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ORIGINAL RESEARCH

Oral Health Status of Young People Infected with

HIV in High Epidemic Area of China
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Fei Chen 1 Purpose: This study aimed to understand the oral hygiene habits and oral health status of
Yuewu Cheng 2 young people infected with human immunodeficiency virus (HIV) in Henan province of
3,4 China.
Tiansheng Xie
1
Methods: Randomized stratified cluster sampling strategy was used to select young people
The Affiliated Hospital of Stomatology,
School of Stomatology, Zhejiang who were receiving highly active anti-retroviral therapy (HARRT) from 6 towns. A total of
University School of Medicine, and Key 104 participants were enrolled and divided into 2 groups, adolescence group and young adult
Laboratory of Oral Biomedical Research
For personal use only.

group. By face-to-face oral interview and examination, well-trained dentists collected general
of Zhejiang Province, Hangzhou,
Zhejiang, 310006, People’s Republic of information, oral hygiene habits and oral health status of the participants.
China; 2Shangcai Center for Disease Results: Fifty-eight of them were adolescence group and 46 of them were young adult
Control and Prevention, Zhumadian,
group. In two groups, most of them brushed their teeth once a day (55.20%, 67.40%), and
Henan, 463800, People’s Republic of
China; 3Zhejiang Sino-German Institute half of them basically brushed their teeth for 2 minutes (51.7%, 50.0%). Majority of
of Life Science and Healthcare, School of participants did not use dental floss (93.1%,91.3%) and also never visited a dentist
Biological and Chemical Engineering,
Zhejiang University of Science and
(81%,78.3%). One-third of participants had spontaneous bleeding, and about half of them
Technology, Hangzhou, Zhejiang, 310023, had gingival bleeding when brushed their teeth. The most frequent mucosal disease was oral
People’s Republic of China; 4State Key ulcers. Moreover, the prevalence of caries remained very high in both groups, which was
Laboratory for Diagnosis and Treatment
of Infectious Diseases, The First Affiliated 82.76% and 84.8%, respectively. Most of the participants in both groups had low education
Hospital of Zhejiang University, School of level and received less than 9 years of education (65.5%, 63%).
Medicine, Zhejiang University, Hangzhou, Conclusion: The participants had poor oral hygiene habits. The economic and education
Zhejiang, 310003, People’s Republic of
China level may associate with the awareness of oral health and care.
Keywords: oral hygiene, oral health, mouth mucosa, HIV infections, adolescent, young
adult

Introduction
In 2019, there were 38,000,000 HIV-infected people worldwide, which included
1,800,000 children under 15 years of age, and 1,700,000 adolescents (10–19
years).1,2 Although the epidemic trend of global HIV infection was declining,
children represented a growing share of people living with HIV worldwide and
China had no exception.2 Shangcai County of Henan province is one of the counties
with the highest rate of HIV infection in China. In late 1980s and early 1990s,
Correspondence: Tiansheng Xie
a large number of rural residents were infected with HIV due to unhygienic paid
Zhejiang Sino-German Institute of Life blood donation, and a large number of children were perinatally infected from their
Science and Healthcare, School of
Biological and Chemical Engineering, mothers.3 The district government carried out the Highly Active Anti-Retroviral
Zhejiang University of Science and Therapy (HAART), social care, psychological counseling and so on for these HIV-
Technology, 318 Liuhe Road, Hangzhou,
Zhejiang Province, 310023, People’s infected children for more than 10 years.4
Republic of China
Tel +86 571 86021350
Standardized and effective HAART altered perceptions on HIV/AIDS from an
Email tianshengxie@zust.edu.cn epidemic to a manageable chronic illness, and reduced the probability of

