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Journal of Pediatric Gastroenterology & Nutrition:
Original Articles

Fecal Microflora in Healthy Infants Born by Different Methods of Delivery: Permanent Changes in Intestinal Flora After Cesarean Delivery

Grölund, Minna-Maija*†; Lehtonen, Olli-Pekka†; Eerola, Erkki‡; Kero, Pentti*

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*Department of Pediatrics, Turku University Central Hospital, Turku, Finland; †Clinical Microbiology, Turku University Central Hospital ‡Department of Medical Microbiology, University of Turku, Finland

Address correspondence and reprint requests to Minna-Maija Grölund, MD, Department of Paediatrics, Turku University Central Hospital, Kiinamyllynkatu 4-8, FI-20520 Turku, Finland.

Received December 18, 1997; Revised April 7 and June 26, 1998; accepted July 1, 1998.

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Background: Newborn infants in modern maternity hospitals are subject to numerous factors that affect normal intestinal colonization-for example, cesarean delivery and antimicrobial agents. To study the duration of the effect of external factors on intestinal colonization, two groups of infants with different delivery methods were investigated.

Methods: The fecal flora of 64 healthy infants was studied prospectively. Thirty-four infants were delivered vaginally, and 30 by cesarean birth with antibiotic prophylaxis administered to their mothers before the delivery. The fecal flora was cultured on nonselective and selective media in infants 3 to 5, 10, 30, 60, and 180 days of age. Gastrointestinal signs were recorded daily by the mothers for 2 months.

Results: The fecal colonization of infants born by cesarean delivery was delayed. Bifidobacterium-like bacteria and Lactobacillus-like bacteria colonization rates reached the rates of vaginally delivered infants at 1 month and 10 days, respectively. Infants born by cesarean delivery were significantly less often colonized with bacteria of the Bacteroides fragilis group than were vaginally delivered infants: At 6 months the rates were 36% and 76%, respectively (p = 0.009). The occurrence of gastrointestinal signs did not differ between the study groups.

Conclusions: This study shows for the first time that the primary gut flora in infants born by cesarean delivery may be disturbed for up to 6 months after the birth. The clinical relevance of these changes in unknown, and even longer follow-up is needed to establish how long-lasting these alterations of the primary gut flora can be.

The neonatal period is crucial for intestinal colonization. Born sterile and undergoing colonization within a few days, infants are an open field for colonization by different types of bacteria. Gestational age, type of delivery, and feeding affect the stool flora of young infants (1), but there is little information on which long-term factors influence the bacterial selection process in the gut of young infants 2.

Infants born vaginally apparently acquire their gut flora from maternal vaginal and fecal flora (3), but the environment also contributes. Within maternity wards, nosocomial spread is shown to exist among healthy newborn infants (4,5). For the colonization of infants born by cesarean delivery (CD), the environment is extremely important (6,7). Likewise, if infants are separated from their mothers for long periods after birth, the environment becomes an important source of colonizing bacteria (5).

Gut colonization is delayed in infants born by CD, and intestinal colonization is consequently abnormal for several weeks (1,8). Most of the studies on gut colonization of infants born by CD have extended only to the first month of life (1,8-10). Overall, however, the long-term stability of the gut flora of newborn infants has been studied systematically in only a few studies 2,11. Such information would clearly be valuable, because changes in the primary gut flora have been associated with gastrointestinal disorders and infantile colic 12-15. We studied the stability of the changes in the fecal flora of newborn infants and the association between certain bacteria and gastrointestinal signs. To study two distinctly different groups of neonates with different gut flora, two study groups were formed: vaginally delivered (VD) infants (n = 34) and infants born by CD to mothers who had received antimicrobial prophylaxis (n = 30). The fecal flora was recorded for 6 months, and gastrointestinal signs were registered daily for 2 months.

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The study included 64 healthy newborn infants of healthy mothers who delivered at the Department of Obstetrics and Gynecology, University Central Hospital, Turku, Finland. Thirty-four VD infants and 30 infants delivered by elective CD were enrolled between February 1995 and June 1996 after written informed consent had been obtained from their parents. The enrollment rate was two to four children per week, because sampling necessitated that the birth took place on Monday through Thursday. The mothers who delivered by cesarean birth received prophylactically 2 g intravenous ampicillin 2 hours before the operation. None of the mothers had received any antimicrobial agents within the month that preceded the delivery. After delivery, the newborns were admitted randomly to one of the two maternity wards for healthy newborn infants.

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Fecal Samples and Bacterial Cultures

Fecal samples were taken when the infants were 3 to 5 days old (taken at the hospital) and 10, 30, 60, and 180 days old (taken at home). The specimens were collected in plastic containers. If not cultured immediately, the samples were stored at 4°C. The specimens obtained at home were taken to the laboratory by the parents. The mean storage time of the specimens was 10.7 hours (range, 0.5-34.5 hours).

An approximate 300-mg portion of the specimen was weighed, diluted, and homogenized in fastidious anaerobe broth (Lab M, Bury, UK). Serial 100-fold dilutions were made in the same broth. Duplicate samples of 10 µl of each dilution were cultured on a variety of nonselective and selective media (Table 1).

Table 1
Table 1
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The MacConkey plates were incubated at 35°C in ambient air for 24 hours. All other cultures were incubated in anaerobic jars with gas-generating kits (Anero Gen, AN35; Oxoid, Basingstoke, UK) at 35°C for 48 hours (fastidious anaerobe agar [FAA], Bacteroides bile esculin agar [BBE] and Clostridium perfringers selective agar), or for 72 hours (Rogosa and modified Petuely's agars). The number of colonies from two parallel plates was counted from a dilution yielding 30 to 300 colony-forming units (CFU)/plate, and average was recorded.

The total number of colonies was counted and recorded from MacConkey and FAA agars. The number of all different types of colonies was counted from BBE, Rogosa, and modified Petuely's agars and the number of distinctive black colonies from Clostridium perfringens agar. All different types of colonies from BBE, Rogosa, and modified Petuely's agars and distinctive black colonies from Clostridium perfringers agar were subcultured for aerotolerance testing and were Gram stained.

