Urban-rural differences in dental caries experience among 6-year-old children in the Russian north

Introduction: Russians residing in rural areas, particularly in the north, have poorer health in general and lower life expectancy compared with urban residents. Little is known about dental health in the north of Russia, given that the last national oral health survey was performed more than 10 years ago. The aim of this study was to estimate the prevalence and experience of dental caries among 6-year-old children in a remote region in Northwest Russia. Methods: In total, 532 children aged 6 years were recruited in 5 randomly selected rural and urban settings of the Arkhangelsk region. Girls comprised 50.8% of the sample. Caries experience was assessed at D3 (cavitation) level by a single calibrated examiner. The prevalence of caries was calculated as the number of children with at least one affected tooth (decayed or missing or filled) divided by the number of examined children x 100% with 95% confidence intervals (CI). Caries experience was estimated using a sum of decayed, missing, filled teeth (dmft index) and presented as means and 95% CIs. Dichotomous and continuous data were analysed using χ2 and Mann–Whitney tests, respectively. Results: The prevalence of caries was 93.4% (95% CI: 90.9-95.2) with a mean dmft of 6.71 (95%CI: 6.37-7.04). On average, there were 5.48 (95% CI: 5.16-5.80) decayed, 0.44 (95% CI: 0.37-0.51) missing and 0.79 (95% CI: 0.67-0.91) filled teeth. Although the overall caries experience was similar in rural and in urban areas (6.52 vs 6.41, p=0.742), the number of decayed teeth in rural areas was greater (5.94 vs 4.91, p=0.001). Moreover, there were fewer missing teeth (0.31 vs 0.59, p<0.001) and filled teeth (0.45 vs 1.19, p<0.001) in rural areas. Boys had a greater number of affected teeth than girls (7.12 vs 6.32, p=0.023). Conclusions: The levels of both caries prevalence and caries experience in the region exceeded the Russian average and corresponding levels in most European countries. Both urban–rural and sex variations in caries experience and its components were


Introduction
Children at the age of 6 years represent a key group recommended by the WHO for assessing caries of the primary teeth 1 .Although the global prevalence of caries among 6-year-old children is decreasing, it remains a major public health problem with a considerable variation among countries 2 .While the prevalence of caries among 6-year-olds was 32% in Spain, 46.9% in Portugal and 49% in Austria [3][4][5] , the corresponding proportions for Turkey, China, India and Ecuador were 77%, 78%, 81% and 87%, respectively [6][7][8][9] .In European countries caries experience expressed as a sum of decayed, missing, filled teeth (dmft index) for the 6-year-olds varied from less than 2 affected teeth per child in Norway, Finland and Switzerland to 4.7 in Belarus 10 ; while in China, the dmft level of 4.5 was observed in the same age group 11 .
The latest nationally representative Russian oral health survey was performed in period 1996-1998 and showed that the prevalence of caries in primary dentition among 6-year-old children was 73% 12 .The mean dmft was 4.8 with decayed teeth (dt) being a predominant component (dt 3.5, mt = 0.1, ft = 1.2).
People who live in remote northern areas of Russia have been reported consistently to have poorer health in general and lower life expectancy compared to the national average 13,14 .Moreover, rural residents, particularly in the north, have greater overall mortality and morbidity than their urban counterparts 15 .According to the results of the oral health survey performed in the Arkhangelsk region, one of the northernmost regions of Russia, in the period 1996-1998 this is also applicable to oral health: the overall prevalence of caries among 6-years-old children in the region was 95% with the mean dmft value of 5.4 exceeding the national average of 73% 12,16 .No adequate information about caries prevalence and experience among children is currently available from the region, particularly its rural areas which suffer poor availability of and accessibility to dental health services.At the same time public dental health is among the least prioritized areas of public health in northern areas.
The development of teeth begins in intrauterine life and many oral health problems in children are attributed to the general health of their mothers and the course of pregnancy 17 .Pregnancy disorders have been shown to be associated with impairment of the enamel during a child's antenatal period 18,19 .Furthermore, preterm birth, low birth weight and infections in infancy are also associated with poor oral health in children 20,21 .A recent report has shown that the health of women in Russia in general and in the Arkhangelsk region in particular has worsened during the time of transition from Socialism to market economy, and that the incidence of pregnancy complications has increased 13 .Thus, one may hypothesize that poorer maternal health combined with nonexistent dental health preventive programs have resulted in a further increase in the prevalence of caries among children in the region.
This study aimed to estimate the prevalence and experience of dental caries among 6-year-old children in the Arkhangelsk region to provide a foundation for the development of preventive measures in the north of Russia.