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opportunistic infections including oral infections in adults months or suffer from systemic diseases were
as well as children.5 Despite dramatic declines in their excluded.104 participants finished this observation study
incidence, opportunistic infections remained important finally Participants who were 12–18 years old were
causes of morbidity after HAART initiation in this regio­ defined as adolescences, and those who were19–24 years
nal cohort of HIV-infected children in Asia.6 Some studies were defined as the young adults.
revealed that the increased incidence of dental caries in
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children with HIV infection was due to intake of sugar- Survey Procedure
containing drugs, sugar-rich diet, Anti-Retroviral The doctor who was in charge of AIDS health care in the
Therapy(ART), poor oral hygiene and reduced saliva Shangcai county called the participants together with the
flow rate.7,8 Nevertheless, developing countries still have help of the Center for Disease Control and the Prevention
a high prevalence of the main HIV-related oral manifesta­ officer. All participants were received interviews and oral
tions because of the persistence of many risk factors, such examinations individually by the same well-trained
as the difficulty to access treatment, poor oral hygiene, low dentist.
socioeconomic status and delay in diagnosis.9 The survey was conducted in line with the basic meth­
Oral diseases are commonly described to have an ods of oral health survey formulated by World Health
impact on quality of life because they may cause pain Organization (WHO,2013, the fifth edition). The contents
and compromise nutrition, speech and appearance.10 of interviews were as follows: (1) general information,
Children’s oral health-related quality of life (OHRQoL) such as education level, whether working or not, etc. (2)
For personal use only.

is related to parental socio-economic status, dental anxiety, information on oral hygiene habits, such as brushing fre­
childhood dental anxiety, oral health behaviours.11 The quency, using dental floss and mouthwash or not, perform­
high caries experiences have significant negative impacts ing regular oral inspections or not, etc. (3) dental
on the children’s QoL, especially during the primary den­ conditions, such as dental caries, loss, repair, biofilm
tition period.12 Frequency of tooth brushing and dental index (BI), modified gingival index (MGI), calculus
visits, intervals between dental visits, negative dental index (CI) and soft tissue diseases, etc. HIV transmission
experiences and dental anxiety are associated with dental routes were obtained by checking the medical records of
caries.13 Brushing the teeth less than two times a day and the participants. They could get a toothpaste set each as an
viral load exceeding 10,000 HIV-RNA copies per millilitre appreciation gift for participation after finishing the
of plasma were directly associated (p < 0.05) with a poorer interview.
oral health-related quality of life.14 Recognizing the fac­ The study was approved by the Ethics Committee of
tors that were associated with poorer OHR-QoL in chil­ The First Affiliated Hospital at the School of Medicine of
dren with AIDS may contribute to the planning of dental Zhejiang University, and conducted according to the
services for this population. Declaration of Helsinki principles. Written informed con­
This study reported an observation on oral health status sents were obtained from participants or their guardians
in HIV-infected young people in poor county of China to (<18 years old).
analyze the possible factors that affect their oral health
status, and tried to provide references for HIV-related oral Data Collection
health prevention in young people. Paper questionnaires of General information and oral
hygiene habits were obtained by face-to-face interviews.
The questions were read one by one followed by the
Methods optional answers for every participant.
Study Design, Settings and Participants Oral examinations were implemented to assess
This study was conducted in Shangcai county of the Decayed, Missing, and Filled Teeth (DMFT), Biofilm
Henan Province, one of the highest incidences of HIV- Index (BI), Modified Gingival Index (MGI), Calculus
infection in China. There are totally 26 towns in this Index (CI) and soft tissue diseases. The participants were
county. Using randomized stratified cluster sampling strat­ examined with a headlamp, disposable oral examination
egy, 6 towns were selected. Young people receiving trays, disposable gloves and masks while they were sitting
HARRT who were 12–24 years old were invited into on a chair in a comfortable position. The examiner used an
study, those who had used antibiotics in the past three electronic recorder to record the participant’s