Anaerobic gram-negative, esculin hydrolysing rods growing on BBE agar were recorded as bacteria of the Bacteroides fragilis group. Anaerobic and aerotolerant nonbranching, grampositive rods with parallel sides from Rogosa agar were recorded as Lactobacillus-like bacteria (LLB). It has been shown that all colonies growing well on Rogosa agar may be considered lactic acid bacteria; some enterococci and pediococci may show reduced growth (16). Anaerobic and aerotolerant gram-positive rods from modified Petuely's agars were recorded as Bifidobacterium-like bacteria (BLB). Modified Petuely's agar is highly selective and efficient for detection of Bifidobacterium from fecal samples. In a previous work by Tanaka and Mutai (17) 175 fecal strains were detected from the modified Petuely's medium; from these 94% were bifidobacteria, 3% eubacteria, and 3% peptostreptococci.

Clostridium perfringens was identified by its distinct colony and Gram-stain morphology, by its anaerobic nature in aerotolerance testing, and by positive results in the reversed CAMP test (18). The bacterial counts were expressed as the log10 of colony-forming units per gram of wet weight of feces.

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Clinical Symptoms

The mothers kept a diary for 2 months of their infants' daily bowel habits, abdominal distension, flatulence, normal and colickly crying, use of antimicrobial agents, and feedings. Crying was defined as colicky if it was a distinctive pain cry, and the infant was difficult to console (19). Abdominal distension and flatulence were given a daily score by the following scale: no signs, a few signs, moderate signs, or heavy signs.

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Statistical Analysis

The results were analysed statistically by Fisher's exact test (to compare the number of infants colonized at each time point), Mann-Whitney's rank sum test (to compare bacteria counts of colonized infants at 3 days and 6 months of age), and analysis of variance of repeated measurements (to compare the gastrointestinal signs). A commercial software program (Statistica, version 5.0; Stat Soft, Tulsa, OK, U.S.A.) was used for these calculations. P < 0.05 was considered statistically significant.

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The study was approved by the joint Committee of Ethics of the Turku University and Turku University Central Hospital.

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The study groups differed slightly by gestational age (VD group, 40 weeks; CD group, 39 weeks; p = 0.04) but the birth weights did not differ statistically (VD group, 3577 g; CD group, 3572 g; p = 0.96). Special attention was paid to the method of feeding the infants. The use of formula was recorded carefully by the mothers. The proportion of infants exclusively breast-fed at 2 months of age or partly breast-fed at 6 months of age did not differ between the study groups (p = 0.2 and 0.8, respectively). Eleven infants received antimicrobial agents during follow-up. All of these therapies were administered when the infants were older than 2 months, and in these infants the subsequent 6-mont fecal samples were excluded from the analysis. (Table 2)

Table 2
Table 2
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Colonization Rates

With the exception of one infant (in the CD group) who was culture-negative at 3 days of age, all infants were colonized with aerobic enteric bacteria in every culture. The colonization rates of BLB and LLB were lower in the CD group 'han in the VD group after birth. The colonization rate of BLB coincided in these groups by 1 month and of LLB by 10 days of age (Figs. 1 and 2). The colonization rate of LLB in the CD group even exceeded that of the VD group in infants 2 and 6 months of age (Fig. 2). The Clostridium perfringens colonization rate was statistically higher in the CD group than in the VD group at 1 month of age (57% vs. 17% p = 0.003; Fig. 3).

Fig. 1
Fig. 1
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Fig. 2
Fig. 2
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Fig. 3
Fig. 3
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The colonization rates of bacteria within the Bacteroides fragilis group differed most markedly of all between the study groups. The Bacteroides colonization rate ranged from 52% to 79% in the VD group (Fig. 4). Only one of the infants in the CD group was Bacteroides positive at 3 days of age. After that, Bacteroides was not recovered in any of the samples from the infants in the CD group before the age of 2 months. In infants 6 months of age, the colonization rate was still statistically lower in the CD group than in the VD group (36% vs. 76%; p = 0.009; Fig. 4).

Fig. 4
Fig. 4
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Colonization Levels

The colonization levels of the different bacteria of the colonized infants are shown in Table 3. The total bacterial counts were significantly lower in the CD group in infants 3 days of age (p = 0.005) and in those 6 months of age (p = 0.03). The aerobic enteric bacterial counts did not differ between the groups. Infants in the CD group had a significantly lower level of BLB when they were 3 days old (p = 0.005) but not when they were 6 months old (p = 0.5). There were no differences in the LLB counts or in the Clostridium perfringens counts between the groups. The amounts of Bacteroides fragilis bacteria did not differ between the groups of infants with colonization at 6 months (p = 0.3).

Table 3
Table 3
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Gastrointestinal Signs

Two mothers in both groups did not complete the follow-up sheets. No statistically significant differences were found between the study groups in the scores of abdominal distension, flatulence, or in the amount of colicky crying, Infantile colic, according to the definition of Wessel et al. (20), was detected in three of the VD infants and in none of the CD infants (p = 0.2; Fisher's exact test).

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This study shows that the fecal flora of infants born by CD with prophylactic antibiotics administered to the mother is very different from that of infants delivered vaginally. The greatest differences were seen in the bacteria of the Bacteroides fragilis group, which is in agreement with studies in infants born by CD; in earlier studies the duration of follow-up, however, was only 10 to 60 days (1,8,10). In the present study, no permanent colonization with Bacteroides fragilis group bacteria was found in the CD group before the infants were 2 months of age. Still, in infants 6 months of age in the CD group, the colonization rate of the Bacteroides fragilis group was only half that of infants in the VD group (36% and 76%, respectively; p = 0.009). Similarly, Bennet and Nord (8) were unable to detect Bacteroides bacteria 3 to 8 weeks after birth in term and preterm infants born by CD.

