Candida species and selected behavioral factors co-associated with severe early childhood caries: Case-control study

. 2022 ; 12 () : 943480. [epub] 20220725

Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid35959372

Severe Early Childhood Caries (sECC) is a multifactorial disease associated with the occurrence of specific oral microorganisms and other environmental, behavioral, and genetic factors. This study aimed to construct a multivariable model including the occurrence of Candida spp. and selected behavioral factors (length of breastfeeding, serving sweet beverages and beginning of brushing child's teeth) to determine their relationships to the occurrence of sECC. In this case-control study 164 children with sECC and 147 children without dental caries were included. MALDI-TOF MS and multiplex qPCR were used to identify Candida spp. and selected bacteria in dental plaque samples, respectively. A questionnaire on oral hygiene, diet, and children's health was filled in by the parents. The constructed multivariable logistic regression model showed an independent influence of the microbial and behavioral factors in sECC etiopathogenesis. The occurrence of C. albicans and C. dubliniensis was associated with higher odds of sECC development (odds ratio, OR: 9.62 and 16.93, respectively), together with breastfeeding of 6 months or less (OR: 2.71), exposure to sweet beverages (OR: 3.77), and starting to brush child's teeth after the 12th month of age (OR: 4.10), all statistically significant (p < 0.01). Considering the high occurrence of C. albicans and C. dubliniensis in dental plaque in children with sECC, we propose them as "keystone pathogens" and risk factors for sECC. The models showed that presence of specific species of Candida in dental plaque may be a better descriptor of sECC than the mentioned behavioral factors.

Zobrazit více v PubMed

Agnello M., Marques J., Cen L., Mittermuller B., Huang A., Chaichanasakul Tran N., et al. . (2017). Microbiome associated with severe caries in Canadian first nations children. J. Dent. Res. 96, 1378–1385. doi: 10.1177/0022034517718819 PubMed DOI PMC

Al-Ahmad A., Auschill T. M., Dakhel R., Wittmer A., Pelz K., Heumann C., et al. . (2016). Prevalence of Candida albicans and Candida dubliniensis in caries-free and caries-active children in relation to the oral microbiota-a clinical study. Clin. Oral. Investig. 20, 1963–1971. doi: 10.1007/s00784-015-1696-9 PubMed DOI

American Academy of Pediatric Dentistry (2017) Policy on early childhood caries (ECC): classifications, consequences, and preventive strategies. Available at: https://www.aapd.org/research/oral-health-policies–recommendations/early-childhood-caries-classifications-consequences-and-preventive-strategies/ (Accessed May 7, 2022). PubMed

Ayadi R., Sitterlé E., d’Enfert C., Dannaoui E., Bougnoux M.-E. (2020). Candida albicans and Candida dubliniensis show different trailing effect patterns when exposed to echinocandins and azoles. Front. Microbiol. 11. doi: 10.3389/fmicb.2020.01286 PubMed DOI PMC

Bachtiar E. W., Bachtiar B. M. (2018). Relationship between Candida albicans and Streptococcus mutans in early childhood caries, evaluated by quantitative PCR. F1000Research 7, 1645. doi: 10.12688/f1000research.16275.2 PubMed DOI PMC

Baillie G. S., Douglas L. J. (1999). Role of dimorphism in the development of Candida albicans biofilms. J. Med. Microbiol. 48, 671–679. doi: 10.1099/00222615-48-7-671 PubMed DOI

Borilova Linhartova P., Deissova T., Musilova K., Zackova L., Kukletova M., Kukla L., et al. . (2018). Lack of association between ENAM gene polymorphism and dental caries in primary and permanent teeth in Czech children. Clin. Oral. Investig. 22, 1873–1877. doi: 10.1007/s00784-017-2280-2 PubMed DOI

Borilova Linhartova P., Kastovsky J., Bartosova M., Musilova K., Zackova L., Kukletova M., et al. . (2016). ACE Insertion/Deletion polymorphism associated with caries in permanent but not primary dentition in Czech children. Caries Res. 50, 89–96. doi: 10.1159/000443534 PubMed DOI

Bratthall D., Hänsel Petersson G. (2005). Cariogram–a multifactorial risk assessment model for a multifactorial disease. Community Dent. Oral. Epidemiol. 33, 256–264. doi: 10.1111/j.1600-0528.2005.00233.x PubMed DOI

Chevalier M., Ranque S., Prêcheur I. (2018). Oral fungal-bacterial biofilm models in vitro: a review. Med. Mycol. 56, 653–667. doi: 10.1093/mmy/myx111 PubMed DOI