Methods
The study is a part of the Russian National Dental Health Survey 22 .The Arkhangelsk region is situated in Northwest Russia and covers a territory of 413 100 km².The population of 1.26 million in 2008 gives the population density of 3 per km² making the region of the most sparsely populated in the country with considerable distances between towns and villages 13 .The number of 6-year-old children in 2008 was 13 203 (6746 boys) with 74.5% living in towns 23 .There are no areas with water fluoridation in the region.
Participants were recruited in 5 randomly selected rural settings (Emetsk, Plesetsk, Konosha, Leshukonskoe and Krasnoborsk) and 4 urban settings (Arkhangelsk, Severodvinsk, Novodvinsk and Velsk) of the Arkhangelsk region.Altogether, there are 13 towns and 20 rural districts in the region so the study includes 30% of the towns and 20% of the rural districts.Arkhangelsk, Novodvinsk, Severodvinsk and Leshukonskoe are situated in the northern area and two areas (Emetsk and Plesetsk) are in the central part.All other settings are located in the southern area of the region (Fig1).
Virtually all Russian children attend kindergarten at the age of 6 years.At least 50 children from each location were recruited according to WHO recommendations 1 , comprising approximately 3% of all 6-year-old children in the region.More detail of the sampling procedure is available elsewhere 24 .Usually, there are 1 or 2 kindergartens in rural areas of the region.Therefore, almost all 6-year-old children in the selected rural areas were included in the study.In each of the urban areas, kindergartens were randomly selected to ensure representativeness of the sample.The overall sample size was 532 children (50.8% girls).
All study participants underwent a clinical dental examination in the selected kindergartens in the areas assigned for this purpose.Clinical criteria for dental caries as defined by WHO were applied 1 .All examinations were performed by a single trained and calibrated dentist (the first author).Special calibration of practical skills was performed at the Moscow State Medical University of Dentistry in 2007.A written permit to conduct this type of examination for research purposes in accordance with the WHO recommendations was obtained to ensure comparability of the results with similar studies and reduce measurement bias.The examination was performed with the child sitting on a chair and the examiner standing or sitting in front of the child.A trained assistant completed registration cards.The average duration of dental examination was 10 min.After each hour of the examination session a 15-20 min break was scheduled to avoid the effects of visual fatigue.
The examination was carried out with a WHO-type periodontal probe and plain mouth mirror.No radiographs were taken.Children at the age of 6 are the index age group of the WHO in assessing dental caries in primary teeth, therefore only primary teeth were taken into consideration.Caries prevalence was calculated as a number of children with at least one affected tooth (decayed or missing or filled) divided by all examined children in the sample and multiplied by 100%.Caries experience was expressed as a sum of decayed, missing, filled teeth (dmft index).Teeth that could be absent because of natural teeth change were not taken into consideration in assessing the missing component.Dental caries was detected visually at the cavitation level (D3level).The study was conducted from November 2007 to December 2008.

Statistical analysis
Dmft index scores were calculated for primary teeth for each child.For the dmft index, teeth that had been extracted due to trauma, or were absent from birth were excluded and they did not contribute to the final score.The prevalence of dental caries in primary teeth was calculated for each setting as well as for all rural and for all urban areas and for the full sample.Ninety-five percent confidence intervals (CI) were calculated using the Wilson's method 25 .Mean dmft index with 95% CI was calculated for each location as recommended by the WHO 1 .Differences in the prevalence of caries between districts were analyzed by Pearson's χ2 tests.Because of the skewed distribution of the data, the differences in dmft and every component of the index between children who lived in rural and urban areas as well as sex differences were analyzed using Mann-Whitney tests while the differences in caries experience between the 9 settings were calculated by Kruskal-Wallis tests.When statistically significant differences by this test were found, post-hoc comparisons were performed using Mann-Whitney tests with Bonferroni correction with critical level of significance of 0.001 to compensate for type I error inflation due to multiple comparisons 26 .All analyses were performed using SPSS v16.0 (www.spss.com).
The overall mean dmft was 6.71 (95%CI: 6.37-7.04).Although the statistically significant differences between the settings by Kruskal-Wallis test were found, post-hoc comparisons between all settings showed that the dmft index reached the critical level of significance of 0.001 only between the rural Emetsk district and the regional capital Arkhangelsk (p<0.001), and Konosha (p=0.001).Detailed information on the dmft index is presented (Table 2).There were no differences in the overall caries experience between rural and urban areas (p=0.742).On average there were significantly more affected teeth in boys (7.12 vs 6.32, p=0.023) than in girls.Decayed, missing and filled primary teeth constituted 81.7%, 6.6%, and 11.7% respectively in the dmft structure.There were: 88.7% versus 73.4% decayed, 4.6% versus 8.8% missing, 6.7% versus 17.8% filled teeth in the dmft structure for the rural and urban areas, respectively.Mean values for the d, m, and f components for all locations are presented (Table 3).
There were on average 5.48 (95%CI: 5.16-5.80)decayed teeth per child.The mean number of decayed teeth in rural areas was higher than in towns (5.94 vs 4.91, p=0.001).There were more decayed teeth in boys than in girls (5.78 vs 5.16, p=0.038).Children in the regional capital had significantly fewer decayed teeth than children in rural towns Novodvinsk, Severodvinsk, Velsk and all rural areas (all p<0.001) but not Konosha.
It was observed that on average there were 0.44 (95%CI: 0.37-0.51)missing teeth per child.In rural areas, there were fewer missing teeth per child compared with urban areas (0.31 vs 0.59, p<0.001).No sex differences in the number of missing teeth were observed (p=0.600).Children from rural Krasnoborsk (p<0.001) and Emetsk districts had significantly fewer missing teeth than children in the towns Velsk, Novodvinsk, Severodvinsk (p<0.001 for Velsk and p=0.001 for Novodvinsk and Severodvinsk).
On average, there were 0.79 (95%CI: 0.67-0.91)filled teeth per child.In rural areas, there were fewer filled teeth per child compared with urban areas (0.45 vs 1.19, p<0.001).No sex differences were found in the number of filled teeth between the areas or in the full sample (p=0.884).Children in all rural areas and in the towns Velsk and Severodvinsk had significantly fewer filled teeth than children in the regional capital (all p<0.001).

