–1021. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  158. Kim, J.-H.; Kim, K.; Kim, W. Gut microbiota restoration through fecal microbiota transplantation: A new atopic dermatitis therapy. Exp. Mol. Med. 2021, 53, 907–916. [Google Scholar] [CrossRef] [PubMed]
  159. Mashiah, J.; Karady, T.; Fliss-Isakov, N.; Sprecher, E.; Slodownik, D.; Artzi, O.; Samuelov, L.; Ellenbogen, E.; Godneva, A.; Segal, E.; et al. Clinical efficacy of fecal microbial transplantation treatment in adults with moderate-to-severe atopic dermatitis. Immun. Inflamm. Dis. 2022, 10, e570. [Google Scholar] [CrossRef] [PubMed]
  160. Allam, J.-P.; Duan, Y.; Winter, J.; Stojanovski, G.; Fronhoffs, F.; Wenghoefer, M.; Bieber, T.; Peng, W.-M.; Novak, N. Tolerogenic T cells, Th1/Th17 cytokines and TLR2/TLR4 expressing dendritic cells predominate the microenvironment within distinct oral mucosal sites. Allergy 2011, 66, 532–539. [Google Scholar] [CrossRef]
  161. Moingeon, P. Update on Immune Mechanisms Associated with Sublingual Immunotherapy: Practical Implications for the Clinician. J. Allergy Clin. Immunol. Pract. 2013, 1, 228–241. [Google Scholar] [CrossRef]
  162. The Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature 2012, 486, 207–214. [Google Scholar] [CrossRef] [Green Version]
  163. Xiao, J.; Fiscella, K.A.; Gill, S.R. Oral microbiome: Possible harbinger for children’s health. Int. J. Oral Sci. 2020, 12, 12. [Google Scholar] [CrossRef] [PubMed]
  164. Lif Holgerson, P.; Harnevik, L.; Hernell, O.; Tanner, A.C.R.; Johansson, I. Mode of birth delivery affects oral microbiota in infants. J. Dent. Res. 2011, 90, 1183–1188. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  165. Jo, R.; Yama, K.; Aita, Y.; Tsutsumi, K.; Ishihara, C.; Maruyama, M.; Takeda, K.; Nishinaga, E.; Shibasaki, K.-I.; Morishima, S. Comparison of oral microbiome profiles in 18-month-old infants and their parents. Sci. Rep. 2021, 11, 861. [Google Scholar] [CrossRef] [PubMed]
  166. Von Mutius, E.; Vercelli, D. Farm living: Effects on childhood asthma and allergy. Nat. Rev. Immunol. 2010, 10, 861–868. [Google Scholar] [CrossRef] [PubMed]
  167. Jarvis, D.; Chinn, S.; Luczynska, C.; Burney, P. The association of family size with atopy and atopic disease. Clin. Exp. Allergy 1997, 27, 240–245. [Google Scholar] [CrossRef] [PubMed]
  168. Mortha, A.; Chudnovskiy, A.; Hashimoto, D.; Bogunovic, M.; Spencer, S.P.; Belkaid, Y.; Merad, M. Microbiota-Dependent Crosstalk Between Macrophages and ILC3 Promotes Intestinal Homeostasis. Science 2014, 343, 1249288. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  169. Vuillermin, P.J.; Macia, L.; Nanan, R.; Tang, M.L.; Collier, F.; Brix, S. The maternal microbiome during pregnancy and allergic disease in the offspring. Semin. Immunopathol. 2017, 39, 669–675. [Google Scholar] [CrossRef] [Green Version]
  170. Vuillermin, P.J.; O’Hely, M.; Collier, F.; Allen, K.J.; Tang, M.L.K.; Harrison, L.C.; Carlin, J.B.; Saffery, R.; Ranganathan, S.; Sly, P.D.; et al. Maternal carriage of Prevotella during pregnancy associates with protection against food allergy in the offspring. Nat. Commun. 2020, 11, 1452. [Google Scholar] [CrossRef] [Green Version]
  171. Wang, S.; Wei, Y.; Liu, L.; Li, Z. Association Between Breastmilk Microbiota and Food Allergy in Infants. Front. Cell. Infect. Microbiol. 2022, 11, 770913. [Google Scholar] [CrossRef]
  172. Thompson-Chagoyán, O.C.; Vieites, J.M.; Maldonado, J.; Edwards, C.; Gil, A. Changes in faecal microbiota of infants with cow’s milk protein allergy—A Spanish prospective case-control 6-month follow-up study. Pediatr. Allergy Immunol. 2010, 21, e394–e400. [Google Scholar] [CrossRef]