Corrêa-Faria P., Martins-Júnior P. A., Vieira-Andrade R. G., Oliveira-Ferreira F., Marques L. S., Ramos-Jorge M. L. (2013). Developmental defects of enamel in primary teeth: prevalence and associated factors. Int. J. Paediatr. Dent. 23, 173–179. doi: 10.1111/j.1365-263X.2012.01241.x PubMed DOI

Cruvinel V. R. N., Gravina D. B. L., Azevedo T. D. P. L., de Rezende C. S., Bezerra A. C. B., de Toledo O. A., et al. . (2012). Prevalence of enamel defects and associated risk factors in both dentitions in preterm and full term born children. J. Appl. Oral. Sci. Rev. FOB 20, 310–317. doi: 10.1590/s1678-77572012000300003 PubMed DOI PMC

Dean A. G., Arner T. G., Sunki G. G., Friedman R., Lantinga M., Sangam S., et al. . (2020) Epi InfoTM, a database and statistics program for public health professionals (Atlanta, GA, USA: CDC; ). Available at: https://www.cdc.gov/epiinfo/index.html (Accessed July 30, 2021).

Deeks J. J., Higgins J. P. (2010) Statistical algorithms in review manager 5. Available at: https://training.cochrane.org/handbook/current/chapter-10-statistical-algorithms-revman-5-1 (Accessed August 17, 2021).

de Jesus V. C., Shikder R., Oryniak D., Mann K., Alamri A., Mittermuller B., et al. . (2020). Sex-based diverse plaque microbiota in children with severe caries. J. Dent. Res. 99, 703–712. doi: 10.1177/0022034520908595 PubMed DOI

Diaz P. I., Dongari-Bagtzoglou A. (2021). Critically appraising the significance of the oral mycobiome. J. Dent. Res. 100, 133–140. doi: 10.1177/0022034520956975 PubMed DOI PMC

Diaz P. I., Strausbaugh L. D., Dongari-Bagtzoglou A. (2014). Fungal-bacterial interactions and their relevance to oral health: linking the clinic and the bench. Front. Cell. Infect. Microbiol. 4. doi: 10.3389/fcimb.2014.00101 PubMed DOI PMC

Eidt G., Waltermann E. D. M., Hilgert J. B., Arthur R. A. (2020). Candida and dental caries in children, adolescents and adults: A systematic review and meta-analysis. Arch. Oral. Biol. 119, 104876. doi: 10.1016/j.archoralbio.2020.104876 PubMed DOI

Ells R., Kock J. L. F., Pohl C. H. (2011). Candida albicans or Candida dubliniensis ? Mycoses 54, 1–16. doi: 10.1111/j.1439-0507.2009.01759.x PubMed DOI

Feldens C. A., Giugliani E. R. J., Vigo Á., Vítolo M. R. (2010). Early feeding practices and severe early childhood caries in four-year-old children from southern Brazil: a birth cohort study. Caries Res. 44, 445–452. doi: 10.1159/000319898 PubMed DOI

Garcia B. A., Acosta N. C., Tomar S. L., Roesch L. F. W., Lemos J. A., Mugayar L. R. F., et al. . (2021). Association of Candida albicans and Cbp(+)Streptococcus mutans with early childhood caries recurrence. Sci. Rep. 11, 10802. doi: 10.1038/s41598-021-90198-3 PubMed DOI PMC

Hajishengallis G., Darveau R. P., Curtis M. A. (2012). The keystone pathogen hypothesis. Nat. Rev. Microbiol. 10, 717–725. doi: 10.1038/nrmicro2873 PubMed DOI PMC

Hajishengallis E., Parsaei Y., Klein M. I., Koo H. (2017). Advances in the microbial etiology and pathogenesis of early childhood caries. Mol. Oral. Microbiol. 32, 24–34. doi: 10.1111/omi.12152 PubMed DOI PMC

Hof H., Eigner U., Maier T., Staib P. (2012). Differentiation of Candida dubliniensis from Candida albicans by means of MALDI-TOF mass spectrometry. Clin. Lab. 58, 927–931. PubMed

Hong L., Levy S. M., Warren J. J., Broffitt B. (2014). Infant breast-feeding and childhood caries: a nine-year study. Pediatr. Dent. 36, 342–347. PubMed PMC

Jabra-Rizk M. A., Shirtliff M., James C., Meiller T. (2006). Effect of farnesol on Candida dubliniensis biofilm formation and fluconazole resistance. FEMS Yeast Res. 6, 1063–1073. doi: 10.1111/j.1567-1364.2006.00121.x PubMed DOI

