Vaginal seeding

Last updated

The Human Microbiome Project (HMP), completed in 2012, laid the foundation for further investigation into the role the microbiome plays in overall health and disease. One area of particular interest is the role which delivery mode plays in the development of the infant/neonate microbiome and what potential implications this may have long term. It has been found that infants born via vaginal delivery have microbiomes closely mirroring that of the mother's vaginal microbiome, whereas those born via cesarean section tend to resemble that of the mother's skin. [1] One notable study from 2010 illustrated an abundance of Lactobacillus and other typical vaginal genera in stool samples of infants born via vaginal delivery and an abundance of Staphylococcus and Corynebacterium, commonly found on the skin surfaces, in stool samples of infants born via cesarean section. [2] From these discoveries came the concept of vaginal seeding, also known as microbirthing, [3] which is a procedure whereby vaginal fluids (and hence vaginal microbes) are applied to a new-born child delivered by caesarean section. The idea of vaginal seeding was explored in 2015 after Maria Gloria Dominguez-Bello discovered that birth by caesarean section significantly altered the newborn child's microbiome compared to that of natural birth. [4] The purpose of the technique is to recreate the natural transfer of bacteria that the baby gets during a vaginal birth. It involves placing swabs in the mother's vagina, and then wiping them onto the baby's face, mouth, eyes and skin. [5] Due to the long-drawn nature of studying the impact of vaginal seeding, there are a limited number of studies available that support or refute its use. [6] The evidence suggests that applying microbes from the mother's vaginal canal to the baby after cesarean section may aid in the partial restoration of the infant's natural gut microbiome with an increased likelihood of pathogenic infection to the child via vertical transmission. [7] [8]

Contents

History

Theodor Rosebury began his study of the human microbiota in 1928. More than thirty years later, he published Microorganisms Indigenous to Man. In this book, he discussed the importance of microbial colonization after birth and its role in forming the infant microbiome. [9] In 2015, Rosebery's perspective of microbial colonization after birth was further elucidated by a group of researchers in the United States. Studies performed by Maria Gloria Dominguez-Bello and her team indicated that the microbiome of a child born by cesarean section was significantly different from that of a child delivered by natural birth. [4] It has been found that infants born via cesarean section lack bacteroide species until 6-18. Interestingly, a study performed at Mass General Hospital published in 2020 found no significant difference in bacteroide species colonization between pre-labor c-sections and post-labor c-sections, indicating that vaginal exposure may not be the sole driving force for bacteroides colonization. [10]

Understanding the Vaginal Microbiome

Given that the vaginal microbiome is thought to be influential in the development of the neonatal microbiome, it is important to understand and acknowledge it's complexity. Early studies into the vaginal microbiome revealed a predominance of Lactobacillus species. Similarly, a 2021 study evaluating impacts of the maternal vaginal microbiome composition on the development of the infant gut microbiome in early life found that the vaginal microbiome of the pregnant participants was dominated by one of several species of Lactobacillus, with four species appearing most common. [11]

Around 1914 the association between anaerobic cocci and abnormal vaginal discharge was first established. Later, in 1955, Gardnerella vaginalis was identified as a causative agent for bacterial vaginosis (BV). This was further complicated in the 1990s when several other species were discovered from anaerobic cultures from individuals with symptoms corresponding to BV. One commonality remained throughout those experiencing symptoms of BV; The depletion of lactic acid producing bacterial species. The presence of BV has been subsequently linked to preterm birth as well as increased risk for development of sexually transmitted disease which is thought to be linked to the deficiency of Lactobacillus species, as they produce lactic acid and H2O2 which is thought to have protective properties against some pathogenic bacteria/viruses. [12] Another interesting component of the vaginal microbiome comes with its stability and variability over time. A 2012 study published in Science Translational Medicine investigated the temporal dynamics of the vaginal microbiota and found that the stability of the vaginal microbiome over time was highly individual. Some of the participants tended to exhibit higher variability over the course of the 16 weeks study with up to three alterations in their vaginal microbiome during that time. In contrast, others exhibited almost complete stability throughout the course of the study. [13]

