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© 2008 American Society for Nutrition

Supplement: Influence of Diet on Infection and Allergy in Infants

Cesarean Delivery May Affect the Early Biodiversity of Intestinal Bacteria1,2

Giacomo Biasucci3,*, Belinda Benenati3, Lorenzo Morelli4, Elena Bessi5 and Günther Boehm6,7

3 Department of Paediatrics and Neonatology, "Guglielmo da Saliceto Hospital," Piacenza, Italy; 4 Institute of Microbiology, Università Cattolica del Sacro Cuore, Piacenza, Italy, 5 AAT- Advanced Analytical Technologies Srl, Piacenza, Italy; 6 Numico Research, Friedrichsdorf, Germany; and 7 Sophia's Hospital, Erasmus University, Rotterdam, The Netherlands

* To whom correspondence should be addressed. E-mail: g.biasucci{at}ausl.pc.it.


   ABSTRACT
TOP
 ABSTRACT
Introduction
 Subjects, Materials, and Methods
 Results and Discussion
 LITERATURE CITED
 
The gastrointestinal tract of neonates becomes colonized immediately after birth with environmental microorganisms, mainly from the mother; strong evidence suggests that the early composition of the microbiota of neonates plays an important role for the postnatal development of the immune system. The present study was designed to evaluate by means of a molecular biology approach the relation between the intestinal ecosystem of the newborn and the mode of delivery. The intestinal bacterial composition on d 3 of life was investigated in 23 infants born by vaginal delivery and in 23 infants delivered by cesarean section. PCR-denaturing gradient gel electrophoresis and PCR-temperature gradient gel electrophoresis have been utilized, together with the specific amplifications for 10 Bifidobacterium species, 3 Ruminococcus species, and Bacteroides. The intestinal microbiota of neonates delivered by cesarean delivery appears to be less diverse, in terms of bacteria species, than the microbiota of vaginally delivered infants. The intestinal microbiota after cesarean delivery is characterized by an absence of Bifidobacteria species. Vaginally delivered neonates, even if they showed individual microbial profiles, were characterized by predominant groups such as B. longum and B. catenulatum. Our data demonstrate that the mode of delivery has a deep impact on the composition of the intestinal microbiota at the very beginning of human life. This study opens the path to further investigations to confirm the link between microbiota composition and immune system development and to identify tools for the modulation of the intestinal microbiota of cesarean-delivered neonates. Additionally, we underline the importance of adequate microbiological tools used to support clinically relevant trials, if intestinal microbiota is considered as a study outcome.


   Introduction
TOP
 ABSTRACT
 Introduction
Subjects, Materials, and Methods
 Results and Discussion
 LITERATURE CITED
 
The intestinal microbiota composition of the neonate has not been clearly defined yet, as many bacterial species living in the gut are unculturable under laboratory conditions. An alternative approach for microbial identification is provided by culture-independent techniques such as the exploitation, by means of molecular biology techniques, of polymorphisms of genes encoding for bacterial 16S rRNA (1). These techniques have been applied to evaluate the gut microbiota composition of adults and infants, but a lack of knowledge still exists on the comparison of gut microbiota of neonates delivered by cesarean section to the microbiota of naturally delivered babies.

The gastrointestinal tract of newborns is sterile, but it becomes colonized immediately after birth with organisms from the environment, mainly from the mother. During vaginal delivery, the contact with the vaginal and intestinal flora is an important source for the start of the infant's colonization (2). During cesarean delivery, direct contact of the mouth of the newborn with the vaginal and intestinal microbiota is absent, and environmental bacteria play an important role for infants' intestinal colonization. Some authors have suggested that the composition of the very first human microbiota could have long-lasting effects, up to months (3) or even years (4).

There is accumulating evidence that intestinal bacteria play an important role in the postnatal development of the immune system (5,6). Thus, if the intestinal flora develops differently depending on the mode of delivery, the postnatal development of the immune system might also be different. Available epidemiological data show that atopic diseases appear more often in infants after cesarean delivery than after vaginal delivery (7–10). The composition of enteric microbiota in early days of life seems therefore to be a very important factor for achieving and maintaining good health in the years to come. It follows that it is fundamental to identify more thoroughly the intestinal ecosystem of the newborn.