Janakiram C., Antony B., Joseph J. (2018). Association of undernutrition and early childhood dental caries. Indian Pediatr. 55, 683–685. doi: 10.1007/s13312-018-1359-4 PubMed DOI

Kassebaum N. J., Smith A. G. C., Bernabé E., Fleming T. D., Reynolds A. E., Vos T., et al. . (2017). Global, regional, and national prevalence, incidence, and disability-adjusted life years for oral conditions for 195 countries 1990–2015: A systematic analysis for the global burden of diseases, injuries, and risk factors. J. Dent. Res. 96, 380–387. doi: 10.1177/0022034517693566 PubMed DOI PMC

Kirkpatrick W. R., Lopez-Ribot J. L., McAtee R. K., Patterson T. F. (2000). Growth competition between Candida dubliniensis and Candida albicans under broth and biofilm growing conditions. J. Clin. Microbiol. 38, 902–904. doi: 10.1128/JCM.38.2.902-904.2000 PubMed DOI PMC

Kirthiga M., Murugan M., Saikia A., Kirubakaran R. (2019). Risk factors for early childhood caries: A systematic review and meta-analysis of case control and cohort studies. Pediatr. Dent. 41, 95–112. PubMed PMC

Kneist S., Borutta A., Sigusch B. W., Nietzsche S., Küpper H., Kostrzewa M., et al. . (2015). First-time isolation of Candida dubliniensis from plaque and carious dentine of primary teeth. Eur. Arch. Paediatr. Dent. Off. J. Eur. Acad. Paediatr. Dent. 16, 365–370. doi: 10.1007/s40368-015-0180-1 PubMed DOI

Kraljevic I., Filippi C., Filippi A. (2017). Risk indicators of early childhood caries (ECC) in children with high treatment needs. Swiss Dent. J. 127, 398–410. PubMed

Lalla R. V., Patton L. L., Dongari-Bagtzoglou A. (2013). Oral candidiasis: pathogenesis, clinical presentation, diagnosis and treatment strategies. J. Calif. Dent. Assoc. 41, 263–268. PubMed

Lemos J. A., Quivey R. G., Koo H., Abranches J. (2013). Streptococcus mutans: a new gram-positive paradigm? Microbiol. Read. Engl. 159, 436–445. doi: 10.1099/mic.0.066134-0 PubMed DOI PMC

Lochman J., Zapletalova M., Poskerova H., Izakovicova Holla L., Borilova Linhartova P. (2019). Rapid multiplex real-time PCR method for the detection and quantification of selected cariogenic and periodontal bacteria. Diagn. Basel Switz. 10, E8. doi: 10.3390/diagnostics10010008 PubMed DOI PMC

Metwalli K. H., Khan S. A., Krom B. P., Jabra-Rizk M. A. (2013). Streptococcus mutans, Candida albicans, and the human mouth: A sticky situation. PloS Pathog. 9, e1003616. doi: 10.1371/journal.ppat.1003616 PubMed DOI PMC

Mittlböck M., Schemper M. (1996). Explained variation for logistic regression. Stat. Med. 15, 1987–1997. doi: 10.1002/(SICI)1097-0258(19961015)15:19<1987::AID-SIM318>3.0.CO;2-9 PubMed DOI

Mohebbi S. Z., Virtanen J. I., Vahid-Golpayegani M., Vehkalahti M. M. (2008). Feeding habits as determinants of early childhood caries in a population where prolonged breastfeeding is the norm. Community Dent. Oral. Epidemiol. 36, 363–369. doi: 10.1111/j.1600-0528.2007.00408.x PubMed DOI

Montelongo-Jauregui D., Lopez-Ribot J. L. (2018). Candida interactions with the oral bacterial microbiota. J. Fungi Basel Switz. 4, E122. doi: 10.3390/jof4040122 PubMed DOI PMC

Moran G. P., Coleman D. C., Sullivan D. J. (2012). Candida albicans versus Candida dubliniensis: Why is C. albicans more pathogenic? Int. J. Microbiol. 2012, 205921. doi: 10.1155/2012/205921 PubMed DOI PMC

Nagelkerke N. J. D. (1991). A note on a general definition of the coefficient of determination. Biometrika 78, 691–692. doi: 10.1093/biomet/78.3.691 DOI

O’Connell L. M., Santos R., Springer G., Burne R. A., Nascimento M. M., Richards V. P. (2020). Site-specific profiling of the dental mycobiome reveals strong taxonomic shifts during progression of early-childhood caries. Appl. Environ. Microbiol. 86, e02825–e02819. doi: 10.1128/AEM.02825-19 PubMed DOI PMC