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examinations, which would later be reorganized to paper Data Analysis

and electronic versions. All data collected by paper-and-pencil surveys were input
manually into a custom-designed database and analyzed
Definition of Index using SPSS for Windows Version 16.0. We organized
The BI was expressed in terms of Ribeiro index.15 BI was demographic information and examined whether there
ranged from 0 to 5 grades. The definitions of the grades were differences between the scale for ages, education
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were described as follows: 0: No visible biofilm; 1: thin levels, working conditions, CD4+ T cells count. All tests
scattered biofilm on anterior or posterior teeth; 2: thin were two-tailed and the significance level was set at p <
scattered biofilm on anterior and posterior teeth; 3: thick 0.05. Differences between the groups were tested by Chi
and firmly attached biofilm on anterior or posterior teeth; square test.
4: thick and firmly attached biofilm and thin scattered
biofilm on posterior teeth or thick and firmly attached
Results
biofilm on posterior teeth and thin scattered biofilm on
anterior teeth; 5: thick and firmly attached biofilm on General Information
anterior and posterior teeth. A total of 104 participants were divided into two groups
Gingival inflammation was evaluated using based on their ages: adolescence (12–18 years) group and
a simplified modified gingival index (MGI) that was young adult (19–24 years) group. The adolescence group
based on that described by Lobene et al.16 The MGI was consisted of 58 participants (33 males, 56.9%), with an
For personal use only.

rated: 0: healthy gingiva, 1: minor inflammation of the average age of 16.29±1.79 years old. The young adult
gingiva, slight change in gingiva color and mild edema, group consisted of 46 participants (27 males, 58.7%),
2: moderate inflammation of the gingiva, red color, and with an average age of 21.89±1.82 years old. Most of the
bright edema, and 3: severe inflammation, significantly participants in both groups had low education level and
swollen or ulcerated. received less than 9 years of education (65.5%, 63%). In
The supragingival calculus was visually assessed and rated the adolescence group, 28 (48.27%) participants already
using a 4-point ordinal scale that were based on the Löe and left the school and began to work. Meanwhile, only 2
Silness calculus index. The CI was rated: 0: no supragingival participants went to universities in the young adult
calculus, 1: less than 1/3 of the tooth surface was covered by group, the rest of them 44 (95.65%) all started to work.
supragingival calculus, 2: 1/3 – 2/3 of the tooth surface was Fifty-three participants (91.4%) in the adolescence group
covered by supragingival calculus, 3: more than 2/3 of the were infected due to mother-child transmission, and 31
tooth surface was covered by supragingival calculus. (67.4%) participants in the young adult group were
DMFT index examination was performed using infected due to mother-child transmission. The average
a dental probe and a dental mirror, followed by examining CD4+ T cells count in both groups was more than 500
of decayed teeth due to caries (decay), missing/removed (571 and 548), which indicated a good disease control.
teeth due to caries (missing), teeth that were patched or The average duration of HAART treatment of participants
filled with caries were examined. DMFT was the sum of was over 10 years (10.28±2.89 and 11.10±2.72 years). See
the number of Decayed, Missing due to caries, and Filled Table 1.
Teeth in the permanent teeth. The mean number of DMFT
was the sum of individual DMFT values divided by the Oral Hygiene Habits of Different Groups
sum of the participants.18 Participants in both groups had poor oral hygiene habits.
Most of the participants brushed their teeth once a day
Laboratory Tests (55.20%, 67.40%). The participants who brushed their
CD4+ T cells count was detected by BECKMAN teeth twice a day were only 43.1% and 32.6%. Half of
COULTER. The viral load was tested using the participants brushed their teeth for 2 minutes (51.7%,
a commercial HIV-1 monitor (Roche) kit by COBAS 50.0%), while participants who brushed for more than 3
AmpliSensor-PCR. The operation was performed accord­ minutes were only 29.3% and 39.1%. The proportion of
ing to the kit instructions, and the results were expressed participants who used mouthwash in the young adult group
as viral copies per mL of plasma, with a minimum test (41.3%) was significantly higher than that in the adoles­
limit of 50 copies. cence group (24.1%). In addition, the participants in both

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Table 1 General Information of Participants

Adolescence (n=58) Young Adult (n=46)

Age(years) Mean±SD 16.29±1.79 21.89±1.82

Range, median age 11–18, 17 18–24, 22.5

Gender, N(%) Male 33(56.90%) 27(58.70%)

Female 25(43.10%) 19(41.30%)
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Education, N(%) Primary school or below 6(10.30%) 4(8.70%)

Junior school 38(65.50%) 29(63.00%)
Senior school or above 14(24.10%) 13(28.30%)

Infection route, N(%) Mother-to-child transmission 53(91.40%) 31(67.40%)

Transfusion transmitted 2(3.40%) 13(28.30%)
Others 3(5.20%) 2(4.30%)

ART, N(%) 2NRTIs+NNRTIs 36(62.10%) 35(76.10%)

2NRTIs+PIs 22(37.90%) 11(23.90%)

CD4+ T cells count(/ul) 571.09±316.55 548±235.74

Diagnosis duration(years) 13.22±2.91 14.20±1.50

For personal use only.

