Article Search
닫기

Microbiology and Biotechnology Letters

총설(Review)

View PDF

Environmental Microbiology (EM)  |  Microbial Ecology and Bioremediation

Microbiol. Biotechnol. Lett. 2021; 49(1): 1-8

https://doi.org/10.48022/mbl.2010.10011

Received: October 19, 2020; Accepted: November 2, 2020

Isolation of Novel Strains of Lactobacillus gasseri EJL and Bifidobacterium breve JTL from Breast Milk and Infant Feces: A Longitudinal Study of a Mother-infant Pair

Heetae Lee1, Chong-Kil Lee2 and Kyungjae Kim1*

1College of Pharmacy, Sahmyook University, Seoul 01795, Republic of Korea 2College of Pharmacy, Chungbuk National University, Cheongju 28644, Republic of Korea

Correspondence to :
Kyungjae Kim,
kimkj@syu.ac.kr

Human breast milk is a potential source of bacteria for the development of the intestinal microbiota of infants. Several species within the genera Lactobacillus and Bifidobacterium were demonstrated to shape the gut microbiota of infants. In this study, the bacterial diversity was investigated in the breast milk and feces of a mother-infant pair, and probiotic candidates were identified. Importantly, the novel L. gasseri EJL and B. breve JTL strains were isolated from breast milk and infant feces samples, respectively; their completed genome was resolved using de novo sequencing. In addition, the bacterial composition in the infant’s feces at 1 week revealed the prevalence of Bifidobacterium and Streptococcus; a higher diversity was observed after 3 weeks. In particular, the abundance of Akkermansia was sharply increased at 7 weeks, further increasing thereafter, up to 15 weeks. Our results suggest that human breast milk and infant’s feces are a source of probiotic candidates.

Keywords: Human breast milk, Lactobacillus gasseri, Bifidobacterium breve, gut microbiota, probiotics

Probiotics are defined as ‘live micro-organisms which when administered in adequate amounts confer a health benefit on the host’ [1]. An increasing number of studies have supported the health benefits of probiotics and highlighted the significant role of probiotics in the modulation of gut microbiota composition [2]. Dysbiosis of gut microbiota can lead to several diseases associated with host energy metabolism and immune system. Recent studies have highlighted the function of probiotics for health improvement [3, 4].

Human breast milk is the ultimate source of nutrition for newborns, and provides not only essential nutrition but also the micro-organisms for the development of initial intestinal microbiota [5, 6]. Several isolated bacterial species belonging to Lactobacillus, Bifidobacterium, and Streptococcus genera are potential probiotics with health benefits [7]. Microbiota in human breast milk is reported to be originated from the gut microbiota of mother’s intestine, and thus breastfeeding can have an important role in mother-to-infant microbial transmission [8, 9]. Moreover, breastfeeding has a protective effect against the development of various allergic diseases, including asthma and atopic dermatitis, in children via shaping of the gut microbiota [8], due to which probiotics of breast milk could be considered as a potential therapy for these diseases. In addition, recent studies have reported that certain Lactobacillus and Bifidobacterium strains isolated from breast milk and infant feces show protective effects against metabolic disorders, including obesity and hyperglycemia [10, 11].

Human breast milk and infant feces contain a variety of bacterial species. However, the potential candidates for use as beneficial probiotics have not been fully identified. This study aims to 1) identify the isolated potential probiotic candidates of Lactobacillus and Bifidobacterium strains, 2) investigate the bacterial diversity and vertical transfer of bacteria from breast milk to infant feces in one mother-to-infant pair.

Subjects and sample collection

One mother-baby pair was recruited in this longitudinal study. The mother was a 35-year-old Korean (BMI: 22.4) and had no underlying diseases. Male infant was delivered at 39 weeks’ gestation by spontaneous vaginal delivery. Mother was administered a probiotic formulation (Duolac-Gold, Cell Biotech Co. Ltd.) daily 20 weeks before delivery and the administration was discontinued after delivery. Probiotics formulation included Bifidobacterium latics (KCTC 11904BP), Bifidobacterium longum (KCTC 12200BP), Bifidobacterium bifidum (KCTC 12199BP), Lactobacillus acidophilus (KCTC 11906BP), Lactobacillus rhamnosus (KCTC 12202BP), and Streptococcus thermophilus (KCTC 11870BP). Mother and infant had no medical history and no antibiotics were used during the sampling period after birth. The infant was alternately fed breast milk and powdered formula without probiotics supplement.

