Prevalence, characteristic features, and complications associated with the occurrence of unerupted permanent incisors

This study examined the prevalence, characteristic features, and complications associated with the occurrence of unerupted permanent incisors among children and adolescents attending a university dental teaching hospital. A retrospective review was performed of the clinical records of children and adolescents who attended the Prince Philip Dental Hospital, Hong Kong between 2005 and 2014. All patients who had at least one unerupted permanent incisor tooth were included. A total of 266 subjects with 320 unerupted permanent incisors were identified. The prevalence of unerupted permanent incisors among children and adolescents was 2.0%. Permanent maxillary central incisors (70.6%) were the most commonly affected teeth. The most common cause for unerupted incisors were dilacerations (n = 83, 36.7%) for maxillary central incisors; developmental dental anomalies (n = 22; 30.6%) together with unfavorable root development (n = 22; 30.6%) for maxillary laterals incisors; and abnormal tooth/tissue ratio (n = 11, 50.0%) for mandibular incisors. A majority of unerupted incisors presented with complications the most common being ectopic/displacement/rotation of the unerupted incisors (46.6%), loss of space (36.9%) and midline shift (27.5%). In conclusion, the causes were distinct for different manifestations of unerupted permanent incisors. As the majority of unerupted incisors presented with complications, a systematic and organized method of history taking as well as clinical and radiographic examinations is mandatory in the diagnosis of unerupted permanent incisors.


Introduction
Delayed eruption of maxillary permanent incisors necessitates intervention when [1] 1. there is eruption of contralateral teeth that occurred greater than six months previously; 2. the lower incisors have erupted greater than one year previously and where both maxillary central incisors remain unerupted; 3. or there is deviation from the normal order of eruption (e.g. lateral incisors erupting prior to the central incisors).
A previous study reported that the incidence of unerupted maxillary incisors in the 5 to 12 year-old age group as 0.13% [2] and more prevalent in Asian races [1]. The etiological factors a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 for delayed eruption of maxillary incisors can be classified into two main categories, namely hereditary and environmental factors. Hereditary factors include supernumerary teeth, cleft lip and palate, odontoma, abnormal tooth/tissue ratio, cleidocranial dysostosis, generalized delayed eruption and gingival fibromatosis. Similarly, trauma, early extraction or loss of primary teeth (with or without space loss), retained primary teeth, cystic formation, endocrine abnormalities, and bone disease are environmental factors that may influence eruption of incisors [1].
To date, published studies have focused on case reports of diagnosis and management of unerupted maxillary teeth [3], retrospective evaluation on eruption [4]; treatment protocol [5]; prevalence of various etiological factors and treatment outcome associated with unerupted incisors [6]; as well as association between unerupted incisors and dental anomalies [7]. However, there is no single study on prevalence, characteristic features and complications associated with unerupted permanent incisors among children and adolescents attending the Prince Philip Dental Hospital (PPDH), which is the only university dental teaching hospital in Hong Kong Special Administrative Region, China. The patient pool in Pediatric Dentistry and Orthodontics (PDO) clinic of PPDH are predominantly those without a referral, followed by referred patients from the School Dental Care Services (a dental health program for almost all primary school children); private general dental practitioners and medical practitioners. Almost all children and adolescents with unerupted permanent incisors are accepted for comprehensive multidisciplinary treatment in the PDO clinic. Therefore, the aim of this retrospective study was to determine the prevalence, characteristic features and complications associated with the occurrence of unerupted permanent incisors among children and adolescents attending a university dental teaching hospital.