ART duration(years) 10.28±2.89 11.10±2.72

Abbreviation: ART, anti-retroviral therapy.

groups hardly ever used dental floss after meals, and the Biofilm index (4.05±0.14, 4.02±0.18) and CI (1.71±0.11,
majority of them never visited a dentist even if they had 1.92±0.15).
dental health problems (81%, 78.3%). See Table 2. Oral ulcers were the most common soft tissue diseases
(15.52%, 24.14%) in both groups. One subject from young
Oral Health Status of Different Groups adult group suffered from mucosal fibrosis due to long-
As shown in Table 3, approximately 1/3 of the participants term chewing of areca. No characteristic linear gingival
in the two groups had spontaneous bleeding. About 1/2 of erythema and no obvious symptoms of candidiasis were
the participants had gingival bleeding when brushing their observed in all the participants.
teeth. The MGI of the adolescence group (0.98±0.09) was The prevalence of dental caries remained very high in
significantly lower than that of the young adult group (1.41 both groups (82.76%, 84.8%). And there was no signifi­
±0.11)(P<0.05). However, the two groups had comparable cant difference between the two groups (3.17±0.42, 3.87

Table 2 Oral Health Behaviors in Two Groups

Adolescence Young Adult Table 3 Oral Health Hygiene in Two Groups
(n=58) (n=46)
Adolescence Young Adult
Frequency of tooth Once 32(55.20%) 31(67.40%) (n=58) (n=46)
brushing, N(%) Twice 25(43.10%) 15(32.60%)
Spontaneous hemorrhage, N(%) 16(27.60%) 15(32.60%)
Brushing continuous 1min 10(17.20%) 5(10.90%)
Brushing teeth bleeding, N(%) 26(44.80%) 26(56.50%)
time, N(%) 2min 30(51.70%) 23(50.00%)
3min 17(29.30%) 18(39.10%) MGI (mean±SD) 0.98±0.09 1.41±0.11*

Using mouth wash, N(%) 14(24.10%) 19(41.30%) BI (mean±SD) 4.05±0.14 4.02±0.18

Using dental floss, N(%) 4(6.90%) 4(8.70%) CI (mean±SD) 1.71±0.11 1.92±0.15

Ever see a dentist, N(%) 11(19.00%) 10(21.70%) Note: *p < 0.05 Chi square test.
Abbreviations: MGI, modified gingival index; BI, biofilm index; CI, calculus index.

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 Dovepress Chen et al

±0.58) concerning the decay-missing-filled index(DMFT). treatment of periodontal diseases and related tooth loss.23
Few participants regularly visited the dentists. There were In the present study, most of the participants lived in the
only 5 and 3 teeth were filled in the adolescence group and rural areas and had low education level. After receiving 9
young adult group, respectively. There were 27 and 24 years of compulsory education, most of them started work­
teeth that should be removed due to dental caries, and 19 ing instead of further education. Only two participants
and 12 teeth were lost in the adolescence and young adult, were studying in the university. They had poor conscious­
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respectively. See Table 4. ness to control dental plaques and maintain good oral
hygiene habits. Only a small proportion of participants
brushed their teeth twice a day for more than 3 minutes.
Discussion They hardly ever used dental floss after the meal. Study
The World Health Organization (WHO) has recently
showed that dental caries was also 1.5 times more among
recognized the need to address the growing problem of
adolescents living with HIV who brush their teeth less
oral health epidemics and also acknowledged poverty,
frequently.24 Caries was lowest in HIV-positive children
inequality and systemic diseases as indicators.19 To pre­
who brushed their teeth at least twice a day.25
vent oral health in high-risk populations, oral health care Different articles have reported varied prevalence of car­
should be paid more attention to prevent oral diseases.20 ies in children with HIV infection. The highest prevalence of
As it is known to all that the plaque should be carefully dental caries (86%) was observed in children with HIV
cleared with a toothbrush twice a day. The plaque between infection in western Africa, while those in Nigeria had the
For personal use only.

