Developmental enamel defects in children born preterm: a systematic review

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1 Eur J Oral Sci 2014; 122: 7 14 DOI: /eos Printed in Singapore. All rights reserved Ó 2013 Eur J Oral Sci European Journal of Oral Sciences Review Developmental enamel defects in children born preterm: a systematic review Jacobsen PE, Haubek D, Henriksen TB, Østergaard JR, Poulsen S. Developmental enamel defects in children born preterm: a systematic review. Eur J Oral Sci 2014; 122: Eur J Oral Sci The purpose of this review was to evaluate the association between developmental enamel defects and children born preterm. An identical search was performed in PubMed and Embase and was limited to human studies and studies written in English, German, Danish, Swedish, or Norwegian. Reviews, case studies, and case series were excluded. A total of 283 articles were identified. Twenty-three publications, of which 19 were follow-up studies, two were case control studies, and two were crosssectional surveys, were enrolled in the review. The majority of the studies (n = 17) dealt with enamel hypoplasia of the primary teeth. Thirteen studies reported an association between preterm birth and enamel hypoplasia, and, in addition, few studies reported an increased risk of enamel opacities in the primary teeth, in children with a birth weight <1500 g. Seven studies dealt with enamel disturbances of the permanent teeth, four of which suggested an increased risk of enamel opacities. This systematic review suggests an increased risk of enamel hypoplasia in primary teeth of children born preterm and enamel opacities in very-low birth-weight children. A larger number of well-designed studies are, however, needed in order to increase the validity of the studies. Pernille E. Jacobsen 1, Dorte Haubek 1, Tine B. Henriksen 2, John R. Østergaard 3, Sven Poulsen 1 1 Section of Pediatric Dentistry, Department of Dentistry, Health, Aarhus University, Aarhus; 2 Perinatal Epidemiology Research Unit, Department of Pediatrics, Aarhus Universty Hospital, Aarhus; 3 Center for Rare Diseases, Department of Pediatrics, Aarhus University Hospital, Aarhus, Denmark Pernille E. Jacobsen, DDS, Section of Pediatric Dentistry, Department of Dentistry, Health, Aarhus University, Vennelyst Boulevard 9, DK-8000 Aarhus C, Denmark pej@odontologi.au.dk Key words: dental enamel hypoplasia; low birth weight; preterm birth; tooth abnormalities; tooth hypomineralization Accepted for publication September 2013 A child is defined as preterm if born before 37 wk of gestation (1). Over the past yr, advances in perinatal care have reduced mortality and morbidity in preterm children (2). The life of a preterm child, however, may not be without complications; the lower the gestational age at birth, the higher the risk of immediate and late complications (3). Some of the more serious complications, seen almost entirely among newborns delivered before 32 wk of gestation, are respiratory distress syndrome, bronchopulmonary dysplasia, intraventricular bleeding, necrotizing enterocolitis, retinopathy of prematurity, and persistent ductus arteriosus, along with risks of infection (4). These conditions may be associated with poor feeding and lack of optimal nutrition, including vitamin and mineral deficiency for shorter or longer periods of time (5). Some of these conditions may result in physical or mental deficiencies later in life (6, 7). Oral abnormalities and defects in children born preterm have frequently been reported in the literature. Previous studies have shown that palatal defects, such as asymmetric and high-vaulted palate and damage to the underlying tooth germ, resulting in hypoplasia of the primary incisors, are frequent outcomes caused by oral intubation and long-term mechanical ventilation (8, 9). However, oral intubation of preterm children in need of mechanical ventilation is now commonly replaced by nasal intubation, which has reduced the likelihood of hypoplasia (10). Prematurity may also result in late tooth eruption and altered tooth-crown dimensions, factors that must be taken into consideration when planning orthodontic treatment (9). Additionally, studies have demonstrated that preterm children may have a higher risk of developing hypomineralized teeth (11, 12). This seems to be most common in the primary dentition, but the permanent teeth may also be affected (12, 13). However, the results are conflicting (11, 14 16). This is consistent with our current knowledge of tooth development, in which the enamel of the primary teeth begins to develop at week 12 postconception and continues throughout the entire pregnancy. Development of the enamel of the first permanent teeth starts at week 28 postconception, whereas mineralization starts at the time of birth and is completed during the first 3 yr of life (17). This indicates different exposure windows for the risk of developmental defects in the two dentitions in relation to prematurity. Dental hypoplasia is a quantitative defect caused by incomplete deposition of immature enamel produced by ameloblasts during the secretory stage. Dental opacities or hypomineralization defects occur as a result of incomplete mineralization or maturation of the enamel,