We used selective culture media to describe intestinal flora in this study. The counts detected from these selective culture media represent mainly the bacterial genera level but cannot detect the absolute counts of different bacterial genera or species, except those of Clostridium perfringens, which were further identified. Nevertheless, this method can identify differences between the delivery groups and the changes taking place in intestinal flora after birth, which was the main purpose of the current study. Furthermore, the main differences in the fecal flora between the delivery groups were found in Bacteroides fragilis group bacteria that were detected from the BBE media, which is highly selective for the Bacteroides fragilis group (21).

The long-lasting changes seen in the primary gut flora of infants born by CD could be the result of one or both of the two abnormal components of their birth: CD itself or the prophylactic ampicillin and administered to the mother 2 hours before the elective CD. Ampicillin is very poorly protein-bound and crosses the placenta readily: maternal and fetal serum ampicillin levels equilibrate within 1 hour after intravenous administration (22). The decline in BLB could be explained by the intravenous ampicillin that the infants were exposed to before delivery, but fecal LBL should not decline with ampicillin therapy, at least this is not the case in older children (10 months to 12 years). Also, only a minor decline is detected in fecal Bacteroides sp. counts in these older children and the Bacteroides sp. counts return to normal stage within only 3 to 6 days after cessation of the ampicillin therapy (23). Thus, it seems unlikely that the long-term changes recorded in the fecal flora of the infants in the CD group in our study could be explained by the administration of ampicillin before delivery. Rather, previous reports imply that this phenomenon is caused by CD itself (1,8). Still, ampicillin could have more profound effects when administered immediately after the birth because the gut is empty, and the drug can select the primary colonizing bacteria.

The changes that took place in the fecal bacterial flora could not be associated with gastrointestinal signs. Any signs were meticulously recorded daily by the mothers for 2 months. In a previous study, Clostridium perfringens has been associated with an increased incidence of gastrointestinal signs, such as flatulence, distended abdomen, foul-smelling stools, diarrhea, and blood in stools (12). In the present study, the infants born by CD had a higher colonization rate of Clostridium perfringens than the VD group of infants at 1 month (57% and 17%, respectively). Even at this time point, the scores of gastrointestinal signs did not differ between the study groups. The inconsistency of the results between these two studies might be explained by the differences between the study populations. In the previous study most of the infants were treated in the intensive care unit and were preterm infants, whereas in the present study all infants were healthy full-term neonates.

There is great variation among the reports of the predominant bacteria in the fecal flora of breast-fed newborns. Some researchers have found bifidobacteria to predominate and Bacteroides to be scarce (2,24,25), whereas others have found the opposite (26,27). However, the predominant bacterium has been classified differently among the studies. Some investigators define the predominant bacterium as the most frequently occurring bacteria (26) and some as the bacterium with the highest counts in fecal samples (28). In the present study, 19 of the 34 VD infants were exclusively breast-fed for 2 months. Among all the VD children, the most frequent bacteria during the first 2 months of life were BLB (85-97%), although Bacteroides fragilis group bacteria were also common (52-79%). The highest colony counts were encountered for BLB (10.2-10.9 log10 CFU/g wet weight of feces). The Bacteroides colony counts were lower (8.7-9.5 log10 CFU/g). These results agree with those in a recent study from Germany (28).

The present study is the first one to show that the changes in the primary intestinal flora of infants born by CD to mothers who have received antimicrobial prophylaxis last for no less than 6 months after birth, maybe longer. We do not know how long these abnormalities in the fecal flora last on the whole, but the primary quality and quantity of colonization of the gut seems to be critical in the selection process between different genera of bacteria. Some bacteria such as Bacteroides are not as easily accessible to the gut of infants delivered the under sterile conditions of CD. Other, perhaps more aerotolerant, bacteria may take over in the intestine and inhibit the subsequent colonization of the gut by Bacteroides. This phenomenon is the generally known as interbacterial inhibition (29). Apparently, the bacterial predominances are not readily subject to change under normal domestic conditions after the first months of the colonization process.

Normal intestinal flora has immunostimulatory functions, as has been demonstrated in numerous animal studies (30-32). Mucosal IgA plasma cells are especially scarce in germ-free animals (33). Additionally, when probiotic bacteria belonging to the normal intestinal flora have been administered orally to children in association with diarrhea or mucosal vaccination, an increase in antigen-specific and nonspecific IgA and IgM responses has been detected (34,35). Secretory IgA and IgM are the main humoral mediators of mucosal immunity in cooperation with a variety of innate protective mechanisms. Well-functioning mucosal immunity is a prerequisite for health, because the mucosal surfaces are favored as portals of entry by most infectious agents, allergens, and carcinogens (36). Further research is under way to determine whether the delay found in intestinal colonization in these infants born by CD has any effect on the development of the gut-associated immune system.

Acknowledgement: The authors thank Mr. Hans Helenius, M.Sc., Department of Biostatistics, University of Turku, for his help with the statistical analysis; and the nurses of the Department of Obstetrics and Gynecology, and Mrs. Satu Ekblad, Department of Pediatrics, for their invaluable help in performing this study.

Supported in part by The South-West Finnish Fund of Neonatal Research.

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Fems Immunology and Medical Microbiology, 30(1): 43-47.

Fems Immunology and Medical Microbiology
Characterizing the composition of intestinal microflora as a prospective treatment target in infant allergic disease
Kirjavainen, PV; Apostolou, E; Arvola, T; Salminen, SJ; Gibson, GR; Isolauri, E
Fems Immunology and Medical Microbiology, 32(1): 1-7.

Archives of Disease in Childhood
Caesarean section and gastrointestinal symptoms, atopic dermatitis, and sensitisation during the first year of life
Laubereau, B; Filipiak-Pittroff, B; von Berg, A; Grubl, A; Reinhardt, D; Wichmann, HE; Koletzko, S
Archives of Disease in Childhood, 89(): 993-997.
Annals of Allergy Asthma & Immunology
Childhood asthma hospitalization risk after cesarean delivery in former term and premature infants
Debley, JS; Smith, JM; Redding, GJ; Critchlow, CW
Annals of Allergy Asthma & Immunology, 94(2): 228-233.

