RESEARCH REPORTS

Clinical

Y. Li1*, P.W. Caufield2, A.P. Dasanayake3, H.W. Wiener4, and S.H. Vermund4
of Basic Science and Craniofacial Biology, of Diagnostics, Infectious Disease and Health Promotion, and 3Department of Epidemiology and Health Promotion, New York University College of Dentistry, 345 East 24th Street, New York, NY 10010-4086, USA; and 4Department of Epidemiology, School of Public Health, University of Alabama at Birmingham, Birmingham, AL 35294, USA; *corresponding author, yihong.li@nyu.edu
2Division 1Department

Mode of Delivery and Other Maternal Factors Influence the Acquisition of Streptococcus mutans in Infants
INTRODUCTION
and after birth, the surfaces the oral cavity of Duringet al.,shortly infants becomeepithelial colonizersinarebacterial speciesa bacterially naïve colonized by various (Murray 2002). In general, these early members of the indigenous biota, and their presence plays an important role in host defense, not only in excluding potential exogenous pathogens, but also as stimuli for the development of the immune system in infants (Marsh, 2000). As members of the indigenous biota, Streptococcus oralis, S. mitis, and S. salivarius are the predominant pioneer streptococci that colonize the oral cavity of infants during the first few days of life (Smith et al., 1993; Pearce et al., 1995). The colonization by two other members of the indigenous biota, S. sanguinis and S. mutans, comes later, approximately at 1 and 2 yrs of age, respectively, following the emergence of primary teeth (Caufield et al., 1993, 2000). Because S. mutans plays a major role in the etiology of dental caries in humans, the acquisition and transmission of this bacterium in various populations have received extensive attention. Individual factors influence the initial acquisition of S. mutans in infants, including high maternal S. mutans levels and caries status, low infant birth-weight, obturators for management of cleft palate, early tooth emergence, and low salivary IgA antibody levels (Klein, 1946; van Houte et al., 1981; Köhler et al., 1988; Smith et al., 1998; Milgrom et al., 2000; Wan et al., 2001, 2003). Tooth enamel defects induced by maternal nutritional deficiency during pregnancy are significantly associated with early colonization by S. mutans in 3- to 5year-old children (Li et al., 1994). Moreover, pre-term infants are 4.4 times more likely to be colonized by S. mutans than are normal-term babies (Wan et al., 2003). Thus, individually tested pre-natal events appear to affect the initial acquisition of S. mutans in infants. The main objective of this study was to examine, comprehensively, a series of maternal and perinatal variables to determine their influence on the initial acquisition of S. mutans in infants.

J Dent Res 84(9):806-811, 2005

ABSTRACT
S. mutans plays a key role in dental caries. The extent to which perinatal events influence the acquisition of S. mutans is unclear. We hypothesized that several maternal factors, including the mode of delivery, influence the initial acquisition of S. mutans in infants. A prospective cohort study was conducted in 156 mother-infant pairs. The study found that maternal gestational age (p = 0.04), S. mutans level (p = 0.02), caries score (p = 0.02), sexually transmitted disease (STD) infection experience (p = 0.01), and family income (p = 0.03) had significant effects on the acquisition of S. mutans. Among infants who became infected, those delivered by Caesarean section acquired S. mutans 11.7 mos earlier than did vaginally delivered infants (p = 0.038). Csection infants harbored a single genotype of S. mutans that was identical to that of their mothers (100% fidelity). Analysis of the data demonstrated the possible perinatal influences on infants' acquisition of a member of the cariogenic microbiota, and its potential effect on caries outcome. KEY WORDS: S. mutans, acquisition, Caesarean, perinatal factors, dental caries.