2 8 Jacobsen et al. following the stage of the secretion. The diagnostic criteria for prematurity are therefore essential for understanding the mechanisms behind the defects seen in the child, and if they are associated with being born premature. The purpose of the present systematic review was to summarize the present knowledge on the association between being born preterm and the risk of developmental enamel defects. Specifically, we aimed to answer the following two questions: Is there an association between being born preterm and enamel opacities? Is there an association between being born preterm and enamel hypoplasia? Material and methods The method followed in the present review is in accordance with the Preferred Reporting Items for Systematic reviews and Meta-analyses (PRISMA) statement (18). The eligibility criteria were follow-up, case control, or crosssectional studies involving children of all ages, which focused on the association between preterm birth and developmental enamel defects. Studies were only included if they had a control group of children born 37 wk of gestation (non-exposed) or an exposed group with at least two levels of exposure (dose response) (i.e. two categories of children born at a gestational age before 37 wk). No further restrictions related to the control group were imposed. Furthermore, the exposure should be defined as either delivered before 37 wk of gestation or delivered with a low birth weight (<2500 g), indicating preterm birth for most children born within this group. Outcomes in both the primary and the permanent dentition were included. The search was limited to human studies and included only articles published in English, German, Danish, Swedish, or Norwegian. The search covered a period from January 1966 to February Search strategy A search in PubMed.gov and embase.com was performed, using identical search strings covering all tooth-related terms, such as dentition (MeSH), tooth (MeSH), dental enamel (MeSH), enamel hypoplasia (MeSH), and hypomineralization, and AND combined with terms such as premature, premature birth, and infant, low birth weight (MeSH). The search was conducted in collaboration with an experienced research librarian (see the Acknowledgements). A detailed search string is available at the European Journal of Oral Sciences website as Figure S1. Selection of studies and data extraction The selection of qualified studies was performed in three stages. The first stage was based on the title alone. The second stage was based on the abstract using the criteria listed in Fig. 1, and the third stage of selection was based on the full-text article. All stages of selection were conducted by three independent reviewers (P.E.J., D.H., and S.P.). Disagreements were discussed in plenum until consensus was reached. Hand-search was carried out of the reference lists of the studies entering the review, in order to identify studies not found in the original search. The data extracted from the articles entering the review were pilot-tested by two of the reviewers (P.E.J. and S.P.) on three randomly chosen papers. Following this, the data-extraction form was revised to facilitate accuracy and clarity in the collection of data. The remaining articles were then evaluated independently by the same two reviewers. Quality assessment Quality assessment was performed using the validated Newcastle Ottawa Quality Assessment Scale (NOS) (19). This scale uses separate assessment tools for cohort and case control studies. The quality of cross-sectional studies was assessed using the NOS for cohort studies. In the NOS, the studies were assigned stars in three categories with a maximum score of nine stars. A study would be categorized as high quality if the total score was seven or higher. In the present review, we were only able to assign a maximum of eight stars in rating the cohort and crosssectional studies, because none of the studies would be able to secure absence of outcome before the exposure (birth). Therefore, these studies only needed six stars to be