O’Donnell L. E., Millhouse E., Sherry L., Kean R., Malcolm J., Nile C. J., et al. . (2015). Polymicrobial Candida biofilms: friends and foe in the oral cavity. FEMS Yeast Res. 15, fov077. doi: 10.1093/femsyr/fov077 PubMed DOI

Pagano M., Gauvreau K. (2000) Principles of biostatistics (Belmont: Brooks/Cole; ). Available at: https://www.routledge.com/Principles-of-Biostatistics/Pagano-Gauvreau/p/book/9781138593145 (Accessed August 17, 2021).

Samaranayake L. P., Keung Leung W., Jin L. (2009). Oral mucosal fungal infections. Periodontol 2000 49, 39–59. doi: 10.1111/j.1600-0757.2008.00291.x PubMed DOI

Schoofs A., Odds F. C., Colebunders R., Ieven M., Goossens H. (1997). Use of specialised isolation media for recognition and identification of Candida dubliniensis isolates from HIV-infected patients. Eur. J. Clin. Microbiol. Infect. Dis. Off. Publ. Eur. Soc Clin. Microbiol. 16, 296–300. doi: 10.1007/BF01695634 PubMed DOI

Schüler I. M., Haberstroh S., Dawczynski K., Lehmann T., Heinrich-Weltzien R. (2018). Dental caries and developmental defects of enamel in the primary dentition of preterm infants: Case-control observational study. Caries Res. 52, 22–31. doi: 10.1159/000480124 PubMed DOI

Setia M. S. (2016). Methodology series module 2: Case-control studies. Indian J. Dermatol. 61, 146–151. doi: 10.4103/0019-5154.177773 PubMed DOI PMC

Stokes C., Moran G. P., Spiering M. J., Cole G. T., Coleman D. C., Sullivan D. J. (2007). Lower filamentation rates of Candida dubliniensis contribute to its lower virulence in comparison with Candida albicans . Fungal Genet. Biol. FG B 44, 920–931. doi: 10.1016/j.fgb.2006.11.014 PubMed DOI

Sullivan D., Haynes K., Bille J., Boerlin P., Rodero L., Lloyd S., et al. . (1997). Widespread geographic distribution of oral Candida dubliniensis strains in human immunodeficiency virus-infected individuals. J. Clin. Microbiol. 35, 960–964. doi: 10.1128/jcm.35.4.960-964.1997 PubMed DOI PMC

Sullivan D. J., Westerneng T. J., Haynes K. A., Bennett D. E., Coleman D. C. (1995). Candida dubliniensis sp. nov.: phenotypic and molecular characterization of a novel species associated with oral candidosis in HIV-infected individuals. Microbiol. Read. Engl. 141 (Pt 7), 1507–1521. doi: 10.1099/13500872-141-7-1507 PubMed DOI

The ADA Division of Communications. The Journal of the American Dental Association and the ADA Council on Scientific Affairs (2005). Tooth eruption: The primary teeth. J. Am. Dent. Assoc. 136, 1619. doi: 10.14219/jada.archive.2005.0095 PubMed DOI

The WHO (2021) Child growth standards. Available at: https://www.who.int/tools/child-growth-standards (Accessed July 30, 2021).

Toumba K. J., Twetman S., Splieth C., Parnell C., van Loveren C., Lygidakis N.A. (2019). Guidelines on the use of fluoride for caries prevention in children: an updated EAPD policy document. Eur. Arch. Paediatr. Dent. 20, 507–516. doi: 10.1007/s40368-019-00464-2 PubMed DOI

van Meijeren-van Lunteren A. W., Voortman T., Elfrink M. E. C., Wolvius E. B., Kragt L. (2021). Breastfeeding and childhood dental caries: Results from a socially diverse birth cohort study. Caries Res. 55, 153–161. doi: 10.1159/000514502 PubMed DOI PMC

Xiao J., Grier A., Faustoferri R. C., Alzoubi S., Gill A. L., Feng C., et al. . (2018. a). Association between oral candida and bacteriome in children with severe ECC. J. Dent. Res. 97, 1468–1476. doi: 10.1177/0022034518790941 PubMed DOI PMC

Xiao J., Huang X., Alkhers N., Alzamil H., Alzoubi S., Wu T. T., et al. . (2018. b). Candida albicans and early childhood caries: A systematic review and meta-analysis. Caries Res. 52, 102–112. doi: 10.1159/000481833 PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...