# COUNTRY PROFILE OF THE EPIDEMIOLOGY AND CLINICAL MANAGEMENT OF EARLY CHILDHOOD CARIES

EDITED BY : Morenike Oluwatoyin Folayan, Wael Sabbah, Maha El Tantawi and Francisco Ramos-Gomez PUBLISHED IN : Frontiers in Public Health

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ISSN 1664-8714 ISBN 978-2-88963-808-6 DOI 10.3389/978-2-88963-808-6

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## COUNTRY PROFILE OF THE EPIDEMIOLOGY AND CLINICAL MANAGEMENT OF EARLY CHILDHOOD CARIES

Topic Editors:

Morenike Oluwatoyin Folayan, Obafemi Awolowo University, Nigeria Wael Sabbah, King's College London, United Kingdom Maha El Tantawi, Alexandria University, Egypt Francisco Ramos-Gomez, University of California, Los Angeles, United States

Image: wavebreakmedia/Shutterstock.com

Citation: Folayan, M. O., Sabbah, W., El Tantawi, M., Ramos-Gomez, F., eds. (2020). Country Profile of the Epidemiology and Clinical Management of Early Childhood Caries. Lausanne: Frontiers Media SA. doi: 10.3389/978-2-88963-808-6

# Table of Contents

	- *85 Assessing the Impact of Early Childhood Caries on the Development of First Permanent Molar Decays*

Fatma Songur, Sera Simsek Derelioglu, Sinan Yilmaz and Zahide Koşan

Mohammad J. Kharazifard

# Editorial: Country Profile of the Epidemiology and Clinical Management of Early Childhood Caries

Morenike Oluwatoyin Folayan1 \*, Maha El Tantawi 2 , Francisco Ramos-Gomez 3 and Wael Sabbah4

*1 Department of Child Dental Health, Obafemi Awolowo University, Ile-Ife, Nigeria, 2 Department of Pediatric Dentistry and Dental Public Health, Faculty of Dentistry, Alexandria University, Alexandria, Egypt, 3 School of Public Health, University of California, Los Angeles, Los Angeles, CA, United States, 4 Faculty of Dentistry, Oral & Craniofacial Sciences, King's College London, London, United Kingdom*

Keywords: early childhood caries, prevalence, policy, structural determinant, elimination, sustainable development goal

#### **Editorial on the Research Topic**

#### **Country Profile of the Epidemiology and Clinical Management of Early Childhood Caries**

Early childhood caries (ECC) is the presence of decayed (cavitated and non-cavitated), filled and missing teeth due to caries, affecting the primary dentition in children less than 72 months old (1). It is the most common non-communicable disease in children (2) and a global endemic problem with those socially disadvantaged (ethnic minorities, immigrants, those of low socioeconomic status or from resource-limited settings) being most affected. The negative impact of ECC on the quality of life, growth, social development, and neurodevelopment of affected children makes it ethically imperative that public epidemiological and clinical management of ECC improves (3). Whether treated or not, ECC is a high-risk factor for caries in the first permanent molar, as highlighted by Songur et al. in this topical issue. Four other manuscripts in this special issue emphasize the urgency of addressing the endemic ECC problem. Musinguzi et al. highlighted that the prevalence of ECC in rural Uganda was 48.6% in 3–5-year-olds, and Castillo et al. showed it was as high as 76.2% in 3–5-year-olds in Peru. Also, Pierce et al. reported a prevalence of 98% in some parts of Canada, and Amalia et al. reported a prevalence of 100% in South Kalimantan, Indonesia.

Twenty years after establishing the definition of ECC, we know a lot more about ECC prevention and management (4), but we still know little about cost-effective integrated management of ECC that can control the disease using life course approaches appropriate for various cultural settings. The World Health Organization guidance document (2) promotes integration of oral healthcare into existing primary care systems. In this special issue, Villalta et al. describe how an integrated primary care model improved the knowledge and attitudes of caregivers regarding child oral health care, and Castillo et al. discuss policies, taxes, and guidelines on ECC management and labeling of food sugar content that are addressing the huge ECC problem in Peru.

Policies and taxes are strong tools for addressing structural barriers and enhancing actions for disease control, as we have learnt from tobacco control programs (5). Increased availability of ECC data will help improve the design and implementation of context-specific public oral health responses to control the disease through which we can learn about effective public health ECC control responses. The epidemiological profiles of ECC in Canada (Pierce et al.), Indonesia (Amalia et al.), Israel (Shmueli et al.), and Peru (Castillo et al.) that were presented in this issue add to our understanding of the risk factors for ECC.

Edited and reviewed by: *Prathip Phantumvanit, Thammasat University, Thailand*

\*Correspondence: *Morenike Oluwatoyin Folayan<EMAIL_ADDRESS>
#### Specialty section:

*This article was submitted to Children and Health, a section of the journal Frontiers in Public Health*

Received: *13 February 2020* Accepted: *03 April 2020* Published: *30 April 2020*

#### Citation:

*Folayan MO, El Tantawi M, Ramos-Gomez F and Sabbah W (2020) Editorial: Country Profile of the Epidemiology and Clinical Management of Early Childhood Caries. Front. Public Health 8:141. doi: 10.3389/fpubh.2020.00141*

Eradication—the permanent reduction of global incidence of ECC to zero—seems ambitious at the present time. However, elimination—the sustained reduction of ECC incidence to zero or levels defined by global oral health authorities—seems possible. Countries such as Finland (0.3%), Nigeria (2.7%), Kuwait (3.0%), Japan (3.9%), Tanzania (5.2%), and Sweden (6.0%) with low ECC prevalence for 0 to 2-year-old children; and Denmark with a low prevalence of 6.3% for 3 to 5-year-old children (6) may serve as global learning centers on best practices for ECC elimination.

The sparse evidence on structural determinants of ECC risk will limit efforts for ECC elimination. For ethical reasons, randomized clinical trials that might answer critical questions on structural determinants of ECC cannot be conducted; thus, the causal pathways for a multitude of inter-related factors for ECC can only be modeled (7). In this issue, Markovic et al. provide ecological data from Serbia, which suggests that structural factors like social and health care expenditures, unemployment rates, population density, and availability of physicians and dentists are determinants of the prevalence and treatment of ECC. Joury provided data suggesting that the risk for ECC in Syria increased during war and crisis, which is contrary to findings of historical studies that found a decrease in caries during war and crisis (8).

When the elimination of ECC becomes the focus of public oral health response for children under the age of 6 years (9), the World Health Organization will have to refine its targets, including setting global goals for ECC (10). Also, indicators to

#### REFERENCES

measure achievement should set elimination goals for 0 to 2 year-old children separate from those for 3 to 5-year-old children as emerging evidence suggests that the epidemiological profile and risk factors for ECC for the two age groups differ (6). In addition, goals and interventions for eliminating ECC should recognize that those most vulnerable to the disease are the less privileged who may be left behind if right-based interventions are not developed (11). Sadly, the populations at increased risk for ECC are likely to have no data on ECC available (6).

The 11 articles published in this topical issue provide information that can help inform policy development, policy review, and program design for the control of, and possible elimination of ECC. They contribute to our understanding of what we can modify to attain goal 3.1 of the Sustainable Development Goal for children below 6 years by 2030. The articles also provide evidence on parent-targeting interventions that can be effective (Al-Batayneh et al.; Razeghi et al.; Villalta et al.). Despite all we know about ECC, we still need more data like these published in this issue, to enable planning for control and possible elimination of ECC.

#### AUTHOR CONTRIBUTIONS

MF developed the first draft of the manuscript. ME, FR-G, and WS revised and made intellectual contributions to the subsequent drafts. All authors approve of the final version of the manuscript and for its submission.

**Conflict of Interest:** 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.

Copyright © 2020 Folayan, El Tantawi, Ramos-Gomez and Sabbah. This is an openaccess article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

# Epidemiology and Clinical Management of Early Childhood Caries in Israel

Aviv Shmueli\*, Moti Moskovitz, Elinor Halperson, Diana Ram and Avia Fux-Noy

Hebrew University-Hadassah School of Dental Medicine, Jerusalem, Israel

Aim: The aim of the present review is to describe the current status of early childhood caries (ECC) in Israel in aspects of epidemiology, prevention, and management.

Methods: PubMed search was performed using the words caries, children, Israel. Demographic data was collected from the Israeli Central Bureau of Statistics.

#### Edited by:

Morenike Oluwatoyin Folayan, Obafemi Awolowo University, Nigeria

#### Reviewed by:

Dayanand Bagdure, University of Maryland, Baltimore, United States Sera Derelioglu, Atatürk University, Turkey Jorge Luis Castillo, Universidad Peruana Cayetano Heredia, Peru Rosa Amalia, Gadjah Mada University, Indonesia

\*Correspondence:

Aviv Shmueli<EMAIL_ADDRESS>
#### Specialty section:

This article was submitted to Children and Health, a section of the journal Frontiers in Public Health

Received: 07 May 2019 Accepted: 18 September 2019 Published: 09 October 2019

#### Citation:

Shmueli A, Moskovitz M, Halperson E, Ram D and Fux-Noy A (2019) Epidemiology and Clinical Management of Early Childhood Caries in Israel. Front. Public Health 7:280. doi: 10.3389/fpubh.2019.00280 Results: The decayed, missing, and filled teeth index was 2.72 in 1992 and 2.56 in 2016. The proportion of restored teeth has increased. A number of preventive programs are ongoing but a general preventive program is lacking at the national level. From 2010, every child in Israel is eligible to receive free dental treatment.

Conclusion: The gaps in understanding of the epidemiological profile of ECC in Israel is a call for more research conduct on ECC in the country.

Keywords: caries, prevalence, early childhood, prevention, Israel

## INTRODUCTION

Israel is a relatively small country with a population of almost 9 million people, located in the Middle East. The population is diverse with about 6.6 million Jews and 1.9 million Arabs. Since the establishment of the State of Israel in 1948, Jewish persons from around the world have immigrated to the country. According to the published registry, Israel's population at the end of 2016 was 8.63 million people of which 2.8 million (aged 0 to 17 years) are children. This is about 33% of the population of which 71.3% are Jews, 25.7% are Arabs (Muslims, Christians, and Druze), and 3% are of other backgrounds (1). Children under age 14 years comprise 28.2% of the population (1). This item is high compares to the population distribution in western countries but relatively low in comparison to Israel's neighboring countries. Percentage of children is higher in the northern and southern parts of Israel. Places where children constitute more than half of the population typically belong to religious population (1).

Israel's relatively small population comprises diverse ethnic groups. These subpopulations have specific socio-demographic and cultural characteristics that may affect the tendency to develop caries in general and early childhood caries in particular. There are some population groups for example the ultra-orthodox Jews that are characterized by large families (more than 4 children per family). In these communities the dental awareness is sometimes low, and many children are referred to dental treatment under sedation or general anesthesia due to their young age and complexity of treatment.

In 1981, water fluoridation was started in Israel. The first fluoridation station was in the capital city, Jerusalem. Despite the significant decline in caries prevalence and severity, which was attributed to water fluoridation, and despite the recommendations of public health experts, the Israeli Minister of Health decided to discontinue public water fluoridation in 2014. The reasons to this step were concerns about the influence of fluoride on general health. Israel is located in the hot region of the Middle East and there is substantial shortage of natural water. Most of the water (about 80%) that will be provided in the coming years will be from water desalination. The implication is that most of the water in Israel will not be fluoridated.

Public debates and discussions are ongoing regarding water fluoridation. The dental professional advisors recommended the minister of health to add fluoride to the drinking water, the current minister of health is willing to do so, hopefully, the problem will be resolved soon, in favor of the dental health of Israeli children (2). The current review describes the status of ECC in Israel, prevention and treatment modalities.

#### EPIDEMIOLOGY OF EARLY CHILDHOOD CARIES (ECC)

There are only a few surveys on ECC conducted in Israel. This is due to difficulties such as the lack of accessibility to a large representative sample of children younger than 5 years, since the compulsory school enrolment begins at this age ("Israeli compulsory education")1 Examining very young children in Mother-and-Child Health Centers raises biases because this population does not necessarily reflect the general population. To absence of a national survey on ECC contributes to the challenges with planning for prevention and early detection of this disease.