Allergic Diseases and the Environment
Oral tolerance and gut maturation
Murch, S
Allergic Diseases and the Environment, 53(): 133-151.

American Journal of Clinical Pathology
Myometrial inflammation in human delivery and its association with labor and infection
Keski-Nisula, LT; Aalto, ML; Kirkinen, PP; Kosma, VM; Heinonen, ST
American Journal of Clinical Pathology, 120(2): 217-224.
Acta Paediatrica
Pro- and pre-biotics administration in preterm infants: colonization and influence on faecal flora
Marini, A; Negretti, F; Boehm, G; Li Destri, M; Clerici-Bagozzi, D; Mosca, F; Agosti, M
Acta Paediatrica, 92(): 80-81.

Biology of the Neonate
Comparison of fecal flora following administration of two antibiotic protocols for suspected maternofetal infection
Bonnemaison, E; Lanotte, P; Cantagrel, S; Thionois, S; Quentin, R; Chamboux, C; Laugier, J
Biology of the Neonate, 84(4): 304-310.
Annals of Epidemiology
Mode of delivery is associated with asthma and allergy occurrences in children
Salam, MT; Margolis, HG; McConnell, R; McGregor, JA; Avol, EL; Gilliland, FD
Annals of Epidemiology, 16(5): 341-346.
Clinical and Experimental Immunology
Mode of delivery directs the phagocyte functions of infants for the first 6 months of life
Gronlund, MM; Nuutila, J; Pelto, L; Lilius, EM; Isolauri, E; Salminen, S; Kero, P; Lehtonen, OP
Clinical and Experimental Immunology, 116(3): 521-526.

Current Opinion in Gastroenterology
Probiotics and gut inflammation
Isolauri, E
Current Opinion in Gastroenterology, 15(6): 534-537.

American Journal of Clinical Nutrition
Probiotics in human disease
Isolauri, E
American Journal of Clinical Nutrition, 73(6): 1142S-1146S.

Influence of mode of delivery on gut microbiota composition in seven year old children
Salminen, S; Gibson, GR; McCartney, AL; Isolauri, E
Gut, 53(9): 1388-1389.

Experimental Animals
Development of intestinal microbiota in mice and its possible interaction with the evolution of luminal IgA in the intestine
Inoue, R; Otsuka, M; Ushida, K
Experimental Animals, 54(5): 437-445.

Clinical and Experimental Allergy
Caesarean section delivery and the risk of allergic disorders in childhood
Renz-Polster, H; David, MR; Buist, AS; Vollmer, WM; O'Connor, EA; Frazier, EA; Wall, MA
Clinical and Experimental Allergy, 35(): 1466-1472.
Pediatric Research
Reduced enterobacterial and increased staphylococcal colonization of the infantile bowel: An effect of hygienic lifestyle?
Adlerberth, I; Lindberg, E; Aberg, N; Hesselmar, B; Saalman, R; Strannegard, IL; Wold, AE
Pediatric Research, 59(1): 96-101.
Prevention of Allergy and Allergic Asthma: World Allergy Organization Project Report and Guidelines
Environmental influences on asthma and allergy
Asher, I; Dagli, E
Prevention of Allergy and Allergic Asthma: World Allergy Organization Project Report and Guidelines, 84(): 36-101.

Current Molecular Medicine
The role of microbiota and probiotics in stress-induced gastrointestinal damage
Lutgendorff, F; Akkermans, LMA; Soderholm, JD
Current Molecular Medicine, 8(4): 282-298.

Journal of Nutrition
Cesarean delivery may affect the early biodiversity of intestinal bacteria
Biasucci, G; Benenati, B; Morelli, L; Bessi, E; Boehm, G
Journal of Nutrition, 138(9): 1796S-1800S.

Journal of Allergy and Clinical Immunology
Intrauterine bacterial growth at birth and risk of asthma and allergic sensitization among offspring at the age of 15 to 17 years
Keski-Nisula, L; Katila, ML; Remes, S; Heinonen, S; Pekkanen, J
Journal of Allergy and Clinical Immunology, 123(6): 1305-1311.
Maternal-to-Infant Transmission of Probiotics: Concept Validation in Mice, Rats, and Pigs
Buddington, RK; Williams, CH; Kostek, BM; Buddington, KK; Kullen, MJ
Neonatology, 97(3): 250-256.
Isme Journal
Developmental microbial ecology of the crop of the folivorous hoatzin
Godoy-Vitorino, F; Goldfarb, KC; Brodie, EL; Garcia-Amado, MA; Michelangeli, F; Dominguez-Bello, MG
Isme Journal, 4(5): 611-620.
Proceedings of the Nutrition Society
Symposium 4: Gut function: effects on over- and undernutrition Nutrition, intestinal defence and the microbiome
Kelly, P
Proceedings of the Nutrition Society, 69(2): 261-268.
Clinical and Experimental Allergy
Thymus size and head circumference at birth and the development of allergic diseases
Benn, CS; Jeppesen, DL; Hasselbalch, H; Olesen, AB; Nielsen, J; Bjorksten, B; Lisse, I; Aaby, P
Clinical and Experimental Allergy, 31(): 1862-1866.