Discussion
The study revealed an extremely high prevalence of caries among children at the age of 6 years (93.4%) which is 2 to 3 times higher than in Western Europe, but similar to the findings from developing settings 3,5,7,9 .The observed prevalence of caries was similar to what was observed in the region 10 years previously (93.4% [95%CI: 90.9-95.2]vs 95.0%, p=0.062) 16 , but is higher than the Russian average of 73.0% in the late 1990s 12 .Considerable differences were observed in the number of decayed, missing and filled teeth between rural and urban areas, but not in the overall prevalence of caries or caries experience.
While the overall prevalence of caries remained essentially unchanged over the 10 year period, the observed caries experience in the region expressed as dmft index increased (6.7 vs 5.4, p<0.001) 12,16 and exceeds the corresponding levels in most European countries and China 10,11 .One may speculate that the observed high levels of the dmft index and its components among 6-year-old children may be explained by traditionally poor oral hygiene in this age group, particularly in rural areas with a low level of parental supervised teeth brushing 27 , and the absence of any special prevention program in the region during the last 10 years for this particular group.Another factor which may partly explain the findings is changes in general health of women and the course of pregnancy during the last 10 years 13 .According to the Federal State Statistical Service in Russia, the number of complications of pregnancy and deliveries increased from 5364.5 per 100 000 in 2000 to 7126.7 per 100 000 in 2008 13 .Other contributing factors include the generally lower health status, socioeconomic disadvantage, poor oral health literacy and poorer access to services of Russian children compared with their European counterparts.
In total, 5.5 decayed teeth were observed per child.The number of decayed teeth is higher than was observed in the region 10 years ago (5.5 vs 3.  of the results 1 .The study was performed by a single trained specialist who calibrated using the WHO methodology, preventing inter-observer variability which threatens validity in similar studies.

Limitations
The results must be interpreted with caution due to potential limitations of the study.The results of the clinical examinations may have varied between districts because the researchers did not have a portable lamp and available illumination varied slightly according to conditions in each area.The small sample size resulted in wide confidence intervals and low statistical power for comparisons of dichotomous data.However, given that the sample was random and taken from northern, central and southern parts of the region it is possible to generalize the results to all 6-year-old children in the Arkhangelsk region.Given the relative homogeneity of neighboring regions it is also possible to generalize the findings to other northwestern areas of Russia.

Conclusions
Although the caries prevalence remained unchanged, the caries experience levels among 6-year-old children in the region increased during the 10 years suggesting further increase in health inequalities in the region, particularly between rural and urban areas.The levels of both caries prevalence and caries experience in the region are considerably higher than the Russian average and two to three times greater than in most European countries.Both urban-rural and sex variations in different components of the dmft index were observed.Urgent preventive dental public health measures at both population and individual levels are needed to improve the situation in the region.Recommended strategies and initiatives include the establishment of a regional preventive dental health program, the introduction of water fluoridation, educational campaigns for children and their parents in kindergartens to increase knowledge of dental health issues, and the introduction of regular dental examinations of children by dentists.

Figure 1 :
Figure 1: Map of the Arkhangelsk region, Northwest Russia.Urban and rural areas included in the study are shown as squares and circles, respectively.

Table 1 :
Sample composition by location and sex

Table 2 :
Prevalence and experience of dental caries with 95% CI by setting and sex among 6 year-old children in the Arkhangelsk region, 2007-2008 dmft, sum of decayed, missing, filled teeth.

Table 3 :
Components of the dmft index (sum of decayed, missing, filled teeth) with 95% CI by setting and sex among 6 year-old children in the Arkhangelsk region, Northwest Russia, 2007-2008