Fluctuations in the vaginal microbiome have been demonstrated with the menstrual cycle and intercourse. Fluctuations brought on during pregnancy have also been an area of interest as nearly all organ systems change during pregnancy to promote and maintain the pregnancy. It is known that pregnancy results in thickening of the vaginal mucosa and an increase in cervical secretions which in turn leads to smooth muscle cell hypertrophy and relaxation of the connective tissue. In addition, vaginal epithelium also exhibits hypertrophy which subsequently leads to crowding of the epithelial cells which themselves are rich in glycogen. Throughout the duration of gestation, the rising estrogen leads to additional increases in glycogen which is then metabolized into lactic acid which causes the vagina to become more acidic. This in turn causes an increase in Lactobacillus growth in the vagina. Interestingly, a 2009 study of longitudinal analysis of the vaginal microflora in pregnancy found that 56.5% of participants who initially had lactobacilli-diminished vaginal microbiomes during the first trimester of pregnancy developed a prevalence of the lactobacilli later in pregnancy, hinting towards the importance this genus may play in a neonate. [14]  

Purpose

In the early life of animals, as well as humans, the development of the immune system and metabolism is influenced by the infant's microbiota, and alteration, dysbiosis, in the microbiota can either prevent or cause disease. [15] [16] The method of birth, whether vaginal or caesarean section, determines the exposure and colonization of the infant's gut microbiota. The purpose behind the practice of vaginal seeding or micro birthing is that it allows an infant delivered via caesarean section to come in contact with microbes from the birth canal. Infants delivered vaginally are exposed to beneficial microorganisms known as microbiota when they travel down the birth canal. Infants are exposed to critical bacteria via vaginal birth, such as Lactobacillus, Prevotella, Bacteroides, Escherichia/Shigella, and Bifidobacterium. Bifidobacterium is a key bacteria in the nourishment of the infants, development of immunity, and maturation of the intestinal tissue. [17] The expectation is that this may boost their gut bacteria and lessen the danger of health issues normally associated with caesarian infants. It contributes to the seeding of the infant's gut. [18]

The baby is exposed to the mother's vaginal microbes that wash over the child in the birth canal, which coves the skin, and enters the baby's eyes, ears, nose, and mouth. These microbes often travel down into the gut after being swallowed. It is said that these microbes are important in the postnatal development of the immune system of the baby. [19]

In the event that a C-section is done before labour starts or before a woman's water breaks, the infant will not come into contact with maternal vaginal fluid or bacteria. Instead, they come in contact with skin microbes, such as Staphylococcus, Streptococcus, Veillonella, and Corynebacterium. [6] a very different set of species. [20] These differences, in turn, have been associated with increased risks of asthma, allergies, obesity, and immune deficiencies. Thus, these differences appear more often in infants after a caesarean delivery than after a vaginal delivery, according to certain epidemiological data. [21] In fact, in the United States, studies have found that 64-82% of neonatal cases of methicillin-resistant Staphylococcus aureus infections of the skin were found to occur in those born via C-section. [22]

Evidence

Evidence suggests that cesarean delivery can increase the risk for inflammatory and metabolic diseases in infants. [8] It is unclear whether vaginal seeding has long-term benefits or whether it is safe. In 2016 a small study of 18 infants was published in the Journal Nature Medicine to look into the benefits of vaginal seeding. The microbiome of the four cesarean delivered infants receiving the microbial transfer was found to have a similar microbiome to the seven vaginally delivered infants. [7] The results of the study suggest that vaginal seeding partially restores the neonatal microbiome. [7] However, the study authors acknowledged that the long-term consequences of vaginal seeding remain unclear due to limited data.

In 2017, a subsequent study was published which found that there was not a big difference, after six weeks, between the microbes of infants born vaginally versus those who delivered by C-section without receiving vaginal seeding. [23] Certain scholars have pointed out that a baby's exposure to bacteria begins even before birth and more research is required on this matter. [24]

Risks

The scientific evidence regarding the short and long-term benefits of vaginal seeding, as well as the risks involved, is limited. Due to the widespread clinical advice given against performing vaginal seeding, there is insufficient support for the procedure. [25] Following a nonclinical vaginal seeding procedure, there was a reported case of localized neonatal herpes simplex virus (HSV) infection, however, it cannot be supported that the infection was due to the procedure or another factor. [25]

Infants delivered by C-section are at a lower danger of exchange of some potentially harmful microbes and infections from the birth canal. Although it remains unknown, vaginal seeding procedures may take these harmful microorganisms, including undetected sexually transmitted infections (STIs) and unintentionally transfer them to the infant. This could potentially cause an infection. [20] It has been proposed that implementing a screening protocol for potential vaginal pathogens may be beneficial when considering vaginal seeding. [26]