MATERIALS & METHODS
Study Population
A total of 218 pregnant women in their third trimester of first pregnancies was enrolled in the study. The selection criteria included mothers who were: (1) seeking pre-natal care at the Jefferson County Department of Health in Birmingham, Alabama, between January, 1995, and December, 1999; (2) healthy and 18 yrs old or older; (3) had more than 10 natural teeth; and (4) gave informed consent as approved by the Institutional Review Board of the University of Alabama at Birmingham and the Jefferson County Department of Health. After delivery, the mother-infant pairs were followed over a four-year period; 62 pairs were lost to follow-up within the first 2 mos of the study. Thus, 156 mothers and their infants, 54.5% males and 45.5% females, were included in

Received October 13, 2004; Last revision April 30, 2005; Accepted June 1, 2005

806

J Dent Res 84(9) 2005

Acquisition of S. mutans in Infants

807

the final data analysis (Fig. 1A). There were no significant differences between the study cohort and the 'lost to follow-up' cohort regarding the mothers' age (20.3 vs. 20.9 yrs), gestational age (39.3 vs. 39.5 wks), infants' gender (54.5% vs. 46.8% male), birthweight (3212 vs. 3197 g), and mode of delivery (17.3% vs. 16.1% Caesarean). The first 55 mother-infant pairs enrolled in the study were also enrolled in an extensive bacterial genomic substudy; 50 of them completed the study. Of these 50 motherinfant pairs, 37 infants became S. mutans-positive in the study period, allowing for examination of the fidelity of S. mutans transmission (Fig. 1B).

Maternal Medical History and Dental Examination
A baseline questionnaire was administered by trained interviewers to all mothers in their 3rd trimester. Information on past medical and pregnancy histories was obtained from the mothers' medical records. A follow-up questionnaire was given to the mothers at follow-up visits (six-month intervals). The key variables examined are listed in Table 1. A dental examination for caries was carried out by two trained dentists at baseline and at 12-month intervals during follow-up visits, according to the criteria defined by the National Institute of Dental and Craniofacial Research for caries diagnosis and recording (USDHHS, 1989).

Bacterial Sample Collection and Cultivation
Saliva and plaque samples were collected at each visit as previously described (Pan et al., 2001). An additional swab sample from each pre-dentate infant was collected and streaked directly onto mitis salivarius, bacitracin-sucrose agar (MSB) (Gold et al., 1973) for direct cultivation of S. mutans. All samples were plated onto MSB medium with the use of a Spiral Autoplate ® 4000 (Spiral Biotech, Inc., Bethesda, MD, USA) within 3 hrs of collection. After a 72-hour incubation at 37°C in an anaerobic atmosphere of 85% N2, 10% H2, and 5% CO2, colony-forming units on each plate were enumerated for the estimation of the S. mutans level in the oral cavity.

S. mutans Identification and Genotyping
The positive detection of S. mutans and the differentiation of S. mutans from S. sobrinus were based on colony morphology (Gold et al., 1973), sugar fermentation tests described originally by Shklair and Keene (1974), and subsequently confirmed by APPCR fingerprinting (Li and Caufield, 1998; Li et al., 2001). The age of S. mutans acquisition for the infants was estimated by use of the midpoint of the age interval between the visit with detectable S. mutans and the immediately prior visit. S. mutans genotyping was performed for all 37 mother-infant pairs of the subgroup when the infants first acquired S. mutans. Genomic DNA of S. mutans was isolated with the use of a Promega Wizard® DNA purification kit (Promega, Madison, WI, USA). Arbitrarily primed polymerase chain-reaction (AP-PCR) was performed to generate DNA fingerprinting profiles for analysis (Li and Caufield, 1998). Fidelity was identified if the infant and mother shared the same type of molecular fingerprint (Li and Caufield, 1995).

Figure 1. A schematic illustration of the overall study design. (A) The mother-child cohort for determination of S. mutans acquisition in the children (N = 156). 3T = 3rd trimester; DL = delivery. (B) A sub-set mother-child cohort for comparison of the fidelity of S. mutans transmission (N = 50).

performed for examination of the age distribution of S. mutans acquisition against mode of delivery. Logistic regression analyses with a backward-elimination-model selection method were applied to ascertain the interactions among different variables and covariables, in relation to the age of S. mutans colonization in the infants. All p values presented are two-tailed.