Fecal samples and milk were collected from motherinfant pair at 1, 3, 5, 7, 9, 11, and 15 weeks. Prior to obtaining the milk samples using breast pump (after UV sterilization), the nipple and areola of the mother were cleaned with 70% isopropyl alcohol swabs. Fecal samples were collected in sterile containers and all samples were stored at -20℃ until shifting them to -70℃ in the laboratory. The study was approved by the Sahmyook University Institutional Review Board (2-104781-AB-N-012016115BR).

Isolation of Lactobacillus and Bifidobacterium

Lactobacillus was isolated from milk (1 week) and Bifidobacterium was isolated from infant feces (15 weeks), respectively. Milk and fecal samples were centrifuged at 5,000 g for 1 min. The supernatants were inoculated on MRS agar supplemented with 0.05% cysteine and incubated for 24−48 h at 37℃ under anaerobic conditions. Positive colonies, determined by PCR using primers for amplification of Lactobacillus (LacF-forward: AGCAGTAGGGAATCTTCCA, LacR-reverse: CACCGCTACACATGGAG) and Bifidobacterium (Bif164-forward: GGGTGGTAATGCCGGATG, Bif662-reverse: CCACCGTTACACCGGGAA), were sub-cultured in MRS broth supplemented with 0.05% cysteine. Bacterial glycerol stocks (20% v/v) were stored at -70℃ [12, 13].

Identification of isolates by 16S rDNA sequencing

Bacterial total DNA was extracted using ExgeneTM Cell SV mini (GeneAll Biotechnology Co., Ltd.), according to manufacturer’s instructions. 16S rRNA gene was amplified using 27f/1492r primer set (forward: 5′-AGAGTTTGATCCTGGCTCAG-3′, reverse: 5′-GGTTACCTTGTTACGACTT-3′). Each 25 μl PCR reaction mixture contained 2.5 μl 10X IP-Taq buffer I, 0.2 μl forward primer (50 uM), 0.2 μl reverse primer (50 uM), 0.5 μl IP - Taq DNA polymerase (2.5 u/ul), 1 μl dNTPs (each 2.5 mM), 1 μl DNA template, and 19.6 μl distilled water. PCR was performed in a T100TM thermal cycler (Bio-Rad Laboratories, Inc.) using the following cycling conditions: initial denaturation at 95℃ for 5 min, 35 cycles of denaturation at 95℃ for 30 s, annealing at 50℃ for 30 s, and extension at 72℃ for 30 s. A final extension was performed at 72℃ for 10 min. Amplified PCR products were separated by electrophoresis on a 1% agarose gel, extracted using FavorPrepTM GEL/PCR Purification Mini Kit (Favorgen Biotech Co.). Sequence analysis of the products was contracted out to a Cosmo Genetech, South Korea. The sequences were compared to those in the GenBank database using the NCBI BLAST search program. Phylogenetic analysis was performed to confirm the taxonomy of the isolated genus Lactobacillus and Bifidobacterium using the neighbor-joining method [14]. The nucleotide sequences were analyzed against the reference sequences of Lactobacillus and Bifidobacterium, using MEGA X software.

De novo whole genome sequencing

Library preparation and sequencing were conducted by Theragen Bio Itex, South Korea. Briefly, sequences of quality control-passed genomic DNA from isolates were produced by PacBio RS II sequencing system. Whole genome de novo assembly was performed using Canu (ver. 1.7). Prokka (ver. 1.13) was used for gene prediction, and gene annotation was performed using UniProt, RefSeq, and Pfam database. Bacterial diversity of breast milk and feces Total bacterial DNA was extracted from milk and fecal samples using a PowerSoil DNA Isolation Kit (MO BIO Laboratories Inc.), according to manufacturer’s instruction. 16S rDNA genes were amplified using the 341F/ 785R primer set targeting the V3-V4 region (forward primer: 5′- TCGTCGGCAGCGTCAGATGTGTATAAGA GACAGCCTACGGGNGGCWGCAG-3′; reverse primer: 5′ GTCTCGTGGGCTCGGAGATGTGTATAAGAGACA GGACTACHVGGGTATCTAATCC-3′). Sequencing of partial bacterial 16S rRNA genes was performed using the MiSeq Reagent Kit V3 (600 cycles) and MiSeq platform (Illumina) at Theragen Etex, Korea. After preprocessing (adaptor trimming, merge paired-end reads, quality control, and removal of chimeric sequence), sequences were assigned to operational taxonomic units (genus level, OTUs, 97% identity) using RDP classifier v.2.11. Additionally, taxonomy profiles of the bacterial species were identified using Cd-hit v.4.6 by comparing with NCBI Megablast database (identify > 99%, coverage > 80%).