categorized as high quality. In some of the categories the reviewers had to predefine some methodologically suitable cut-off points for evaluation. The chosen cut-off points were discussed and agreed in the whole author group and was as follows: a suitable follow-up period (item 2 under Outcome ) was set at 3 yr of age because the primary dentition is expected to be fully erupted in children at this age. The primary confounder was decided to be the overall health of the mother and the studies received one star if they had controlled for this factor and an additional star if they had controlled for other possible confounders, such as smoking or gender, in the design or the analysis (items 1a and 1b under Comparability ). Finally, the participation rate was required to be larger than 50%. Results Quality assessment Using the NOS for cohort studies, only two studies reached the maximum score of eight stars (20, 21) and another seven studies were classified as high quality (13, 15, 22 26) (Table 1). Using the scale for case control studies only, the study by LUNARDELLI et al. was categorized as a high-quality study (Table 2). The remaining 13 studies were categorized as low quality (11, 12, 14, 16, 27 35). Owing to the weaker evidence of the results in the low-quality studies, we only report the results from the high-quality studies in the present review. Details of all follow-up studies are available as supporting information online (Table S1). Basic results The studies were published during a period spanning almost 40 yr, the first being the study by GRAHNEN et al. in 1974 (22) and the latest a study published by RYTHEN et al. in 2012 (36). The studies were conducted in all parts of the world. Four were performed in

3 Developmental enamel defects 9 Literature search February 1st 2013 Pubmed 243 Embase 172 Duplicate 132 Reviewed based on title 283 Excluded 163 Reviewed based on abstract 120 Excluded 88 Reason for exclusion: 18: abstract, review, etc. 8: other oral problems Reviewed based on article 32 36: craniofacial syndromes 26: not relevant Located by hand search 1 Excluded 10 Reason for exclusion: 5: exposure not premature birth Included 23 1: outcome not enamel defects 3: no control group 1: data already presented Fig. 1. Search procedure and exclusion criteria for the present review. Europe (15, 20, 22, 36), one in the USA (21), two in Australia (23, 26), and three in Brazil (24, 25, 37). The most common study design was the follow-up design, in which children were recruited at the time of the dental examination and information concerning the exposure was collected retrospectively (15, 20, 21, 21 25, 36). One study was a case control study (37) and another was a cross-sectional study (26). The age of the children enrolled in the studies varied from 2 to 16 yr. The definition of preterm delivery differed between the studies. Four studies used birth weight as the measure of exposure (20, 21, 23, 37) and five studies used gestational age (15, 22, 25, 36, 37). A single study used a combination of birth weight and gestational age (24), and one study did not provide the level of the exposure (26). All studies, except one, used medical records as the source of information concerning the gestational age and birth weight. Arrow (26) relied on parental recall. All studies used controls recruited from the same area and born during the same time period as the exposed children. were examined in six of the studies (20, 22 25, 37). Three studies examined the permanent teeth (15, 21, 26) and one study examined both the primary and the permanent teeth (36). The studies were published over a long period of time and the diagnostic criterion for the outcome varied considerably between the studies. The oldest study used no specific index to describe developmental defects of enamel (22). In 1981, the developmental defect of the enamel (DDE) index was introduced (38) and this index was used in three studies (21, 24, 26). The DDE index was modified in 1992 (39) and the modified version was used in five of the studies (20, 23, 25, 36, 37). Lately, the criteria introduced by WEERHEIJM et al. (40), with the specific purpose of diagnosing and classifying molar incisor hypomineralization (MIH), were used in one study (15). All studies used both enamel opacities and hypoplasia as their outcomes. Of these, only one reported a combined estimate for enamel opacities and hypoplasia (24). The results were, in almost all studies, reported as prevalence rates with a P-value in case of significant differences. In the following section a description of the followup studies is provided. These results are summarized in Table 3.