An editorial written in the British Medical Journal is advising practitioners and parents to not perform vaginal seeding as there is not enough evidence that it is beneficial for infants and could potentially put babies' health at risk. [27]

The American College of Obstetricians and Gynecologists (ACOG) also does not encourage or recommend vaginal seeding due to lack of evidence. [28]

Additional Areas of Interest Regarding the Infant Microbiome

Currently, the establishment of the infant microbiome including what influences are associated with optimal versus dysbiotic outcomes remains as a key component of health research. As of late, there have been only few studies evaluating the potential relationship between the maternal vaginal microbiome and the gut microbiome of the infant from the species or strain level. In context of the bacterial baptism hypothesis, this is essential, as merely reporting a genre (such as Lactobacillus) would fail to provide insight for the assessment of vertical transmission. [29] Presence or absence of certain species within the same genre may greatly alter functionality, making further investigation into the implication of specie variation an important component of both further research of the vaginal microbiome and development of the infant microbiome. Additionally, maternal alterations in the intestinal microbiome during pregnancy may also play a role in the microbial colonization of vaginally delivered infants. When comparing stool samples from first and third trimester women, a 2012 study, Host remodeling of the gut microbiome and metabolic changes during pregnancy, discovered there is an increase in Proteobacteria as pregnancy progresses. [30] Given the potential maternal fecal contamination that is prone to occur during vaginal delivery, it is important to consider how alterations in the intestinal microbiome during pregnancy may influence microbial colonization of the infant. Furthermore, examination of the intestinal microbiome of infants born via cesarean versus vaginal delivery have revealed differences in colonization between the two groups however, further studies have suggested that the bacterial enzymes were not altered in the stool of these infants between the two delivery modes, making it unclear whether the type of microbe or the enzymatic activities and byproducts it produces are more important for the infant [31] .   

See also

Related Research Articles

<span class="mw-page-title-main">Caesarean section</span> Surgical procedure in which a baby is delivered through an incision in the mothers abdomen

Caesarean section, also known as C-section or caesarean delivery, is the surgical procedure by which one or more babies are delivered through an incision in the mother's abdomen. It is often performed because vaginal delivery would put the mother or child at risk. Reasons for the operation include obstructed labor, twin pregnancy, high blood pressure in the mother, breech birth, shoulder presentation, and problems with the placenta or umbilical cord. A caesarean delivery may be performed based upon the shape of the mother's pelvis or history of a previous C-section. A trial of vaginal birth after C-section may be possible. The World Health Organization recommends that caesarean section be performed only when medically necessary.

<span class="mw-page-title-main">Human microbiome</span> Microorganisms in or on human skin and biofluids

The human microbiome is the aggregate of all microbiota that reside on or within human tissues and biofluids along with the corresponding anatomical sites in which they reside, including the gastrointestinal tract, skin, mammary glands, seminal fluid, uterus, ovarian follicles, lung, saliva, oral mucosa, conjunctiva, and the biliary tract. Types of human microbiota include bacteria, archaea, fungi, protists, and viruses. Though micro-animals can also live on the human body, they are typically excluded from this definition. In the context of genomics, the term human microbiome is sometimes used to refer to the collective genomes of resident microorganisms; however, the term human metagenome has the same meaning.

<span class="mw-page-title-main">Gut microbiota</span> Community of microorganisms in the gut

Gut microbiota, gut microbiome, or gut flora are the microorganisms, including bacteria, archaea, fungi, and viruses, that live in the digestive tracts of animals. The gastrointestinal metagenome is the aggregate of all the genomes of the gut microbiota. The gut is the main location of the human microbiome. The gut microbiota has broad impacts, including effects on colonization, resistance to pathogens, maintaining the intestinal epithelium, metabolizing dietary and pharmaceutical compounds, controlling immune function, and even behavior through the gut–brain axis.

Caesarean delivery on maternal request (CDMR) is a caesarean section birth requested by the pregnant woman without a medical reason.

Dysbiosis is characterized by a disruption to the microbiome resulting in an imbalance in the microbiota, changes in their functional composition and metabolic activities, or a shift in their local distribution. For example, a part of the human microbiota such as the skin flora, gut flora, or vaginal flora, can become deranged, with normally dominating species underrepresented and normally outcompeted or contained species increasing to fill the void. Similar to the human gut microbiome, diverse microbes colonize the plant rhizosphere, and dysbiosis in the rhizosphere, can negatively impact plant health. Dysbiosis is most commonly reported as a condition in the gastrointestinal tract or plant rhizosphere.