  173. Bunyavanich, S.; Shen, N.; Grishin, A.; Wood, R.; Burks, W.; Dawson, P.; Jones, S.M.; Leung, D.Y.M.; Sampson, H.; Sicherer, S.; et al. Early-life gut microbiome composition and milk allergy resolution. J. Allergy Clin. Immunol. 2016, 138, 1122–1130. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  174. Fazlollahi, M.; Chun, Y.; Grishin, A.; Wood, R.A.; Burks, A.W.; Dawson, P.; Jones, S.M.; Leung, D.Y.M.; Sampson, H.A.; Sicherer, S.H.; et al. Early-life gut microbiome and egg allergy. Allergy 2018, 73, 1515–1524. [Google Scholar] [CrossRef] [PubMed]
  175. Savage, J.H.; Lee-Sarwar, K.A.; Sordillo, J.; Bunyavanich, S.; Zhou, Y.; O’Connor, G.; Sandel, M.; Bacharier, L.B.; Zeiger, R.; Sodergren, E.; et al. A prospective microbiome-wide association study of food sensitization and food allergy in early childhood. Allergy 2018, 73, 145–152. [Google Scholar] [CrossRef] [PubMed]
  176. Hua, X.; Goedert, J.J.; Pu, A.; Yu, G.; Shi, J. Allergy associations with the adult fecal microbiota: Analysis of the American Gut Project. eBioMedicine 2016, 3, 172–179. [Google Scholar] [CrossRef] [Green Version]
  177. Feehley, T.; Plunkett, C.H.; Bao, R.; Hong, S.M.C.; Culleen, E.; Belda-Ferre, P.; Campbell, E.; Aitoro, R.; Nocerino, R.; Paparo, L.; et al. Healthy infants harbor intestinal bacteria that protect against food allergy. Nat. Med. 2019, 25, 448–453. [Google Scholar] [CrossRef]
  178. Lyons, A.; O’Mahony, D.; O’Brien, F.; MacSharry, J.; Sheil, B.; Ceddia, M.; Russell, W.M.; Forsythe, P.; Bienenstock, J.; Kiely, B.; et al. Bacterial strain-specific induction of Foxp3+T regulatory cells is protective in murine allergy models. Clin. Exp. Allergy 2010, 40, 811–819. [Google Scholar] [CrossRef]
  179. Stefka, A.T.; Feehley, T.; Tripathi, P.; Qiu, J.; McCoy, K.; Mazmanian, S.K.; Tjota, M.Y.; Seo, G.-Y.; Cao, S.; Theriault, B.R.; et al. Commensal bacteria protect against food allergen sensitization. Proc. Natl. Acad. Sci. USA 2014, 111, 13145–13150. [Google Scholar] [CrossRef] [Green Version]
  180. Berni Canani, R.; Sangwan, N.; Stefka, A.; Nocerino, R.; Paparo, L.; Aitoro, R.; Calignano, A.; Khan, A.A.; Gilbert, J.A.; Nagler, C.R. Lactobacillus rhamnosus GG-supplemented formula expands butyrate-producing bacterial strains in food allergic infants. ISME J. 2016, 10, 742–750. [Google Scholar] [CrossRef]
  181. Guest, J.F.; Fuller, G.W. Effectiveness of using an extensively hydrolyzed casein formula supplemented with Lactobacillus rhamnosus GG compared with an extensively hydrolysed whey formula in managing cow’s milk protein allergic infants. J. Comp. Eff. Res. 2019, 8, 1317–1326. [Google Scholar] [CrossRef] [Green Version]
  182. Luu, M.; Visekruna, A. Short-chain fatty acids: Bacterial messengers modulating the immunometabolism of T cells. Eur. J. Immunol. 2019, 49, 842–848. [Google Scholar] [CrossRef] [Green Version]
  183. Arpaia, N.; Campbell, C.; Fan, X.; Dikiy, S.; Van Der Veeken, J.; DeRoos, P.; Liu, H.; Cross, J.R.; Pfeffer, K.; Coffer, P.J.; et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 2013, 504, 451–455. [Google Scholar] [CrossRef] [PubMed]
  184. Furusawa, Y.; Obata, Y.; Fukuda, S.; Endo, T.A.; Nakato, G.; Takahashi, D.; Nakanishi, Y.; Uetake, C.; Kato, K.; Kato, T.; et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 2013, 504, 446–450, Erratum in Nature, 2014, 506, 254. [Google Scholar] [CrossRef] [PubMed]
  185. Smith, P.M.; Howitt, M.R.; Panikov, N.; Michaud, M.; Gallini, C.A.; Bohlooly, Y.-M.; Glickman, J.N.; Garrett, W.S. The Microbial Metabolites, Short-Chain Fatty Acids, Regulate Colonic Treg Cell Homeostasis. Science 2013, 341, 569–573. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  186. Cait, A.; Cardenas, E.; Dimitriu, P.A.; Amenyogbe, N.; Dai, D.; Cait, J.; Sbihi, H.; Stiemsma, L.; Subbarao, P.; Mandhane, P.J.; et al. Reduced genetic potential for butyrate fermentation in the gut microbiome of infants who develop allergic sensitization. J. Allergy Clin. Immunol. 2019, 144, 1638–1647.e3. [Google Scholar] [CrossRef] [Green Version]