In this study, we investigated the influence of mode of delivery (cesarean delivery vs. vaginal delivery) on the intestinal microbial composition on d 3 of life using PCR-denaturing gradient gel electrophoresis (DGGE) and PCR-temperature gradient gel electrophoresis (TGGE). Both DGGE and TGGE analyses have been utilized, together with the specific amplifications for 10 Bifidobacterium species, 3 Ruminococcus species, and Bacteroides, all playing a very relevant physiological role in the intestinal ecosystem of the newborn (11).


   Subjects, Materials, and Methods
TOP
 ABSTRACT
 Introduction
 Subjects, Materials, and Methods
Results and Discussion
 LITERATURE CITED
 
Forty-six term infants born in October 2003 at the Guglielmo da Saliceto Hospital, Piacenza, Italy were eligible for the study (Table 1).


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  		TABLE 1 Clinical characteristics of subjects enrolled1

 
The study protocol was approved by the local Medical Ethical Committee. In this study, written informed consent was obtained from parents of all the enrolled newborns, whether born by vaginal or cesarean delivery. The study was designed to consecutively recruit all the eligible cesarean and the immediately following spontaneously delivered babies. Exclusion criteria were prematurity, maternal infections during pregnancy, maternal clinical illness, maternal specific dietary regimen (i.e., vegetarian or any exclusion diet for any reason) as reported by means of last-week dietary recall, maternal antibiotic administration, or probiotic supplementation during the last 2 wk of gestation, intrapartum antibiotic prophylaxis, and babies given antibiotic prophylaxis or therapy. All babies enrolled were of Caucasian origin; none of the babies enrolled were fed infant formula; and all were breast-fed on demand. The fecal samples were obtained on d 3 of life, before the infants' discharge from the hospital and were stored at –20°C in sterile containers until the analysis.

DNA analysis

Bacterial DNA was extracted using PSP Spin Stool DNA kit (Invitek, Berlin).

The differentiation of the amplicons obtained through the amplification of bacterial DNA was achieved by DGGE and TGGE techniques.

    DGGE and TGGE analysis with PCR amplification. To amplify V6-V8 regions on bacterial DNA, we utilized U968-GC-f and L1401-r primers (11). To amplify specific regions for Bifidobacterium spp., primers Bif164-f and Bif662-GC-r were used (12).

    DGGE analysis of amplified samples. The fragments obtained by PCR as reported were separated through DGGE (Biorad) as described by Favier et al. (11), using a 40–50% gradient for separating fragments obtained by amplification of regions V6-V8 and a 45–55% gradient for fragments obtained with primers for Bifidobacterium. The electrophoretic run was carried out for 16 h at 85 V. DNA fragments, separated by DGGE, were extracted from the electrophoretic gel and identified by sequencing and successive alignment with sequences of the GenBank (www.ncbi.nlm.nih.gov/BLAST/) database (13).

    TGGE analysis of amplified samples. The fragments coding for regions V6-V8 on bacterial DNA obtained by PCR have been separated by TGGE as described by Satokari et al. (14), with a 37°C to 46°C temperature gradient, 0.5 ramp, and an 18-h run at 85 V.

    PCR amplification with species-specific primers. Some microbial species considered to be very important in the neonatal intestinal microbiota have been investigated by PCR with species-specific primers (Table 2) (14–16).


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  		TABLE 2 Species-specific primers used to detect microbial flora in fecal samples

 
The presence of bacteria belonging to the genus Bifidobacterium, with the exception of B. catenulatum and B. lactis, was also investigated by species-specific multiplex PCR. Species-specific amplification of B. lactis has been carried out according to Ventura et al. (17). Bacteroides fragilis group, R. obeum group, R. callidus e R. bromii PCR-based detection was carried out according to Yamashita et al. (15) and Wang et al. (16).