RESULTS
Maternal Characteristics
All 156 participants were low-income, primigravid mothers; 92.9% of them were single mothers; 91.0% were AfricanAmerican, 8.3% were white, and 0.6% Hispanic. Approximately 8.3% of the mothers consumed alcohol, and 11.8% smoked tobacco cigarettes on a regular basis; 45.1% had a history of STD infection, and 91.7% were treated before or during the pregnancy. The mean maternal age at time of delivery was 21.1 yrs (range, 16.3 to 34.5), and average gestational age was 39.3 wks (range, 29.3 to 42.1). Of the 156 children, 127 (81.4%) were delivered by normal spontaneous vaginal delivery and 29 (18.6%) by Caesarean section (Csection). The average birth weight was 3212 grams (range,

Statistical Analyses
Based on bacterial colony counts per milliliter of saliva, S. mutans levels were calculated and were transformed to a logarithm (log10) value. Univariate analyses were performed by analysis of variance (ANOVA), Spearman's correlation coefficient, and non-parametric Mann-Whitney U tests, for comparisons of continuous variables, and Pearson chi-square and Fisher's Exact Test, for comparisons of discrete variables (SPSS 12.0 for Windows). Survival analysis was

808

Li et al.

J Dent Res 84(9) 2005

Table 1. Comparisons between the Initial Acquisition of S. mutans in the Infants and the Key Variables Examined Children with Nondetectable S. mutansa N = 101 (%) 55 (54.5) 46 (45.5) 7 ( 6.9) 94 (93.1) 81 (80.2) 20 (19.8) 21 (26.3) 59 (73.8) 13 (12.9) 72 (71.3) 16 (15.8) 6 ( 8.2) 67 (91.8) 30 (29.7) 71 (70.3) 16 (15.8) 85 (84.2) 20 (47.6) 22 (52.4) 9 (13.6) 57 (86.4) 6 ( 9.4) 58 (90.6) 25 (40.3) 37 (59.7) 21 (33.9) 41 (66.1) 13 (15.1) 47 (54.7) 26 (30.2) 61 (60.4) 21 (20.8) 19 (18.8) Children with Detectable S. mutansa N = 55 (%) 30 (54.5) 25 (45.5) 3 ( 5.5) 52 (94.5) 46 (83.6) 9 (16.4) 15 (30.0) 35 (70.0) 9 (16.4) 29 (52.7) 17 (30.9) 4 ( 8.0) 46 (92.0) 14 (25.5) 41 (74.5) 12 (21.8) 43 (78.2) 20 (58.8) 14 (41.2) 4 ( 9.1) 40 (90.9) 3 ( 6.8) 41 (93.2) 21 (52.5) 19 (47.5) 10 (25.0) 30 (75.0) 6 (11.8) 25 (49.0) 20 (39.2) 15 (27.3) 23 (41.8) 17 (30.9) Age of Acquisition, mean ± SD, month

Variables Examined Infant key factors Gender Birth weight Mode of delivery Breast-feeding Maternal key factors Age, yrs

p Valueb

p Valuec

Male Female < 2500 g > 2500 g Vaginal C-section Yes No

0.99 0.72 0.60 0.64

23.4 ± 13.1 21.1 ± 9.4 31.4 ± 15.8 21.8 ± 11.3 28.8 ± 1.8 17.1 ± 1.4 20.9 ± 10.9 22.6 ± 11.3 20.5 ± 13.8 21.4 ± 11.0 24.8 ± 11.5 25.6 ± 5.9 23.2 ± 11.8 28.6 ± 15.0 20.3 ± 9.5 28.3 ± 12.4 20.6 ± 10.9 24.3 ± 11.8 23.5 ± 13.3 20.8 ± 8.0 24.3 ± 12.3 22.8 ± 8.4 24.1 ± 12.3 23.0 ± 13.4 26.2 ± 11.5 24.5 ± 17.1 24.5 ± 10.9 22.9 ± 8.9 21.9 ± 11.6 22.4 ± 11.9 18.8 ± 10.2 23.4 ± 12.0 24.0 ± 11.6

0.47 0.16 0.038 0.63

< 18 18-22 > 23 Caries status DMFT = 0 DMFT > 1 S. mutans levels in saliva < Log10 5.5 > Log10 5.5 < 38 Gestational age, wks > 38 < 30 Weight gain, lbs. > 30 Regular cigarette smoking Yes No Regular alcohol drinking Yes No History of STD infection Yes No Use antibiotics during pregnancy Yes No Mother's education, yrs < 12 13-16 > 17 Annual family income < $1000 $1000-$10,000 > $10,000

0.049

0.55

0.96 0.57 0.35 0.33 0.56 0.73 0.23

0.74 0.02 0.04 0.86 0.58 0.87 0.42

0.34 0.54

0.99 0.97

< 0.001

0.39

a b c

The numbers of children with non-detectable S. mutans and detectable S. mutans were 101 and 55, respectively. Totals of less than 101 or 55 are due to missing observations. Pearson Chi-square test or Fisher's Exact test for comparison of percentage distributions. ANOVA statistics for mean comparisons.