The findings of a national survey of 5-year-old children were published in 1992 (3). The sample of 767 children were recruited from 25 kindergartens around the country and examined using World Health Organization (WHO) criteria. No radiographs were taken. The mean decayed, missing and filled teeth (dmft) were 2.72 for children aged 5 to 6 years, and the prevalence of caries was 58.7%. No differences were found between genders or between urban and rural populations (3).

Another survey was performed in Ashkelon, a peripheral but large city (above 100,000 residents) in southern Israel (4). Of the 182 5-year-old children examined in that survey, 57% had caries. The mean dmf (t) was 2.08 + 2.64. An interesting finding of this survey was that the f component of the dmft was 0, which means that these children were not treated (4). Children at the lower end of the socio-economic scale showed high rates of severe early childhood caries. Populations that are predominantly low on the socio-economic scale are Bedouins, Ultra-Orthodox Jews, refugees from Africa and immigrants. These populations are characterized by low income and a high number of children. According to the Israeli national insurance institute, 463,300, families in Israeli were of low socio—economic level in 2016, among them 842,300 children (5). In 2007, a survey among 5 year-olds in 28 of 70 local authorities providing school dental services reported that 64.7% of children had tooth decay, with an average dmft of 3.31 (6).

Livny et al. (7), by using visual caries detection method, examined 102 Bedouin children for caries, using the World Health Organization (WHO) (1997) criteria. The children were aged 12 to 36 months from the Jahalin tribe, a previously nomadic tribe dwelling on the eastern outskirts of Jerusalem. White spot lesions were not recorded as caries. The investigators reported severe early childhood caries in 17.6% of the children. The prevalence of early childhood caries was significantly associated with older children's age (25 to 36 months), larger family size, and mother's lower education level and poorer dental appearance. The average number of children per family in that study was 4.6 and the maximum was 13. The researchers assumed that in a large family, it is more difficult for the parents to provide optimal healthcare according to each child's needs, including healthy feeding and oral hygiene practice (8).

In attempting to understand the prevalence trends of caries in Israel, and specifically ECC, Sgan-Cohen et al. (9) compared average defs (decayed extracted filled surfaces) and dmfs among first-grade children in south-west Jerusalem. According to municipality records, the neighborhoods surveyed represent the lower middle class. The examinations were conducted in 1983, 1992, and 2005, in accordance with the 1977 WHO's recommendations. Data indicated a consistent decline in disease severity: a reduction in the defs from 13.95 to 8.09 and 5.07 in 1983, 1992, and 2005, respectively.

In 2016, Natapov et al. (10) published a survey of 6 yearold-children residing in 23 local authorities that were randomly selected nationwide. Although Ecc is defined as caries before age six. Trends can be learned from this data about the caries experience of this children in their early years of life. The children were examined according to the WHO Oral Health Survey Methods 4th edition protocol. Of 1,210 children examined, 61.7% had dental decay and only 38.3% were caries free. The mean dmft was 2.56: d−1.41 (teeth with untreated caries), f = 1.15 (teeth damaged by decay and restored); no teeth were missing due to caries. The prevalence of dental caries was rather consistent, an average of over 2 teeth were affected per child. In this survey, the f component was higher than previously reported, especially in the Jewish sector, yet still lower in the Arab sector.

#### EARLY CHILDHOOD CARIES PREVENTION PROGRAMMES

#### The Impact of Free Access to Toothbrush and Toothpastes on Early Childhood Caries Incidence

A study was conducted to assess the impact of access to free toothbrushes and toothpastes on the incidence of ECC in 1,500 6-month-old infants recruited from Mother-and-Child Health Centers over a 2-year period. At age 2.5 years, 596 of the 1,500 children were examined. The early childhood caries prevalence

1The Israeli compulsory education law. Available online at: http:// www.google.com/url?sa=t&rct=j&q=&esrc=s&source=web&cd=5&ved= 2ahUKEwip0eeBp8PkAhUFa1AKHabqBE0QFjAEegQIAxAC&url= http%3A%2F%2Fedu.gov.il%2FDocuments%2Flimudchova.doc&usg= AOvVaw0fn3bowWd59V\_cDnVqL4lB.

was 15.3%. No difference in caries prevalence was found between children whose parents received the study intervention and those whose parents did not. The proportion of children who brushed twice daily was 13.9%, while 26.8% of the children did not brush at all. Eighty-one percent of the parents reported that their children went to bed at night with a bottle. Among children who drank sugar-sweetened beverages, the prevalence of early childhood caries was significantly higher than among those who drank milk or natural juice (18.8 vs. 8.9%). The study highlighted that tooth brushing might not be the only nor optimal public health response for early childhood caries in Israel (8).

#### Community Health Education, Bottle-Feeding Practices and Tooth Brushing Behavior of Infants in Jerusalem

In this quasi-experimental study designed to compare the impact of a structured health education programme on infant's bottle feeding and tooth brushing behavior, parents of 727 children aged 6 to 12 months from Mother-and-Child Health Centers in Jerusalem were recruited (8). Parents in the intervention group received structured health education information over the telephone, and half were randomized to receive fluoridated toothpaste and tooth brushes. The control group received did not receive an organized educational intervention. Six months into the study, parents in the control group reported a 32.5% increase in tooth brushing for infants, compared to baseline. Tooth brushing frequency increased by 45.1% for infants of parents who received toothpaste and toothbrushes, by 43.7% for infants whose parents received health education information only, and by 60.4% for infants whose parents received health education, toothpaste, and toothbrushes (P = 0.0002) (8). Modification of bottle-drinking practices in this programme was unsuccessful. The study therefore recommended that free distribution of toothpaste and toothbrushes, in conjunction with a structured oral health education programme to parents of infants, is effective in promoting good oral hygiene practices (11).

#### The Impact of a Prenatal Infant Oral Health Programme Implemented Through Baby Clinics

In 2003, members of the Pediatric Dentistry Department of the Hadassah School of Dental Medicine initiated a Baby Clinic in Jerusalem, based on the Brazilian concept of prenatal prevention. The objective of the project was to describe the implementation and outcome of a prenatal infant oral health programme that focused on pre- and post-natal oral health education for parents, and caries prevention in their first-born babies. The intervention commenced in late pregnancy and continued until the child reached age 3 years. Twenty-four, 30-min long prenatal powerpoint dental education lectures were delivered to 300 young, first-time parents to be, from the 8 to 9th month of pregnancy. Participants attended the "Course for Birth Preparation" at the Hadassah Hospital, Jerusalem. Lectures were given by pediatric dentists. The lectures emphasized the relation between the mother's oral health and the oral health of the expected baby, and provided recommendations about feeding and oral habits for the expected baby. Parents were invited to bring their babies for the first visit when their first tooth erupted or between ages 6 and 12 months. A brochure containing a summary of the information from the lecture was distributed at the first or second follow-up visit, to provide parents the opportunity to review the information at home and share it with other family members or friends who did not attend the lectures.

At each recall appointment, the young parents received anticipatory guidance for prevention of dental disease, and brushing instructions were demonstrated in the child's mouth, using the "lift the lip technique." Follow-up visits were recommended according to a protocol, based on individual caries risk assessment: low risk, every 6 months; medium risk, every 4 months; and high-risk babies, every 2 months. For the highrisk group, the teeth at risk were treated with fluoride varnish. A "dental home" was also achieved for the participating families. The intervention significantly reduced the incidence of early childhood caries. By the first visit, 70% of the 137 parents who attended already brushed their children's teeth. The incidence of early childhood caries was 2.9% over the 3 years of the study, a figure significantly lower (p < 0.001) than the 15.3% reported by Livny and Sgan-Cohen (12).

#### Caries Risk Assessment Tool and Prevention Protocol for Public Health Nurses in Mother-and-Child Health Centers, Israel

In Israel, Mother-and-Child Health Centers provide free preventive services for pregnant women and children by public health nurses. A caries prevention program in health centers started in 2015. Nurses underwent special training regarding caries prevention. A customized Caries Risk Assessment Tool and Prevention Protocol for nurses, based on the tool implemented by the American Academy of Pediatric Dentistry, was introduced. A two-step evaluation was conducted, which included a questionnaire and in-depth phone interviews. Of 46 health centers included in the study, 28 returned a completed questionnaire. Most nurses believed that oral health preventive services should be incorporated into their daily work. In the in-depth phone interviews, nurses stated that the integration of the program into their busy daily schedule was realistic and appropriate. The lack of a specific dental module for managing computerized data was mentioned as an implementation difficulty (13).

## EARLY CHILDHOOD CARIES TREATMENT

#### The National Health Insurance Scheme

Pediatric dental service was not part of the national health services until June 2010. Prior to this date, dental services such as dental examination, preventive treatments and pediatric dental treatments were not provided by the Ministry of Health. Access to dental services was limited, especially for underprivileged populations and those living in the peripheral districts of the country. The June 2010 legislation of the National Health Insurance for children under age 8 years affords access, for every preschool child, to preventive and operative care, which was usually provided by general dental practitioners. The service is operated by four health maintenance organizations that provide all the other public medical healthcare services. The service includes the provision of all operative dentistry needs of children in the public healthcare service and operating referral centers. At such centers, very young children are usually treated under conscious sedation or general anesthesia. Specialists in pediatric dentistry generally provide the care (14).

#### CONCLUSION

The prevalence of early childhood caries in Israel has not changed much over the years. According to the latest survey, treated caries

#### REFERENCES

are more prevalent in children than in the past but dmft is still relatively high. Particular emphasis on preventive measures are needed, especially in underprivileged populations.

#### AUTHOR CONTRIBUTIONS

All authors have made substantial contributions to the conception and design of the work, the acquisition, analysis, or interpretation of data for the work, and have made substantial contributions to the drafting the work and revising it critically for important intellectual content. All authors approved the final version to be published and agreed to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

**Conflict of Interest:** 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.

Copyright © 2019 Shmueli, Moskovitz, Halperson, Ram and Fux-Noy. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

# The Burden of Early Childhood Caries in Canadian Children and Associated Risk Factors

Andrew Pierce1,2†, Sarbjeet Singh1,2†, JuHae Lee1,2, Cameron Grant 1,2 , Vivianne Cruz de Jesus 1 and Robert J. Schroth1,2,3 \*

*1 Dr. Gerald Niznick College of Dentistry, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, MB, Canada, 2 Children's Hospital Research Institute of Manitoba, Winnipeg, MB, Canada, 3 Maxy Rady College of Medicine, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, MB, Canada*

Introduction: Early childhood caries (ECC) is any caries in the primary dentition occurring in children under the age of six. ECC is common in many population groups in Canada.

Objective: The purpose of this review was to describe the burden of ECC in Canada, the prevalence and associated risk factors for ECC, and its impact on childhood health based on the existing published literature.

#### Edited by:

*Morenike Oluwatoyin Folayan, Obafemi Awolowo University, Nigeria*

#### Reviewed by:

*Dayanand Bagdure, University of Maryland, United States Aviv Shmueli, Hebrew University of Jerusalem, Israel*

> \*Correspondence: *Robert J. Schroth<EMAIL_ADDRESS>
*†These authors have contributed equally to this work and share first authorship*

#### Specialty section:

*This article was submitted to Children and Health, a section of the journal Frontiers in Public Health*

Received: *02 May 2019* Accepted: *24 October 2019* Published: *12 November 2019*

#### Citation:

*Pierce A, Singh S, Lee J, Grant C, Cruz de Jesus V and Schroth RJ (2019) The Burden of Early Childhood Caries in Canadian Children and Associated Risk Factors. Front. Public Health 7:328. doi: 10.3389/fpubh.2019.00328* Methods: A review was conducted to assess published Canadian studies on ECC identified through searches of electronic databases. Databased searched included PubMed, Medline, Cinahl, and the library catalog of the University of Manitoba. Known publications on ECC that were not identified by the electronic search were also considered. Only the studies that reported the prevalence of ECC or caries in preschool aged children were considered. In-depth assessments were restricted to those studies that employed logistic regression analysis to investigate relationship between ECC and risk factors or nutritional status and quality of life.