   Results and Discussion
TOP
 ABSTRACT
 Introduction
 Subjects, Materials, and Methods
 Results and Discussion
LITERATURE CITED
 
DGGE profiles obtained by means of universal primers on fecal samples of newborns delivered either by cesarean section or vaginally were usually characterized by few bands, most of which were in common with all the other subjects in each of the 2 groups considered (Fig. 1, Fig. 2). In particular, bands corresponding to Klebsiella oxytoca and Bifidobacterium pseudolongum seem to be present in all the lines obtained from the feces of vaginally delivered infants.


Figure 1
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  		FIGURE 1  DGGE analysis of PCR product, with U968-r and L1401-f universal primers, of fecal samples from cesarean-delivery babies. (§) These bands were not sequenced because, after amplification, they did not produce any analyzable products.

 

Figure 2
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  		FIGURE 2  DGGE analysis of PCR product, with U968-r and L1401-f universal primers, of fecal samples from vaginal-delivery babies (§). These bands were not sequenced because, after amplification, they did not produce any analyzable products.

 
Slight differences have been found, on the other hand, with respect to E. coli (Fig. 2). This microbial group, in fact, was found in 9 of 23 (39.1%) spontaneously delivered newborns, whereas overlapping bands were founds only in 2 of 23 (8.7%) cesarean-delivered newborns (Fig. 1).

DGGE analysis, carried out with Bifidobacterium-specific primers, revealed the presence of this genus in 13 of 23 (56.5%) samples derived from vaginally delivered newborns but in none of the samples obtained from newborns delivered by cesarean section.

TGGE analysis, carried out with universal primers on fecal samples of both groups of subjects, showed greater inter- and intragroup profile variations, particularly in the group of babies born by vaginal delivery (Fig. 3). In contrast, those born by cesarean section displayed more constant TGGE profiles (Fig. 4).


Figure 3
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  		FIGURE 3  TGGE analysis of PCR product, with U968-r and L1401-f universal primers, of fecal samples from vaginal-delivery babies (§). These bands were not sequenced because, after amplification, they did not produce any analyzable products.

 

Figure 4
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  		FIGURE 4  TGGE analysis of PCR product, with U968-r and L1401-f universal primers, of fecal samples from cesarean-delivery (§). These bands were not sequenced because, after amplification, they did not produce any analyzable products.

 
PCR analysis with Bifidobacterium species-specific primers showed that naturally delivered infants had a large number of bifidobacterial species, whereas in cesarean-delivered babies, only 2 samples (8.7%) gave positive results, 1 for B. longum and the other for B. gallicum.

With regard to the qualitative pattern, spontaneously delivered babies show greater differences concerning investigated Bifidobacterium species; the most represented are Bifidobacterium catenulatum group and Bifidobacterium longum; B. breve was detected in 52.2% of samples, B. bifidum in 39.1%; B. infantis, B. gallicum, and B. adolescentis species were more scarce (17.4, 4.3, and 21.7%, respectively). In all babies enrolled, microorganisms belonging to Ruminococcus species are absent, and Bacteroides has been found in 8.7% of spontaneously delivered babies only.

Species-specific PCR analysis shows the presence of B. catenulatum and B. longum in 43.5% of vaginally delivered babies, sometimes accompanied by the presence of B. breve, B. bifidum, or B. adolescentis.

Specifically, in this group of newborns, 17.4% are colonized at the same time by B. breve, B. bifidum, the B. catenulatum group, and B. longum, whereas B. breve, the B. catenulatum group, and B. longum are present in 8.7% of babies.

Although some studies (11) demonstrate that bifidobacteria appear after d 2 or 3 of life and usually dominate after the first 2 wk of life, because of feeding-related differences in the colonization time, little is known concerning the first 3 d after birth. Our study demonstrates that the newborn's intestinal microbiota, with respect to presence of bacteria, is strongly influenced, within 3 d of life, by the mode of delivery. From a qualitative point of view, the intestinal flora of cesarean- and vaginally delivered infants appears to be very different. The intestinal flora of infants by cesarean delivery is characterized by a substantial absence of Bifidobacteria species. Infants by vaginal delivery show subject-specific microbial profiles, although predominant groups such as B. longum and B. catenulatum group could be identified.