<span class="mw-page-title-main">Vaginal flora</span> Microorganisms present in the vagina

Vaginal flora, vaginal microbiota or vaginal microbiome are the microorganisms that colonize the vagina. They were discovered by the German gynecologist Albert Döderlein in 1892 and are part of the overall human flora. The amount and type of bacteria present have significant implications for an individual's overall health. The primary colonizing bacteria of a healthy individual are of the genus Lactobacillus, such as L. crispatus, and the lactic acid they produce is thought to protect against infection by pathogenic species.

<span class="mw-page-title-main">Vaginal delivery</span> Delivery through the vagina

A vaginal delivery is the birth of offspring in mammals through the vagina. It is the most common method of childbirth worldwide. It is considered the preferred method of delivery, with lower morbidity and mortality than caesarean sections (C-sections).

<span class="mw-page-title-main">Oral microbiology</span>

Oral microbiology is the study of the microorganisms (microbiota) of the oral cavity and their interactions between oral microorganisms or with the host. The environment present in the human mouth is suited to the growth of characteristic microorganisms found there. It provides a source of water and nutrients, as well as a moderate temperature. Resident microbes of the mouth adhere to the teeth and gums to resist mechanical flushing from the mouth to stomach where acid-sensitive microbes are destroyed by hydrochloric acid.

<span class="mw-page-title-main">Human Microbiome Project</span> Former research initiative

The Human Microbiome Project (HMP) was a United States National Institutes of Health (NIH) research initiative to improve understanding of the microbiota involved in human health and disease. Launched in 2007, the first phase (HMP1) focused on identifying and characterizing human microbiota. The second phase, known as the Integrative Human Microbiome Project (iHMP) launched in 2014 with the aim of generating resources to characterize the microbiome and elucidating the roles of microbes in health and disease states. The program received $170 million in funding by the NIH Common Fund from 2007 to 2016.

<span class="mw-page-title-main">Microbiota</span> Community of microorganisms

Microbiota are the range of microorganisms that may be commensal, mutualistic, or pathogenic found in and on all multicellular organisms, including plants. Microbiota include bacteria, archaea, protists, fungi, and viruses, and have been found to be crucial for immunologic, hormonal, and metabolic homeostasis of their host.

Prevotella is a genus of Gram-negative bacteria.

The initial acquisition of microbiota is the formation of an organism's microbiota immediately before and after birth. The microbiota are all the microorganisms including bacteria, archaea and fungi that colonize the organism. The microbiome is another term for microbiota or can refer to the collected genomes.

The vaginal flora in pregnancy, or vaginal microbiota in pregnancy, is different from the vaginal flora before sexual maturity, during reproductive years, and after menopause. A description of the vaginal flora of pregnant women who are immunocompromised is not covered in this article. The composition of the vaginal flora significantly differs in pregnancy. Bacteria or viruses that are infectious most often have no symptoms.

<span class="mw-page-title-main">Placental microbiome</span>

The placental microbiome is the nonpathogenic, commensal bacteria claimed to be present in a healthy human placenta and is distinct from bacteria that cause infection and preterm birth in chorioamnionitis. Until recently, the healthy placenta was considered to be a sterile organ but now genera and species have been identified that reside in the basal layer.

<span class="mw-page-title-main">Uterine microbiome</span>

The uterine microbiome is the commensal, nonpathogenic, bacteria, viruses, yeasts/fungi present in a healthy uterus, amniotic fluid and endometrium and the specific environment which they inhabit. It has been only recently confirmed that the uterus and its tissues are not sterile. Due to improved 16S rRNA gene sequencing techniques, detection of bacteria that are present in low numbers is possible. Using this procedure that allows the detection of bacteria that cannot be cultured outside the body, studies of microbiota present in the uterus are expected to increase.