Results: A total of 36 studies were identified that related to ECC in Canadian children. Overall, 27 related to prevalence and 12 reported on risk factors, four related to the association between severe ECC and nutritional health and well-being, while only one related to the oral microbiome composition. Published studies reveal that the prevalence of ECC can be as high as 98% in some parts of Canada. Commonly identified risk factors include age, sex, socio-economic status, parental beliefs, family characteristics, debris/plaque, enamel hypoplasia, and behavioral (oral health or feeding behaviors) tendencies.

Conclusions: Current literature reveals that many Canadian children are affected by ECC. The development of ECC appears to be strongly associated with social determinants of health including low household income and the level of parental education or employment status. Associations were also observed between ECC and the child's age at first dental visit and parental beliefs about child's oral health. Children with enamel hypoplasia are also at significantly greater odds for experiencing caries. Future research should include assessments of developmental defects of enamel to better understand the association between enamel hypoplasia and ECC.

Keywords: early childhood caries (ECC), Canada, preschool child, risk factors, nutritional status, burden of caries

## INTRODUCTION

Decay involving the primary dentition in children younger than 6 years of age is termed Early Childhood Caries (ECC) (1). ECC is a multifactorial chronic disease, which is influenced by biomedical factors such as diet, the oral microbiome, tooth integrity and by underlying social determinants of health (1, 2). This includes low socioeconomic status (SES), parental education, maternal nutrition, and psychosocial issues (3–5).

Numerous young Canadian children experience significant oral health problems, particularly ECC. This is especially true for First Nations, Inuit and Metis children, recent refugees and immigrants (i.e., newcomers), those living in low SES households, and children from geographically remote regions of the country (6–12). It is now well-established that up to 90% of children in some northern and remote Indigenous communities are affected (13–15). Usually, urban children are considered low-risk for caries, but there is also data available that signify that ECC is prevalent in disadvantaged urban communities in Canada (11, 16, 17). The challenge is that those most at risk for ECC are often those with the greatest barriers in accessing oral health care services.

Although national data on the true prevalence of ECC is missing, as children <6 years of age were not included in the Canadian Health Measures Survey, ECC continues to be a problem in Canada today (3, 18). One reason is due to the failure of previous interventions of being able to address successfully the underlying causative biomedical, behavioral, and social factors known to contribute to the development of caries (12).

If left untreated, early childhood caries advances to a more rampant form of disease, which further leads to malocclusions, abscess and pain. This situation is further compounded by the fact that there are long waiting lists for operative treatment in hospitals (19, 20). Furthermore, Severe Early Childhood Caries (S-ECC) among young children can negatively impact oral health related quality of life, nutritional status and growth (12, 21–23). There is also a growing body of evidence that the reoccurrence of dental caries and relapse following restorative dental treatment under general anesthesia is high (24–26).

In the absence of national prevalence data, national rates of pediatric dental surgery to treat ECC under general anesthesia can serve as a proxy measure (3, 27). National data reveals that the rate of dental surgery for ECC is 12.1 per 1,000 children and is recognized as the most common surgical procedure performed in preschool children at most Canadian hospitals (3, 28). This report also found that children from rural regions had rates of dental surgery to treat ECC 3.2 times higher than rates of urban-dwelling children (31.2 per 1,000 vs. 9.8 per 1,000) (3).

Due to potential for ECC to affect childhood growth and development and the associated treatment costs, the prevalence and etiology of ECC must be examined more closely to inform clinical management, policy, and prevention activities. The purpose of this review was to describe the burden of ECC in Canada, particularly its prevalence, associated risk factors, and its impact on childhood health and well-being based on the existing literature.

#### METHODS

Electronic databases were searched to identify all Canadian published studies on ECC. The search strategy by Schroth and Grant informed our work for this current review and provided a recent listing of relevant publications (18). Keywords (used alone and in various combinations) were: baby, babies, Canada, Canad∗ , caries, cavities, cavit∗ , child, "dental caries," "dent∗ and cavit∗ ," "early childhood caries," ECC, infant, preschool∗ , "severe early childhood caries," S-ECC, and toddler. The search terms were used for title, abstract, and where possible full text. As the term and case definition for early childhood caries was adopted in 1998 (29), the literature search was limited to sources published in the English language spanning from 1990 to 2019. Databases searched included PubMed, Medline, Cinahl, Scopus, Cochrane Library, and the Library Catalog of the University of Manitoba. Similar search strategies were used to identify web resources using the Google search engine. Known publications on ECC that were not identified by the electronic search were also considered.

For the purpose of this review, ECC was defined according to American Academy of Pediatric Dentistry's case definition (1). Studies were included if they involved children <72 months of age, involved Canadian children and either focused on ECC, reported the prevalence of caries in the primary dentition (i.e., ECC, dmft > 0, dmfs >0), examined the risk factors for ECC, investigated the associated microbiome with modern techniques, or discussed associations between ECC and nutritional status and well-being. Studies relating to parental reported ECC were not included (27, 30). In depth assessments were restricted to those studies that employed logistic regression analysis to investigate the relationship between ECC and risk factors or nutritional status and quality of life. Studies exploring the oral microbiome were also reviewed in detail.

Common risk factors for ECC investigated by Canadian studies were identified with variables grouped into 15 overarching categories: childhood age, sex, SES, community of residence, family characteristics, ethnicity, parental beliefs, prenatal nutrition, child behaviors, feeding behaviors (e.g., bottle-feeding and breastfeeding), dental history, enamel hypoplasia, tooth debris score, fluoride exposure, and oral health behaviors (e.g., brushing habits). SES risk factors included any demographic characteristics relating to the level of parental education and annual household income. Family characteristics encompassed variables related to the family size or composition and whether the caregiver had legal custody of the child.

#### RESULTS

A total of 36 published Canadian studies were identified and reviewed in detail; 27 reporting prevalence, 11 reporting associated risk factors following logistic regression analyses, six exploring associations with nutrition and well-being, and one involving the oral microbiome (**Table 1**). Twenty-one of the studies reviewed were cross-sectional in nature, seven were case-control studies, three were randomized control trials, three were retrospective chart reviews, and two studies employed a prospective cohort design. A total of 14 studies involved

*(Continued)* ECC in

Canada: Burden and Risk Factors

Pierce et al.

# Frontiers in Public Health | www.frontiersin.org

#### TABLE 1 | Continued

ECC in

Canada: Burden and Risk Factors

#### TABLE 1 | Continued

*(Continued)* ECC in

#### TABLE 1 | Continued

Indigenous children (i.e., First Nations, Inuit, or Metis), six included children of newcomers (immigrants and refugees) to Canada, and 11 were with ethnically diverse populations.

Among the entire number of studies reviewed, only 14 incorporated multiple logistic regression into their analysis to investigate the presence of any significant relationships between ECC and several associated variables (**Table 2**). Eleven of these studies focused their analysis on risk factors that may contribute to the onset of ECC, while three examined how severe forms of ECC are associated with underlying nutritional status of affected children.

Overall, the prevalence of ECC in the literature reviewed ranged between 0 and 98.9% (**Table 1**). Many of the identified publications involved preschool children from Manitoba (n = 16). As seen in **Table 1**, the prevalence of ECC appears to be high among Indigenous children, often affecting 85% of children or more. Prevalence was also considerably high among children from newcomer communities reaching as high as 79.5%.

Among the 27 studies reviewed that reported on the prevalence of ECC, seven also reported the prevalence of S-ECC. The average rates of S-ECC are lower than that of ECC, however, prevalence of S-ECC still varied greatly depending on the communities and participants involved (range: 21– 95.8%). In one First Nation community, the prevalence of S-ECC among Indigenous children ranged from 81.9 to 95.8%. By contrast, the prevalence of S-ECC from several different communities including Hutterite, Indigenous, and immigrant or refugee families in southern Manitoba ranged as low as 21% to as high as 42.4%.

#### Risk Factors

Childhood age is a recognized predictor of ECC and six of the reviewed Canadian studies considered it as a risk factor for ECC (**Table 3**). In 2007, a retrospective chart review to determine the prevalence of preschool dental decay reported that children who did not have their first dental visit before 24 months of age had increased odds of developing decay (40). These findings were further supported in a subsequent prospective study conducted by Schroth et al. (50) where they discovered that infants aged ≥14 months of age at the time of their first dental examination were significantly more likely to have ECC. Similarly, a 2010 study investigating the prevalence of ECC among Hutterite preschool children reported that childhood age was the strongest independent predictor of ECC (OR = 3.49) (47). More recently, Azrak et al. (11) found that older children had a mildly greater risk for developing ECC. Lastly, logistic regression analysis used in a serial cross-sectional study among four Manitoba communities revealed that childhood age was significantly related to S-ECC (**Table 2**) (51).

Another potential risk factor for caries development that was investigated among some of the Canadian studies was the sex of the child. However, out of five studies that employed logistic regression to investigate this relationship, only one 2007 study found males to be at 38% greater risk for developing ECC than females (**Tables 2**, **3**) (40).

Three studies examined the dental history of children as a potential risk factor for caries development (**Tables 2**, **3**). Children with a baseline decayed and filled surface (dfs) score of ≥5 were 4.88 times more likely to have caries over a 2 year interval vs. those whose dfs score was between 0 and 4 (45). In addition, one publication reported that children with a history of missed dental appointments had an 82% greater risk for developing ECC (OR = 1.82) (40). However, a more recent study did not find the location at which dental care was received to be a significant risk indicator for caries (11).

Three studies observed the relationship between debris score and ECC (**Table 3**). Two of these studies did not find the association to be statistically significant. However, one documented that the presence of debris on primary teeth was significantly and independently associated with ECC and S-ECC (11).

Enamel hypoplasia has been identified as additional risk factor in ECC development. Two studies reported that enamel hypoplasia was significantly and independently associated with ECC (**Table 3**). This was first verified in a prospective cohort study where they found that infants with enamel hypoplasia in the form of pits and missing enamel were significantly more likely to have ECC (50). Another study reported that children with enamel hypoplasia were 6.1 and 3.9 times more likely to have ECC and S-ECC, respectively (11).

Specific behavioral factors were categorized and examined for any relationships with ECC. One study investigated difficult child behaviors as a potential risk indicator for caries and found it to be significantly associated to the onset of ECC but not S-ECC (**Table 2**) (41). Three studies also considered how different feeding practices may contribute to ECC development; two of which were reported to be significant (**Table 3**) (10, 41, 44). Certain behaviors such as the bottle propping, the frequency of snack consumption, or having liquids in the mouth for prolonged periods of time were associated with ECC, however the results remain mixed. Lastly, behaviors related to child oral health practices were explored by two studies as possible risk indicators for ECC (**Table 3**). One reported that children who had difficulty brushing were significantly more likely to get ECC but not S-ECC (41). The other reported that independent brushing by the child did not contribute to the onset of ECC (47).

Four studies have considered the influence of caregiver beliefs and attitudes on the incidence of ECC in preschool children (**Table 3**). In 2007, Schroth et al. (38) found that children whose caregivers who believed it is safe to allow an infant to nurse throughout the night in bed were 45% less likely to experience decay in the form of caries(OR = 0.55). In addition, parents who believed that rotten teeth could impact their child's health were more than four times as likely to have children with ECC (OR = 4.33). However, whether parents agreed with the practice of bottle-feeding children after 1 year of age was not associated with ECC (**Table 2**) (38).

Certain socioeconomic factors such as low household income and the level of parental education or employment status can significantly increase the threat of caries development. Among these factors, two studies specifically assessed whether low annual household income is a risk indicator for both ECC and S-ECC TABLE 2 | Identified risk factors for ECC in Canadian studies.

#### TABLE 2 | Continued

#### TABLE 2 | Continued

*OR, Odds ratios; RR, Relative risk.*

(**Table 2**). In each instance, a lower household income increased the strength of an association with both forms of caries (23, 40). These findings were further supported in a cross-sectional study of 349 Inuit children that documented a higher family income as a significant protective factor against caries onset. Four studies also investigated the relationship between paternal education and employment status with presence of decay. Schroth and Cheba (40) did not find any significant differences between maternal employment status and deft scores. Similarly, no associations were observed between ECC and the mother's level of education when logistic regression was performed on participants from a rural Manitoban community (10). This finding was further supported by a RCT conducted with children in Ontario, where they did not find the level of parental education to be related to the child's development of ECC (OR = 1.27, p = 0.138) (45). These results were in sharp contrast to a subsequent pilot study investigating the relationship between vitamin D and S-ECC, which reported that children with parents whose educational attainment was ≤ grade 12 were 9.3 times more likely to have S-ECC (49).