If the intestinal colonization could have health effects, the clear difference in the intestinal flora between vaginally delivered and cesarean-delivered infants would be of clinical relevance. Because only 2 infants born by cesarean delivery had not yet received a detectable amount of breast milk within 3 d of life, at least at this early age, the kind of nutrition seems to have a less crucial impact in modulating intestinal microbiota composition. In addition, we point out the great importance of an adequate microbiological approach in this kind of study.

DGGE analysis seems to be less sensitive than species-specific PCR analysis because the latter has provided the identification of a larger number of Bifidobacterium species not detected by DGGE. TGGE, on the other hand, seems to have a greater discrimination power than DGGE and to allow more differentiated profiles with respect to individual intestinal microbiota.

There is an increasing body of evidence that the intestinal microbiota could play an essential role in the postnatal development of the immune system (18,19). Malamitsi-Puchner et al. (20) found that only vaginal delivery promotes the production of various cytokines implicated in neonatal immunity. Hällström et al. (21) found a link among mode of cesarean delivery, disturbed intestinal colonization, and, possibly, occurrence of necrotizing enterocolitis in preterm infants.

Although the link between mode of delivery and clinical outcome is multifactorial, there is also evidence that the circumstances of a cesarean delivery have influence on the later outcome. In epidemiological studies, it could be demonstrated that elective cesarean delivery provides an increased risk for allergic diseases in later childhood (7–10). The particular role of the starting intestinal flora for long-term effects was emphasized by all investigators (7–10).

Data available from several studies indicate a delayed onset of lactation with cesarean section (22–24). Thus, many infants who were born by cesarean delivery also lacked the early support of breast milk as stimulator for a physiological intestinal flora. Both, the nonphysiological start of colonization and the missing early dietary support by delayed start of lactation might result in these long-lasting effects.

In summary, our data indicate that the early stage of the bacterial intestinal colonization in infants born by cesarean delivery is altered from that of infants born vaginally, with no or little influence of the type of feeding. Additionally, our results emphasize the importance of the methodological aspects for determining intestinal microbiota in clinical trials, if intestinal microbiota composition is to be considered a measure of postnatal adaptation.

Other articles in this supplement include references (25–34).


   FOOTNOTES
 
1 Published as a supplement to The Journal of Nutrition. Presented at the symposium "Infant Nutrition" held in Rotterdam, The Netherlands, September 8, 2006. The symposium was organized by the Sophia Children's Hospital, Erasmus University, Rotterdam, The Netherlands, and was cosponsored by Danone Research Wageningen, The Netherlands. Supplement coordinators: G. Boehm and J. B. van Goudoever, Erasmus University, The Netherlands. Supplement coordinator disclosures: G. Boehm is an employee of Danone Research, the sponsor of the supplement; J. B. van Goudoever, no relationships to disclose. Back

2 Author disclosures: G. Boehm is an employee of Danone Research, the sponsor of the supplement; G. Basucci, B. Benenati, L. Morelli, and E. Bessi, no conflicts of interest. Back


   LITERATURE CITED
TOP
 ABSTRACT
 Introduction
 Subjects, Materials, and Methods
 Results and Discussion
 LITERATURE CITED
 

1. Harmsen HJ, Wildeboer-Veloo AC, Raangs GC, Wagendorp AA, Klijn N, Bindels JG, Welling GW. Analysis of intestinal flora development in breast-fed and formula-fed infants by using molecular identification and detection methods. J Pediatr Gastroenterol Nutr. 2000;30:61–7.[CrossRef][Medline]

2. Orrhage K, Nord CE. Factors controlling the bacterial colonization of the intestine in breast fed infants. Acta Paediatr. 1999;88: Suppl(430):47–57.