4 10 Jacobsen et al. Table 1 Methodological quality for all 23 cohort studies identified by the search strategy, assessed using the Newcastle-Ottowa-Scale References Year Country Study design Criteria Selection Comparability Outcome/Exposure Total score Maximum GRAHNEN et al. (22) 1974 Sweden Follow-up * * * * * * 6 MELLANDER et al. (27) 1982 Sweden Follow-up * * * * * 5 JOHNSEN et al. (28) 1984 USA Follow-up * * * * 4 SEOW et al. (8) 1984 Australia Follow-up * * * * * 5 FEARNE et al. (30) 1990 England Follow-up * * * * * 5 KOPRA &DAVIS (31) 1991 USA Follow-up * * * * * 5 DRUMMOND et al. (32) 1992 England Follow-up * * * * 4 SEOW (10) 1997 Australia Follow-up * * * * * 5 LAI et al. (23) 1997 Australia Follow-up * * * * * * * 7 AINE et al. (11) 2000 Finland Follow-up * * * * 4 FRANCO et al. (14) 2007 Brazil Follow-up * * * * 4 FERRINI et al. (12) 2008 Brazil Follow-up * * * * 4 VELLO et al. (20) 2010 Spain Follow-up * * * * * * * * 8 TAKAOKA et al. (24) 2010 Brazil Follow-up * * * * * * 6 CRUVINEL et al. (25) 2010 Brazil Follow-up * * * * * * 6 NELSON et al. (21) 2010 USA Follow-up * * * * * * * * 8 BROGARDH-ROTH et al. (15) 2011 Sweden Follow-up * * * * * * * 7 BANSAL (33) 2012 India Follow-up * 1 RYTHEN et al. (36) 2012 Sweden Follow-up * * * * * * 6 LI et al. (34) 1995 China Cross-sectional * * * * * 5 ARROW (26) 2009 Australia Cross-sectional * * * * * * * 7 Criteria. 1) Representativeness of the exposed cohort. 2) Selection of the non-exposed cohort. 3) Ascertainment of exposure. 4) Comparability on the basis of confounding control in the design or analysis. 5) Additional confounding control. 6) Assessment of outcome. 7) Duration of follow-up period. 8) Adequacy of follow-up. The stars represent the methodological quality of the studies which are important for the validity of the results. Furthermore, it can be seen as a guideline for future studies to increase the quality of the research on the topic. Table 2 Methodological quality for case control studies, assessed using the Newcastle-Ottowa-Scale References Year Country Study design Criteria Selection Comparability Exposure Total score Maximum: 9 LUNARDELLI et al. (37) 2006 Brazil Case control * * * * * * * * 8 LYGIDAKIS et al. (35) 2008 Greece Case control * * * * * 5 Criteria. 1) Adequate case definition. 2) Representativeness of the cases. 3) Selection of controls. 4) Definition of controls. 5) Comparability on the basis of confounding control in the design or analysis. 6) Additional confounding control. 7) Assessment of exposure. 8) Same methods for cases and controls. 9) Non-response rate. The stars represent the methodological quality of the studies which are important for the validity of the results. Furthermore, it can be seen as a guideline for future studies to increase the quality of the research on the topic. Hypoplasia was the most frequently reported outcome, and three (20, 23, 25) out of the four studies found an association between prematurity and enamel hypoplasia. With the two outcomes, opacities and hypoplasia, pooled in an overall category entitled developmental enamel defects, two studies found a significant difference between the exposed and non-exposed subjects (22, 24). Two out of four studies reporting on opacities in the primary dentition found a significant difference between the exposed subjects and the controls (23, 36). Permanent teeth Two studies listed in Table 3 found no association with prematurity for either opacities or hypoplasia in the permanent teeth (15, 36). Besides the studies listed in Table 3, we identified a follow-up study, performed by NELSON et al. (21), on very-low birth-weight children and enamel defects. However, the results were not presented in a way that allowed comparison with the follow-up studies summarized in Table 3, but the authors conclude that there was a significant increase of demarcated opacities in the

5 Developmental enamel defects 11 Table 3 Summary of the high-quality follow-up studies on the association between prematurity, low birth weight, and developmental enamel defect Reference Year Material, number of subjects and age Definition of exposure Methods Diagnostic criteria Teeth examined Outcome(s) recorded Findings (prevalence) P-value GRAHNEN et al. (22) children, 2 3 yr GA < 38 wk BW normal for GA Own criteria : 21%; Controls: 10% Not given 39 children, 2 3 yr : Healthy full-term children GA > 38 wk 22%; Controls: 5% Not given Enamel defects* : 43%; Controls: 15% P < 0.01 LAI et al. (23) children 4 5 yr VLBW < 1500 g Modified DDE-index Opacities, hypoplasia and combined defect : 79%; Controls: 30% P < children, 4 5 yr Full-term children with normal BW : 67%; Controls: 10% P < VELL O et al. (20) children, 4 5 yr LBW < 2500 g Modified DDE-index Primary dentition : 77%; Controls: 80% NS 50 children, 4 5 yr BW 2500 g : 60%; Controls: 16% P < 0.05 TAKAOKA et al.