Materials and methods
This retrospective study reviewed hospital records of children and adolescents who had unerupted permanent incisors and were treated in the PDO clinic at the PPDH, The University of Hong Kong, Hong Kong SAR, between January 2005 and December 2014. The study protocol was approved by the Institutional Review Board of the University of Hong Kong/Hospital Authority Hong Kong West Cluster (UW 15-538). The records were reviewed from 15,987 children and adolescents who had attended the PDO Clinic of the PPDH. All patients who had at least one unerupted permanent incisor that matched the definition of unerupted permanent incisors which was adapted from the clinical guidelines of Royal College of Surgeons of England [1] were included. Those subjects were defined as having unerupted permanent incisors when any of the following occurred: • eruption of contralateral incisors that occurred greater than six months previously; • both maxillary central incisors remain unerupted and the lower incisors have erupted greater than one year previously; • there is deviation from the normal sequence of eruption (e.g. lateral incisors erupting prior to the central incisors).
Clinical records of those patients were excluded from this study if they presented with • medical complications (metabolic and endocrine disorders, syndromes, orofacial cleft / craniofacial malformations etc.) • congenital missing permanent incisors.
After obtaining a list of included patients, clinical notes and radiographs were retrieved to obtain the necessary information. A customized data entry form was used to record all relevant information of each patient. Two qualified dentists who worked in the PDO clinic of the PPDH were involved in the data collection stage. The assessment process of clinical reports and radiographs was blinded. The inter-and intra-examiner reliability were assessed by using the Cohen's Kappa statistics.
For each patient included in the study, the relevant information that was recorded included: 1. General descriptive data about the patients that includes gender, date of birth, date of diagnosis 2. Relevant clinical information such as, • The type of radiographs used for assessment and diagnosis of unerupted incisors All the data were entered and processed using the Statistical Package for Social Sciences Version 20.0 for Windows1 (SPSS Inc., Chicago, Illinois, USA). Numerical data were summarized. Any significant differences and possible associations among variables were compared using Chi-square test. Fisher's exact test was used when 20% or more of the cells in the table with expected frequencies less than 5. The binomial test was used to determine any difference in between proportion of presence and absence of complications associated with the occurrence of unerupted permanent incisors. The p-value was set at 0.05.

General descriptive data
A total of 266 subjects with 320 unerupted permanent incisors were identified from the 15,987 subjects in the study, which represented a prevalence of 2.0%. Out of 266 subjects, male subjects (n = 139; 52.3%) were slightly higher than female (n = 127; 47.7%). The age of diagnosis ranged from 7.3 years to 13.8 years with a mean age of 10.6 years (S1 Table).

Type of radiographs used
There were good intra-examiner and inter-examiner reliability with Kappa values ranging from 0.85 to 0.87 and 0.80 to 0.83, respectively. Panoramic (OPG), upper anterior occlusal view (UAO) and periapical (PA) view radiographs were the most common combinations of radiographs used for assessment and diagnosis of unerupted incisors (n = 115, 35.9%). Only 46 cases (14.4%) incorporated Cone Beam Computed Tomography (CBCT) in diagnosis and treatment planning of unerupted incisors.

History of dental/ maxillofacial trauma
Among all the 14 causes of unerupted permanent incisors, dilacerations (p<0.001), ectopic position of tooth bud (p = 0.012) and ankylosed/impacted primary teeth (p = 0.039) had significant association with positive history of trauma.  Prevalence, characteristic features, and complications associated with the unerupted permanent incisors