3. Grönlund MM, Lehtonen OP, Eerola E, Kero P. Fecal microflora in healthy infants born by different methods of delivery: permanent changes in intestinal flora after caesarean delivery. J Pediatr Gastroenterol Nutr. 1999;28:19–25.[CrossRef][Medline]

4. Salminen S, Gibson GR, McCartney AL, Isolauri E. Influence of mode of delivery on gut microbiota composition in seven years old children. Gut. 2004;53:1388–9.[Free Full Text]

5. Heavey P, Rowland I. The gut microflora of the developing infant: microbiology and metabolism. Microb Ecol Health Dis. 1999;11:75–83.

6. Björksten B, Sepp E, Julge K, Voor T, Mikelsaar M. Allergy development and the intestinal flora during the first year of life. J Allergy Clin Immunol. 2001;108:516–20.[CrossRef][Medline]

7. Negele K, Heinrich J, Borte M, von Berg A, Schaaf B, Lehmann I, Wichmann HE, Bolte G.; LISA Study Group.Mode of delivery and development of atopic diseases during the first 2 years of life. Pediatr Allergy Immunol. 2004;15:48–54.[CrossRef][Medline]

8. Debley JS, Smith JM, Redding GJ, Critchlow CW. Childhood asthma hospitalization risk after caesarean delivery in former term and premature infants. Ann Allergy Asthma Immunol. 2005;94:228–33.[Medline]

9. Laubereau B, Filipiak-Pittroff B, von Berg A, Grübl A, Reinhardt D, Wichmann HE, Koletzko S.; GINI Study Group.Caesarean section and gastrointestinal symptoms, atopic dermatitis, and sensitation during the first year of life. Arch Dis Child. 2004;89:993–7.[Abstract/Free Full Text]

10. Eggesbo M, Botten G, Stigum H, Nafstad P, Magnus P. Is delivery by cesarean section a risk factor for food allergy? J Allergy Clin Immunol. 2003;112:420–6.[Medline]

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12. Satokari RM, Vaughan EE, Akkermans AD, Saarela M, de Vos WM. Bifidobacterial diversity in human feces detected by genus specific PCR and Denaturing Gradient Gel Electrophoresis. Appl Environ Microbiol. 2001;67:504–13.[Abstract/Free Full Text]

13. GenBank DatabaseNucleic Acids Res. 2007;35: Database issue:D21–5.[Abstract/Free Full Text]

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18. Fanaro S, Chierici R, Guerrini P, Vigi V. Intestinal flora in early infancy: composition and development. Acta Paediatr Suppl. 2003;91:48–55.[Medline]

19. Boehm G, Jelinek J, Knol J, M'Rabet L, Stahl B, Vos P, Garssen J. Prebiotics and immune responses. J Pediatr Gastroenterol Nutr. 2004;39:S772–3.[Medline]

20. Malamitsi-Puchner A, Protonotariou E, Boutsikou T, Makrakis E, Sarandakou A, Creatsas G. The influence of the mode of delivery on circulating cytokine concentrations in the perinatal period. Early Hum Dev. 2005;81:387–92.[CrossRef][Medline]

21. Hällström M, Eerola E, Vuento R, Janas M, Tammela O. Effects of mode of delivery and necrotizing enterocolitis in the intestinal microflora in preterm infants. Eur J Clin Microbiol Infect Dis. 2004;23:463–70.[CrossRef][Medline]

22. Dewey KG, Nommsen-Rivers LA, Heinig MJ, Cohen RJ. Risk factors for suboptimal infant breast feeding behavior, delayed onset of lactatation, and excess neonatal weight loss. Pediatrics. 2003;112:607–19.[Abstract/Free Full Text]

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24. Butler S, Williams M, Tukuitonga C, Paterson J. Factors associated with not breastfeeding exclusively among mothers of a cohort of Pacific infants in New Zealand. N Z Med J. 2004;117:U908.[Medline]

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