Pediatric Research
Perinatal events, vitamin D, and the development of allergy - Commentary
Annesi-Maesano, I
Pediatric Research, 52(1): 3-5.
Pediatric Research
Mode of delivery and asthma - Is there a connection?
Kero, J; Gissler, M; Gronlund, MM; Kero, P; Koskinen, O; Hemminki, E; Isolauri, E
Pediatric Research, 52(1): 6-11.
Annual Review of Nutrition
Nutritional impact of pre- and probiotics as protective gastrointestinal organisms
Teitelbaum, JE; Walker, WA
Annual Review of Nutrition, 22(): 107-138.
Monatsschrift Kinderheilkunde
Modulation of intestinal flora with probiotics and prebiotics
Braegger, CP
Monatsschrift Kinderheilkunde, 151(): S21-S23.
American Journal of Clinical Nutrition
Effects of galactooligosaccharide and long-chain fructooligosaccharide supplementation during pregnancy on maternal and neonatal microbiota and immunity - a randomized, double-blind, placebo-controlled study
Shadid, R; Haarman, M; Knol, J; Theis, W; Beermann, C; Rjosk-Dendorfer, D; Schendel, DJ; Koletzko, BV; Krauss-Etschmann, S
American Journal of Clinical Nutrition, 86(5): 1426-1437.

Clinical Infectious Diseases
Impact of the intestinal microbiota on the development of mucosal defense
Gaskins, HR; Croix, JA; Nakamura, N; Nava, GM
Clinical Infectious Diseases, 46(): S80-S86.
Caesarean section is associated with an increased risk of childhood-onset type 1 diabetes mellitus: a meta-analysis of observational studies
Cardwell, CR; Stene, LC; Joner, G; Cinek, O; Svensson, J; Goldacre, MJ; Parslow, RC; Pozzilli, P; Brigis, G; Stoyanov, D; Urbonaite, B; Sipetic, S; Schober, E; Ionescu-Tirgoviste, C; Devoti, G; de Beaufort, CE; Buschard, K; Patterson, CC
Diabetologia, 51(5): 726-735.
Journal of Nutrition
The impact of enteral insulin-like growth factor 1 and nutrition on gut permeability and amino acid utilization
van Goudoever, JB; Corpeleijn, W; Riedijk, M; Schaart, M; Renes, I; van der Schoor, S
Journal of Nutrition, 138(9): 1829S-1833S.

The impact of caesarean delivery and type of feeding on cow's milk allergy in infants and subsequent development of allergic march in childhood
Sanchez-Valverde, F; Gil, F; Martinez, D; Fernandez, B; Aznal, E; Oscoz, M; Olivera, JE
Allergy, 64(6): 884-889.
Annual Review of Immunology, Vol 28
Intestinal Bacteria and the Regulation of Immune Cell Homeostasis
Hill, DA; Artis, D
Annual Review of Immunology, Vol 28, 28(): 623-667.
Journal of Clinical Microbiology
Effects of intrapartum penicillin prophylaxis on intestinal bacterial colonization in infants
Jaureguy, F; Carton, M; Panel, P; Foucaud, P; Butel, MJ; Doucet-Populaire, F
Journal of Clinical Microbiology, 42(): 5184-5188.
Birth-Issues in Perinatal Care
Carol Sakala's letter from North America: An uncontrolled experiment: Elective delivery predominates in the United States
Sakala, C
Birth-Issues in Perinatal Care, 33(4): 332-335.

Fems Microbiology Ecology
Genomic diversity of cultivable Lactobacillus populations residing in the neonatal and adult gastrointestinal tract
Wall, R; Fitzgerald, G; Hussey, S; Ryan, T; Murphy, B; Ross, P; Stanton, C
Fems Microbiology Ecology, 59(1): 127-137.
Agro Food Industry Hi-Tech
Bacterial colonisation of the infant gut, the influence of diet and its role in health
Edwards, CA
Agro Food Industry Hi-Tech, 17(5): 13-15.

American Journal of Respiratory and Critical Care Medicine
Maternal complications and procedures in pregnancy and at birth and wheezing phenotypes in children
Rusconi, F; Galassi, C; Forastiere, F; Bellasio, M; De Sario, M; Ciccone, G; Brunetti, L; Chellini, E; Corbo, G; La Grutta, S; Lombardi, E; Piffer, S; Talassi, F; Biggeri, A; Pearce, N
American Journal of Respiratory and Critical Care Medicine, 175(1): 16-21.
Journal of Hospital Infection
Healthcare-associated infections in neonatal units: lessons from contrasting worlds
Srivastava, S; Shetty, N
Journal of Hospital Infection, 65(4): 292-306.
Development of intestinal bacterial enzymes in infants - Relationship to mode of delivery and type of feeding
Gronlund, MM; Salminen, S; Mykkanen, H; Kero, P; Lehtonen, OP
Apmis, 107(7): 655-660.

Toll of allergy reduced by probiotics
Murch, SH
Lancet, 357(): 1057-1059.

Monatsschrift Kinderheilkunde
Probiotics and allergy
Hauer, AC
Monatsschrift Kinderheilkunde, 150(7): 829-+.
International Journal of Food Microbiology
Gut bacteria and health foods - the European perspective
Saarela, M; Lahteenmaki, L; Crittenden, R; Salminen, S; Mattila-Sandholm, T
International Journal of Food Microbiology, 78(): 99-117.
PII S0168-1605(02)00235-0
Nutrition Research
Galactooligosaccharide in combination with Bifidobacterium and Bacteroides affects the population of Clostridium perfringens in the intestine of gnotobiotic mice
Morishita, Y; Oowada, T; Ozaki, A; Mizutani, T
Nutrition Research, 22(): 1333-1341.
PII S0271-5317(02)00455-4
Journal of Clinical Microbiology
High rate of transfer of Staphylococcus aureus from parental skin to infant gut flora
Lindberg, E; Adlerberth, I; Hesselmar, B; Saalman, R; Strannegard, IL; Aberg, N; Wold, AE
Journal of Clinical Microbiology, 42(2): 530-534.
Journal of General and Applied Microbiology
Development of the intestinal microbiota in the piglet
Inoue, R; Tsukahara, T; Nakanishi, N; Ushida, K
Journal of General and Applied Microbiology, 51(4): 257-265.

Factors influencing the composition of the intestinal microbiota in early infancy
Penders, J; Thijs, C; Vink, C; Stelma, FF; Snijders, B; Kummeling, I; van den Brandt, PA; Stobberingh, EE
Pediatrics, 118(2): 511-521.
World Journal of Gastroenterology
Do probiotics have a therapeutic role in gastroenterology?
Limdi, JK; O'Neill, C; McLaughlin, J
World Journal of Gastroenterology, 12(): 5447-5457.