  187. Urschel, D.; Hernandez-Trujillo, V. Butyrate as a Bioactive Human Milk Protective Component Against Food Allergy. Pediatrics 2021, 148, S21–S22. [Google Scholar] [CrossRef]
  188. Luu, M.; Monning, H.; Visekruna, A. Exploring the Molecular Mechanisms Underlying the Protective Effects of Microbial SCFAs on Intestinal Tolerance and Food Allergy. Front. Immunol. 2020, 11, 1225. [Google Scholar] [CrossRef]
  189. Di Costanzo, M.; Carucci, L.; Canani, R.B.; Biasucci, G. Gut Microbiome Modulation for Preventing and Treating Pediatric Food Allergies. Int. J. Mol. Sci. 2020, 21, 5275. [Google Scholar] [CrossRef]
  190. Berni Canani, R.; Di Costanzo, M.; Bedogni, G.; Amoroso, A.; Cosenza, L.; Di Scala, C.; Granata, V.; Nocerino, R. Extensively hydrolyzed casein formula containing Lactobacillus rhamnosus GG reduces the occurrence of other allergic manifestations in children with cow’s milk allergy: 3-year randomized controlled trial. J. Allergy Clin. Immunol. 2017, 139, 1906–1913.e4. [Google Scholar] [CrossRef] [Green Version]
  191. Wopereis, H.; Van Ampting, M.T.J.; Yavuz, A.C.; Slump, R.; Candy, D.C.A.; Butt, A.M.; Peroni, D.G.; Vandenplas, Y.; Fox, A.T.; Shah, N.; et al. A specific synbiotic-containing amino acid-based formula restores gut microbiota in non-IgE mediated cow’s milk allergic infants: A randomized controlled trial. Clin. Transl. Allergy 2019, 9, 27. [Google Scholar] [CrossRef]
  192. Fox, A.T.; Wopereis, H.; Van Ampting, M.T.J.; Oude Nijhuis, M.M.; Butt, A.M.; Peroni, D.G.; Vandenplas, Y.; Candy, D.C.A.; Shah, N.; West, C.E.; et al. A specific synbiotic-containing amino acid-based formula in dietary management of cow’s milk allergy: A randomized controlled trial. Clin. Transl. Allergy 2019, 9, 5. [Google Scholar] [CrossRef]
  193. Candy, D.C.A.; Van Ampting, M.T.J.; Oude Nijhuis, M.M.; Wopereis, H.; Butt, A.M.; Peroni, D.G.; Vandenplas, Y.; Fox, A.T.; Shah, N.; West, C.E.; et al. A synbiotic-containing amino-acid-based formula improves gut microbiota in non-IgE-mediated allergic infants. Pediatr. Res. 2018, 83, 677–686. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  194. Tang, M.L.K.; Ponsonby, A.-L.; Orsini, F.; Tey, D.; Robinson, M.; Su, E.L.; Licciardi, P.; Burks, W.; Donath, S. Administration of a probiotic with peanut oral immunotherapy: A randomized trial. J. Allergy Clin. Immunol. 2015, 135, 737–744.e8. [Google Scholar] [CrossRef] [PubMed]
  195. Borody, T.J.; Khoruts, A. Fecal microbiota transplantation and emerging applications. Nat. Rev. Gastroenterol. Hepatol. 2011, 9, 88–96. [Google Scholar] [CrossRef] [PubMed]
  196. Gupta, S.; Allen-Vercoe, E.; Petrof, E.O. Fecal microbiota transplantation: In perspective. Ther. Adv. Gastroenterol. 2015, 9, 229–239. [Google Scholar] [CrossRef] [PubMed] [Green Version]
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Figure 1. Maternal influencing factors for development of allergic diseases in infants. Maternal infectious diseases [35,36], asthma [37], antibiotic exposure [38,39], and high fat (energy) diet increase the risk of asthma in infants. High fiber diet [40], and Vitamin D [41] supplement during pregnancy could decrease the rate of asthma in children. Maternal stress [42,43] and high age [44] contribute to the development of food allergy in infants. High-energy diet during pregnancy increases the risk of AD in infants [45], while probiotics or a mixture of probiotics protects infants from AD risk [46]. High maternal age and certain geographic location (i.e., Asia) are closely related to increased infant allergic sensitization [47]. (Arrows, upward: increased risk for allergic diseases; downward: decreased risk for allergic diseases). (Created with BioRender.com).