1250 to 4630); 6.5% of the infants had low birth weights (< 2500 grams). Among the mothers, 91.1% were the primary caregivers of their infants; 23.1% breastfed their infants for an average length of 3.6 mos (range, 0.3 to 12). In addition, dental caries was present in 75.3% of the mothers. The mean DMFT (decayed, missing, and filled tooth) and DMFS (tooth surface) were 8.7 ± 5.3 and 17.8 ± 14.3, respectively.

S. mutans Acquisition and Transmission
S. mutans was detected in 55 of the 156 infants (35.3%), with the average acquisition age of 22.3 ± 11.6 mos (median = 20.3). There were no statistically significant correlations between the incidence and the age of initial acquisition of S. mutans with the infant's gender, birth weight, or breast-feeding

experience. Univariate analyses demonstrated that most of the maternal factors exerted no measurable influence on S. mutans colonization in the infants. However, maternal age (p = 0.049), gestational age (p = 0.04), S. mutans level (p = 0.02), and family annual income (p < 0.01) had an effect on either the percentage of colonization or the age of acquisition by S. mutans in the infants (Tables 1, 2). The C-section infants acquired S. mutans at a younger age compared with the vaginally delivered infants (17.1 vs. 28.8 mos, p = 0.038). Although the percentage of infants with detectable S. mutans was similar between the two groups (31.0% for C-section vs. 36.7% for vaginal), the age range was greater for the vaginally delivered children (3.3 to 49.2 mos; median = 21.3) than for the C-section children (7.7 to 21.4 mos; median = 16.7). The

J Dent Res 84(9) 2005
survival analysis also suggested that the mode of delivery was significantly associated with earlier S. mutans acquisition in infants (Chi-square for Wilcoxon test, p = 0.039) (Fig 2). In the multivariable model, C-section (p = 0.01), higher maternal DMFT score (p = 0.02), past maternal STD infection experience (p = 0.01), and lower family annual income (p = 0.03) remained significant predictors for early S. mutans colonization after adjustment for all other maternal factors listed in Table 1. The reduced model accounted for 35.9% of the variance in the time to infection by S. mutans (Chi-square for the model coefficients = 10.6; -2 log likelihood = 53.7; r2 = 0.359; p = 0.48 indicates that the model fit well). Complete S. mutans genomic DNA fingerprint profiles were obtained for the 37 mother-infant pairs (six C-section and 31 vaginal deliveries). The overall fidelity of the children's S. mutans genotypes (identical to that of their mothers) was 88.9%. All six children in the C-section group harbored only 1 genotype of S. mutans, which was identical to that of their mothers (100% fidelity). In vaginally delivered children, the average number of genotypes was 1.7 (ranging from 1 to 3), with an 83.3% match to their mothers'. Thus, the fidelity for C-section children was higher compared with that for the vaginally delivered children (p = 0.001; non-parametric Mann-Whitney U test).

Acquisition of S. mutans in Infants
Table 2. Comparison of Maternal Key Factors with Mode of Delivery among the Infants Mode of Delivery Caesarean Vaginal N = 29 N = 127 Caries present, % 24 (96.0) DMFT, mean ± SD 7.12 ± 4.0 DMFS, mean ± SD 12.6 ± 6.8 S. mutans levels in saliva < Log 5.5 3 (10.3) 10 > Log10 5.5 26 (89.7) mean, Log10 5.8 ± 0.4 Gestational age, wks ± SD 39.4 ± 2.1 Birth weight, g ± SD 3179.4 ± 550.6 Weight gain, lbs ± SD 31.5 ± 6.3 Age at delivery, yrs ± SD 21.8 ± 4.3 Self-reported regular cigarette smoking Yes, % 4 (23.5) Self-reported regular alcohol consumption Yes, % 2 (12.5) History of STD infection Yes, % 11 (61.1) Family annual income < $1000, % 9 (31.0) $1000-$10,000, % 11 (37.9) > $10,000, % 9 (31.0) mean ± SD 6251.7 ± 6381.0
a