(24) children, 2 3 yr 46 children, 2 4 yr BW < 2000 g GA < 37 wk : BW > 2000 g GA > 37 > 42 wk DDE-index Primary dentition Primary incisors Enamel defects: : 87%; Controls: 44% P < CRUVINEL et al. (25) children, 5 10 yr GA < 37 wk Modified DDE-index Mixed dentition : 65%; Controls: 63% P = children, 5 10 yr GA > 37 wk : 38%; Controls: 8% P = BROG ARDH- ROTH et al. (15) VPT children, 9 12 yr 20 EPT children, 9 12 yr 82 children 9 12 yr VPT: 29 < GA < 32 wk EPT: 24 < GA < 28 wk GA > 37 Weerheijm criteria MIH Modified DDE-index for all permanent teeth Demarcated opacities, diffuse opacities and hypoplasia Permanent teeth (MIH) : 38%; Controls: 16% DDE (including MIH) : 55%; Controls: 44% 2%: Controls: 1% P < P = 0.2 P = 1.0 RYTHEN et al. (36) VPT children,12 16 yr + dental records at age 9 40 children,12 16 yr + dental records at age 9 GA < 29 wk GA > 37 wk Modified DDE-index Primary dentition Opacities Permanent dentition Opacities at age 9: : 16%; Controls: 0% Permanent teeth : 40%; Controls: 30% P < NS : 5%; Controls: 10% NS *A combined count of opacities and hypoplasia. BW, birth weight; DDE-index, Developmental Defects Enamel-index; EPT, extremely preterm; GA, gestational age; LBW, low birth weight; MIH, molar incisor hypomineralization; NS, not significant at the significance level chosen; VLBW, very low birth weight; VPT, very preterm.

6 12 Jacobsen et al. permanent incisors and first permanent molars in verylow birth-weight children. Finally, a case control study (37) and a crosssectional study (26) qualified for entering the review according to the criteria described above. LUNARDELLI et al. (37) reported around twice the risk (OR = 2.6; 95% CI = ) of enamel defects in the primary teeth in low birth-weight children. In a study on the permanent teeth, Arrow (26) reported similar results (OR = 2.11; 95% CI = ) on the risk of enamel defects in the permanent first molars. Discussion The systematic evaluation of the publications included in the present review indicates an association between preterm birth and developmental enamel defects in the primary dentition, whereas the evidence for an association with developmental defects in the permanent dentition is weaker. Considerable methodological differences were found between the studies with respect to, e.g. design, choice of outcome, study size, diagnostic criteria and analytic approach. Furthermore, the consideration of potential confounders in the studies varied extensively. This made it difficult to compare the results of one study with those of another. Analyses varied from simple analysis of tables to multivariate analyses with over 30 explanatory variables. Because of this heterogeneity between studies, common to observational studies, a meta-analysis is not recommended (41). Instead, we validated the studies based on criteria for selection, comparability, and outcome measurements according to the NOS (Tables 1, 2). The fact that only 10 of 23 studies were categorized as high quality confirms the need for further well-designed studies. The most common design was the follow-up design, with collection of information from medical or hospital records, which makes it possible to secure adequate power and, to some extent, to control for confounders and reduce potential bias from differential recall. Some studies have relied on parental recall of gestational age and are therefore less reliable and have potentially biased exposure information, which may decrease the validity of these studies. There is a risk of selection bias if only children who enter a specific postnatal follow-up program are examined. It is therefore very important to describe the criteria for entry into the follow-up program and reasons for non-participation in order to be able to interpret the results. Only three out of the original 23 studies in the present review provided such a description (21, 22, 26). Furthermore, only four studies (21, 26, 34, 37) were blinded. In unblinded assessment of dental diseases, information bias may hamper the validity. The majority of the studies, categorized as high quality, have been conducted within the latest 5 yr ( ). This indicates increased awareness of the importance of studies with high validity in both the researcher groups as well as among publishers. Still, when comparing the results from high-quality studies, the results are inconclusive in relation to enamel defects in the permanent teeth, whereas they all found a significant increase of hypoplasia or enamel defects in the primary teeth. The treatment and care of premature children has improved considerably during the last