Restrictive type of anorexia nervosa (AN) is still one of the most severe eating diseases worldwide with an uncertain prognosis as 1.2–2.2% of girls/women are suffering from full-blown anorexia nervosa (AN) during their lifetime; even more, than 4% are considered as an atypical form (1–3). Unfortunately, some of the cases are not included in statistics due to a lack of insight into the disease or reluctance to start therapy (2). Anorexic type of eating disorder (ED) often begins quite early, even at 12-years-old or younger (1). A reason why oral status is vital at this age may be explained by their developmental period when the permanent teeth mineralization and periodontal tissue are formulated (4). Any case of oral imbalance may provide long-lasting consequences in their future oral health. Severely ill adolescents with AN are at risk of extremely low body weight, macro/micronutrient deficiencies (5), and combined with diminished salivation and neglecting of hygiene habits, protection for dental or periodontal tissues may be lost at an older age (6–8). Significant dental caries, erosive tooth wear, and loss of periodontal health were observed in other studies considering adult AN subjects (8, 9). However, in the available literature, few scientific reports focused on the oral status among AN individuals under the age of 18 and affected by disease < 5 years, i.e., during the first acute stage of ED (10, 11). It is proven that AN patients should be encouraged to undertake psychiatric/psychotherapy (11). However, whether they should be included in careful dental care may still be considered in an open discussion. Therefore, each oral health assessment among young AN patients may provide important directions for dental care and answer questions about what type of oral care elements should be considered in adolescent AN patients.

The study aimed to establish the oral status regarding caries incidence, tooth wear, gingival inflammation, and oral hygiene levels among severely ill adolescent inpatients diagnosed with AN.

The null hypothesis assumed no significant difference in the oral disease symptoms between patients with AN and healthy individuals matched in early adolescence.

In our study, patients from the AN group presented a higher incidence of oral-related complications regarding dental status and erosive tooth wear, less efficient control of plaque, and gingival inflammation than healthy subjects. A novel of our report is a collection of AN subjects in the youngest age under 18-years-old. After reviewing the literature on EDs, it should be noted that most oral clinical trials involved adult female patients (over 20 years of age) with a longer duration of AN than 5 years. Eating disorders are thus chronic diseases and are often associated with taking antidepressants and psychotropic drugs (26). Few dental analyses were based on a younger population of patients; the majority were limited in the number of cases and included a wide age range from 18 to 60-years-old (9, 27–40). Based on the analysis of the scientific literature, we found only nine studies separately involving young AN patients aged 18-years-old, as shown in Table 4 (8, 27–34). The rest of the published studies related to the symptoms in the oral cavity of various types of EDs or AN patients represented <10% study group (9, 35–40). Selected results from 9 original studies indicated a significantly worse dental status in AN patients, which increased with their age and disease duration (8, 27–34). This is also in line with the literature reviews on the ED and oral implications (9, 41, 42).

Our subjects from the study group were young female AN patients up to 18 years of age in whom the disease only first developed. A dentist's support could counteract side effects and thus prevent permanent changes in oral homeostasis, which is also crucial for their health in the future (43–51). In the case of ED, including AN, the disease symptoms at an early age give an uncertain prognosis and reduce the chances of success in psychiatric therapy (3). The same thesis seems to apply to oral health. While in the case of the non-physiological destruction of teeth such as dental attrition or abrasion, implementation of changes in the patient's dental habits may stop tooth wearing. Unfortunately, the protection of teeth against caries or erosion is more multivariate, as it is often not conducive to the patient's general condition (44–52), selective low pH diet (52, 53), the insufficient activity of the salivary glands (6–8), salivary buffering capacity (54). Moreover, the dentist's commitment to dental patients affected by AN may motivate them to undertake general treatment and combat the disease (41, 42). Multidisciplinary support in the case of patients' severe psychosomatic conditions seems to be not only an empathetic or ethical but definitely a therapeutic indication (55, 56). Nevertheless, the multidisciplinary assessment of the AN adolescent population in longitudinal studies may be suggested for future research.

