Skip to main content

Advertisement

SpringerLink
Log in

Comparative evaluation of the effects of human breast milk and plain and probiotic-containing infant formulas on enamel mineral content in primary teeth: an in vitro study

  • Original Scientific Article
  • Published:
European Archives of Paediatric Dentistry Aims and scope Submit manuscript

Abstract

Aim

This study quantitatively investigated the changes in enamel mineral content of primary teeth after immersion in human breast milk and plain and probiotic-containing infant formulas.

Methods

Thirty-six sound primary anterior teeth were collected and assessed for mineral content (calcium and phosphorus content in wt%) using scanning electron microscope attached with energy-dispersive X-ray analyser (SEM–EDXA). In order to create a microbial-induced caries model, the enamel surfaces of the teeth were inoculated with mutans streptococci and then each tooth was randomly assigned to one of three groups: human breast milk, plain infant formula or probiotic-containing infant formula (n = 12) each. Teeth were then soaked in the designated type of milk, and the solutions were replenished every day for 1 week after which the mineral content was measured again using SEM–EDXA. Wilcoxon signed-rank test was used to study the changes by time within each group, and the significance level was set at P ≤ 0.05.

Results

Treatment of enamel surface with breast milk has significantly increased mean Ca wt%, while no significant changes were detected in mean P wt%. On the other hand, when primary teeth were soaked in plain or probiotic-containing infant formulas, both mean values of both Ca and P wt% significantly decreased.

Conclusions

In conclusion, whereas breast milk might confer some protective effect against enamel demineralisation, infant formulas whether plain or supplemented with some probiotics might promote loss of minerals from enamel surface.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aarthi J, Muthu MS, Sujatha S. Cariogenic potential of milk and infant formulas: a systematic review. Eur Arch Paediatr Dent. 2013;14(5):289–300.

    PubMed  Google Scholar 

  • Alianmoghaddam N, Phibbs S, Benn C. Reasons for stopping exclusive breastfeeding between three and six months: a qualitative study. J Pediatr Nurs. 2018;39:37–43.

    PubMed  Google Scholar 

  • American Academy of Pediatric Dentistry (AAPD). Policy on early childhood caries (ECC): classifications, consequences and preventive strategies. Revised. http://www.aapd.org/media/policies_guidelines/p_eccclassifications.pdf (2014). Accessed 12 Jan 2018.

  • Anderson DM. From Pediatric nutrition. In: Samour PQ, Helm KK, editors. Handbook of pediatric nutrition. 3rd ed. Sudbury, MA: James and Bartlett Publishers; 2005. p. 53–71.

    Google Scholar 

  • Anil S, Anand PS. Early childhood caries: prevalence, risk factors and prevention. Front Pediatr. 2017;5:157.

    PubMed  PubMed Central  Google Scholar 

  • Azevedo TD, Bezerra AC, de Toledo OA. Feeding habits and severe early childhood caries in Brazilian preschool children. Pediatr Dent. 2005;27:28–33.

    PubMed  Google Scholar 

  • Ballard O, Morrow AL. Human milk composition: nutrients and bioactive factors. Pediatr Clin N Am. 2013;60(1):49–74.

    Google Scholar 

  • Becker MR, Paster BJ, Leys EJ, et al. Molecular analysis of bacterial species associated with childhood caries. J Clin Microbiol. 2002;40(3):1001–9.

    PubMed  PubMed Central  Google Scholar 

  • Beighton D. The complex oral microflora of high-risk individuals and groups and its role in the caries process. Community Dent Oral Epidemiol. 2005;33(4):248–55.

    PubMed  Google Scholar 

  • Beighton D, Manji F, Baelum V, et al. Associations between salivary levels of Streptococcus mutans, Streptococcus sobrinus, Lactobacilli, and caries experience in Kenyan adolescents. J Dent Res. 1989;68(8):1242–6.

    PubMed  Google Scholar 

  • Beighton D, Al-Haboubi M, Mantzourani M, et al. Oral Bifidobacteria: caries-associated bacteria in older adults. J Dent Res. 2010;89(9):970–4.

    PubMed  Google Scholar 

  • Bissar A, Schiller P, Wolff A, et al. Factors contributing to severe early childhood caries in south-west Germany. Clin Oral Investig. 2014;18:1411–8.