Phylogenetic analysis of isolated Lactobacillus and Bifidobacterium strains

Amplified PCR products of 16S rRNA gene from milk and infant feces were identified as novel strains of L. gasseri and B. breve, respectively, using the NCBI BLAST search program. In the phylogenetic analysis, the isolates from milk and infant feces were compared to 16 representative Lactobacillus strains and 13 Bifidobacterium strains, and were confirmed to be L. gasseri and B. breve, respectively (Figs. 1A and 1B).

Figure 1.Phylogenetic tree of bacterial species of genus Lactobacillus (A) and Bifidobacterium (B). The tree was constructed using the MEGA X software with neighbor-joining method. Bacillus subtilis and Lactobacillus acidophilus were used as the outgroup micro-organisms. The GenBank accession numbers are shown in parenthesis. *: Isolates in this study.

Whole-genome sequencing of L. gasseri EJL and B. breve JTL

The genomic attributes of L. gasseri EJL and B. breve JTL are provided in Table 1. The final assembly of L. gasseri EJL was composed of total 2,289,039 bp, with a mean G + C content of 35.0% from three contigs, and contained 2,325 coding genes (CDS), 14 of rRNA genes, and 65 of tRNA genes. In B. breve JTL, total 2,289,549 of bp, with a mean G + C content of 58.5% from one contig were identified, and contained 1,874 coding genes (CDS), 6 of rRNA genes, and 54 of tRNA genes. The nucleic acid sequences of novel L. gasseri EJL and B. breve JTL strains were deposited into GenBank and assigned Gen- Bank accession numbers CP054875 and CP053940, respectively.

Table 1 . Genome features of L. gasseri EJL and B. breve JTL.

AttributesStrains
L. gasseri EJLB. breve JTL
No. of bases2,289,0392,289,549
G + C content (%)35.058.5
No. of contigs31
Coding genes (CDS)2,3251,874
rRNA146
tRNA6554


Bacterial community profiles of the fecal and breast milk microbiota from mother and infant

Infant’s fecal samples (n = 7) at 1, 3, 5, 7, 9, 11, and 15 weeks and mother’s fecal (n = 2) and milk (n = 2) samples at 1 and 15 weeks were analyzed for bacterial community. A total of 1,168,314 sequence reads were generated from 11 samples. An average of 97,360 ± 33,681 reads were covered per sample. The lowest Shannon diversity index was observed in infant’s feces at 1 week, which increased after 3 weeks. The Shannon diversity index of mother’s feces and milk were higher than that of infant’s feces (Fig. S1).

Composition of the fecal and milk microbiota obtained from mother and infant

In mother’s fecal samples, the most abundant bacterial phyla at 1 and 15 weeks were Bacteroidetes (56.9% and 59.1%), followed by Firmicutes (39.8% and 33.7%). In contrast, in breast milk, Firmicutes (61.1% and 41.5%) was the most abundant bacterial phylum, while Bacteroidetes (0.9% and 8.1%) was relatively low, instead Proteobacteria was 14.1% and 30.1%, Actinobacteria was 22.3% and 15.7% at 1 and 15 weeks, respectively. In infant fecal samples, Firmicutes (58.1% and 27.1%) was most abundant, while Bacteroidetes was under 1% at both 1 and 15 weeks. In contrast, Proteobacteria was 0.2% and 15.1%, Actinobacteria was 41.6% and 20.4% at 1 and 15 weeks, respectively. Interestingly, Verrucomicrobia was hardly detected at 1 week, but increased to 37.3% at 15 weeks. The relative abundances of the bacterial phyla are described in Figure S2.

