Severity and Prevalence of Plaque-Induced Gingivitis in the Chinese Population

Study Populations
Prior to initiating the research, the study protocol and letter of informed consent were approved by the Institutional Review Board (IRB) of Guangdong Provincial Stomatological Hospital. A total of 1143 subjects (550 females and 593 males, ages 18 to 90 years) participated. The patients were recruited from three areas of China: 1) Guangzhou (379 people), which is comprised of five communities and villages in Guangdong province; 2) Shenyang (393 individuals), which is in north China; and 3) Nanjing (371 patients), which is in the southeast China. Separate IRB approvals were obtained for Shenyang and Nanjing.

The patients were healthy males and females ≥ 18 years old who had at least 20 natural teeth. Each study site recruited participants by placing IRB-approved advertisements in local publications. The advertisements provided a synopsis of the study and instructed potential participants to contact the research clinic for more information. These individuals were interviewed by telephone to determine eligibility. Those who were interested were scheduled for clinical visits. Each prospective participant was given a full explanation of the study, an informed consent form to sign, and a copy of the signed form.

Materials and Methods
Demographic information (age, gender, and race) and a brief medical questionnaire were collected from each patient, who then received gingivitis and plaque examinations. Individuals presenting with gross pathologic changes of gingival tissues were excluded. The Loe-Silness gingival index (GI)¹¹ and the modified Quigley-Hein plaque index (PLI)¹² were used for evaluating the gingival health and plaque levels of all natural teeth, except third molars. The scoring scale for these indices is as follows:

Loe-Silness gingival index:

0 = Absence of inflammation

1 = Mild inflammation: slight change in color and texture

2 = Moderate inflammation: moderate redness, edema, glazing, hypertrophy; bleeding on probing

3 = Severe inflammation: marked redness and hypertrophy, a tendency to spontaneous bleeding (elicited by air syringe) and/or ulceration

Modified Quigley-Hein plaque index:

0 = No plaque

1 = Separate flecks of plaque at the cervical margin of the tooth

2 = A thin, continuous band of plaque (up to 1 mm) at the cervical margin of the tooth

3 = A band of plaque wider than 1 mm, but covering less than one third of the side of the crown of the tooth

4 = Plaque covering at least one third, but less than two thirds of the side of the crown of the tooth

5 = Plaque covering two thirds or more of the side of the crown of the tooth

Two trained examiners conducted the study using 1143 patients at the three sites. Interoperator reliability was assessed employing Kappa statistics (k = 0.82).¹³ When the predetermined number of participants was reached at each site, enrollment ceased. The data of age, gender, urban/rural, GI, and PLI were compiled for each location, as well as for all three sites. In addition, patients were divided into four age groups (≤ 30, 31 to 44, 45 to 59, and > 60 years of age) to examine the prevalence and severity of gingivitis and plaque. Statistical analyses were performed at a 5% level of significance. One-way analysis of variance (ANOVA) was used to examine age differences among the three sites and the four age groups, while Kruskal-Wallis one-way ANOVA by ranks was performed to analyze the GI and PLI among the three study sites and the four age groups. The effect of gender and urban/rural variables on GI and PLI was evaluated by two-tailed Student t-test. The Pearson correlation coefficient was used to examine the relationship between GI and age, as well as PLI and age.

Among the 1143 participants, there were 550 females (48%) and 593 males (52%) from 18 to 90 years of age with an average age of 42.2 ± 14.8 years (Table 1). The average age and standard deviation were similar in the three populations. The gender and the urban/rural compositions were comparable among Guangzhou, Shenyang, and Nanjing participants (48.8%, 47.3%, and 48% females, respectively, and 54.6%, 53.2%, and 53.9% rural residents, respectively). In general, the composition reflected data recorded by the 2008 Chinese census (48.5% females, 54.3% rural residents).¹⁴

The average and standard deviation of GI and PLI were 1.101 ± 0.239 and 3.394 ± 0.578 respectively, from 0.05 to 2.71 and 1.31 to 5.0, respectively, for all Chinese adults. As presented in Table 2, only 2.1% of the participants had a GI lower than 0.5. For 97.9% of the patients, the average GI was 0.5 or higher. In 82.2% of participants, the GI was 1.0 or higher, and 1% of the patients had a GI higher than 2.0. A total of 0.4% had a PLI lower than 2.0. For 99.6% of patients, the average PLI was 2.0 or higher. Two thirds (75.4%) had a PLI or higher (Table 3).

As shown in Table 4, the average GI and PLI scores were significantly different among the four age groups (F = 11.696, P < .0001; F = 84.896, P < .0001), respectively; pa-tients younger than 30 years of age had significantly lower GI and PLI scores (P < .0001; P < .0001) than the three older groups. With the older patients, the average GI and PLI values were higher, while the average GI values were comparable between the 31- to 44-year-old and 45- to 59-year-old patients. The oldest group (> 59 years) had significantly higher GI and PLI values than the other groups. Therefore, a positive correlation was observed between the GI score and age, as well as PLI score and age (Figure 1 and Figure 2).

No significant difference was noted between the GI in males and females, while the males' PLI values were significantly higher than that of the females (P < .001). The average scores for the males and females were 3.515 ± 0.552 and 3.265 ± 0.577, respectively. The urban population's GI and PLI scores were significantly lower than that of rural inhabitants (Table 5).