809

p Valuea

89 (90.8) 6.9 ± 5.3 14.7 ± 14.5 41 (32.3) 86 (67.7) 5.6 ± 0.9 39.3 ± 2.0 3219.9 ± 519.9 28.7 ± 10.4 20.9 ± 3.3 9 ( 9.7) 7 ( 7.6) 35 (41.7) 67 (52.8) 33 (26.0) 27 (21.3) 4701.5 ± 6188.2

0.397 0.880 0.502 0.018 0.150 0.692 0.709 0.355 0.205 0.115 0.619 0.132 0.108

0.228

Comparisons of percentage distributions were performed with the Pearson Chi-square test or Fisher's Exact test. Comparisons of means were performed with ANOVA statistics.

DISCUSSION
Discovering that the mode of delivery significantly affected the time of acquisition of S. mutans in the infants, although novel, was not totally unexpected. However, the finding that C-section infants become colonized 11.7 mos earlier than do vaginally delivered infants was. We hypothesized that the Caesarean-delivery-accelerated initial acquisition of S. mutans may be due to less exposure to the maternal microbiota at birth. Logically, vaginally delivered newborns come into contact with greater numbers and varieties of bacteria from the perineum (vagina and anus) earlier and with greater intensity than do the relatively aseptically delivered Caesarean-born babies. But it is not clear how early colonization of the total microbes would influence the colonization of S. mutans occurring some 2 yrs later. Gibbons and co-workers demonstrated that the initial pioneer microbes entering the oral cavity influence the pattern of microbial succession, and that the succession is associated with the availability of colonization sites (Gibbons, 1989). Bacteria that subsequently attempt to colonize must compete with other micro-organisms for colonization sites and essential nutrients. Additionally, they must survive in the presence of adverse metabolic endproducts and antimicrobial products that may be produced by other members of the indigenous oral biota. Once established, early-colonizing species tend to persist in the mouth (Cole et al., 1998; Könönen et al., 1999). Because the Caesarean-born infants may have experienced less exposure to maternal and

environmental microbial challenges at birth, an atypical microbial environment may prevail, providing more potential biological binding niches for 'latecomers' such as S. mutans. Hence, the difference observed in this study, in 'time to

Figure 2. Comparison of survival experience suggests that children who were vaginally delivered (N = 127) experienced significantly delayed acquisition of S. mutans compared with the children who were delivered by Caesarean section (N = 29) (p = 0.039). The x-axis is the infant's age; the y-axis is the probability that children were S. mutans-free (survival) at a given age. Since all children were initially S. mutans-free at birth (100% survival), the y value on the graph starts at 1. On average, children delivered by Caesarean section acquired S. mutans 11.7 mos earlier than did vaginally delivered infants (Wilcoxon statistic; p = 0.039).

810

Li et al.