At the genus level, Bacteroides (43.5%), Gemmiger (11.1%), and Megamonas (8.0%) were most abundant at 1 week, while Bacteroides (51.1%), Megamonas (10.5%), and Parabacteroides (3.7%) were most abundant at 15 weeks in the mother’s fecal samples. In breast milk, Streptococcus (26.8%), Rothia (16.1%), and Veillonella (14.8%) were most abundant at 1 week, and Streptococcus (20.3%), Haemophilus (14.3%), and Rothia (12.3%) were most abundant at 15 weeks. The bacterial composition in infant feces at 1 week included genus Bifidobacterium(41.4%) and Streptococcus (57.8%), and a higher diversity was observed after 3 weeks. Relative abundances of Bifidobacterium and Streptococcus gradually decreased to 20.3% and 5.1%, respectively, at 15 weeks, and were replaced by Lactobacillus, Veillonella, Klebsiella, and Enterococcus. In particular, a sharp increase in the abundance of Akkermansia was seen at 7 weeks (51.6%) and continued until 15 weeks (37.3%). The relative abundances of the bacterial genera are described in Figs. 2 and S3.

Figure 2.Relative abundance of bacteria at genus level in infant feces from 1 to 15 weeks after birth. Top 20 abundant bacterial genera are shown. Sequencing of partial bacterial 16S rRNA genes targeting to V3-V4 region was performed using the MiSeq Reagent Kit V3 (600 cycles) and MiSeq platform (Illumina), and sequences were assigned to operational taxonomic units (genus level, OTUs, 97% identity) using RDP classifier v.2.11. Bacterial composition in infant feces at 1 week were mostly comprised of genus Bifidobacterium and Streptococcus, and a higher diversity was observed after 3 weeks. Abundances of Lactobacillus, Veillonella, Klebsiella, and Enterococcus increased after birth and replaced the abundance of Bifidobacterium and Streptococcus. In particular, the abundance of Akkermansia was sharply increased at 7 weeks, continued until 15 weeks.

Relative abundance of Lactobacillus and Bifidobacterium strains in feces and breast milk

The relative abundance of genus Lactobacillus and Bifidobacterium were 0.4% and 0.05% at 1 week and 1.1% and 0.6% at 15 weeks, respectively, in fecal samples, and 6.3% and 0.04% at 1 week, and 1.3% and 0.06% at 15 weeks in breast milk. In infant fecal samples, Lactobacillus was hardly detected at 1 week and was 1.6% at 15 weeks, whereas Bifidobacterium was 41.4% and 20.3% at 1 and 15 weeks, respectively. In the mother’s fecal samples, four Lactobacillus species and one Bifidobacterium species were identified at 1 week and 15 weeks, respectively. In breast milk, 12 Lactobacillus species and 3 Bifidobacterium species and 12 Lactobacillus species and 4 Bifidobacterium species were identified at 1 week and 15 weeks, respectively. In infant fecal samples, B. longum (41.4%) was only identified at 1 week, which was the same as the species found in the probiotics formulation. In addition, B. breve (17.5%) and B. stellenboschense (0.005%) were identified at 15 weeks. L. rhamnosus, the same species as in the probiotics formulation, was identified in breast milk (0.002%) and infant fecal samples (0.03%) at 15 weeks. In addition, L. gasseri (0.3% and 1.5%), and L. johnsonii (0.01% and 0.02%) were identified at 15 weeks in both milk and infant fecal samples. The relative abundances of the bacterial genera are described in Table S1.

Breast milk was identified as a source of abundant bacteria, using culture-independent genome sequencing. Two novel strains, namely L. gasseri EJL and B. breve JTL, were isolated in breast milk and infant feces, respectively, and their complete genomes were constructed using de novo sequencing. In addition, as breastfeeding has an impact on the construction of intestinal microbial community in infants, the changes in fecal microbiota composition of infant was investigated for 15 weeks after birth.