The mean DMFT score among AN subjects was significantly higher than the control group in the presented study. Other studies conducted on adult AN patients are similar (8, 33, 48). However, DMFT values usually reported higher numbers due to the older age of enrolled patients (>20-years-old), the chronic character of the disease (>5 years earlier AN diagnosis before oral examination), and psychotropic pharmacotherapy, which may limit salivary flow and make easier dental plaque colonization (8, 32, 48). Compared to a nationwide epidemiological oral health survey conducted in Poland among healthy age groups (15-year-olds, n = 2,000), the DMFT index among girls was estimated at the same level or higher than the obtained results (57–59). However, it may be commented that additional factors could influence the DMFT results as the different countryside living locations, mineral composition, the buffer capacity of saliva secretion, the frequency of tooth brushing, and the number of consumed meals, including carbohydrates (57–59).

The assessment of the BEWE index showed a low risk of dental erosion. It is worth noting that AN young patients (symptoms of ED had been observed for an average of 12 months) reported rare vomiting inducing. We suspect that the purging episodes had to occur much less frequently than in patients with bulimia nervosa (BN), in whom the severity of erosion is reported in the literature from 30 to 70% (49, 50, 52, 60–62). Pallier et al. (8) found a high risk of erosion in 16.7% of AN patients, but they studied much older adult female patients with long-term, chronic disease. However, the AN subgroups with purging episodes showed worse results concerning dental erosion. Apart from vomiting, more factors influence the BEWE score. The role of an acid diet may be crucial; foods and drinks predispose to decrease the pH of the oral cavity, especially in persons with severe ED when unstimulated saliva secretion is diminished (52, 53, 60, 61). Finally, it may also be connected with loss of hard tissues due to accompanying attrition or abrasion (62, 63). Shellis and Addy (63) pointed out that these processes coexist and have strong relationships. Comparing the findings on erosive changes among healthy 15-year-olds from southern Poland (n = 181), Kaczmarek et al. (62) observed only initial enamel erosion and more often observed it in boys than in girls. It is suggested that a low pH diet, especially drinks, and excessive physical activity may limit salivary buffer capacity at this age and stimulate non-carious dental tissue loss (64, 65).

It should be noted that AN subjects often perform excessive physical activities and prefer acid beverages, but they limit the amount of food consumption (32). The abovementioned data showed that dental erosion might occur among adolescents in various degrees of tooth wear with age. It is vital to adopt the hypothesis about the potential incidence of erosion among children (65).

In the AN group, poor dental hygiene and gingival inflammation are in line with other ED reports (11, 28, 32, 37, 40). In comparing our research with a national survey among healthy adolescents aged 16–18 years, Pietrzak et al. reached better dental hygiene results (66). We may explain our worse results; those dental examinations carried out in the first week after admission to the hospital ward might impact the worse oral hygiene conditions. The beginning of the hospital treatment seems to be a challenging period for AN patients, as they are mainly weakened and, at the same time, subjected to additional stress related to the hospital stay. All inpatients were enrolled in a behaviorally oriented nutritional rehabilitation program. They ate meals under the supervision of nursing personnel for 1-h observation. Thus, they could not perform hygienic procedures immediately after eating. Due to the nature of the therapy, meals contained a lot of simple sugars with a sticky consistency (e.g., jams, sweetened tea, white bread). Based on our observation and literature data, poor motivation to maintain good oral hygiene may also be influenced by a difficult life situation and the related apathy, depressed mood, psychomotor drive, and suicidal tendencies (67, 68). Other investigations indicated that a diet low in protein, vitamins, and unsaturated fatty acids contributes to metabolic and biochemical disturbances that cause an imbalance between oxidants and antioxidants (5–7, 53, 69). We agree with other authors that the pervasive state of malnutrition, especially in highly severe AN, influenced medical complications and a risk of rapid gingival inflammation (8, 9, 34). Obtained correlations to PCR and BOP indexes with lower neutrophile count results may suggest a relationship to the risk of gingival inflammation. It is worth quoting from other laboratory studies that about 80% of AN patients are affected by anemia, leukopenia 29%, neutropenia 79%, thrombocytopenia 25%, and 17% develop thrombocytosis (70). In our study, severe malnutrition and the laboratory-tested neutrophiles may explain the relationship between nutritional deficiencies and body defense and susceptibility to gingival complications (71, 72).