Figure 1. Maternal influencing factors for development of allergic diseases in infants. Maternal infectious diseases [35,36], asthma [37], antibiotic exposure [38,39], and high fat (energy) diet increase the risk of asthma in infants. High fiber diet [40], and Vitamin D [41] supplement during pregnancy could decrease the rate of asthma in children. Maternal stress [42,43] and high age [44] contribute to the development of food allergy in infants. High-energy diet during pregnancy increases the risk of AD in infants [45], while probiotics or a mixture of probiotics protects infants from AD risk [46]. High maternal age and certain geographic location (i.e., Asia) are closely related to increased infant allergic sensitization [47]. (Arrows, upward: increased risk for allergic diseases; downward: decreased risk for allergic diseases). (Created with BioRender.com).
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Figure 2. Influencing factors in the development of allergic diseases in infancy. Factors such as antibiotic exposure [77], preterm birth [78], formula feeding [79], and cesarean section delivery [80] increase the development of asthma in infants, while living in a big family [81] and farming environment [82] decrease asthma incidents. Increased birth weight [83] and combined feeding of breast milk and formula [84] increase food allergy development in childhood. (Arrows, upward: increased risk for allergic diseases; downward: decreased risk for allergic diseases). (Created with BioRender.com).
Figure 2. Influencing factors in the development of allergic diseases in infancy. Factors such as antibiotic exposure [77], preterm birth [78], formula feeding [79], and cesarean section delivery [80] increase the development of asthma in infants, while living in a big family [81] and farming environment [82] decrease asthma incidents. Increased birth weight [83] and combined feeding of breast milk and formula [84] increase food allergy development in childhood. (Arrows, upward: increased risk for allergic diseases; downward: decreased risk for allergic diseases). (Created with BioRender.com).
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Figure 3. The role of maternal gut and milk microbiota and infant gut and lung microbiota in the development of asthma [59,91,105,117,127,128,129]. (Arrows, upward: increased relative abundance; downward: decreased relative abundance). (Created with BioRender.com).
Figure 3. The role of maternal gut and milk microbiota and infant gut and lung microbiota in the development of asthma [59,91,105,117,127,128,129]. (Arrows, upward: increased relative abundance; downward: decreased relative abundance). (Created with BioRender.com).
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Figure 4. The role of maternal gut and milk microbiota and infant gut and skin microbiota in the development of AD [33,137,138,139,140,141,142]. (Arrows, upward: increased relative abundance; downward: decreased relative abundance). (Created with BioRender.com).
Figure 4. The role of maternal gut and milk microbiota and infant gut and skin microbiota in the development of AD [33,137,138,139,140,141,142]. (Arrows, upward: increased relative abundance; downward: decreased relative abundance). (Created with BioRender.com).
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Figure 5. The role of maternal gut and milk microbiota and infant gut and oral microbiota in the development of FA [140,142,169,170,171]. (Arrows, upward: increased relative abundance; downward: decreased relative abundance). (Created with BioRender.com).
Figure 5. The role of maternal gut and milk microbiota and infant gut and oral microbiota in the development of FA [140,142,169,170,171]. (Arrows, upward: increased relative abundance; downward: decreased relative abundance). (Created with BioRender.com).
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Tuniyazi, M.; Li, S.; Hu, X.; Fu, Y.; Zhang, N. The Role of Early Life Microbiota Composition in the Development of Allergic Diseases. Microorganisms 2022, 10, 1190. https://doi.org/10.3390/microorganisms10061190

AMA Style

Tuniyazi M, Li S, Hu X, Fu Y, Zhang N. The Role of Early Life Microbiota Composition in the Development of Allergic Diseases. Microorganisms. 2022; 10(6):1190. https://doi.org/10.3390/microorganisms10061190

Chicago/Turabian Style

Tuniyazi, Maimaiti, Shuang Li, Xiaoyu Hu, Yunhe Fu, and Naisheng Zhang. 2022. "The Role of Early Life Microbiota Composition in the Development of Allergic Diseases" Microorganisms 10, no. 6: 1190. https://doi.org/10.3390/microorganisms10061190

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