Breast milk is the potential source of bacteria for infant intestinal track (estimated as 1 × 105 to 1 × 107 bacteria daily in 800 ml/day of breast milk) [15]. Specific bacterial strains such as Bifidobacterium, Lactobacillus, and Staphylococcus are transferred from mother to infant, and thus mother and infant share similar bacterial strains through breast-feeding [16, 17]. Among them, Lactobacillus strains such as L. fermentum L. rhamnosus, and L. gasseri have demonstrated potential probiotic properties, and were reported to have beneficial health effects, including anti-inflammation and metabolic improvements [18, 19]. In this study, a novel Lactobacillus strain, L. gasseri EJL, was isolated in breast milk and its complete genome was identified. This strain would be further evaluated for potential clinical applications in future studies.

Moreover, the composition of microbiota in breast milk varies within individuals and at different time periods, which in turn may be affected by the type of birth and maternal clinical factors [20, 21]. A recent study reported that Lactobacillus strains were not detected in colostrum [22]. Interestingly, in this study, Lactobacillus strains were more abundant in colostrum (6.3%) when compared to that in mature breast milk (0.8%). In addition, while several Lactobacillus strains, including L. rhamnosus, L. salivarius, L. fermentum, and L. reuteri, are known components of breast milk [23], this study identified additional Lactobacillus strains, such as L. johnsonii and L. oris from breast milk. Recently, the probiotic properties and health benefits of these strains have been reported [24, 25]. Thus, breast milk can be considered as a source of potential probiotics. Although there is a consensus that breast milk is the gold standard for infant nutrition, the effect of compositional differences of breast milk on the infant’s health is not clear. Therefore, to better understand the importance of breast milk, the role of the breast milk-associated microbiota should be investigated in future studies.

In this study, B. breve JTL was another isolate identified in the feces of the infant after receiving breast milk. Low concentrations of Bifidobacterium strains comprised the microbiota of breast milk, whereas Bifidobacterium was the major component of the microbiota in infant feces. Moreover, B. longum was the only Bifidobacterium strain identified in infant at 1 week and the diversity of Bifidobacterium strains increased through breastfeeding. In particular, the abundance of B. breve was more dominant than B. longum at 15 weeks. Recent studies have reported that the transfer of B. breve to infant occurs through breast milk [26, 27], and human milk oligosaccharides (HMOs), which are the major components of breast milk, promote the dominance of Bifidobacterium sp. in early infancy [28]. In this study, B. breve JTL may have been transferred from mother to infant through breastfeeding. In addition, the supplementation of Bifidobacterium to infant had an impact on the fecal microbiota and metabolome [29]. Settled Bifidobacterium strains, such as B. longum and B. breve. in infant gut may have beneficial effects in the development of immune system and metabolism. For example, early gut colonization by Bifidobacterium had protective effects on allergic diseases [30, 31], and abundance of these strains in early infancy have been related with the vaccine response [32].

Among the bacterial strains in probiotics formulation that the mother was administered during pregnancy, B. longum, L. rhamnosus, and S. thermophilus were detected in mother’s feces, breast milk, and infant feces, whereas B. bifidum was detected only in breast milk. Since the coincidence of these sequences was not confirmed, it is not reasonable to consider the strains in infant feces the same as those in the probiotics formulation. Nevertheless, it could be used as a reference while selecting a probiotics formulation for pregnancy and breastfeeding because the microbial composition of breast milk is suggested to be originated from the gut microbiota of the mother [9].

In conclusion, novel strains of L. gasseri EJL and B. breve JTL were isolated from breast milk and infant feces, respectively, and their completed genomes were constructed using de novo sequencing. Diverse probiotics candidates were identified in breast milk and infant feces in this longitudinal study of one mother-infant pair. L. gasseri EJL and B. breve JTL may have been transferred from mother to infant through breastfeeding. The potential probiotic properties for clinical application will be evaluated in the future.

This work was supported by the Sahmyook University Research Fund [RI12020003 (2020)].

The authors have no financial conflicts of interest to declare.