Gastroenterologie Clinique Et Biologique
Establishment of the intestinal microflora in neonates
Campeotto, F; Waligora-Dupriet, AJ; Doucet-Populaire, F; Kalach, N; Dupont, C; Butel, MJ
Gastroenterologie Clinique Et Biologique, 31(5): 533-542.

Issues in Complementary Feeding
The microbiological risk
Morelli, L
Issues in Complementary Feeding, 60(): 79-90.

Twin Research and Human Genetics
Asthma and mode of birth delivery: A study in 5-year-old Dutch twins
van Beijsterveldt, TCEM; Boomsma, DI
Twin Research and Human Genetics, 11(2): 156-160.

Journal of Allergy and Clinical Immunology
Birth by cesarean section, allergic rhinitis, and allergic sensitization among children with a parental history of atopy
Pistiner, M; Gold, DR; Abdulkerim, H; Hoffman, E; Celedon, JC
Journal of Allergy and Clinical Immunology, 122(2): 274-279.
International Dairy Journal
Specific metabolite production by gut microbiota as a basis for probiotic function
Ross, RP; Mills, S; Hill, C; Fitzgerald, GF; Stanton, C
International Dairy Journal, 20(4): 269-276.
Drugs Under Experimental and Clinical Research
Bifidobacteria and lactobacilli in human health
Orrhage, K; Nord, CE
Drugs Under Experimental and Clinical Research, 26(3): 95-111.

British Journal of Nutrition
Intestinal microflora of human infants and current trends for its nutritional modulation
Mountzouris, KC; McCartney, AL; Gibson, GR
British Journal of Nutrition, 87(5): 405-420.
Bjog-An International Journal of Obstetrics and Gynaecology
II. The unfacts of 'request' caesarean section - Commentary
Bewley, S; Cockburn, J
Bjog-An International Journal of Obstetrics and Gynaecology, 109(6): 597-605.
PII S1470-0328(02)07106-9
Fems Microbiology Ecology
Vertical and horizontal transmission of intestinal commensal bacteria in the rat model
Inoue, R; Ushida, K
Fems Microbiology Ecology, 46(2): 213-219.
Indian Journal of Medical Microbiology
Gupta, V; Garg, R
Indian Journal of Medical Microbiology, 27(3): 202-209.
Journal of Allergy and Clinical Immunology
Is delivery by cesarean section a risk factor for food allergy?
Eggesbo, M; Botten, G; Stigum, H; Nafstad, P; Magnus, P
Journal of Allergy and Clinical Immunology, 112(2): 420-426.
Acta Paediatrica
Intestinal microflora in early infancy: composition and development
Fanaro, S; Chierici, R; Guerrini, P; Vigi, V
Acta Paediatrica, 92(): 48-55.

Agro Food Industry Hi-Tech
Usefulness of infant formulae supplemented with probiotics or prebiotics?
Waligora-Dupriet, AJ; Campeotto, F; Kalach, N; Dupont, C; Butel, MJ
Agro Food Industry Hi-Tech, 17(2): 56-59.

Embo Reports
The gut flora as a forgotten organ
O'Hara, AM; Shanahan, F
Embo Reports, 7(7): 688-693.
Digestive Diseases and Sciences
Colonization and impact of disease and other factors on intestinal microbiota
Thompson-Chagoyan, OC; Maldonado, J; Gil, A
Digestive Diseases and Sciences, 52(9): 2069-2077.
Journal of Asthma
Birth-related exposures and asthma and allergy in adulthood: A population-based cross-sectional study of young adults in North Staffordshire
Mallen, CD; Mottram, S; Wynne-Jones, G; Thomas, E
Journal of Asthma, 45(4): 309-312.
Inflammatory Bowel Diseases
Association Between Early-life Factors and Risk of Child-onset Crohn's Disease Among Victorian Children Born 1983-1998: A Birth Cohort Study
Ponsonby, AL; Catto-Smith, AG; Pezic, A; Dupuis, S; Halliday, J; Cameron, D; Morley, R; Carlin, J; Dwyer, T
Inflammatory Bowel Diseases, 15(6): 858-866.
American Journal of Epidemiology
Maternal and Perinatal Characteristics and the Risk of Cow's Milk Allergy in Infants up to 2 Years of Age: A Case-Control Study Nested in the Finnish Population
Metsala, J; Lundqvist, A; Kaila, M; Gissler, M; Klaukka, T; Virtanen, SM
American Journal of Epidemiology, 171(): 1310-1316.
Pediatric Research
Immunologic tolerance and dietary antigens - A review of: Newberry RD, Stenson WF, Lorenz RG 1999 cyclooxygenase-2-dependent arachidonic acid metabolites are essential modulators of the immune response to dietary antigen. Nature Med 5 : 900-906
Murch, SH
Pediatric Research, 47(4): 430.

American Journal of Physiology-Regulatory Integrative and Comparative Physiology
Elective cesarean delivery affects gut maturation and delays microbial colonization but does not increase necrotizing enterocolitis in preterm pigs
Siggers, RH; Thymann, T; Jensen, BB; Molbak, L; Heegaard, PMH; Schmidt, M; Buddington, RK; Sangild, PT
American Journal of Physiology-Regulatory Integrative and Comparative Physiology, 294(3): R929-R938.
Pediatric Research
Influence of Maternal Bifidobacteria on the Establishment of Bifidobacteria Colonizing the Gut in Infants
Mikami, K; Takahashi, H; Kimura, M; Isozaki, M; Izuchi, K; Shibata, R; Sudo, N; Matsumoto, H; Koga, Y
Pediatric Research, 65(6): 669-674.