Specific characteristics of the families children belonged to were also assessed for the presence of any significant associations with ECC (**Table 3**). Three studies considered the impact of family size on a child's likelihood for developing ECC. Neither Schroth and Moffatt (10) nor Lawrence et al. (45) found that children from larger families were at increased risk for developing ECC (**Table 2**). These findings were further supported by a pilot study of Hutterite children in southwest Manitoba (OR = 1.54, p = 0.10) (47). However, a subsequent regression model that controlled for childhood age did report statistical significance between family size and ECC (OR = 1.94) (47). One study reported that children coming from single parent households were more likely to be caries-free than those living with two parents (40).

The same pilot study of Hutterite preschool children did not find any significant association between the maternal rating (fair/poor/very poor) of their child's teeth and ECC (OR = 4.06, p = 0.17) (47). However, when age was excluded from regression analysis, low maternal ratings of childhood oral health were 7.49 times more likely to develop ECC (47). Since then, other studies have reported similar findings where lower parental ratings of their child's general or oral health was associated with a greater likelihood of experiencing caries (11, 23).

An in depth analysis on the prevalence of caries was conducted in preschool children under the care of the Children's Aid Society of Toronto (CAST), a not-for-profit agency that provides alternate care for young abused or neglected children. The results suggested that the period of time spent under CAST care did not significantly influence the risk of having S-ECC (OR = 1.29, p = 0.73) (43). However, they found that having permanent guardianship status of the children in care was protective against ECC development but not S-ECC (OR = 0.14, 0.22) (43). Conversely, an increase in the number of times children were admitted to CAST care was protective against the onset of S-ECC but not ECC (OR = 0.16, 0.42) (43).

One study investigated how differential access to dental care is related to ECC (44) (**Table 2**). This study was conducted on Portuguese-speaking immigrants in Toronto and revealed that children with ECC were more likely to be from families without reliable access to dental care and often lacking dental insurance.

Two studies analyzed the association between ECC and community of residence (urban/rural). One determined the prevalence of ECC among children accessing a community dental clinic and found that the prevalence of ECC among children from Winnipeg did not differ significantly from those residing in rural Manitoba (**Table 2**) (40). Alternatively, the other reported that the prevalence of ECC differed significantly between a southern First Nation and Thompson and a northern First Nation and Thompson, but not between the two urban centers investigated (51). In addition, significant differences in S-ECC were observed between the southern First Nation and Thompson, the northern First Nation and Thompson, but not between Winnipeg and Thompson (51).

Fluoride exposure or the lack thereof was investigated by several studies as a potential risk factor for ECC. A RCT reported that the scheduled application of fluoride varnish (FV) over a 2 year interval led to an 18.3% reduction in ECC among First Nation children and 24.5% reduction in the overall study population (45). Logistic regression further revealed that participants in the FV treatment group were 1.96 times less likely to have caries than comparable controls (45). By contrast, the presence of fluoridated water was not found to be protective against ECC or S-ECC development in another included study (41).

#### Nutrition and Well-Being

Recently, more robust analysis involving logistic regression performed by our group has validated these initial findings of associations between ECC and nutritional health and well-being (**Table 2**). In 2013, a case-control study involving nearly 300 preschool children and documented that children with S-ECC were nearly twice the odds of having low ferritin and over six times more likely to have IDA than caries free children (22). The authors further extended their nutritional analysis to investigate the relationship between caries and vitamin D status. They reported that S-ECC was significantly associated with lower levels of vitamin D and elevated levels of parathyroid hormone (PTH) (23, 49). In 2014, a prospective study further supported the relationship between caries and vitamin D status as they found that low maternal prenatal vitamin D levels were associated with an increased risk of caries in infants (50).

#### Microbiome

Only one study was identified that explored the composition of the oral microbiome of children with S-ECC (**Table 1**). This case control study involved First Nations and Métis children with and without ECC (54). The microbiome analysis of the 16S rRNA gene identified 10 phyla, 95 genera, and 290 species (54). The alpha (Within-sample) diversity analysis did not show any differences in species richness and phylogenetic diversity between groups (54). However, the beta diversity analysis revealed a significant cluster of samples according to cariesstatus (caries-free vs. S-ECC) (54). Taxonomic classification revealed that the levels of 28 species were significantly different between the groups (54). The caries-free group had 5 and 2-fold higher abundances of Streptococcus gondonii and Streptococcus sanguinis, respectively (54). Conversely, the S-ECC group had 7 and 9-fold higher levels of Haemophilus species (HOT 036) and Porphyromonas species (HOT 284) (54). Further, Veillonella species (HOT 780) was 4.6 times higher in the S-ECC group (54). Streptococcus mutans was detected in both groups, but was three times higher in the S-ECC group (54). These findings indicate that S-ECC is related to the structure of the plaque microbial communities.

## DISCUSSION

This review reveals that there have been numerous investigations in Canada on ECC over the last two decades. Many of the studies involved populations often to be considered at high risk for caries, including Indigenous children, those from disadvantaged communities, and newcomer populations to Canada. Unfortunately, there have been no national representative samples to study the true prevalence of ECC in the Canadian population. In the absence of such data, we must rely on regional studies, review national surveys of parental reported ECC in specific populations, or look to pediatric dental surgery under general anesthesia to treat ECC as a proxy measure for the burden of disease in the infant and preschool population in Canada (3, 27, 28).

Despite all the advancements in preventive dentistry, ECC continues to be the most common reason for pediatric day surgery in Canadian hospitals and surgical centers (3). While the average national rate for surgery under general anesthesia to treat caries is 12.1/1,000 children, it is apparent that rates are considerably higher in certain regions of Canada, including rural and remote northern communities, where rates can exceed 100/1,000 children (3, 28). Children living in communities with a high proportion of Indigenous persons are nearly eight times more likely to undergo dental surgery for ECC while those living in rural regions are over three times as likely (3). In addition, children from the least affluent communities are 3.7 times more likely to undergo rehabilitative dental surgery than children from more affluent communities (3).

SES is a well-recognized determinant of oral health and was identified as a risk factor in several of the Canadian studies reviewed. Poverty, inability to pay for or lack of dental insurance can limit access to primary dental care and prevention and increase the risk for ECC and complex dental treatment (3, 4, 57). It can also prevent families from purchasing nutritious foods and oral hygiene supplies, which prevents parents from adopting dental friendly routines at home (8). Parental education and employment status are also some of the social determinants that influence caries development (58). Unfortunately, oral health is not part of Canada's universal healthcare system.

Some of the Canadian studies reviewed provide evidence that past oral health status and the presence of plaque are associated with ECC. Previous caries experience is actually the strongest predictor of future caries (59, 60). Unfortunately, there is considerable variability in what clinical assessments (e.g., plaque/debris levels, developmental defects of enamel) are made during examinations of preschool children in research studies. In fact, only two studies examined enamel hypoplasia as a risk factor, with both finding that these developmental defects of enamel are strongly associated with increased caries risk (11, 50). For many years, enamel hypoplasia has been an underappreciated risk factor for ECC, but there is increasing awareness of its contribution to the caries process as it is easily colonized by cariogenic microorganisms, which allows the caries process to progress more rapidly in these areas as either enamel is thinner or missing (50, 61–64). Future epidemiological studies into ECC should also collect clinical measures of enamel hypoplasia to understand its prevalence, role, and to identify those factors that are associated with its increased prevalence.

Infant feeding practices, such as bottle-feeding and breastfeeding, are complex processes that are difficult to investigate in typical studies on ECC (65). The lack of standardized questioning on these practices and the degree of breastfeeding (e.g., exclusive breastfeeding, partial breastfeeding, mixed feeding with expressed breastmilk), pose challenges as does the fact that such questioning can also be subject to recall bias. Many studies have not properly controlled for other potential modifiers such as the introduction of solids, other dietary behaviors, vitamin D supplementation, and the child's oral hygiene routine (65). While breastfeeding has sometimes been mistaken as a risk factor for ECC in the past, it is actually protective and associated with lower odds for caries (1, 27, 66, 67). However, breastfeeding beyond 24 months of age has been reported to be associated with an increased risk for ECC (68, 69).

Several Canadian publications have reported on the association between ECC and childhood nutritional health status and well-being and have added to our understanding of the oral-systemic relationship (22, 23, 49, 55, 56). The first Canadian report on the potential association between S-ECC and malnourishment suggested that many children with S-ECC suffered from low ferritin and met the definition for both iron deficiency (ID) and iron deficiency anemia (IDA) (21). Low maternal prenatal vitamin D concentrations was identified as a risk factor in one Canadian study (50). Since then, other investigators have also identified that vitamin D levels and prenatal vitamin D intake are associated with increased risk for ECC (70–72). In the few years it has been revealed that children with S-ECC are more likely to have lower serum levels of vitamin D, lower iron concentrations, and be both ID and have IDA than caries-free children (22, 23, 49). In many of these children these nutritional deficiencies actually co-exist (55). This provides more evidence that ECC is not just about teeth. Canadian children with S-ECC are also known to have higher BMI z-scores than caries-free counterparts. Current research is underway with our team to see whether nutritional status and well-being improve for these children following rehabilitative dental surgery under GA.

The advancement of modern microbiological techniques is undoubtedly enhancing our understanding behind the composition of the microbiome and risk for ECC. While only one Canadian study was identified, the field continues to grow (54, 73, 74). This will inevitably lead to future discussions on incorporating microbiological assessments into caries risk assessment (CRA) and risk prediction at the individual level (74, 75) Current research funded by the Canadian Institutes of health Research is underway to determine the role of taste genes and functional plaque microbiome in caries risk in young children in Manitoba Canada.

CRA is garnering increasing attention and is assisting in shifting our approach to managing caries from a restorative approach one that is non-restorative and minimally invasive. CRA can assists dental providers in tailoring clinical care decisions unique to the individual (76). It is vital that dental professionals familiarize themselves on how to undertake regular CRA of their young patients. CRA tools can also be used by non-dental primary healthcare professionals to screen children, determine their caries-risk, and provide prevention services, including fluoride varnish and anticipatory guidance. Several dental and pediatric organizations have developed CRA tools that can be used to help guide practitioners in determining someone's likelihood of developing caries. As parental belief and values can influence whether caries risk, it might be prudent to consider incorporating questions into CRA tools (38).

Early visits offer tremendous hope to curbing the problem of ECC. While there is growing awareness of the importance for such preventive dental practices, not all Canadian children are benefiting (77–80). Professional dental organizations, including the Canadian Dental Association call for the first dental visit no later than 12 months of age (81). In an attempt to increase dentist and public awareness, the Manitoba Dental Association established its Free First Visit program and the Canadian Dental Association introduced its First Visit First Tooth initiative (77–79).

As previously mentioned, many of the studies assessed in our review focused on Indigenous children, those from newcomer families, and those from disadvantaged communities, all who are known to have a higher burden of ECC than many other Canadian children. Different populations can have different risk factors for ECC as cultural practices and beliefs can play a role. However, one thing that is often common between our diverse at-risk populations is limited access to care and early childhood oral health promotion. Several programs and early childhood oral health initiatives are underway in regions of Canada. The federal Children's Oral Health Initiative is focused on improving the oral health status of young First Nations and Inuit children in Canada by emphasizing prevention and minimally invasive approaches to caries management over traditional restorative methods (82).

The Healthy Smile Happy Child (HSHC) initiative in Manitoba, Canada is a well-established, multidisciplinary partnership that works to address the problem of ECC while also considering the contributing health determinants (16, 51, 83, 84). HSHC is guided by three key pillars; (1) community engagement and development, (2) knowledge exchange, and (3) research, evaluation, and quality improvement (51, 85).