  1. Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, et al. 2014. Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat. Rev. Gastroenterol. Hepatol. 11: 506-514.
    Pubmed CrossRef
  2. Valdes AM, Walter J, Segal E, Spector TD. 2018. Role of the gut microbiota in nutrition and health. BMJ 361: k2179.
    Pubmed KoreaMed CrossRef
  3. Hemarajata P, Versalovic J. 2013. Effects of probiotics on gut microbiota: mechanisms of intestinal immunomodulation and neuromodulation. Therap. Adv. Gastroenterol. 6: 39-51.
    Pubmed KoreaMed CrossRef
  4. Amabebe E, Robert FO, Agbalalah T, Orubu ESF. 2020. Microbial dysbiosis-induced obesity: role of gut microbiota in homoeostasis of energy metabolism. Br. J. Nutr. 123: 1127-1137.
    Pubmed CrossRef
  5. Bravi F, Wiens F, Decarli A, Dal Pont A, Agostoni C, Ferraroni M. 2016. Impact of maternal nutrition on breast-milk composition: a systematic review. Am. J. Clin. Nutr. 104: 646-662.
    Pubmed CrossRef
  6. Gopalakrishna KP, Hand TW. 2020. Influence of maternal milk on the neonatal intestinal microbiome. Nutrients 12: 823.
    Pubmed KoreaMed CrossRef
  7. Damaceno QS, Souza JP, Nicoli JR, Paula RL, Assis GB, Figueiredo HC, et al. 2017. Evaluation of potential probiotics isolated from human milk and colostrum. Probiotics Antimicrob. Proteins 9: 371-379.
    Pubmed CrossRef
  8. Le Doare K, Holder B, Bassett A, Pannaraj PS. 2018. Mother's milk: A purposeful contribution to the development of the infant microbiota and immunity. Front. Immunol. 9: 361.
    Pubmed KoreaMed CrossRef
  9. Fernandez L, Langa S, Martin V, Maldonado A, Jimenez E, Martin R, et al. 2013. The human milk microbiota: origin and potential roles in health and disease. Pharmacol. Res. 69: 1-10.
    Pubmed CrossRef
  10. Jung SP, Lee KM, Kang JH, Yun SI, Park HO, Moon Y, et al. 2013. Effect of Lactobacillus gasseri BNR17 on overweight and obese adults: A randomized, double-blind clinical trial. Korean J. Fam. Med. 34: 80-89.
    Pubmed KoreaMed CrossRef
  11. Bozzi Cionci N, Baffoni L, Gaggia F, Di Gioia D. 2018. Therapeutic microbiology: The role of Bifidobacterium breve as food supplement for the prevention/treatment of paediatric diseases. Nutrients 10: 1723.
    Pubmed KoreaMed CrossRef
  12. Walter J, Hertel C, Tannock GW, Lis CM, Munro K, Hammes WP. 2001. Detection of Lactobacillus, Pediococcus, Leuconostoc, and Weissella species in human feces by using group-specific PCR primers and denaturing gradient gel electrophoresis. Appl. Environ. Microbiol. 67: 2578-2585.
    Pubmed KoreaMed CrossRef
  13. Satokari RM, Vaughan EE, Akkermans AD, Saarela M, de Vos WM. 2001. Bifidobacterial diversity in human feces detected by genus-specific PCR and denaturing gradient gel electrophoresis. Appl. Environ. Microbiol. 67: 504-513.
    Pubmed KoreaMed CrossRef
  14. Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406-425.
  15. Heikkila MP, Saris PE. 2003. Inhibition of Staphylococcus aureus by the commensal bacteria of human milk. J. Appl. Microbiol. 95: 471-478.
    Pubmed CrossRef
  16. Ferretti P, Pasolli E, Tett A, Asnicar F, Gorfer V, Fedi S, et al. 2018. Mother-to-infant microbial transmission from different body sites shapes the developing infant gut microbiome. Cell Host Microbe. 24: 133-145. e.
    Pubmed KoreaMed CrossRef
  17. Martin V, Maldonado-Barragan A, Moles L, Rodriguez-Banos M, Campo RD, Fernandez L, et al. 2012. Sharing of bacterial strains between breast milk and infant feces. J. Hum. Lact. 28: 36-44.
    Pubmed CrossRef
  18. Oh NS, Joung JY, Lee JY, Kim Y. 2018. Probiotic and anti-inflammatory potential of Lactobacillus rhamnosus 4B15 and Lactobacillus gasseri 4M13 isolated from infant feces. PLoS One 13: e0192021.
    Pubmed KoreaMed CrossRef