Discussion
The demographic data in our study showed that male subjects (n = 139; 52.3%) were slightly higher than female (n = 127; 47.7%) with a mean age of 10.6 years. This is in accordance with other retrospective studies, which also reported higher prevalence of unerupted maxillary central incisors in males with a mean age of 10.6 and 9.4 years [5,8]. The contributing factors for unerupted incisors among male patients could be explained by a greater prevalence of supernumerary teeth in males [9,10] and also possible involvement of sexual chromosomes in the etiology of tooth eruption disturbances [8].
In the present study, the most common combination of radiographs that were used in assessment and management of unerupted permanent incisors were panoramic radiograph, UAO view and PA view radiographs. This is like another retrospective study [10], in which a combination of more than one film was used in 95% of cases to enable localization of the unerupted teeth using the parallax method. A study by Jacobs [11] suggested that a panoramic radiograph with an anterior occlusal radiograph is the preferred combination of radiographs to localize unerupted mandibular anterior teeth. Radiographs may be justified when there are abnormal incisor relationships, localization of tooth position is necessary to formulate a treatment plan, and where a reasonable expectation that pathology exists on clinical grounds [12]. Cone Beam Computed Tomography (CBCT) could be used to provide valuable information in qualitative analysis of dento-osseous structures, morphological alterations and exact tri -Fig 2. a. Upper anterior occlusal view of a 12-year-old girl who presented with a crown and root dilacerations of #8 as well as positive history of traumatic injury to the primary incisor when she was 4-year-old. b. Intra-operative photograph of the same subject which shows the orientation of the dilacerated crown. c. Postoperative photograph of the same subject with the extracted #8 and its associated tooth follicle. https://doi.org/10.1371/journal.pone.0199501.g002 Prevalence, characteristic features, and complications associated with the unerupted permanent incisors dimensional positioning of the unerupted teeth and adjacent structures [13]. As a general principle, the recommendations from clinical guidelines of the Royal College of Surgeons of England [1] and the American Academy of Pediatric Dentistry [14] should be adopted during radiographic assessment of unerupted permanent incisors.
Findings from the present study showed diversities in the hereditary and environmental causes for each specific type of unerupted permanent incisors (Table 2). Trauma in the primary dentition has the potential to cause eruption disturbances of permanent incisors, especially maxillary central incisors as shown by this study. Acute trauma to the primary dentition can cause dilaceration of the long axis of the permanent successor [15]. Any trauma during odontogenesis can affect the morphogenic stages of dental development and malformations, such as partial or complete arrest of root formation which occur during root formation [16]. Development of odontoma-like malformations in the permanent dentition caused by intrusion of a primary incisor has also been reported [16,17]. Therefore, the clinician should advise the parents regarding the possible complications following traumatic dental injuries of the primary dentition. Regular follow-up as recommended by the International Association of Dental Traumatology (IADT) guidelines [18] is also mandatory so that early detection and treatment of possible severe developmental disturbances can be carried out.
In addition, the results of this study also identified that the etiologies of unerupted incisors may also occur in isolation or in combination, specifically for maxillary permanent lateral incisors, which were most commonly affected by unfavorable root development (extremely delayed/arrested root development) and developmental dental anomalies (malformed/microdontic/underdeveloped) (Fig 4) [19,20]. Surgical removal should only be performed when proven complications, such as obstruction of eruption, displacement or root resorption of adjacent teeth, or pathological cystic changes have occurred .   Fig 3. a. Periapical radiograph of an 8-year-old boy who presented with an unerupted #8 due to the inverted mesiodens between #8 and #9. b. Frontal view of the same subject with erupting #7 and #8 after one month of surgical removal of the inverted mesiodens between #8 and #9. c. Occlusal view of the same subject showing talon's cusps and dens invaginatus on palatal surface of erupted #10 (black arrow) after six months of surgical removal of the inverted mesiodens between #8 and #9.
https://doi.org/10.1371/journal.pone.0199501.g003  Along with maxillary incisors, this study also addressed the occurrence and key characteristic features of 22 cases of unerupted mandibular incisors which were rarely reported in the literature likely due to its low prevalence. This study showed that causes for most unerupted mandibular incisors were due to crowding (abnormal tooth tissue ratio), followed by retained primary incisors and ectopic position of tooth buds. This condition was also often complicated with further space loss and midline shift as shown in Fig 5. Therefore, recognition of potential crowding during primary dentition and early mixed dentition by the clinician is the first important step in reducing the occurrence of unerupted mandibular incisors. Likewise, lack of space in the primary dentition during routine dental examination may raise the concern of future crowding in the permanent dentition [21]. Moreover, any over-retained primary tooth should be extracted to prevent obstruction to the eruption of the permanent successor [1].
Findings of the present study revealed that complications associated with the occurrence of unerupted permanent incisors can have an effect on the rest of the dentition (Fig 5), such as loss of space [22,23] and midline shift [24,25]. Other reported complications, which were also well documented in several published studies, include enlarged follicle or cystic changes of unerupted incisors [26,27] or association with supernumerary teeth [28,29], root resorption and early exfoliation of adjacent teeth. Complications may also be associated with ectopic/ displacement/ rotation of the impacted incisor itself [30,31] or the adjacent structures/ teeth [32]. For instance, a microdont maxillary lateral incisor displaying delayed development may inhibit eruption of maxillary central incisor(s) and maxillary canine(s) (Fig 6). In a case series, Kobayashi et al. [19] reported that developmental anomalies and immaturity involving adjacent permanent lateral incisors could be associated with eruption failure of maxillary permanent central incisors. However, the immature tooth germ does not change the eruptive direction of the tooth as much as do the presence of odontomas and supernumerary teeth, even if the developing tooth germ is positioned close to the unerupted tooth [19]. Nevertheless, early detection of unerupted permanent incisors would be essential to prevent the impact of the above-mentioned complications, reduce the treatment complexity and thus improve the clinical outcome.
Due to the retrospective nature of the present study, the major limitation was information bias which could have led to missing data for analysis and interpretation. This was also compounded by the lack of completeness and standardized method of history taking, clinical and radiographic examinations in the information gathering process.

Conclusions
1. The prevalence of unerupted permanent incisors among children and adolescents attending a university dental teaching hospital was 2.0%.
2. The most common etiologies for unerupted incisors were dilacerations for maxillary central incisors; developmental dental anomalies together with unfavorable root development for maxillary laterals incisors; and abnormal tooth/tissue ratio for mandibular incisors.
3. The majority of unerupted incisors presented with complications, which can have an effect on the remaining dentition (i.e. space loss and midline shift), as well as on the impacted incisor itself and/or its adjacent structures/teeth. Prevalence, characteristic features, and complications associated with the unerupted permanent incisors Supporting information S1 Table. Original data of 266 subjects with unerupted permanent incisors from clinical record and radiographs. (XLSX)