J Dent Res 84(9) 2005

colonization' as a function of the mode of delivery, may result from alterations in the sequence and diversity of oral microbes preceding S. mutans colonization. This study examined a series of maternal and perinatal variables and revealed that a reduced multivariable model— including C-section, maternal caries status, STD infection experience, and family annual income—could account for 35.9% of the variance in the time to infection by S. mutans in the infants. A univariate analysis showed a positive correlation between a higher level of S. mutans in the mothers' saliva and earlier colonization of S. mutans in the infants, as suggested by others (Köhler et al., 1983; Köhler and Andreen, 1994; Li et al., 2000); the significance was diminished after adjustment for all other maternal variables in the multivariable regression analysis. It could be that since 86.5% of the mothers had high levels of S. mutans at 10 5-10 7 per mL in their saliva, the predictive model was less robust. Another potential mediator could be the use of antibiotics during pregnancy and infancy. However, the study did not find a significant correlation among exposure to antibiotics, mode of delivery, and the time to infection by S. mutans in the infants. Part of this lack of difference might be due to the high rate of antibiotic usage (91.7%) for the treatment and prevention of transmission of STDs. Therefore, the role of antibiotics in 'time to colonization' could not be definitively determined and remains a possible contributor to the difference in S. mutans acquisition. Another significant finding is that all of the Caesarean-born children had only 1 genotype of the S. mutans strain that was identical to their mothers', compared with as many as 3 different genotypes found in vaginally delivered children. Previously, Isenberg et al. (1988) reported that Caesarean-born children had significantly decreased numbers of bacterial species and colony-forming units of conjunctivae than did vaginally delivered children, suggesting that, by avoiding passage through the birth canal, C-section infants may be less likely to be exposed to various bacterial species and strains from the mothers. Previously, we reported that the fidelity of S. mutans transmission among mother-infant pairs was 70.6% in a Birmingham, AL, cohort (Li and Caufield, 1995). We also noted that African-American mothers transmitted S. mutans with greater fidelity than Caucasian mothers, and this difference approached statistical significance. In the present study, the overall fidelity rate was 88.9%, and most of the mothers (91.0%) were African-Americans, supporting our previous observation that the mother was the main source of S. mutans transmission to the child. In conclusion, in this four-year follow-up study, we observed a positive association between Caesarean delivery and initial acquisition and transmission of S. mutans in a mother-infant cohort. Analysis of the data also suggests that an infant born by C-section from a mother with a low socioeconomic status, and who experienced tooth decay, acquired S. mutans earlier than did a normal vaginally born infant. Since earlier colonization of S. mutans was significantly associated with higher incidence and more severe dental caries in children (Köhler et al., 1988; Li et al., 1994; Lai et al., 1997), the mode of delivery may be an appropriate question to be included in past medical history for further determination of why some children are at greater risk for caries than others.

ACKNOWLEDGMENTS
This investigation was supported under the auspices of the Specialized Caries Research Center at the University of Alabama at Birmingham and was funded by the National Institute of Dental and Craniofacial Research (Grants DE11147 and DERR10595), National Institutes of Health, Bethesda, MD 20892. We thank Dr. Shelia White, Ms. Loretta Rucker, Dr. Zhenmei Lu, and Dr. Winnie Lee for their technical assistance in collecting and processing the samples for this research project, and Ms. Janice Wu for proofreading this manuscript. We also thank Dr. Gary Cutter, Professor of Biostatistics at the School of Public Health at the University of Alabama at Birmingham, and Dr. Karen Hendricks-Munoz, Director and Associate Professor of the Neonatology Program at the New York University School of Medicine, for their insightful comments on this manuscript.

REFERENCES
Caufield PW, Cutter GR, Dasanayake AP (1993). Initial acquisition of mutans streptococci by infants: evidence for a discrete window of infectivity. J Dent Res 72:37-45. Caufield PW, Dasanayake AP, Li Y, Pan Y, Hsu J, Hardin JM (2000). Natural history of Streptococcus sanguinis in the oral cavity of infants: evidence for a discrete window of infectivity. Infect Immun 68:4018-4023. Cole MF, Bryan S, Evans MK, Pearce CL, Sheridan MJ, Sura PA, et al. (1998). Humoral immunity to commensal oral bacteria in human infants: salivary antibodies reactive with Actinomyces naeslundii genospecies 1 and 2 during colonization. Infect Immun 66:4283-4289. Gibbons RJ (1989). Bacterial adhesion to oral tissues: a model for infectious diseases. J Dent Res 68:750-760. Gold OG, Jordan HV, van Houte J (1973). A selective medium for Streptococcus mutans. Arch Oral Biol 18:1357-1364. Isenberg SJ, Apt L, Yoshimori R, McCarty JW, Alvarez SR (1988). Source of the conjunctival bacterial flora at birth and implications for ophthalmia neonatorum prophylaxis. Am J Ophthalmol 106:458-462. Klein H (1946). The family and dental disease. IV. Dental disease (DMF) experience in parents and offspring. J Am Dent Assoc 33:735-743. Köhler B, Andreen I (1994). Influence of caries-preventive measures in mothers on cariogenic bacteria and caries experience in their children. Arch Oral Biol 39:907-911. Köhler B, Bratthall D, Krasse B (1983). Preventive measures in mothers influence the establishment of the bacterium Streptococcus mutans in their infants. Arch Oral Biol 28:225-231. Köhler B, Andreen I, Jonsson B (1988). The earlier the colonization by mutans streptococci, the higher the caries prevalence at 4 years of age. Oral Microbiol Immunol 3:14-17. Könönen E, Kanervo A, Takala A, Asikainen S, Jousimies-Somer H (1999). Establishment of oral anaerobes during the first year of life. J Dent Res 78:1634-1639. Lai PY, Seow WK, Tudehope DI, Rogers Y (1997). Enamel hypoplasia and dental caries in very-low birthweight children: a case-controlled, longitudinal study. Pediatr Dent 19:42-49. Li Y, Caufield PW (1995). The fidelity of initial acquisition of mutans streptococci by infants from their mothers. J Dent Res 74:681-685. Li Y, Caufield PW (1998). Arbitrarily primed polymerase chain reaction fingerprinting for the genotypic identification of mutans