Key objectives of the HSHC initiative are to (1) promote the initiative and gain community awareness and acceptance of the importance of early childhood oral health, (2) use existing early childhood and family focused community-based programs, services and activities to deliver the oral health promotion and ECC prevention activities, and (3) recruit and train natural leaders, including service providers, to assist in program development and to deliver the ECC prevention program on an ongoing basis (51, 84). Further goals are to (4) scale-up capacity within existing programs and communities to assist in the sustainability of the promotional and educational program; and 5) determine the impact this would have on preschool oral health, parental knowledge, and attitudes regarding ECC, and knowledge of existing services and health care providers of the importance of prevention (51, 84). Evidence arising from the HSHC initiative's community development experiences over the past 18 years reveal that their approach is successful in improving parents' and caregivers' knowledge, attitudes, and behaviors toward early childhood oral health and results in significant reductions in caries scores and the prevalence of S-ECC over time (51, 83).

During our review of the Canadian ECC literature, it became apparent that there are some limitations with the Canadian literature. Many studies are cross-sectional in nature, with many being convenience samples of children and parents. A significant challenge with comparing risk factors between studies is the fact that investigators are not using a standardized set of questions or survey instruments. This means that different investigations into the same risk factors may yield differing findings even with the same population. The phrasing of questions into feeding and lifestyle behaviors are extremely variable. Further, not all studies are consistently looking at the risk factors. There is a lack of consistency in how questions about behaviors are being asked, which means that there is no uniformity in how risk factor variables are defined and measured between studies.

While there is finally consensus on how ECC and S-ECC are defined (1), there still is a lack of consensus of what is recorded as caries in epidemiological studies. The World Health Organization recommends that caries be diagnosed if pit and fissure or smooth surface lesions are cavitated and does not record incipient lesions as caries (86). This can result in an underestimation of the actual caries burden in high-risk children. While the recent Bangkok Declaration confirms the clinical definition of ECC, it does not speak to S-ECC (87, 88). However, S-ECC is still an important outcome to track in populations known to be at high risk for caries.

Going forward, researchers would be encouraged to try to use validated survey tools to help standardize data collection and analysis. Clinical researchers should also identify and record non-cavitated caries lesions. Lastly, researchers should continually strive to undertake more robust data analyses, such as multivariate regression (e.g., multiple logistic regression for ECC), to control for confounding variables.

#### CONCLUSION

Current literature reveals that many Canadian children are affected by ECC. The development of ECC appears to be strongly associated with social determinants of health including low household income and the level of parental education or employment status. Associations were also observed between ECC and the child's age at first dental visit and parental beliefs about child's oral health. Children with enamel hypoplasia are also at significantly greater odds for experiencing caries. Future research should include assessments of developmental defects of enamel to better understand the association between enamel hypoplasia and ECC. Multiple logistic regression should become

#### REFERENCES

standard practice to identify true risk factors for ECC as this methodology can help to control for confounders.

#### AUTHOR CONTRIBUTIONS

AP and SS contributed to design, acquisition, analysis, and interpretation, drafted manuscript, critically revised the manuscript, gave final approval, and agrees to be accountable for all aspects of work ensuring integrity and accuracy. JL contributed to design, drafted manuscript, contributed to interpretation, critically revised the manuscript, gave final approval, and agrees to be accountable for all aspect of work ensuring integrity and accuracy. VC drafted manuscript, critically revised manuscript, gave final approval, and agrees to be accountable for all aspects of work ensuring integrity and accuracy. CG contributed to acquisition, critically revised manuscript for important intellectual content, gave final approval, and agrees to be accountable for all aspects of work ensuring integrity and accuracy. RS contributed to conception and design, contributed to acquisition, contributed to analysis, contributed to interpretation, drafted the manuscript, critically revised the manuscript, gave final approval, and agrees to be accountable for all aspect of work ensuring integrity and accuracy.

#### ACKNOWLEDGMENTS

RS holds a Canadian Institutes of Health Research Embedded Clinician Researcher salary award in Improving access to oral health care and oral health care delivery for at-risk young children in Manitoba. Operating funds for this research were provided through RS's CIHR Embedded Clinician Researcher program funds.

in a First Nations community. Can J Public Health. (2006) 97:237– 40. doi: 10.1007/BF03405594

**Conflict of Interest:** 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.

Copyright © 2019 Pierce, Singh, Lee, Grant, Cruz de Jesus and Schroth. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

# Syria Profile of the Epidemiology and Management of Early Childhood Caries Before and During the Time of Crisis

#### Easter Joury\*

Centre for Dental Public Health and Primary Care, Institute of Dentistry, Queen Mary University of London, London, United Kingdom

#### Edited by:

Maha El Tantawi, Alexandria University, Egypt

#### Reviewed by:

Metin Güngörmü ¸s, University of Gaziantep, Turkey Hams Hamed Abdelrahman, Alexandria University, Egypt

> \*Correspondence: Easter Joury<EMAIL_ADDRESS>
#### Specialty section:

This article was submitted to Children and Health, a section of the journal Frontiers in Public Health

Received: 30 April 2019 Accepted: 09 September 2019 Published: 24 September 2019

#### Citation:

Joury E (2019) Syria Profile of the Epidemiology and Management of Early Childhood Caries Before and During the Time of Crisis. Front. Public Health 7:271. doi: 10.3389/fpubh.2019.00271 Syria has witnessed the greatest humanitarian crisis of forcibly displaced population since World War II. The present review aimed to outline Syria's profile of the epidemiology and management of early childhood caries (ECC). Before the crisis, the burden of ECC amongst Syrian pre-schoolers had been growing in prevalence and severity. Comparable data showed an increase in the burden of ECC amongst Syrian children aged five years, rising from 74% in 1991 to 81% in 2011, with a dmft value of 8.6. A similar increase was observed in the burden of ECC amongst Syrian children aged three years, rising from 50% in 1991 to 56% in 2011, with a dmft value of 6.1. Whilst there are no data on the burden of ECC during the current crisis, estimates could be extrapolated from data on the current burden of dental caries amongst Syrian primary school children living inside Syria or in informal settlements outside Syria. Such data suggested that the burden of ECC might have further increased amongst Syrian pre-schoolers during the crisis time. This is due to the crisis exacerbating effect on ECC risk factors, in terms of increasing the existing high sugar intake amongst Syrian pre-schoolers as well as increasing different barriers Syrian families face to fresh foods, sugar-free medicines, oral hygiene and fluoride products and accessing essential preventative dental care. Tackling the growing burden of ECC amongst Syrian pre-schoolers should not be postponed till post-crisis time. The seed work for relevant public health interventions could start and be embedded in different health and social initiatives taking place during the time of crisis. A number of public health interventions informed by relevant international and local (Syrian) studies conducted during the time of crisis have been suggested to tackle the burden of ECC amongst Syrian young children. They include a mix of upstream, midstream, and downstream interventions that aim to reduce sugar intake, improve feeding and oral hygiene practices, increase access to an appropriate source of fluoride and build the capacity of the Syrian dental and wider workforce to tackle the growing burden of ECC in Syrian pre-schoolers.

Keywords: Syria, early childhood caries, oral health, pubic health interventions, humanitarian crisis

## BACKGROUND

Syria is a Mediterranean country located in the Middle East, with a population of nearly 24 million people. Before the crisis, Syria was classified as a middle income country, with a health profile characterized by a high burden of non-communicable diseases (NCDs), including obesity, cardiovascular diseases, type 2 diabetes, and dental caries. Syria had a universal health care system with a vaccination coverage of nearly 99% (1).

Recently, Syria has witnessed the greatest humanitarian crisis of forcibly displaced population since World War II. According to the UNHCR, the recent marked increase in the global population of forcibly displaced people was driven mainly by the Syrian crisis (2). The latter has resulted in more than 13 million Syrians displaced within and outside Syria, of which over 5 million refugees are in neighboring countries: Lebanon, Jordan, Iraq, Turkey and Egypt (2). More than half of these refugees are children (2).

The present review aimed to outline Syria's profile in terms of the epidemiology and management of early childhood caries (ECC). More specifically, the objectives of the current work were to:

This review of literature searched MEDLINE via PubMed through August 2019. The following key words were used for the PubMed search: Syria∗ and (oral or dent∗ ). Additionally, other resources of gray literature relevant to oral health in Syria were searched. There was no language restriction.

#### PREVALENCE, TREND, AND IMPACT OF ECC IN SYRIA BEFORE THE TIME OF CRISIS

Before the current crisis, Syria, like other countries in the Middle East, had a high burden of dental caries amongst children aged 5 years and under. Few studies have been conducted to estimate this burden. They varied in their methodological approaches and rigor. Most of them used the World Health Organization criteria for caries diagnosis and were conducted in Damascus (the capital city). Very few studies were carried out in other cities (e.g., Latakia and Aleppo). There are no Syrian national dental health survey data for pre-schoolers.

Taking into consideration the aforementioned limitations in terms of the quantity and quality of available (published and unpublished) studies, and using "comparable" data to make inference on ECC trends, it seems that the burden of ECC amongst Syrian 5-year-olds had been increasing from 74% in 1991 (3) to 81% in 2011 (4), with a dmft value of 8.6. The prevalence of severe ECC among pre-schoolers at the age of five was 77% (4). Amongst 3 year old Syrian children, a similar increase in the prevalence of ECC had been observed, rising from 50% in 1991 (3) to 56% in 2013 (4), with a dmft value of 6.1. The majority of pre-schoolers had untreated ECC (dt) (3, 4).

The impact of ECC on the quality of life of Syrian young children and their families was reported in a cross-sectional study (4). The latter used the Arabic version of Early Childhood Oral Health Impact Scale and included a sample of Syrian preschoolers with ECC aged between 3 and 5 years. The most frequently reported impact of ECC (experienced occasionally, often or very often) was pain (75%) followed by family feeling upset (52%) and having difficulty to chew food (48%).

#### PREVALENCE, TREND, AND IMPACT OF EARLY CHILDHOOD CARIES (ECC) IN SYRIA DURING THE TIME OF CRISIS

During the Syrian crisis, no studies have to date been conducted to estimate the burden of ECC amongst pre-schoolers (including those who have or have not been internally or externally displaced). Emerging evidence from protracted Syrian refugee informal settlements in Lebanon suggests that the burden of ECC might have increased amongst refugee pre-schoolers. Such estimation is based on the findings related to the burden of dental caries amongst older Syrian children attending refugee primary schools in Bekkaa, Lebanon (5). The prevalence of dental caries has hit a record high of over 90% amongst these children. Oral pain was reported by 57%, of which 55% had moderate to severe oral pain and 38% had oral pain for more than a month (5). Furthermore, 9% had dental abscess. The difference in the number of teeth with untreated dental caries between children in a protracted displacement situation and those who have been displaced for <5 years was highly statistically significant (5). This suggested that protracted displacement might lead to an increase in the burden of dental caries amongst children and the deterioration of their oral health. Similar findings were reported by another study conducted on a small convenience sample of Syrian refugee children aged 6–12 years at al-Zaatari camp in Jordan (6).

Indeed, when comparing oral health between Syrian refugee children and their counterparts who had not been displaced or had been internally displaced within Syria it appears that the former had a much higher burden of dental caries compared with the latter. For example, a recent cross-sectional survey (7), conducted on Syrian children aged 8–12 years living in Damascus, reported 79.1% caries prevalence. The latter is more than 10% lower than the caries prevalence found amongst Syrian refugee children of the same age group (5). It is worth mentioning that Damascus is one of the Syrian cities that have had the highest prevalence of dental caries and now is hosting a mix of children that had not been displaced as well as children who had been internally displaced in Syria. This implies that the prevalence of oral diseases amongst Syrian refugee children in low and middleincome countries is much higher than the highest prevalence of oral diseases found in the country of origin (Syria). In other words, the Syrian crisis affected negatively the whole Syrian child population on a scale of intensity that is proportionate to the extent of displacement.

Syrian refugee caregivers had voiced strong concerns about their children's oral health in humanitarian settings and its considerable impact on families (8). Child's dental pain had been repeatedly reported to cause considerable distress for Syrian refugee parents (and children) and served as a trigger for deeper feelings of anger, frustration and helplessness (8). This might explain why international humanitarian organizations such as the UNICEF and UNHCR have become highly interested in addressing the burden of dental caries amongst displaced and refugee children (9, 10).