    PubMed  Google Scholar 

  • Blumenshine SL, Vann WF, Gizlice Z, et al. Children’s school performance: impact of general and oral health. J Public Health Dent. 2008;68(2):82–7.

    PubMed  Google Scholar 

  • Bron PA, van Baarlen P, Kleerebezem M. Emerging molecular insights into the interaction between probiotics and the host intestinal mucosa. Nat Rev Microbiol. 2011;10:66–78.

    PubMed  Google Scholar 

  • Brown CR, Dodds L, Legge A, et al. Factors influencing the reasons why mothers stop breastfeeding. Can J Public Health. 2014;105:179–85.

    Google Scholar 

  • Burns E, Triandafilidis Z. Taking the path of least resistance: a qualitative analysis of return to work or study while breastfeeding. Int Breastfeed J. 2019;4(14):15.

    Google Scholar 

  • Bussell RM, Nichol R, Toumba KJ. Fluoride levels in UK infant milks. Eur Arch Paediatr Dent. 2016;17(3):177–85.

    PubMed  PubMed Central  Google Scholar 

  • Çaglar E, Kargul B, Tanboga I. Bacteriotherapy and probiotics’ role on oral health. Oral Dis. 2005;11(3):131–7.

    PubMed  Google Scholar 

  • Caufield PW, Schön CN, Saraithong P, et al. oral lactobacilli and dental caries. A model for niche adaptation in humans. J Dent Res. 2015;94(9 Suppl):110–8.

    Google Scholar 

  • De Matos BM, Brighenti FL, Do T, et al. Acidogenicity of dual-species biofilms of Bifidobacteria and Streptococcus mutans. Clin Oral Investig. 2017;21(5):1769–76.

    PubMed  Google Scholar 

  • Dilley GJ, Dilley DH, Machen JB. Prolonged nursing habit: a profile of patients and their families. ASDC J Dent Child. 1980;47:102–8.

    PubMed  Google Scholar 

  • Eidelman AI. Breastfeeding and the use of human milk: an analysis of the American Academy of Pediatrics 2012 Breastfeeding Policy Statement. Breastfeed Med. 2012;7(5):323–4.

    PubMed  Google Scholar 

  • Erickson PR, Mazhari E. Investigation of the role of human breast milk in caries development. Pediatr Dent. 1999;21(2):86–90.

    PubMed  Google Scholar 

  • European Commission Directive 2006/141/EC. http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2006:401:0001:0033:EN:PDF (2006). Accessed 3 Feb 2018.

  • Feldens CA, Giugliani ER, Vigo Á, et al. Early feeding practices and severe early childhood caries in four-year-old children from southern Brazil: a birth cohort study. Caries Res. 2010;44:445–52.

    PubMed  Google Scholar 

  • Gao SS, Zhang S, Mei ML, et al. Caries remineralisation and arresting effect in children by professionally applied fluoride treatment - a systematic review. BMC Oral Health. 2016;16:12.

    PubMed  PubMed Central  Google Scholar 

  • Gold OG, Jordan HV, Van Houte J. A selective medium for Streptococcus mutans. Arch Oral Biol. 1973;18(11):1357–64.

    PubMed  Google Scholar 

  • Haukioja A, Söderling E, Tenovuo J. Acid production from sugars and sugar alcohols by probiotic Lactobacilli and Bifidobacteria in vitro. Caries Res. 2008;42(6):449–53.

    PubMed  Google Scholar 

  • Hegde MN, Moany A. Remineralization of enamel subsurface lesions with casein phosphopeptide-amorphous calcium phosphate: a quantitative energy dispersive X-ray analysis using scanning electron microscopy: an in vitro study. J Conserv Dent. 2012;15(1):61–7.

    PubMed  PubMed Central  Google Scholar 

  • Hegde MN, Shetty S, Pardal D. Remineralization of enamel sub-surface lesion using casein phosphopeptide amorphous calcium phosphate. J Conserv Dent. 2007;10:19–25.

    Google Scholar 

  • Hinds LM, Moser EA, Eckert G, et al. Effect of infant formula on Streptococcus mutans biofilm formation. J Clin Pediatr Dent. 2016;40(3):178–85.