J Dent Res 84(9) 2005

Acquisition of S. mutans in Infants

811

streptococci from humans. Oral Microbiol Immunol 13:17-22. Li Y, Navia JM, Caufield PW (1994). Colonization by mutans streptococci in the mouths of 3- and 4-year-old Chinese children with or without enamel hypoplasia. Arch Oral Biol 39:1057-1062. Li Y, Wang W, Caufield PW (2000). The fidelity of mutans streptococci transmission and caries status correlate with breast-feeding experience among Chinese families. Caries Res 34:123-132. Li Y, Caufield PW, Emanuelsson IR, Thornqvist E (2001). Differentiation of Streptococcus mutans and Streptococcus sobrinus via genotypic and phenotypic profiles from three different populations. Oral Microbiol Immunol 16:16-23. Marsh PD (2000). Oral ecology and its impact on oral microbial diversity. In: Oral bacterial ecology: the molecular basis. Kuramitsu HK, Ellen RP, editors. Norfolk, England: Horizon Scientific Press, pp. 11-65. Milgrom P, Riedy CA, Weinstein P, Tanner AC, Manibusan L, Bruss J (2000). Dental caries and its relationship to bacterial infection, hypoplasia, diet, and oral hygiene in 6- to 36-month-old children. Community Dent Oral Epidemiol 28:295-306. Murray PR, Rosenthal KS, Kobayashi GS, Pfaller MA (2002). Commensal and pathogenic microbial flora in humans. In: Medical microbiology. St. Louis, MO: Mosby, Inc., pp. 78-87. Pan YP, Li Y, Caufield PW (2001). Phenotypic and genotypic diversity of Streptococcus sanguis in infants. Oral Microbiol Immunol 16:235-242.

Pearce C, Bowden GH, Evans M, Fitzsimmons SP, Johnson J, Sheridan MJ, et al. (1995). Identification of pioneer viridans streptococci in the oral cavity of human neonates. J Med Microbiol 42:67-72. Shklair IL, Keene HJ (1974). A biochemical scheme for the separation of the five varieties of Streptococcus mutans. Arch Oral Biol 19:1079-1081. Smith DJ, Anderson JM, King WF, van Houte J, Taubman MA (1993). Oral streptococcal colonization of infants. Oral Microbiol Immunol 8:1-4. Smith DJ, King WF, Akita H, Taubman MA (1998). Association of salivary immunoglobulin A antibody and initial mutans streptococcal infection. Oral Microbiol Immunol 13:278-285. USDHHS (1989). Oral health of United States children. Washington, DC: Government Printing Office. van Houte J, Yanover L, Brecher S (1981). Relationship of levels of the bacterium Streptococcus mutans in saliva of children and their parents. Arch Oral Biol 26:381-386. Wan AK, Seow WK, Walsh LJ, Bird P, Tudehope DL, Purdie DM (2001). Association of Streptococcus mutans infection and oral developmental nodules in pre-dentate infants. J Dent Res 80:19451948. Wan AK, Seow WK, Purdie DM, Bird PS, Walsh LJ, Tudehope DI (2003). A longitudinal study of Streptococcus mutans colonization in infants after tooth eruption. J Dent Res 82:504-508.

Sign up to vote on this title
UsefulNot useful