#### RISK FACTORS FOR ECC AMONGST SYRIAN CHILDREN

A number of studies explored the proximal (behavioral) and distal (social) risk factors of ECC amongst Syrian pre-schoolers. Behavioral risk factors focused on poor feeding practices, high sugar intake, poor oral hygiene, limited exposure to an appropriate source of fluoride and low dental care utilization. The role of the current Syrian humanitarian crisis as an exacerbator for ECC risk factors was noted in the literature.

#### Poor Feeding Habits Amongst Syrian Pre-schoolers

Although breastfeeding is the most common type of infant feeding in Syria some poor feeding practices were identified.  The use of exclusive bottle feeding was more common amongst working mothers (11). Nearly 50% of Syrian infants who used the bottle were put to sleep with the bottle (11, 12), increasing therefore the risk of having ECC. Additionally, other poor infant's feeding practices such as the prolonged use of bottle-feeding (beyond the child's first birthday) were identified among Syrian pre-schoolers with ECC (12).

#### High Sugar Intake Amongst Syrian Pre-schoolers

A number of studies have highlighted the high intake of sugar (i.e., free sugars) among Syrian pre-schoolers, which tends to start early during their first year of life. Nearly 43% of Syrian infants had high frequency of sugar intake (>4 times a day) (11). Furthermore, 75% had sugar added to their beverages (11). Amongst Syrian pre-schoolers aged 3 to 5 years, 86% had 3–4 meals and/or snacks with high sugar content daily (12).

In regard to child's liquid medicines available on the Syrian market, the vast majority has sugar. The number of sugar-free medicines has dropped during the current Syrian crisis (13). Additionally, a cross-sectional study found that only 18% of Syrian pediatricians were aware of sugar-free liquid medications available on the Syrian market and only 10% prescribed such medications (13).

#### Poor Oral Hygiene and Limited Access to an Appropriate Source of Fluoride Amongst Syrian Pre-schoolers

Less than six percent of 1 year old infants had their teeth cleaned regularly with a toothbrush or piece of clean gauze (11). The percentage of pre-schoolers aged 3–5 years who had their teeth cleaned at least twice a day had increased from 1.4% in 2007 (12) to 12.3% in 2011 (4). Fluoride toothpaste was rarely used amongst Syrian infants (11).

Community-based water or salt fluoridation schemes have to date not been possible in Syria (3). Very few Syrian areas contain naturally fluoridated water at either sufficient levels to protect tooth decay (nearly 1 ppm) or excessive levels that might cause fluorosis (e.g., Palmyra and Alhasak) (3).

A recent study highlighted that preventive oral care products, including fluoride toothpastes, gels, and varnishes, that adhered to evidence-based recommendations were either few in number or not available on the Syrian market (14). Several fluoride toothpastes had fluoride concentrations that were low (i.e., below the effective concentration for caries prevention), or high with potential long-term toxic effects in children. Thirteen toothpastes with fluoride concentration <1,000 ppm claimed to have anticaries effects. Another three fluoride toothpastes did not declare their fluoride concentration. Additionally, 17 toothpastes with high fluoride concentration were available for purchase without prescription and had instructions for use in children younger than the safe evidence-based recommended age. In terms of fluoride gels and varnishes, only three fluoride gels were available (14). No fluoride varnish was found (14), which is known to be more effective than the gels for prevention of dental caries (15). During the current Syrian crisis, the number of preventive oral care products available on the market has decreased and some of the currently available products are still non-adherent to evidence-based recommendations (14).

#### Low Dental Care Utilization Amongst Syrian Pre-schoolers

Low dental care utilization is another risk factor of ECC amongst Syrian pre-schoolers. Less than two percent of young Syrian children had visited the dentist by their first birthday (11).

#### Social Risk Factors of ECC Amongst Syrian Pre-schoolers

A few studies documented social inequalities in ECC amongst Syrian pre-schoolers (4). Socioeconomic inequalities were also identified in the frequency of sugar intake among Syrian infants (11). Infants whose fathers were not working were more likely to have high frequency of sugar intake compared to their counterparts whose fathers were working. Furthermore, Syrian infants whose mothers had low knowledge about infant's oral health behavior or high frequency of sugar intake were more

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likely to have high frequency of sugar intake (11). Mother's knowledge of infant's oral health behavior and her frequency of sugar intake explained the socioeconomic inequality in infant's frequency of sugar intake. This suggested the importance of addressing such factors (i.e., mother's knowledge of infant's oral health behavior and her frequency of sugar intake) to reduce inequalities in pre-schoolers' oral health. The vast majority of Syrian mothers reported the importance of primary teeth (94%) and voiced their desire to receive information about infant's oral health (99%) (11). Only 6% of Syrian mothers reported receiving information about child's oral health (11).

#### The Syrian Humanitarian Crisis as an Exacerbator for ECC Risk Factors Amongst Syrian Pre-schoolers

The Syrian humanitarian crisis has created many political, economic and social negative circumstances that had a profound impact on different living aspects of the Syrian population. The levels of mal- and under-nutrition had increased as a result of the disturbance in food channels during crisis time. For example, many Syrian refugee families mentioned barriers related to the availability and affordability of fresh foods (e.g., fresh fruits and vegetables) (8). The latter is expected in view of complex emergences and disaster context (16). Foods and drinks with high sugar content are usually more available at the camps' tuck shops at affordable prices. Additionally, due to forced displacement the family's daily routine is likely to be negatively affected and parents and carers are more likely to experience loss of control over their children's behaviors. The latter might be one of the reasons behind the increase in children's sugar consumption.

Similar to fresh food, refugee parents and carers face multiple barriers to oral hygiene products and accessing dental care, leading to the deterioration of their children's oral health.

#### RECOMMENDATIONS FOR THE MANAGEMENT OF ECC IN SYRIA

Tackling the growing burden of ECC amongst Syrian preschoolers should not be postponed till post-crisis period. It is acknowledged that there are many barriers to implement public health interventions to tackle the ECC burden in Syria during crisis time as opposed to post-crisis period. Nonetheless, the seed work for such interventions could start and be embedded in different health and social initiatives taking place at the time of crisis.

The following suggestions for public health interventions are not only guided by evidence emerging from international studies, but also and more importantly they are informed by evidence emerging from local studies showing the feasibility, acceptability and preliminary effectiveness and cost-effectiveness of such interventions within the Syrian context during crisis time. Yet, it should be acknowledged that institutionalizing such recommendations and rolling them out across the country during the time of crisis would need further larger national studies dedicated for investigating barriers and enablers to implementing these recommendations on a national scale. The dependency on external aids should be minimized, as such aids are unlikely to create sustainable changes (17).

Syrian oral health strategies should aim to decrease sugar intake, promote good feeding, and oral hygiene practices, increase exposure to an appropriate source of fluoride and build the capacity of the Syrian dental and wider workforce to promote oral health and tackle the growing burden of ECC across multisectoral settings.

A mix of sustainable and affordable upstream, midstream, and downstream interventions are recommended. The principles of propionate universalism (18) should guide the roll out of suggested interventions to ensure that the scale of their delivery is proportionate to the intensity and levels of needs.

#### Reducing Sugar Intake Amongst Syrian Pre-schoolers

Reducing sugar intake would not only improve the oral health of Syrian pre-schoolers, but also it would improve their general health. High sugar intake is a common risk factor for child's mal-/under-nutrition and dental caries.

The main effective and cost-effective means to reduce sugar intake amongst Syrian pre-schoolers is to develop and implement public health policies with related regulations and legislations. The following is evidence-based recommendations to inform governmental leaders and policymakers regarding potential public health policies and strategies to reduce sugar consumption particularly amongst young Syrian children.

The Syrian government should formulate country-specific goals to decrease the high levels of sugar consumption and reach the latest recommended maximum of 5% of total energy (19). This equates to ∼22 g/day for 4–6 year olds and 16 g/day for 1–3-year-old children (20).

Furthermore, the Syrian government should adopt the Health in All Policies (HiAP) framework. The latter would aid in developing intersectoral partnership among the Syrian ministries and yield large returns on investment as a result of targeting a common risk factor (i.e., high sugar intake), and preventing thereby a spectrum of childhood diseases (e.g., dental caries, malnutrition and obesity) (21, 22) as well as other sugar-related NCDs that young children are likely to develop over the life course (e.g., adulthood obesity, type 2 diabetes and dental caries) (23, 24). The HiAP approach should include:

the sugar content in their products and offer a wide range of sugar-free alternatives (25). Appropriate legislations are needed to support such efforts. Additionally, clear and unbiased labeling is key. Products containing more than 2.5% free sugars should be labeled as "high."

#### Promoting Good Feeding and Oral Hygiene Practices and Increasing Exposure to an Appropriate Source of Fluoride Amongst Syrian Pre-schoolers

Public health interventions should aim to promote good feeding and oral hygiene practices as well as increase exposure to an appropriate source of fluoride amongst Syrian pre-schoolers. Fluoride toothpaste might be the only vehicle that could provide Syrian infants and pre-schoolers with access to fluoride (28). However, this should not cease efforts to explore the feasibility of salt or water fluoridation schemes in Syria. Water fluoridation mapping and feasibility studies were conducted in Syria during the 1980s and thus they are quite dated now. The following is evidence-informed recommendations based on a number of recent local studies (14, 28–30):

• Running community-based programmes to establish toothbrushing with fluoride toothpaste and bottle feeding termination practices amongst Syrian infants: a randomized controlled trail demonstrated the feasibility, acceptability and preliminary effectiveness and cost-effectiveness of such interventions in the Syrian context (28). This trail integrated the intervention within the Syrian national vaccination programme and delivered an oral health promotion package free of charge, without health workers' counseling. The package included an infant oral health pamphlet, a baby toothbrush, fluoride toothpaste (1,000 ppm) and a trainer cup. Infants who received this package were less likely to have old plaque (as a measure of tooth brushing behavior) and more likely to stop bottle-feeding than their counterparts who did not receive the package.

#### Building the Capacity of the Syrian Dental and Wider Workforce to Tackle the Burden of ECC Amongst Syrian Pre-schoolers

As there is "No health without health workforce" (31), it is important to ensure that the Syrian dental workforce has the right capacity and capability to tackle the growing burden of ECC. Before the crisis, there were nearly 20,000 registered Syrian dentists with nearly 2,000 new dental graduates annually. Although there are no data on the current capacity and capability of the Syrian dental workforce it is expected that these two aspects have been negatively affected during the current Syrian crisis. A brain drain of the Syrian dental workforce had taken place during the crisis time. Thus, it is important to develop capacity building strategies and interventions to ensure that the Syrian dental and wider workforce is able to address the burden of ECC in Syria. The following is recommendations based on a number of recent regional and local studies (14, 17, 29, 30):

#### REFERENCES

• Establishing a national team responsible of conducting regular national oral health surveys for Syrian children aged 5 years: this is highly important to monitor the trends in ECC among Syrian children and evaluate the national and local oral health interventions aiming to tackle the ECC burden in Syria.

#### CONCLUSION

Syria has witnessed the greatest humanitarian crisis of forcibly displaced population since World War II. The burden of ECC amongst Syrian pre-schoolers had continued to grow in prevalence and severity. The humanitarian crisis had exacerbated ECC risk factors, in terms of increasing the existing high sugar intake amongst Syrian pre-schoolers as well as increasing different barriers Syrian families face to fresh foods, sugar-free medicines, oral hygiene and fluoride products and accessing essential preventative dental care. The seed work to tackle the burden of ECC could start and be embedded in different health and social initiatives taking place during the time of crisis. A number of public health interventions informed by international and local (Syrian) studies have been suggested to tackle the ECC burden amongst Syrian young children. They include a mix of upstream, midstream, and downstream interventions that aim to reduce sugar intake, improve feeding and oral hygiene practices, increase access to an appropriate source of fluoride and build the capacity of the Syrian dental and wider workforce to tackle the growing burden of ECC in Syrian preschoolers.

#### AUTHOR CONTRIBUTIONS

The author confirms being the sole contributor of this work and has approved it for publication.