    PubMed  Google Scholar 

  • Hirai Y, Kawakata N, Satoh K, et al. Concentrations of lactoferrin and iron in human milk at different stages of lactation. J Nutr Sci Vitaminol (Tokyo). 1990;36(6):531–44.

    Google Scholar 

  • Iida H, Auinger P, Billings RJ, et al. Association between infant breastfeeding and early childhood caries in the United States. Pediatrics. 2007;120:944–52.

    Google Scholar 

  • Kramer MS, Vanilovich I, Matush L, et al. The effect of prolonged and exclusive breast-feeding and dental caries in early school-age children. Caries Res. 2007;41:484–8.

    PubMed  Google Scholar 

  • Lamont RJ, Demuth DR, Davis CA, et al. Salivary-agglutinin-mediated adherence of Streptococcus mutans to early plaque bacteria. Infect Immun. 1991;59:3446–50.

    PubMed  PubMed Central  Google Scholar 

  • Lemos JA, Abranches J, Burne RA. Responses of cariogenic streptococci to environmental stresses. Curr Issues Mol Biol. 2005;7:95–107.

    PubMed  Google Scholar 

  • Lodi CS, Sassaki KT, Fraiz FC, et al. Evaluation of some properties of fermented milk beverages that affect the demineralization of dental enamel. Braz Oral Res. 2010;24(1):95–101.

    PubMed  Google Scholar 

  • Majorana A, Cagetti MG, Bardellini E, et al. Feeding and smoking habits as cumulative risk factors for early childhood caries in toddlers, after adjustment for several behavioral determinants: a retrospective study. BMC Pediatr. 2014;14:45.

    PubMed  PubMed Central  Google Scholar 

  • Mantzourani M, Fenlon M, Beighton D. Association between Bifidobacteriaceae and the clinical severity of root caries lesions. Oral Microbiol Immunol. 2009a;24:32–7.

    PubMed  Google Scholar 

  • Mantzourani M, Gilbert SC, Sulong HN, et al. The isolation of bifidobacteria from occlusal carious lesions in children and adults. Caries Res. 2009b;43:308–13.

    PubMed  Google Scholar 

  • Martinhon CC, Italiani Fde M, Padilha Pde M, et al. Effect of iron on bovine enamel and on the composition of the dental biofilm formed “in situ”. Arch Oral Biol. 2006;51:471–5.

    PubMed  Google Scholar 

  • Mohebbi SZ, Virtanen JI, Vahid-Golpayegani M, et al. Feeding habits as determinants of early childhood caries in a population where prolonged breastfeeding is the norm. Community Dent Oral Epidemiol. 2008;36:363–9.

    PubMed  Google Scholar 

  • Naase L, Hatakka K, Savilahti E, et al. Effect of long-term consumption of a probiotic bacterium, Lactobacillus rhamnosus GG, in milk on dental caries and caries risk in children. Caries Res. 2001;35:412–20.

    Google Scholar 

  • Nakajo K, Takahashi N, Beighton D. Resistance to acidic environments of caries-associated bacteria: Bifidobacterium dentium and Bifidobacterium longum. Caries Res. 2011;44:431–7.

    Google Scholar 

  • Ongtenco KL, Anthonappa RP, Itthagarun A, et al. Remineralization of initial enamel carious lesions using fluoridated milk in vitro. Acta Odontol Scand. 2014;72(8):737–44.

    PubMed  Google Scholar 

  • Peres RC, Coppi LC, Volpato MC, et al. Cariogenic potential of cows’, human and infant formulas and effect of fluoride supplementation. Br J Nutr. 2009;101:376–82.

    PubMed  Google Scholar 

  • Petersson LG, Magnusson K, Hakestam U, et al. Reversal of primary root caries lesions after daily intake of milk supplemented with fluoride and probiotic lactobacilli in older adults. Acta Odontol Scand. 2011;69(6):321–7.

    PubMed  Google Scholar 

  • Prabhakar AR, Kurthukoti AJ, Gupta P. Cariogenicity and acidogenicity of human milk, plain and sweetened bovine milk: an in vitro study. J Clin Pediatr Dent. 2010;34(3):239–47.

    PubMed  Google Scholar 

  • Richards D. Breastfeeding up to 12 months of age not associated with increased risk of caries. Evid Based Dent. 2016;17(3):75–6.

