Oral status of HIV‐infected children aged 12 years or younger who attended a Paediatric Infectious Diseases Clinic in Cape Town

Abstract Background Children continue to suffer from the impact of the human immunodeficiency virus‐acquired immunodeficiency syndrome (HIV/AIDS) pandemic. In Cape Town, these children receive medical care including antiretroviral therapy from facilities like Tygerberg Hospital's Paediatric Infectious Diseases Clinic. HIV‐infected children may experience an increased caries experience when compared with their healthy peers. Aim The aim of this study was to determine the oral health status of HIV‐infected children younger than 12 years receiving antiviral drugs at the Paediatric Infectious Diseases Clinic. Design A cross‐sectional survey was conducted among children aged between 2 and 12 years presenting at this clinic. Caregivers were interviewed to obtain information regarding health seeking behaviour, oral hygiene practices and dietary habits. A single clinician undertook a standardized clinical intraoral examination according to the World Health Organization guidelines, with modifications. Results Sixty‐six children were recruited. A high prevalence of dental caries (78.8%) and an unmet treatment need of 90.4% were recorded among the participants. Most children had never visited the dentist, and those who did had mainly received emergency dental care. Conclusion The high prevalence of severe dental caries in this population highlights the need for oral health awareness and the inclusion of oral health care in the comprehensive care of children with HIV. Why this paper is important to paediatric dentists The study highlights the importance of collaborating with health professions outside of dentistry. Doctors and nurses are often the first health professionals to come into contact with children with special needs. They should therefore be made aware of the early signs of decay so that these patients can be referred for dental treatment timeously. Holistic management of children with special healthcare needs is essential to improve their overall well‐being.


| INTRODUCTION
Since the discovery of the human immunodeficiency virus (HIV) in 1981, the virus has continued to wreak havoc globally with new infections continuing to surface and HIV-related deaths still being regis- Higher risk of dental caries is a problem in children with HIV especially in the developing world. HIV-infected children may experience an increased caries experience when compared with their healthy peers for various reasons (dos Santos et al., 2009;Howell, Palumbo, & Houpt, 1992). Immunocompromised children from resource-limited populations (Naidoo & Chikte, 2004;Ramos-Gomez, 2002) are particularly vulnerable. Higher caries risk has been attributed to socio-economic factors such as poor access to medical resources and preventive measures (Ramos-Gomez & Folayan, 2013). One study reported an increased caries rate in HIV-infected children mainly due to the inappropriate dietary habits brought on by the failure to thrive (Madigan, Murray, Houpt, Catalanotto, & Feurman, 1996). Some studies have suggested that the caries experience in children is related to the acidic and sugary syrup medications consumed by these HIV patients, opportunistic infections and reduction in the salivary flow rate (dos Santos et al., 2009;Jetpurwala & Jain, 2011). An increased caries incidence has also been attributed to negligence on the caregiver's part concerning oral health and dietary habits of the child (Nokta, 2008 The objectives of the study were to determine the following in the study population: • the caries experience; • the dental treatment need; and • factors contributing to the oral health status. Even though children up to the age of 16 years are seen at this clinic, only children with a confirmed HIV-positive status between 2 and 12 years of age were enrolled in the study, as the upper age limit for paediatric dental patients at the adjacent Tygerberg Oral Health Centre is 12 years of age. In order to be included in the study, children had to be in possession of a consent form signed by the legal guardian, providing permission for their child to be enrolled in the study. Children who did not comply with the clinical examination as well as those who were not in possession of a signed consent form were excluded from the sample. However, brief oral health advice was given to all the children and their caregivers.

| MATERIALS AND METHODS
A simple convenience sampling method was employed to choose candidates who fit the selection criteria. Children living with HIV/AIDS are seen at Tygerberg PIDC from Monday to Wednesday. On the days of the examination, all patients attending the outpatient clinic who were eligible for inclusion in the study were recruited. A statistician was consulted to assist with an estimation of the sample size. After doing a power calculation, 50 patients were found to be representative of the study population.
A total number of 66 patients met the inclusion criteria and were recruited for the study. Participants were made aware of the study and given all the relevant information both verbally and in writing.
Participation was entirely voluntary, with participants given the freedom to drop out of the study at any point in time. A written consent form was thoroughly explained and issued to each parent in English. In an effort to protect the identity and the confidentiality of the participants of this study, the patients' names were not recorded on the data capture sheet. Instead, the patients' medical record numbers were used for identification purposes.
The data collection process consisted of both quantitative and qualitative aspects. The former was used to capture the DMFT/dmft.
The DMFT/dmft index has been used in several studies to record the caries experience. It is expressed as DMFT for permanent teeth and dmft for primary teeth (Klein & Knutson, 1938) and reported as a percentage of the total number of teeth present intraorally.