yr, resulting in improved survival and health. The specialized neonatal care units are now capable of ensuring the survival of children with extremely-low birth weight. Accordingly, the extent of the medical treatment has evolved. Our knowledge of medical interaction with dental development is limited, but it could influence the risk of developmental defects, even in the permanent dentition, and therefore should be taken into consideration. Thus, preterm or low birth-weight children from earlier studies may not be comparable with those from more recent studies. Also, we found definitions of prematurity of children enrolled in the studies that varied from birth weight <1500 g to gestational age at birth of <38 wk, which decreases comparability. The phase during which the child is at risk of developing enamel hypoplasia is the phase of the matrix development (before mineralization). In order to understand the variation of the results between different studies, it is essential to consider the fact that most mineralization of the primary teeth takes place during the third trimester (17). Therefore, children born close to term with a normal birth weight may not have the same risk of development of enamel opacities as the very preterm children because mineralization of the primary teeth is almost complete. In addition, very small children born close to term may have an increased risk of both hypoplasia and opacities because low birth weight could be an indicator of poor prenatal growth. Accordingly, it may be critical to separate gestational age from fetal growth restriction in order to understand the mechanisms behind a potential association with developmental enamel defects. Many prenatal factors might influence the development of the primary and possibly the permanent teeth, such as maternal health, intake of medicine, smoking, coffee, and alcohol. The major difference between the high-quality studies and the low-quality studies is their effort and ability to control for such possible confounders. A few studies found a significant difference in the prevalence of opacities in the primary teeth. Common to these studies is that the inclusion criterion was birth weight <1500 g. This indicates that only children with a very-low birth weight are at risk of developing opacities, which is in accordance with the disturbances in the calcium metabolism seen in these children. On the contrary, almost all studies focusing on the primary teeth found a difference in prevalence in hypoplasia, regardless of the level of the exposure. This is more difficult to comprehend because the development of dental hypoplasia occurs before mineralization. Therefore, children born close to term should not be at risk of developing dental hypoplasia in the primary teeth unless growth restriction or other confounders are involved.

7 Developmental enamel defects 13 Not enough studies are available to allow reliable conclusions to be made about the association between prematurity and developmental enamel defects in permanent teeth. In conclusion, we found the following: an association between birth weight <1500 g and the risk of enamel opacities in the primary teeth; an association between being born preterm and the risk of developing enamel hypoplasia in the primary teeth; and currently no evidence that being born prematurely influences development of the permanent teeth. Further, well-designed studies are needed. In particular, efforts must be devoted to increase the validity of these studies. Furthermore, it is desirable if the study differentiates between gestational age and birth weight to accommodate growth restriction as a potential cause for the development of enamel defects. A longitudinal study design in which both the primary and, later, the permanent teeth are examined in the same children would be the most optimal design for answering the question concerning the risk of development of enamel defects in premature children. Acknowledgements We wish thank our research librarian, Janne Lytoft Simonsen, MSc, for her kind help with the literature search. We would also like to express our gratitude to the Calcin foundation from the Danish Dental Association, the DOFT foundation from the Association of Community Dental Service, and the Aarhus University research foundation for their financial support. Conflicts of interest The authors declare no conflicts of interest. References 1. WORLD HEALTH ORGANIZATION (WHO). International Statistical Classification of diseases and related health problems (rev. 10, vols. 1-2;ICD-10). Geneva: WHO, PEARSON G, SHANN F, BARRY P, VYAS J, THOMAS D, POWELL C, FIELD D. Should paediatric intensive care be centralised? 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