<span class="mw-page-title-main">Pharmacomicrobiomics</span>

Pharmacomicrobiomics, proposed by Prof. Marco Candela for the ERC-2009-StG project call, and publicly coined for the first time in 2010 by Rizkallah et al., is defined as the effect of microbiome variations on drug disposition, action, and toxicity. Pharmacomicrobiomics is concerned with the interaction between xenobiotics, or foreign compounds, and the gut microbiome. It is estimated that over 100 trillion prokaryotes representing more than 1000 species reside in the gut. Within the gut, microbes help modulate developmental, immunological and nutrition host functions. The aggregate genome of microbes extends the metabolic capabilities of humans, allowing them to capture nutrients from diverse sources. Namely, through the secretion of enzymes that assist in the metabolism of chemicals foreign to the body, modification of liver and intestinal enzymes, and modulation of the expression of human metabolic genes, microbes can significantly impact the ingestion of xenobiotics.

<span class="mw-page-title-main">Human milk microbiome</span> Community of microorganisms in human milk

The human milk microbiota, also known as human milk probiotics (HMP), encompasses the microbiota–the community of microorganisms–present within the human mammary glands and breast milk. Contrary to the traditional belief that human breast milk is sterile, advancements in both microbial culture and culture-independent methods have confirmed that human milk harbors diverse communities of bacteria. These communities are distinct in composition from other microbial populations found within the human body which constitute the human microbiome.

<span class="mw-page-title-main">Human milk immunity</span> Protection provided to immune system via human milk

Human milk immunity is the protection provided to the immune system of an infant via the biologically active components in human milk. Human milk was previously thought to only provide passive immunity primarily through Secretory IgA, but advances in technology have led to the identification of various immune-modulating components. Human milk constituents provide nutrition and protect the immunologically naive infant as well as regulate the infant's own immune development and growth.

<span class="mw-page-title-main">María Gloria Domínguez-Bello</span> American microbial ecologist

María Gloria Domínguez-Bello is a Venezuelan-American microbial ecologist that has worked on adaptations of gut fermentation organs in animals, gastric colonization by bacteria, assembly of the microbiota in early life, effect of practices that reduce microbiota transmission and colonization in humans, and effect of urbanization. She is the Henry Rutgers Professor of Microbiome and Health at Rutgers University, New Brunswick. Her lab at collaborates in multidisciplinary science, integrating microbiology, immunology, pediatrics, nutrition, anthropology, environmental engineering and architecture/urban studies, and microbial ecology.