  19. Asan-Ozusaglam M, Gunyakti A. 2019. Lactobacillus fermentum strains from human breast milk with probiotic properties and cholesterol-lowering effects. Food Sci. Biotechnol. 28: 501-509.
    Pubmed KoreaMed CrossRef
  20. Hermansson H, Kumar H, Collado MC, Salminen S, Isolauri E, Rautava S. 2019. Breast milk microbiota is shaped by mode of delivery and intrapartum antibiotic exposure. Front. Nutr. 6: 4.
    Pubmed KoreaMed CrossRef
  21. Moossavi S, Sepehri S, Robertson B, Bode L, Goruk S, Field CJ, et al. 2019. Composition and variation of the human milk microbiota are influenced by maternal and early-life factors. Cell Host Microbe. 25: 324-335. e.
    Pubmed CrossRef
  22. Parnanen K, Karkman A, Hultman J, Lyra C, Bengtsson-Palme J, Larsson DGJ, et al. 2018. Maternal gut and breast milk microbiota affect infant gut antibiotic resistome and mobile genetic elements. Nat. Commun. 9: 3891.
    Pubmed KoreaMed CrossRef
  23. Martin R, Heilig GH, Zoetendal EG, Smidt H, Rodriguez JM. 2007. Diversity of the Lactobacillus group in breast milk and vagina of healthy women and potential role in the colonization of the infant gut. J. Appl. Microbiol. 103: 2638-2644.
    Pubmed CrossRef
  24. Davoren MJ, Liu J, Castellanos J, Rodriguez-Malave NI, Schiestl RH. 2019. A novel probiotic, Lactobacillus johnsonii 456, resists acid and can persist in the human gut beyond the initial ingestion period. Gut Microbes 10: 458-480.
    Pubmed KoreaMed CrossRef
  25. Anandharaj M, Sivasankari B. 2014. Isolation of potential probiotic Lactobacillus oris HMI68 from mother's milk with cholesterol-reducing property. J. Biosci. Bioeng. 118: 153-159.
    Pubmed CrossRef
  26. Kordy K, Gaufin T, Mwangi M, Li F, Cerini C, Lee DJ, et al. 2020. Contributions to human breast milk microbiome and enteromammary transfer of Bifidobacterium breve. PLoS One 15: e0219633.
    Pubmed KoreaMed CrossRef
  27. Mikami K, Takahashi H, Kimura M, Isozaki M, Izuchi K, Shibata R, et al. 2009. Influence of maternal bifidobacteria on the establishment of bifidobacteria colonizing the gut in infants. Pediatr. Res. 65: 669-674.
    Pubmed CrossRef
  28. Lawson MAE, O'Neill IJ, Kujawska M, Gowrinadh Javvadi S, Wijeyesekera A, Flegg Z, et al. 2020. Breast milk-derived human milk oligosaccharides promote Bifidobacterium interactions within a single ecosystem. ISME J. 14: 635-648.
    Pubmed KoreaMed CrossRef
  29. Bazanella M, Maier TV, Clavel T, Lagkouvardos I, Lucio M, Maldonado-Gomez MX, et al. 2017. Randomized controlled trial on the impact of early-life intervention with bifidobacteria on the healthy infant fecal microbiota and metabolome. Am. J. Clin. Nutr. 106: 1274-1286.
    Pubmed CrossRef
  30. Ismail IH, Boyle RJ, Licciardi PV, Oppedisano F, Lahtinen S, Robins-Browne RM, et al. 2016. Early gut colonization by Bifidobacterium breve and B. catenulatum differentially modulates eczema risk in children at high risk of developing allergic disease. Pediatr. Allergy Immunol. 27: 838-846.
    Pubmed CrossRef
  31. Reddel S, Del Chierico F, Quagliariello A, Giancristoforo S, Vernocchi P, Russo A, et al. 2019. Gut microbiota profile in children affected by atopic dermatitis and evaluation of intestinal persistence of a probiotic mixture. Sci. Rep. 9: 4996.
    Pubmed KoreaMed CrossRef
  32. Huda MN, Ahmad SM, Alam MJ, Khanam A, Kalanetra KM, Taft DH, et al. 2019. Bifidobacterium abundance in early infancy and vaccine response at 2 years of age. Pediatrics 143: e20181489.
    Pubmed KoreaMed CrossRef

Starts of Metrics

Share this article on :

Related articles in MBL

Most Searched Keywords ?

What is Most Searched Keywords?

  • It is most registrated keyword in articles at this journal during for 2 years.