    PubMed  Google Scholar 

  • Ripa LW. Nursing caries: a comprehensive review. Pediatr Dent. 1988;10:268–82.

    PubMed  Google Scholar 

  • Salone LR, Vann WF Jr, Dee DL. Breastfeeding: an overview of oral and general health benefits. J Am Dent Assoc. 2013;144(2):143–51.

    PubMed  Google Scholar 

  • Saxelin M, Tynkkynen S, Mattila-Sandholm T, et al. Probiotic and other functional microbes: from markets to mechanisms. Curr Opin Biotechnol. 2005;16:204–11.

    PubMed  Google Scholar 

  • Sheiham A. Dental caries affects body weight, growth and quality of life in pre-school children. Br Dent J. 2006;201:625–6.

    PubMed  Google Scholar 

  • Stensson M, Koch G, Coric S, et al. Oral administration of Lactobacillus reuteri during the first year of life reduces caries prevalence in the primary dentition at 9 years of age. Caries Res. 2014;48(2):111–7.

    PubMed  Google Scholar 

  • Tan SF, Tong HJ, Lin XY, et al. The cariogenicity of commercial infant formulas: a systematic review. Eur Arch Paediatr Dent. 2016;17:145–56.

    PubMed  Google Scholar 

  • Tanaka K, Miyake Y. Association between breastfeeding and dental caries in Japanese children. J Epidemiol. 2012;22(1):72–7.

    PubMed  PubMed Central  Google Scholar 

  • Tanzer JM, Livingston J, Thompson AM. The microbiology of primary dental caries in humans. J Dent Educ. 2001;65:1028–37.

    PubMed  Google Scholar 

  • Teughels W, Van Essche M, Sliepen I, et al. Probiotics and oral healthcare. Periodontol. 2008;2000(48):111–47.

    Google Scholar 

  • Torlakovic L, Klepac-Ceraj V, Ogaard B, et al. Microbial community succession on developing lesions on human enamel. J Oral Microbiol. 2012;4:1.

    Google Scholar 

  • Valdez RM, Dos Santos VR, Caiaffa KS, et al. Comparative in vitro investigation of the cariogenic potential of Bifidobacteria. Arch Oral Biol. 2016;71:97–103.

    PubMed  Google Scholar 

  • Weber D, Janson A, Nolan M, et al. Female employees’ perceptions of organisational support for breastfeeding at work: findings from an Australian health service workplace. Int Breastfeed J. 2011;6:19.

    PubMed  PubMed Central  Google Scholar 

  • Weber-Gasparoni K, Kanellis MJ, Levy SM, et al. Caries prior to age 3 and breastfeeding: a survey of La Leche League members. J Dent Child. 2007;74:52–61.

    Google Scholar 

  • WHO and FAO. Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. Report of a joint FAO/WHO expert consultation on evaluation of health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria (2001).

  • World Health Organization (WHO). Oral Health Fact sheet N°318 April. http://www.who.int/mediacentre/factsheets/fs318/en/ (2012).

  • World Health Organization (WHO) and UNICEF. Global strategy for infant and young child feeding. http://apps.who.int/iris/bitstream/10665/42590/1/9241562218.pdf (2003).

Download references

Author information

Authors and Affiliations

  1. Faculty of Oral and Dental Medicine, Future University in Egypt, 4 Omar Ebn El Khattab Street, Ismailia Square, Heliopolis, Cairo, Egypt

    A. A. M. Aly

  2. Faculty of Medicine, Ain Shams University, Cairo, Egypt

    D. Erfan

  3. Faculty of Dentistry, Ain Shams University, Cairo, Egypt

    R. K. Abou El Fadl

Authors
  1. A. A. M. Aly
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. D. Erfan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. R. K. Abou El Fadl
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. A. M. Aly.

Ethics declarations

Conflict of interest

None of the authors had a financial or personal conflict of interest in relation to this study.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Aly, A.A.M., Erfan, D. & Abou El Fadl, R.K. Comparative evaluation of the effects of human breast milk and plain and probiotic-containing infant formulas on enamel mineral content in primary teeth: an in vitro study. Eur Arch Paediatr Dent 21, 75–84 (2020). https://doi.org/10.1007/s40368-019-00448-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40368-019-00448-2

Keywords

Search

Navigation