Consensus Report of the European Federation of Conservative Dentistry on eating disorders concluded that dental caries and erosion prevention objectives reduce or arrest the progression of these two processes, screening and monitoring recall dental sessions (73). Our dental data indicated that the main tasks should include three directions: oral hygiene, remineralization, and diet advice (73–78). Figure 3 shows that all preventive approaches may be applied (73, 79).

The present study's authors are aware of its limitations and recall most of them. The participants were not checked whether gastroesophageal reflux (GERD) or any other condition could have exposed their teeth to intrinsic sources of acid other than purging behavior. However, a qualified physician excluded any somatic diseases during a diagnostic interview. All patients were asked to express any digestive system ailments and did not report any symptoms. It is worth noting that all patients were hospitalized the first time after the onset of the AN disease. At this phase, a crucial hospitalization role was making the correct diagnosis but detecting any additional symptoms. The final diagnosis of all patients was the restrictive subtype of AN.

In addition, we can assume that the subjects had no comparable diet habits due to AN disease. It would be worth analyzing nutritional intake according to quantity and quality important from the point of view of oral health safety. According to diet behaviors in early disease development, anorexics do not have the same opinion on diet preferences. They often claim that they eat larger meals than before and start a selective diet. However, it is not easy to rely on such data. Studies have shown that their diet is low in carbohydrates (eliminated as the first ingredient). At the same time, protein and fat intake are maintained at an acceptable level, especially at the beginning of the disease (71, 80, 81). Besides protein-energy malnutrition (PEM), any deficiencies related to counts may raise the risk of bacterial infection.

It seems essential to consider a significant risk factor for erosive tooth wear among adolescents with purging/bulimic symptoms. Professional food and drink advice may have a preventive role to avoid erosive tooth wear (79). A significant limitation was a lack of data according to earlier oral status in both AN and Ctrl groups. This comparison could give additional conclusions for all children suffering from ED. Longer follow-up periods may be suggested to evaluate the clinical approach to oral health among AN patients.

Nevertheless, one may argue that we examined a small cohort of young AN patients under real-life conditions. Besides, family members were not included in the dental examination because living a long distance from the hospital clinic. Moreover, our project was also refined by the case-control design, and the assessment of oral clinical markers was based on visual criteria when examining the oral cavity. In detecting and assessing caries, digital devices could be implemented, e.g., DIAGNOdent Pen, DIAGNOcam and CarieScan PRO, but the visual DMFT index makes the results comparable to previously performed studies that focused on ED and AN. To our knowledge, this is the first clinical trial that compared such a group of AN patients in terms of homogeneity of subtype symptoms, adolescent age, sex, living area, nutritional status, and duration of disease, fewer than 5 years.

Even if our results are not enough to prove oral conditions among anorexic subjects, our limitations do not undermine the representativeness of the examined group.

Determination of AN restrictive subtype in adolescence may indicate numerous oral-related complications from dental caries, the beginning of erosive tooth wear, gingival inflammation development, and failure to cope with dental hygiene. Although the obtained results did not reveal any severe oral condition, there is a need for adequate oral hygiene/diet instructions combined with regular oral care to prevent forward complications in the patients' future.

Dental problems need to be tackled together with medical insight and interaction with physicians in the future. These disturbances to oral health should be routinely investigated, monitored, and treated during the perception of the primary disease. Multidisciplinary management of AN is essential to prevent the chronicity of the disorder and the potential severity of negligence.

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

The studies involving human participants were reviewed and approved by Bioethics Committee of the Poznan University of Medical Sciences (Resolution No. 66/12). Written informed consent to participate in this study was provided by the participants' legal guardian/next of kin.

EP, MT-N, and AS contributed to the conception and design of the study. AH, MR, KJ, and EP organized the database. MR performed the statistical analysis. EP performed clinical examinations. All authors contributed to manuscript revision and read and approved the submitted version.

Poznan University of Medical Sciences handed over funding sources for the research.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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