Syrian refugee children. J Int Soc Prev Community Dent. (2017). 7:191–6. doi: 10.4103/jispcd.JISPCD\_212\_17

**Conflict of Interest:** The author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Copyright © 2019 Joury. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

# Early Childhood Caries in Peru

Jorge L. Castillo\*, Camila Palma and Ailín Cabrera-Matta

*Department of Dentistry for Children and Adolescents, Universidad Peruana Cayetano Heredia, Lima, Peru*

Early Childhood Caries (ECC) is a global oral health problem, and Peru may be one of the countries with high prevalence of untreated ECC in South America. In this study, we constructed an epidemiologic profile of ECC in Peru through a comprehensive review of published data. The prevalence of ECC, risk factors for it, its impact on child development, and public oral health interventions on ECC have been included. The study revealed extremely high rates of ECC in Peru and significant oral-health disparities. Risk factors for ECC were poverty, high sugar consumption, and low oral health literacy. However, the number of studies is limited and their quality questionable. Oral health has not received high public-health priority in Peru. However, in recent years, new regulations and evidence-based documents (the first Clinical Practice Guideline for the Prevention, Diagnosis, and Management of Caries in Children; the Guideline for Children's healthy Growth and Development; the Law on Healthy Diet; and the Manual on Food Advertising) give hope for the future of infants' oral health in the nation.

Keywords: early childhood caries, dental caries, Peru, oral health education, oral health children, oral health related quality of life

#### Edited by:

*Maha El Tantawi, Alexandria University, Egypt*

#### Reviewed by:

*Nneka Kate Onyejaka, University of Nigeria, Nigeria Nourhan Mostafa Aly, Alexandria University, Egypt*

> \*Correspondence: *Jorge L. Castillo<EMAIL_ADDRESS>
#### Specialty section:

*This article was submitted to Children and Health, a section of the journal Frontiers in Public Health*

Received: *30 April 2019* Accepted: *28 October 2019* Published: *15 November 2019*

#### Citation:

*Castillo JL, Palma C and Cabrera-Matta A (2019) Early Childhood Caries in Peru. Front. Public Health 7:337. doi: 10.3389/fpubh.2019.00337*

#### OVERVIEW OF PERU

Peru is the third largest country in South America, located in the western side of the continent, facing the Pacific Ocean. Peru is divided into three regions: the Andean region; the Amazon jungle; and the coast, facing the Pacific Ocean. The three regions have unique geography, culture, ethnicity, and economic development.

The estimated population of Peru was 31,237,385 inhabitants according to the most recent census (1). Children under 14 years of age constituted 26.4% of the population, and the total population of children 0–5 years old was 3,405,500. Peru is considered a developing country, with upper-middle income economy, according to the World Bank (2).

This article presents an overview of the status of early childhood caries (ECC) in Peru, a country with limited public health resources.

#### EPIDEMIOLOGIC PROFILE OF ECC (PREVALENCE)

Only two national epidemiologic studies on caries in primary teeth have been carried out in Peru. Both studies were designed by the National Center of Epidemiology, Prevention, and Disease Control of the Ministry of Health. The first study, conducted during 2001–2002, found that the prevalence of caries at age 6 years was 87.3% (n = 1,280), with an average dmft (decayed, missing, and filled teeth) of 6.7; the contribution of the decayed component was 6 of 6.7, revealing a high proportion of untreated caries (3). Although this study did not include younger children, results revealed that ECC has been a public health problem in Peru for more than 15 years (4).

The second national study found a caries prevalence of 76.2% in 3–5-year-old children (n = 2,195). The data were collected in all 25 Peruvian cities, across the three regions, between 2012 and 2014. The average dmft at this age range was five, with the decayed component contributing 4.5 to this score (4). Even though this study is the biggest ever conducted in the country and played an important role in better understanding of the extent and magnitude of ECC, the prevalence might be underestimated because WHO criteria were used and initial non-cavitated lesions were not considered. This methodologic problem was evident in three recent studies in Lima, which reported prevalence in two populations: those with and those without non-cavitated lesions (5–7). From those investigators' results, the prevalence of ECC is underestimated by about 11.9–24.8%, depending on the type of population. Severity measures, such as number of affected teeth, are also greatly underrated when cavities are the caries diagnostic threshold.

A selection of studies on ECC prevalence in Peru published in the last 10 years is shown in **Table 1**. More than 50% of the studies were conducted in children 3–5 years old with complete primary dentition. Although sample sizes were small, there were some important findings: Reported prevalence according to WHO criteria is above 70% in all studies, and average dmft is between 3.6 and 5 (6, 9, 11, 13, 14, 16, 17, 20). Data on younger children are sparse; only two studies have reported prevalence on children younger than 3 years (12, 15). Both studies included initial non-cavitated lesions in their criteria for assessment of caries, and they found a prevalence of 65.8 and 46.3% in 1–3 yearold and 6–36 month-old children, respectively. It is noteworthy also that, overall, higher prevalence was found in underserved groups, a finding that is supported by a recent systematic review of parental factors influencing ECC in developing nations, in which socioeconomic status was found significantly associated with ECC in 13 studies (21).

The studies on ECC in Peru, shown in **Table 1**, have limitations. Few of these reports have undergone a peer-review publication process; most are undergraduate theses published in online national repositories. Moreover, many of the reports did not describe the calibration process, and most did not report intra- and inter-Kappa coefficients. Another limitation is that the variation in levels of caries detection limits our ability to compare prevalence rates in cities in Peru and worldwide. Among the criteria used in national studies, we found these: WHO, WHO plus initial non-cavitated lesions, and International Caries Detection and Assessment System (ICDAS) (**Table 1**).

According to the article published by Kassebaum et al. (22), the age-standardized prevalence and incidence rates of untreated dental caries in deciduous teeth in 2010 for both sexes combined in the Andean region, which Peru is part of, was 8.3 and 14,470, respectively. Also, El Tantawi et al. reported that Peru is in the group of countries with highest prevalence of caries in children aged 36–71 months, between 75–100% (23).

Summarizing, dental caries in Peru is the most prevalent disease in school and preschool children and the main reason for external visits in primary healthcare centers. The prevalence and severity of this disease are dramatic, and they increase with age. Since Peru is among countries with the highest prevalence of caries in children in South America, urgent action is needed to reverse this situation.

#### RISK FACTORS OF ECC IN PERU

According to the most recent definition of ECC, made during the ECC consensus meeting in Thailand, in 2018, dental caries is a dynamic and multifactorial disease, mediated by the biofilm and driven by sugar, that results in phasic demineralization and remineralization of the dental hard tissues. Dental caries also is determined by biological, behavioral, and psychological factors.

In this section, we will review the risk factors for ECC that have been studied in our country, considering that the number of studies is limited to specific groups, and extrapolation of the data to the whole population is difficult. We must remember that Peru is a diverse country with high disparities in oral health among the population.

#### Sugars as a Risk Factor for ECC

Latin America has the highest sugar consumption per capita (41.8 kg/years in the 2015–2017 period) among developed and developing regions in the world (24). In Peru, the per capita consumption is about 38.2 kg/years (25). WHO guidelines recommend that intake of free sugars provide ≤10% of energy intake, with further reductions to <5% of energy intake throughout life to protect dental health (26). Peruvian children consume sugars from a very early age (27). According to a study by the National Institute of Health (INS), in 2015, children aged 6–36 months old have a high carbohydrate consumption, averaging 126.7 grams per day. Children consume diverse products that may produce a high risk for dental caries, such as sugar cane, which may be chewed habitually (28), and panatela, a combination of rice and sugars and other components. Parents sometimes add sugars or honey to liquids their babies consume to produce a better flavor, but the parents have little knowledge about the harm these practices do to the dental tissues. Villena and Bernal (29), found that 73% of children started eating sugars in liquid form before 6 months of age; 30% of children under 5 months of age consumed sugars an average of 2.5 times a day, and the rate increased to 4.6 times a day in children 1 year of age. In a study by Castillo et al. (30), most Peruvian children were found to like milk sweetened with some type of sugar, and, whereas only 44% of children liked plain milk, 96% liked sugared milk.

Many studies about the relationship of sugar consumption and ECC in children under 6 years old have been published in Peru. Unfortunately, many of these studies have methodologic problems and uncertainty about representation of the sample. Some studies have found a correlation between ECC and sugar consumption in various forms (27, 27, 31, 32). A study by Flores and Montenegro (33), however, found no relationship between the daily consumption of sugars and ECC, but all the patients were at high risk, which may have biased the results.

#### Oral Hygiene

Peltroche et al. (34) found that among 3- to 6-year-old children with high caries risk, the most common factor was inadequate oral hygiene and visits to the dentist. Diaz et al. (35) found a relationship between poor oral hygiene and ECC in children under 3 years old. According to Rios (36) and Vega (37), the main

#### TABLE 1 | Caries prevalence in children under 6 years old in Peru, 2010–2019.

\**Initial non-cavitated lesions (white spot) included.*

\*\**dmft- decayed, missing, filling per tooth.*

*NR, Not reported.*

tools used for oral hygiene in children under 6 years old was a piece of gauze or a toothbrush.

#### Oral Health Literacy

According to Cupé-Araujo and García-Rupaya (38), 29.2% of Peruvian mothers of infants have deficient or irregular knowledge or oral health. Chambi (39) found that the level of oral health knowledge was poor in young mothers of children under 5 years old; those mothers did not receive any information about oral health when they were pregnant. Benavente et al. (40) found that even with a higher knowledge of oral health in mothers of children under 5 years old (77.6% of mothers had regular and good knowledge of oral health), ECC levels were high. Clemente and Ortiz (12) found that 55.4% of mothers of children under 3 years old did not receive any information about oral health.

#### Nutrition and Dental Caries

Several studies on nutrition and dental caries have been conducted in Peru (41–43). The authors have found that one mild-to- moderate malnutrition episode during the first year of life is associated with increased caries in both the deciduous and permanent teeth. In another study, Delgado-Angulo et al. (44) found that stunting was a significant risk indicator for caries in permanent teeth over a 3.5-years period, independent of other well-known risk factors for caries development. Another study found no correlation between nutrition status and dental caries (45), although others (46) have reported a possible connection between malnutrition, enamel defects, and dental caries.

#### Socioeconomic Factors

Several studies worldwide have found a relationship between dental caries and socioeconomic and education status. The only study that addressed this issue in Peru was that of Delgado-Angulo et al. (47), who found that poverty and social exclusion were associated with dental caries in primary and permanent dentition, and that children living in poor households had 2.25 times more risk for dental caries than did children living in nonpoor households; although this study is the only one published regarding socioeconomic factors and ECC in Peru, the relation between poverty and ECC seems evident.

Despite the small sample size in many of the studies described above, which limits the generalizability of the results in the overall Peruvian population, many risk factors that influence the presence of ECC in Peruvian children have been established.

#### IMPACT OF ECC ON IMMEDIATE AND LONG-TERM GROWTH, DEVELOPMENT, SOCIAL, AND MENTAL HEALTH, AND WELL-BEING

During the ECC Summit in Thailand (2018), dental caries was described as common, usually untreated, and having a deep impact on children's lives. According to Martins et al. (48), dental caries is the main oral condition with the greatest impact on children's quality of life. Several studies have reported the impact of untreated dental caries on the quality of life of preschool children (49, 50). Lopez-Ramos and Garcia-Rupaya (16), using the Early Childhood Oral Health Impact Scale, validated in Spanish, found that ECC had a negative impact on oral health-related children's quality of life. However, there is little information published on the impact of ECC on the quality of life of Peruvian children.

A study by Diaz-Pizan (51) evaluated the quality of life related to oral health before and after dental treatment in children from Lima younger than 6 years of age. The average total score before treatment of children with ECC was 17.89, which decreased to 2.57 after treatment.

#### PUBLIC ORAL HEALTH INTERVENTIONS AND DOCUMENTS

Untreated dental caries is a huge burden for Peru's health economy (52). However, public health policies haven't given priority to oral health, probably because of the greater demands of life-threatening, prevalent diseases. Most community programmes have had no impact on reducing ECC prevalence in Peru, especially in the younger and underprivileged populations.