Clinical Nutrition
Development of intestinal bifidobacteria and lactobacilli in breast-fed neonates
Chen, JJ; Cai, W; Feng, Y
Clinical Nutrition, 26(5): 559-566.
International Dairy Journal
Gut microbiota: Changes throughout the lifespan from infancy to elderly
O'Toole, PW; Claesson, MJ
International Dairy Journal, 20(4): 281-291.
American Journal of Primatology
Fecal Bacterial Diversity of Human-Habituated Wild Chimpanzees (Pan troglodytes schweinfurthii) at Mahale Mountains National Park, Western Tanzania
Szekely, BA; Singh, J; Marsh, TL; Hagedorn, C; Werre, SR; Kaur, T
American Journal of Primatology, 72(7): 566-574.
Pediatric Pulmonology
To the editor: Comment on Mallol et al
Renz-Polster, H; Wall, M
Pediatric Pulmonology, 32(3): 263.

Revue Francaise D Allergologie Et D Immunologie Clinique
Medicines for asthma, rhinitis and allergies - Precautions for pregnancy and breastfeeding
Demoly, P; Piette, V; Autret-Leca, E; de Blic, J; Francoual, C; Jacqz-Aigrain, E; Daures, JP
Revue Francaise D Allergologie Et D Immunologie Clinique, 43(): 3S-49S.

Medical Science Monitor
Model of the epidemic of childhood atopy
Schmidt, WP
Medical Science Monitor, 10(2): HY5-HY9.

Journal of Infectious Diseases
Cesarean Delivery and Risk of Intestinal Bacterial Infection
Bager, P; Simonsen, J; Ethelberg, S; Frisch, M
Journal of Infectious Diseases, 201(6): 898-902.
Perinatology 2001, Vols 1 and 2
Pro- and pre-biotics administration in preterm infants: Colonization and influence on the fecal flora
Marini, A; Boehm, G; Negretti, F; Destri, ML; Clerici-Bagozzi, D; Mosca, F; Agosti, M
Perinatology 2001, Vols 1 and 2, (): 455-459.

Gut flora in health and disease
Guarner, F; Malagelada, JR
Lancet, 361(): 512-519.

Pediatric Allergy and Immunology
Mode of delivery and development of atopic disease during the first 2 years of life
Negele, K; Heinrich, J; Borte, M; von Berg, A; Schaaf, B; Lehmann, I; Wichmann, HE; Bolte, G
Pediatric Allergy and Immunology, 15(1): 48-54.

European Journal of Clinical Microbiology & Infectious Diseases
Effects of mode of delivery and necrotising enterocolitis on the intestinal microflora in preterm infants
Hallstrom, M; Eerola, E; Vuento, R; Janas, M; Tammela, O
European Journal of Clinical Microbiology & Infectious Diseases, 23(6): 463-470.
Journal of Biological Chemistry
Functional genomic and metabolic studies of the adaptations of a prominent adult human gut symbiont, Bacteroides thetaiotaomicron, to the suckling period
Bjursell, MK; Martens, EC; Gordon, JI
Journal of Biological Chemistry, 281(): 36269-36279.
Dynamics of gut colonization and source of intestinal flora in healthy newborn infants
Tapiainen, T; Ylitalo, S; Eerola, E; Uhari, M
Apmis, 114(): 812-817.

Acta Paediatrica
Comparative analysis of neonatal morbidity for vaginal and caesarean section deliveries using hospital charge
Chang, JH; Hsu, CY; Lo, JC; Chen, CP; Huang, FY; Yu, SC
Acta Paediatrica, 95(): 1561-1566.
Clinical Nutrition
The effect of glutamine-enriched enteral nutrition on intestinal microflora in very low birth weight infants: A randomized controlled trial
van den Berg, A; van Elburg, RM; Westerbeek, EAM; van der Linde, EGM; Knol, J; Twisk, JWR; Fetter, WPF
Clinical Nutrition, 26(4): 430-439.
Pediatric Clinics of North America
Probiotics in children
Kligler, B; Hanaway, P; Cohrssen, A
Pediatric Clinics of North America, 54(6): 949-+.
Journal of Allergy and Clinical Immunology
Probiotics prevent IgE-associated allergy until age 5 years in cesarean-delivered children but not in the total cohort
Kuitunen, M; Kukkonen, K; Juntunen-Backman, K; Korpela, R; Poussa, T; Tuure, T; Haahtela, T; Savilahti, E
Journal of Allergy and Clinical Immunology, 123(2): 335-341.
Arquivos Brasileiros De Endocrinologia E Metabologia
Translational research into gut microbiota: new horizons in obesity treatment
Tsukumo, DM; Carvalho, BM; Carvalho, MA; Saad, MJA
Arquivos Brasileiros De Endocrinologia E Metabologia, 53(2): 139-144.

Inflammatory Bowel Diseases
Preterm birth but not mode of delivery is associated with an increased risk of developing inflammatory bowel disease later in life
Sonntag, B; Stolze, B; Heinecke, A; Luegering, A; Heidemann, J; Lebiedz, P; Rijcken, E; Kiesel, L; Domschke, W; Kucharzik, T; Maaser, C
Inflammatory Bowel Diseases, 13(): 1385-1390.
World Journal of Gastroenterology
Breath test for differential diagnosis between small intestinal bacterial overgrowth and irritable bowel disease: An observation on non-absorbable antibiotics
Esposito, I; de Leone, A; Di Gregorio, G; Giaquinto, S; de Magistris, L; Ferrieri, A; Riegler, G
World Journal of Gastroenterology, 13(): 6016-6021.

Journal of Nutrition
Postnatal development of intestinal microflora as influenced by infant nutrition
Morelli, L
Journal of Nutrition, 138(9): 1791S-1795S.

Journal of Tropical Pediatrics
Prophylactic Probiotics for Prevention of Necrotizing Enterocolitis in Very Low Birth Weight Newborns
Samanta, M; Sarkar, M; Ghosh, P; Ghosh, JK; Sinha, MK; Chatterjee, S
Journal of Tropical Pediatrics, 55(2): 128-131.
Clinical and Experimental Allergy
Caesarean section increases the risk of hospital care in childhood for asthma and gastroenteritis
Hakansson, S; Kallen, K
Clinical and Experimental Allergy, 33(6): 757-764.