References

  1. ↑ Stinson, Lisa F. (2018). "A Critical Review of the Bacterial Baptism Hypothesis and the Impact of Cesarean Delivery on the Infant Microbiome". Frontiers in Medicine. 5 (135). doi: 10.3389/fmed.2018.00135 . PMC   5945806 . PMID   29780807.
  2. ↑ Dos Santos, Scott; Pakzad, Zahra; Elwood, Chelsea; Albert, Arianne; Gantt, Soren; Manges, Amee; Dumonceaux, Tim (2021). "Early Neonatal Meconium Does Not Have a Demonstrable Microbiota Determined through Use of Robust Negative Controls with cpn60-Based Microbiome Profiling". Microbiology Spectrum. 9 (2): e0006721. doi:10.1128/Spectrum.00067-21. PMC   8557823 . PMID   34585952.
  3. ↑ Smith L (23 August 2017). "Vaginal seeding: Doctors warn new mothers not to embrace dangerous 'microbirthing' trend". Independent UK. Retrieved 19 April 2018.
  4. 1 2 Shin H, Pei Z, Martinez KA, Rivera-Vinas JI, Mendez K, Cavallin H, Dominguez-Bello MG (December 2015). "The first microbial environment of infants born by C-section: the operating room microbes". Microbiome. 3 (1): 59. doi: 10.1186/s40168-015-0126-1 . PMC   4665759 . PMID   26620712.
  5. ↑ "What is vaginal seeding?". Tommy's Midwives' blog. 31 August 2017. Archived from the original on 27 October 2018. Retrieved 27 October 2018.
  6. 1 2 Mueller NT, Hourigan SK, Hoffmann DE, Levy L, von Rosenvinge EC, Chou B, Dominguez-Bello MG (December 2019). "Bacterial Baptism: Scientific, Medical, and Regulatory Issues Raised by Vaginal Seeding of C-Section-Born Babies". The Journal of Law, Medicine & Ethics. 47 (4): 568–578. doi:10.1177/1073110519897732. PMC   7908762 . PMID   31957590.
  7. 1 2 3 Dominguez-Bello MG, De Jesus-Laboy KM, Shen N, Cox LM, Amir A, Gonzalez A, et al. (March 2016). "Partial restoration of the microbiota of cesarean-born infants via vaginal microbial transfer". Nature Medicine. 22 (3): 250–3. doi:10.1038/nm.4039. PMC   5062956 . PMID   26828196.
  8. 1 2 Haahr T, Glavind J, Axelsson P, Bistrup Fischer M, Bjurström J, Andrésdóttir G, et al. (April 2018). "Vaginal seeding or vaginal microbial transfer from the mother to the caesarean-born neonate: a commentary regarding clinical management". BJOG. 125 (5): 533–536. doi: 10.1111/1471-0528.14792 . PMID   28626982. S2CID   35508700.
  9. ↑ Yong E (2016). I contain multitudes : the microbes within us and a grander view of life (First ed.). New York, NY. ISBN   978-0-06-236859-1. OCLC   925497449.{{cite book}}: CS1 maint: location missing publisher (link)
  10. ↑ Mitchell, Caroline M.; Mazzoni, Chiara; Hogstrom, Larson; Bryant, Allison; Bergerat, Agnes; Cher, Avital; Pochan, Shawna; Herman, Penelope; Carrigan, Maureen; Sharp, Karen; Huttenhower, Curtis; Lander, Eric S.; Vlamakis, Hera; Xavier, Ramnik J.; Yassour, Moran (December 2020). "Delivery Mode Affects Stability of Early Infant Gut Microbiota". Cell Reports Medicine. 1 (9): 100156. doi:10.1016/j.xcrm.2020.100156. ISSN   2666-3791. PMC   7762768 . PMID   33377127.
  11. ↑ Dos Santos, Scott; Pakzad, Zahra; Elwood, Chelsea; Albert, Arianne; Gantt, Soren; Manges, Amee; Dumonceaux, Tim (2021). "Early Neonatal Meconium Does Not Have a Demonstrable Microbiota Determined through Use of Robust Negative Controls with cpn60-Based Microbiome Profiling". Microbiology Spectrum. 9 (2): e0006721. doi:10.1128/Spectrum.00067-21. PMC   8557823 . PMID   34585952.
  12. ↑ Price, Amanda L.; Chu, Derrick M.; Seferovic, Maxim D.; Antony, Kathleen M.; Ma, Jun; Aagaard, Kjersti M. (2015). "The Perinatal Microbiome and Pregnancy: Moving Beyond the Vaginal Microbiome". Cold Spring Harbor Perspectives in Medicine. 5 (6): a023051. doi: 10.1101/cshperspect.a023051 . PMC   4448707 . PMID   25775922.
  13. ↑ Gajer, Pawel; Brotman, Rebecca M.; Bai, Guoyun; Sakamoto, Joyce (2013). "Temporal Dynamics of the Human Vaginal Microbiota". Science Translational Medicine. 4 (132). doi:10.1126/scitranslmed.3003605. PMC   3722878 . PMID   22553250.
  14. ↑ Verstraelen, Hans; Verhelst, Rita; Claeys, Geert; De Backer, Ellen; Temmerman, Marleen; Vaneechoutte, Mario (2009). "Longitudinal analysis of the vaginal microflora in pregnancy suggests that L. crispatus promotes the stability of the normal vaginal microflora and that L. gasseri and/or L. iners are more conducive to the occurrence of abnormal vaginal microflora". BMC Microbiology. 9 (116): 116. doi: 10.1186/1471-2180-9-116 . PMC   2698831 . PMID   19490622.