the teeth should be removed by using dental floss every 24 lowest prevalence of caries (12.1%).26,27 In other countries,
hours to prevent gingivitis and dental caries. The the prevalence rates of dental caries were all very high and
American Dental Association recommends brushing teeth the differences between them were not big.15,28–31 The jour­
twice a day for duration of at least 2 minutes.21 Evidence nal of AIDS revealed that PHIV youth who received combi­
had shown that the oral hygiene efficacy increased with nation ART(cART)containing an integrase inhibitor had
the time of brushing.22 Therefore, it is encouraged to brush a significantly higher number of untreated active caries than
the teeth for 2 minutes or more while the choice of tooth­ those on cART without an integrase inhibitor in 2018.32 The
brush is less important. Increasing the brushing time might prevalence of untreated caries was significant associated with
be the easiest way to control daily brushing effectively. low socioeconomic status eating habits (high frequency of
Adherence to the recommended oral hygiene regimen is sugar consumption) and poor clinical conditions (HIV viral
also regarded as a basic factor for the prevention and load and severity of symptoms).33 The increase in the num­
ber of dental caries was also related to the reduction of
Table 4 Conditions of Permanent Teeth salivary flow rate, high-sugar and high-carbohydrate diet,
deficient oral hygiene and parental irresponsibility.34
Adolescence Young
(n=58) Adult DMFT scores were negatively associated with the CD4+
(n=46) cell count in male children with HIV infected in Phnom,
Cambodia.35 However, one study had pointed out that there
Decayed(Teeth), N 174 169
was no statistical significance between the CD4+ cell count
Missing(Teeth), N 19 12
and caries in HIV-positive children treated with ART in
Filled(Teeth), N 5 3 Mangaluru, India.36 In this study, the prevalence of caries
Pulp involvement*(Teeth), N 5 6
remained very high in both groups, which was 82.75% in the
adolescence group and 84.8% in the young adult group.
Tooth extraction due to caries**, N 27 24
Participants in this study had received HAART for a long
DMFT (Mean±SD) 3.17±0.42 3.87±0.58 period, and achieved good therapeutic effect. The high pre­
Prevalence of dental Caries(%)*** 82.76% 84.8%
valence of caries might be related to poor oral hygiene habits
and low education level. At the same time, further research
Notes: *Pulp involvement, root remains also considered pulp involvement; **it is
necessary to extract teeth due to caries, and it is impossible to retain the disabled should pay attention to the participants’ salivary flow rate,
roots due to caries during oral examination; ***prevalence of dental Caries=(the
number of DMFT>0/the sum of the participants)×100%.
dietary preferences and parents’ oral health awareness as
Abbreviation: DMFT, decayed+missing+filled teeth. well.

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Most parents were unaware of their children’s oral (LQ19H280007), and the National Natural Science
hygiene. For this reason, educational interventions should Foundation of China (No.81602943), and the Mega-Project
be provided to increase the parents’ knowledge and skill. for National Science and Technology Development
They should be educated to realize their children’s dental (2017ZX10105001). The funders had no role in study design,
needs, especially for those low-socio-economy parents and data collection and analysis, decision to publish, or prepara­
whose children with poor oral hygiene.37 It was reported that tion of the manuscript.
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teenagers whose parents had high educational achievement

used flossing regularly.38 Previous studies have revealed that
educational pattern videos, lectures and pamphlets for the
Disclosure
The authors report no conflicts of interest in this work.
parents and children exerted similar effect on reducing the
plaque index.39 To improve children’s oral hygiene, parents
should encourage them to brush their teeth from their young References
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