Fortunately, during the last few years, the Peruvian Ministry of Health has issued official documents on the importance for children's oral health (described below) (53). It remains to be seen if those documents will standardize oral health messages among health professionals and increase the use of protective factors during the first year of life.

#### Community Programs

• In 1985, the Peruvian Ministry of Health approved a resolution to add fluoride to all commercially available salt (200 ppm of sodium fluoride per kg) (54). To date, there is no epidemiological data available on the effectiveness and/or employment of this resolution.

#### New Documents

a healthier diet for all children and regulate commercial food labeling (black and white octagons). All food and beverages that contain high amounts of sugar, sodium or saturated fats, must indicate that in the corresponding octagons on the front of its package. The law was planned in two stages so that industries have time to adapt. The first stage is mandatory from June 2019. It states that all food products containing sugar ≥22.5 g/100 g and beverages containing sugar ≥6 g/100 ml should have a "High in Sugar" Octagon. The second stage, due September 2021, will require all food products containing sugar ≥10 g/100 g and beverages containing sugar ≥5 g/100 mL to have the "High in Sugar" Octagon. Moreover, an ordinance for "Healthy Kiosks" was passed, so that all public schools offer healthy food options for all students inside and outside their premises (61).

#### CONCLUSIONS

Early childhood caries has recently been designated a global health problem (48, 62, 63). Despite limitations and variability across studies that have been conducted in Peru, we believe that

#### REFERENCES

Peru is amongst the countries with the highest prevalence of untreated ECC in the region, with negative consequences on the quality of life of preschoolers. High sugar consumption and oral health disparities (poverty, social exclusion, and low oral health literacy) may contribute to the high prevalence of ECC. From a research point of view, greater effort should be made to standardize methods in studies on ECC prevalence and related risk factors. It is also crucial to include children younger than 3 years old in national epidemiological studies, as was concluded in the recent WHO Global Consultation on ECC (63). Historically, public health policies have not given oral health high priority, but in the past 3 years, new regulations and evidence-based documents project a more favorable view on infant oral health in Peru.

#### AUTHOR CONTRIBUTIONS

JC has worked on the abstract, risk factors, quality of life, and conclusions sections. CP has worked on the abstract, prevention, quality of life, and conclusions sections. AC-M has worked on the epidemiology and conclusions section.

online at: https://busquedas.elperuano.pe/normaslegales/decreto-supremoque-aprueba-el-reglamento-de-la-ley-n-30021-decreto-supremo-n-017- 2017-sa-1534348-4/ (accessed August 20, 2019).

63. Phantumvanit P, Makino Y, Ogawa H, Rugg-Gunn A, Moynihan P, Petersen PE, et al. WHO Global Consultation on Public Health Intervention against Early Childhood Caries. Commun Dent Oral Epidemiol. (2018) 46:280–7. doi: 10.1111/cdoe.12362

**Conflict of Interest:** 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.

Copyright © 2019 Castillo, Palma and Cabrera-Matta. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

# Indonesia: Epidemiological Profiles of Early Childhood Caries

#### Rosa Amalia1 \*, Fania Chairunisa1 , M. Fahmi Alfian1 and Al Supartinah2

*1 Preventive and Community Dentistry Department, Faculty of Dentistry, Universitas Gadjah Mada Yogyakarta, Yogyakarta, Indonesia, 2 Pediatrics Dentistry Department, Faculty of Dentistry, Universitas Gadjah Mada Yogyakarta, Yogyakarta, Indonesia*

The Indonesia government has succeeded in achieving national health development targets and has invested heavily in public health. Many positive results have been achieved, which indicate an increasing number of school-aged children free of caries and a decrease in caries experience scores. However, result of previous studies on early childhood caries (ECC) in pre-school children showed high prevalence and severity. Understanding the link between the epidemiology of the ECC and components of health development is critical for formulating appropriate actions. The purpose of this study is to provide a comprehensive review of the epidemiology of ECC in Indonesia based on the results of the national basic health surveys. The complementary data describes access, utilization and profile of oral health personnel in Indonesia.

#### Keywords: early childhood caries, Indonesia, caries, policy, children

#### Edited by:

*Morenike Oluwatoyin Folayan, Obafemi Awolowo University, Nigeria*

#### Reviewed by:

*Selda Rizalar, Istanbul Medipol University, Turkey Katalin Dr. Papp, University of Debrecen, Hungary*

> \*Correspondence: *Rosa Amalia<EMAIL_ADDRESS>
#### Specialty section:

*This article was submitted to Children and Health, a section of the journal Frontiers in Public Health*

Received: *30 April 2019* Accepted: *15 July 2019* Published: *06 August 2019*

#### Citation:

*Amalia R, Chairunisa F, Alfian MF and Supartinah A (2019) Indonesia: Epidemiological Profiles of Early Childhood Caries. Front. Public Health 7:210. doi: 10.3389/fpubh.2019.00210*

## INTRODUCTION

Dental caries affects people of all ages and remains the major problem of dental health among children worldwide (1). For preschool children, early childhood caries (ECC) defined as the presence of one or more decayed (non-cavitated or cavitated lesions), missing (due to caries) or filled tooth surfaces in any primary tooth in children <71 months of age (2). ECC is highly prevalent (3), associated with multiple risk factor (4), and reduces the quality of life (5). If ECC treatment is delayed, the condition of the child worsens and becomes harder to treat, increasing the treatment cost.

ECC is also highly prevalence in preschool children living in developing countries like Indonesia (6). Every 5 years, the Indonesian government conducts basic health surveillance. There are surveillance reports on oral health and caries in children for the years 2007, 2013 and 2018 (7–9). Unfortunately, direct comparison of data is difficult because the reporting format is not in a same manner for each year. This study will therefore be limited to a comprehensive review of the available data on ECC accessible from the basic health surveillance reports, and data from the scientific publications on ECC in Indonesia. Situational analysis of oral health services in Indonesia will also be explored. This description is intended to be a highlight of the factors associated with ECC in Indonesia that may facilitate the review of a national oral health policy for Indonesia.

#### ANALYSIS ON POLICY OPTIONS AND IMPLICATIONS

#### Epidemiological Data Analysis on ECC in Indonesia

**Table 1** presents an overview of the prevalence of ECC and possible risk factors in Indonesia extracted from the basic health surveys conducted in 2007, 2013, and 2018 (7–9). This table is quite revealing in several ways. It is apparent from the table that more than half of children aged

*NA, Not available.*

*Source: Ministry of Health Republic Indonesia (7–9).*

5 years were experiencing oral health problem. Unfortunately, those who got treatment were only 9.5%. The data also looks unsatisfactory since only 2% of the children received treatment of fillings or extraction. The most disappointing results to emerge from the national survey is that a high prevalence of ECC and poor behavior on brushing teeth properly.

However, a comparison of the data could not be conducted because of inconsistencies in the measures of the oral variables used for the surveillances. ECC severity using the dmft index, was only conducted in 2018. Also, the data on the dmft was not disaggregated. Data on the proportion of preschoolers who brush their teeth properly was only available in 2018. Despite this limitation, the table highlights a few important issues. First, it suggests that prevalence of ECC is increasing over the study period, and second, it suggests that children age 3–4 years contribute significantly to the high prevalence of ECC in the country. Caries severity also appears to increase by almost a third between the ages 3–4 and 5 years.

Publications on ECC in Indonesia has been limited in scope. Most of them were conducted in cities with few participants. In 1992, a study on preschool-aged children in the Jakarta area showed an ECC prevalence of 85.17% (10). Other research on ECC conducted in Jakarta in 2001 and 2008 reported prevalence of 81.2% (11) and 80.95% (12), respectively. The study in 200l was conducted in children 3–5 year old while that in 2008 was conducted in 3 year olds. The studies suggest that the prevalence of caries increased with age. Lower prevalence were reported in studies conducted in West and East Java; in West Java ECC prevalence was 70% (13) while it was 42.9% or children aged 3 years in East Java. The prevalence of severe ECC was 57.1% in East Java (14). Caries prevalence of 94.3% was reported in 4– 6 year old children in Yogyakarta (15), and a prevalence of 100 and 88.5% reported in 5-year-olds resident in South Kalimantan and North Sulawesi, respectively (16, 17). Identified risk factors for ECC studies in Indonesia include low maternal education (12, 15), poor maternal knowledge of oral health (13, 16), and consumption of cariogenic foods, which had a significant relationship with the severity of ECC (12). Children who do not brush their teeth regularly from an early age also had high risk of ECC (15).

#### Socio-Demographic Context

Indonesia is an archipelago state which is located between two continents (Asia and Australia) and two oceans (Indian and Pacific). The width of land area in Indonesia is around 1,916,862.2 km2 , while the width of its sea is about 3,257,483 km2 . Indonesia is a country with the fourth largest population worldwide (18). Indonesian people are comprised of many ethnics and cultures. There are more than 700 local languages and dialects in the daily life of its people (19).

It is evident that variations in caries prevalence among children are associated with multiple factors, including ethnicity and culture. Results of national basic health surveys in Indonesia also show that prevalence and severity of oral disease varies across ethnic groups. Yearly, the highest average caries index is found on the island of Borneo, followed by Java and Sulawesi. Factors like socioeconomic status, natural fluoride content in the water, and the culture of sweet food consumption have been suggested as causes of the high caries prevalence. unfortunately the data is presented in general for all ages, while specific data about ECC in children is not available. Interestingly, since the causes of caries are the same at all ages, it can be hypothesized that the variation in the prevalence of ECC across ethnic groups will not be much different.

#### Health Policy Implications on ECC

Indonesia is classified as a country with lower-middle income population with increasing rate of national income per capita (20, 21). Despite this, 6.8% of Indonesians are living below the poverty line (22). To secure sufficient and sustainable health financing, The National Health Insurance (NHI) scheme was initiated to improve the access of all citizens to health. The scheme was started in January 2014 with the aim of covering

about 250 million by 2019, thereby making it the world's largest social health insurance (23). In the Indonesia NHI scheme, oral health service is included as one of the benefit packages received by people. Benefit package for oral care in primary care including counseling, curative treatment (teeth restoration and minor surgery) and dental emergency care (24). This NHI package is valid for all ages, including children. The package also includes treatments for caries in children, including preventive restoration of fissure sealants. Unfortunately, to date, there is no detailed data available regarding utilization by groups of children under 5 years of age and what types of care are received by children related to ECC.

Recently, Ministry of Health developed the oral health provision grand design for 2015–2030 with the goal of having a healthy Indonesia free of caries by 2030. The Healthy Indonesia Free Caries campaign roadmap is revised every 5 years. The Road map started with the issuance of the National Act Plan of Oral Health Service which focused on strengthening policy, resources, and oral health service delivery. Targets were set for caries control in 12 years old children, oral health program at Community Health Centers (CHCs) were standardized, and the role of school-based dental programs and community-based health efforts were strengthened (25). The grand design of oral health provision accompanied the emergence of national policy on oral health laid out in the Ministry of Health Decree No. 89/2015 which identified oral health as an integral part of general health (26). Oral health services for infants focus on maintaining the health of the oral cavity before the teething stage, up to the age of 12 months. Information on oral health is provided to the parents and other family members by (a) counseling them about the growth phase of primary teeth, the conditions that accompany the process of teething and related abnormalities or diseases that often occur in infants as well as (b) educating them on how to maintain the health of their infant's oral cavity before teething until the incisors grow fully. It is stated that oral health services for children under the age of 5 years (between 12 and 72 months) is not very different from that for infants (26). The synergy of oral health policy for pre school and school children is expected to be a good foundation for reaching the target because, in the first 6 years, parents are expected to get good education about caries prevention for children, and the next 6 years of oral health education are applied directly to the children.

It is worthy to note that recently, the government of Indonesia has implemented the decentralization policy in the health sector, under Law No. 23/2014 on Local Government, stated that local government has a responsibility to focus on the delivery of defined essential services (which include health) while the central government has the responsibility to determine the expected standard for the provision of services. Decentralization plays a part, with each authority having an important role in setting policy in its region; every region has a unique approach depending on its individual needs. Unfortunately, reports about the success of ECC prevention program that take advantage of the opportunity for decentralization have not been published.