Best Practice & Research in Clinical Gastroenterology
Isolauri, E; Salminen, S; Ouwehand, AC
Best Practice & Research in Clinical Gastroenterology, 18(2): 299-313.
Journal of Complementary Medicine
The hygiene hypothesis and probiotics in children
Dingle, P
Journal of Complementary Medicine, 6(4): 4-+.

Pediatric Allergy and Immunology
Is caesarean delivery associated with sensitization to food allergens and IgE-mediated food allergy: A systematic review
Koplin, J; Allen, K; Gurrin, L; Osborne, N; Tang, MLK; Dharmage, S
Pediatric Allergy and Immunology, 19(8): 682-687.
Isme Journal
16S rRNA gene-based analysis of fecal microbiota from preterm infants with and without necrotizing enterocolitis
Wang, YW; Hoenig, JD; Malin, KJ; Qamar, S; Petrof, EO; Sun, J; Antonopoulos, DA; Chang, EB; Claud, EC
Isme Journal, 3(8): 944-954.
Cesarean Delivery Is Associated With Celiac Disease but Not Inflammatory Bowel Disease in Children
Decker, E; Engelmann, G; Findeisen, A; Gerner, P; Laass, M; Ney, D; Posovszky, C; Hoy, L; Hornef, MW
Pediatrics, 125(6): E1433-E1440.
Archives of Disease in Childhood
Importance of intestinal colonisation in the maturation of humoral immunity in early infancy: a prospective follow up study of healthy infants aged 0-6 months
Gronlund, MM; Arvilommi, H; Kero, P; Lehtonen, OP; Isolauri, E
Archives of Disease in Childhood, 83(3): F186-F192.

Pediatrics International
Effects of bifidobacterium breve supplementation on intestinal flora of low birth weight infants
Li, YD; Shimizu, T; Hosaka, A; Kaneko, N; Ohtsuka, Y; Yamashiro, Y
Pediatrics International, 46(5): 509-515.

Journal of Clinical Gastroenterology
Bacterial colonization, probiotics, and necrotizing enterocolitis
Claud, EC; Walker, WA
Journal of Clinical Gastroenterology, 42(6): S46-S52.

Pediatric Allergy and Immunology
An anthroposophic lifestyle and intestinal microflora in infancy
Alm, JS; Swartz, J; Bjorksten, B; Engstrand, L; Engstrom, J; Kuhn, I; Lilja, G; Mollby, R; Norin, E; Pershagen, G; Reinders, C; Wreiber, K; Scheynius, A
Pediatric Allergy and Immunology, 13(6): 402-411.

Proceedings of the Nutrition Society
Dietary fibre in infancy and childhood
Edwards, CA; Parrett, AM
Proceedings of the Nutrition Society, 62(1): 17-23.
Journal of Allergy and Clinical Immunology
Mode of delivery at birth and development of asthma: A population-based cohort study
Juhn, YJ; Weaver, A; Katusic, S; Yunginger, J
Journal of Allergy and Clinical Immunology, 116(3): 510-516.
Clinical and Experimental Allergy
Maternal breast-milk and intestinal bifidobacteria guide the compositional development of the Bifidobacterium microbiota in infants at risk of allergic disease
Gronlund, MM; Gueimonde, M; Laitinen, K; Kociubinski, G; Gronroos, T; Salminen, S; Isolauri, E
Clinical and Experimental Allergy, 37(): 1764-1772.
Journal of Allergy and Clinical Immunology
Asthma and obesity: Common early-life influences in the inception of disease
Litonjua, AA; Gold, DR
Journal of Allergy and Clinical Immunology, 121(5): 1075-1084.
Fems Microbiology Ecology
Development of the intestinal microbiota in rats and its possible interactions with the evolution of the luminal IgA in the intestine
Inoue, R; Ushida, K
Fems Microbiology Ecology, 45(2): 147-153.
Ecological and evolutionary forces shaping microbial diversity in the human intestine
Ley, RE; Peterson, DA; Gordon, JI
Cell, 124(4): 837-848.
Clinical Nutrition
The intestinal bacterial colonisation in preterm infants: A review of the literature
Westerbeek, EAM; van den Berg, A; Lafeber, HN; Knol, J; Fetter, WPF; van Elburg, RM
Clinical Nutrition, 25(3): 361-368.
Mutation Research-Fundamental and Molecular Mechanisms of Mutagenesis
Importance of microbial colonization of the gut in early life to the development of immunity
Kelly, D; King, T; Aminov, R
Mutation Research-Fundamental and Molecular Mechanisms of Mutagenesis, 622(): 58-69.
Clinical and Experimental Allergy
Birth by caesarean section and asthma
Adams, M; Doull, I
Clinical and Experimental Allergy, 38(4): 554-556.
American Journal of Epidemiology
Perinatal factors and the risk of asthma in childhood - A population-based register study in Finland
Metsala, J; Kilkkinen, A; Kaila, M; Tapanainen, H; Klaukka, T; Gissler, M; Virtanen, SM
American Journal of Epidemiology, 168(2): 170-178.
Birth-related increase in intracolonic hydrogen gas and nitric oxide as indicator of host-microbial interactions
Sobko, T; Norman, M; Norin, E; Gustafsson, LE; Lundberg, JO
Allergy, 60(3): 396-400.
Archives De Pediatrie
Early bacterial colonisation of the intestine: why it matters?
Langhendries, JP
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Effect of Maternal Consumption of Lactobacillus GG on Transfer and Establishment of Fecal Bifidobacterial Microbiota in Neonates
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Back to Top | Article Outline

Bacteroides; Cesarean delivery; Colic; Colonization; Gut; Intestine

© 1999 Lippincott Williams & Wilkins, Inc.


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