| RESULTS
Out of the 66 children who were recruited for this study, 28 (42.4%) were female and 38 (57.6%) were male. All had one or more remaining deciduous teeth, except two study participants who had only permanent teeth (n=64). The overall caries experience in the primary teeth (dmft>0) was 78.1% (95% CI, 66.0-87.5), with minor differences between the two age and gender subgroups (Table 1).
Thirty study participants had only deciduous teeth, and 36 had one or more permanent teeth. The caries experience (DMFT>0) was 41.7% (95% CI, 25.5-59.2), with minor differences between the two gender subgroups (Table 2). Table 3 depicts the distribution of mean decayed (D-/d), missing (M-/m-) and filled (F-/f-) teeth among the different age groups. The distribution of decayed, missing and filled deciduous and permanent teeth was 6.3 (SD 5.0) and demonstrated minor differences between the two age subgroups (Table 3).
According to the questionnaires completed by the parent or guardian, the most common frequencies were 60.6% (never experienced discomfort), 60.6% (never visited the dentist), 13.6% (experienced discomfort), 42.4% (brushed once per day), 60.6% (made use of adult toothpaste). No problems were reported by 67.9% of study participants (Table 4). The consumption of carbohydrates related to dietary habits was relatively high (Table 5).
Looking at the severity of the caries experience in the deciduous dentition, the mean dmft was 6.0 ± 4.70 with no significant T A B L E 1 Caries experience in the primary dentition according to gender and age group (n=64) There was no significant difference in the mean dmft of the two age groups, that is, 2 to 6 years and 7 to 12 years. In the scientific literature, the reported mean dmft ranges between 1.5 and 11.8 (Cerqueira, Portela, & Pomarico, 2010;dos Santos et al., 2009;Madigan et al., 1996;Meless et al., 2014). Contrary to the findings of the current study, another study found the dmft in children with perinatally acquired HIV was significantly lower and comparable to that of normal children (Sahana, Krishnappa, & Krishnappa, 2013). A meta-analysis concluded that even though studies reported a high dmft, there was no significant association between the caries experience and HIV-infection (Oliveira et al., 2015).
In the permanent dentition, the mean DMFT for the sample population was 0.86 ± 1.29. There was no significant variation between girls (0.89 ± 1.37) and boys (0.83 ± 1.20). Several studies have reported mean DMFT ranging from 0.5 to 4.0 (Cerqueira et al., 2010;dos Santos et al., 2009;Madigan et al., 1996;Meless et al., 2014;Sahana et al., 2013). The results of the current study highlighted an overall low caries experience (mean DMFT) in the permanent dentition. Similarly, another study found that the data on the caries experience in the permanent dentition although insufficient, revealed a low mean DMFT (Oliveira et al., 2015).
The older age group, 7 to 12 years had a higher mean decayed   (Ramphoma, 2016;Singh, 2011). The results of the current study are therefore no different from other findings with regards the caries experience among children in South Africa.
Medically compromised children who are on long-term medications are generally classified as having a high caries risk (Foster, 2005).
Children living with HIV have been found to be susceptible to dental caries (Leão, Ribeiro, Carvalho, Frezzini, & Porter, 2009). Studies have established a direct relationship between caries risk and HIV, particularly with respect to the potentially cariogenic and xerostomic antiretroviral medication (Nittayananta, Chanowanna, & Winn, 2010;Nittayanata, 2016;Oliveira et al., 2015). Other factors implicated in the increased prevalence of dental caries among children with HIV include diminished flow of saliva and a reduction in salivary antibodies (dos Santos et al., 2009;Oliveira et al., 2015). Due to the absence of an HIV-negative control group in this study, a direct relationship between the HIV infection and caries prevalence/severity could not be established. This is therefore a potential area of research that should be explored in future clinical studies.
Control of oral disease is often dependent upon several environmental factors such as dietary factors, family factors, behavioural factors and access to oral health services (Hashim, Thomson, Ayer, Lewsey, & Awad, 2006). The family and social environment include the child's caretaker, the number of siblings in a household as well as household crowding (Petersen, Bourgeois, Ogawa, Estupinan-Day, & Ndiaye, 2005;Wang et al., 2012). In this study, 21.2% of children were under the care of an institution or foster care, categorised as "other." The institutionalized children were orphaned and had concomitant ailments. Children under the care of a relative were cared for by a grandparent, an aunt or an uncle. Most of the children hailed from poor households. The association between poor oral health in children and low socioeconomic status of the family has been widely documented in the literature (Castilho, Mialhe, Barbosa, de, & Puppin-Rontani, 2013;Petersen et al., 2005).
Access to oral health care is a crucial factor in the prevention and management of dental caries (Singh, 2011). In the present study, out of the entire sample, only 21.2% had had a dental visit in the previous year; 60.6% had never been to the dentist nor had a dental check-up.
Negligence towards oral health has been shown to be among the leading factors related to the development and progression of dental caries (Castilho et al., 2013). In addition, oral hygiene practices as well as exposure to fluoride have been shown to play a key role as protective factors in minimising the caries risk (Yengopal et al., 2016). In the present study, 42.4% of the sample admitted to brushing their teeth only once a day, and 18.2% either brushed occasionally or had never brushed. These inadequate tooth brushing practices could be linked to the high caries experience.
The impact of diet and nutrition, especially the role played by refined sugary substances on the development and progression of dental caries has been widely discussed in the literature (Rwenyonyi et al., 2011). The dietary habits of children were explored, particularly the consumption of sugary foods. In this study, a large proportion of children consumed sugary snacks and drinks several times a day. The frequency of these sugar attacks was exceptionally high. This data also reflects the need for a collaborative effort between the PIDC and paediatric dental clinics to provide oral health services to children with HIV. Doctors and nurses are often the first health professionals that come into contact with these patients. Training these professionals to recognize the early signs of dental caries will therefore go a long way to providing appropriate holistic care for these patients. This can only be facilitated by improved screening and referral processes between the medical and dental professions.