  15. ↑ Cunnington AJ, Sim K, Deierl A, Kroll JS, Brannigan E, Darby J (February 2016). ""Vaginal seeding" of infants born by caesarean section" (PDF). BMJ. 352: i227. doi:10.1136/bmj.i227. hdl: 10044/1/29238 . PMID   26906151. S2CID   34819384. Archived from the original (PDF) on 3 March 2016.
  16. ↑ CBEd, Sam McCulloch Dip (7 April 2016). "Is Vaginal Seeding Dangerous?". BellyBelly.
  17. ↑ Salas Garcia, Mariana C.; Yee, Alyson L.; Gilbert, Jack A.; Dsouza, Melissa (2018). "Dysbiosis in Children Born by Caesarean Section". Annals of Nutrition and Metabolism. 73 (Suppl. 3): 24–32. doi: 10.1159/000492168 . ISSN   0250-6807. PMID   30041170.
  18. ↑ Dominguez-Bello MG, De Jesus-Laboy KM, Shen N, Cox LM, Amir A, Gonzalez A, et al. (March 2016). "Partial restoration of the microbiota of cesarean-born infants via vaginal microbial transfer". Nature Medicine. 22 (3): 250–3. doi:10.1038/nm.4039. PMC   5062956 . PMID   26828196.
  19. ↑ Neu J, Rushing J (June 2011). "Cesarean versus vaginal delivery: long-term infant outcomes and the hygiene hypothesis". Clinics in Perinatology. 38 (2): 321–31. doi:10.1016/j.clp.2011.03.008. PMC   3110651 . PMID   21645799.
  20. 1 2 Cunnington A (26 March 2016). "What Is Vaginal Seeding?". IFLScience. Archived from the original on 31 March 2016. Retrieved 27 October 2018.
  21. ↑ Laubereau B, Filipiak-Pittroff B, von Berg A, Grübl A, Reinhardt D, Wichmann HE, Koletzko S (November 2004). "Caesarean section and gastrointestinal symptoms, atopic dermatitis, and sensitisation during the first year of life". Archives of Disease in Childhood. 89 (11): 993–7. doi:10.1136/adc.2003.043265. PMC   1719727 . PMID   15499049.
  22. ↑ Stinson, Lisa F. (2018). "A Critical Review of the Bacterial Baptism Hypothesis and the Impact of Cesarean Delivery on the Infant Microbiome". Frontiers in Medicine. 5 (135). doi: 10.3389/fmed.2018.00135 . PMC   5945806 . PMID   29780807.
  23. ↑ O'Malley K (18 April 2018). "Vaginal Seeding: What Is It And Why Is It So Controversial?". ELLE. Retrieved 27 October 2018.
  24. ↑ Martinelli K (November 2017). "Why Vaginal Seeding May Be a Trend to Avoid" . Retrieved 27 October 2018.
  25. 1 2 Mueller, Noel T.; Hourigan, Suchitra K.; Hoffmann, Diane E.; Levy, Lauren; von Rosenvinge, Erik C.; Chou, Betty; Dominguez-Bello, Maria-Gloria (2019). "Bacterial Baptism: Scientific, Medical, and Regulatory Issues Raised by Vaginal Seeding of C-Section-Born Babies". Journal of Law, Medicine & Ethics. 47 (4): 568–578. doi:10.1177/1073110519897732. ISSN   1073-1105. PMC   7908762 . PMID   31957590.
  26. ↑ Limaye, Meghana A.; Ratner, Adam J. (2020). "'Vaginal seeding' after a caesarean section provides benefits to newborn children". BJOG: An International Journal of Obstetrics & Gynaecology. 127 (2): 302. doi:10.1111/1471-0528.15977. ISSN   1471-0528. PMID   31692198. S2CID   207902502.
  27. ↑ Cunnington AJ, Sim K, Deierl A, Kroll JS, Brannigan E, Darby J (February 2016). ""Vaginal seeding" of infants born by caesarean section" (PDF). BMJ. 352: i227. doi:10.1136/bmj.i227. hdl: 10044/1/29238 . PMID   26906151. S2CID   34819384. Archived from the original (PDF) on 3 March 2016.
  28. ↑ Committee on Obstetric Practice (November 2017). "Vaginal Seeding Not Recommended for Infants - ACOG". The American College of Obstetricians and Gynecologists (ACOG). Retrieved 27 October 2018.
  29. ↑ Stinson, Lisa F. (2018). "A Critical Review of the Bacterial Baptism Hypothesis and the Impact of Cesarean Delivery on the Infant Microbiome". Frontiers in Medicine. 5 (135). doi: 10.3389/fmed.2018.00135 . PMC   5945806 . PMID   29780807.
  30. ↑ Koren, Omry; Goodrich, Julia K; Cullender, Tyler C.; Spor, Ayme; Laitinen, Krisi (2013). "Host remodeling of the gut microbiome and metabolic changes during pregnancy". Cell. 150 (3): 470–480. doi: 10.1016/j.cell.2012.07.008 . PMC   3505857 . PMID   22863002. S2CID   12107857.
  31. ↑ Gronlund, M M; Salminen, S; Mykkanen, H; Kero, P; Lehtonen, O P (1999). "Development of intestinal bacterial enzymes in infants-- relationship to mode of delivery and type of feeding". APMIS. 107 (7): 655–660. doi:10.1111/j.1699-0463.1999.tb01455.x. PMID   10440061. S2CID   23217535.

This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.