The average GI values for Guangzhou, Shenyang, and Nanjing sites were 1.085 ± 0.146, 1.073 ± 0.263, and 1.148 ± 0.280, respectively (Table 5). The average PLI values were 3.320 ± 0.572, 3.396 ± 0.605, and 3.471 ± 0.546, respectively. The mean GI and PLI measurements of Nanjing site were significantly higher than the other two locations; the average GI and PLI values were comparable between the Guangzhou and Shenyang patients.

Gingivitis begins in early childhood, increases in prevalence and severity to the early teenage years, and then subsides slightly and levels off until approximately 20 years of age.¹⁵

However, gingivitis in adulthood is more difficult to characterize due to the lack of comprehensive data; estimates of the general prevalence of adult gingivitis are approximately 50% to 100%.¹⁶ According to the Third National Epidemiological Survey on Oral Health in China,¹⁷ 14.5% of the population between ages 35 years and 44 years had a healthy periodontium, while 77.3% had gingival bleeding, 14.1% between 65 to 74 years displayed no periodontal disease, and 68.0% had gingival bleeding. Although the prevalence of gingivitis varies according to age in the Chinese populations, the comprehensive data, including the average bleeding index (BI), GI, and other values, were not presented. Until now, data including specific indices about gingivitis in the Chinese population were not reported. The present study found that 97.9% of the 1143 patients had a GI at 0.50 or higher, with 82.1% presenting with a GI at 1.0 or higher. The oldest group (> 59 years) had significantly higher GI values than the other groups. A retrospective survey¹⁰ of dental records of 6575 Chinese freshman students at Peking University found 60.87% exhibited gingivitis with varying severity (the prevalence in males was significantly higher than in females). The participants were young adults, most of whom received routine professional dental prophylaxis, which explained the lower prevalence and severity of gingivitis when compared to the general population.

The three sites selected for the present study represent different study populations used for clinical trials assessing the antigingivitis efficacy of oral hygiene products. Guangzhou is in south China, and patients are urban residents in nearby communities or rural inhabitants in neighboring villages. Shenyang is in north China, and Nanjing is in the east. The average age and variations were similar among populations of the three sites. The gender and urban/rural compositions of the participants were similar among the three sites. In general, the composition reflects that of the 2008 census data of the Chinese population. Therefore, these study groups and their GI and PLI scores may indicate the oral hygiene status of the general Chinese population. The average GI and PLI scores of the Nanjing site were significantly higher than those of the other two sites. The data suggest a higher prevalence of plaque-associated gingivitis in that province compared with Guangzhou and Shenyang.

In addition to the location, the results of the present study show that the age, gender, and urban/rural compositions can influence the prevalence and severity of plaque-associated gingivitis, as measured by the GI and PLI. The average GI and PLI values tend to increase for older patients (Table 4). The difference is especially evident between those younger than 30 years and people older than 60; the older group had approximately 13% higher GI scores and 24% higher PLI values. The gender can have a similar impact on the average PLI of a study population, other than the average GI. The urban population's GI and PLI values were significantly lower than those of the rural population. The disproportion of the age, gender, and urban/rural mix in a study population may significantly distort the average GI score and misrepresent the population of intended product users.

In addition to the numerous oral hygiene products on the market, new products are being actively developed to combat gingivitis. The lack of information regarding the characteristics of the population tested could hinder evaluations of the products' efficacies. It is well known that the choice of different indices, such as the GI, modified gingival index (MGI), BI, and a combination of the GI and BI, can influence the outcome of a clinical antigingivitis study.¹⁵ The MGI uses a 5-point index (0 to 4), which is a wider scale than the GI (0 to 3). Research have shown that, when used properly, the MGI appears to help detect the difference in antigingivitis effects of the oral hygiene products without distorting the overall data.^8,17-25 The results of the present study have demonstrated that the characteristics of a study population may have a non-negligible impact on the accuracy and reliability of the efficacy data reported. The importance of usingan appropriate study population is not limited to meeting the representation requirements of the intended users of the product.^26,27 Results from a misrepresented study population may provide erroneous or misleading conclusions as to the efficacy of an antigingivitis product. Based on the data from the present study, the Chinese population of primarily females younger than 30 years will most likely have a GI significantly lower than 1.1, making the antigingivitis efficacy detected in this population questionable compared with the general population. Of more concern is the possible exaggeration of the antigingivitis efficacy of a product in a study population with an average GI lower than usual. For example, a GI reduction of 0.1 can be interpreted as a 20% increase in antigingivitis efficacy in a study population with an average baseline GI of 0.5. Therefore, clinical trials aiming at assessing the antigingivitis efficacy of an oral hygiene product should consider recruiting patients from a population that represents the intended users. Variables should include gender, race, age, and geographical location.

There was a significant correlation between the age, gender, geographical location (rural vs urban), and the gingival and plaque indices studied. For epidemiologic surveys in China, requiring the use of GI and PLI, as well as proper subject source, age, gender, and racial compositions, needs to be considered for meaningful results in assessing study outcomes.

The study was supported through a grant from Colgate-Palmolive Company. Dr. Zhang, Dr. De Vizio, and Dr. Panagakos are Colgate-Palmolive employees. Dr. Dibart has revieved honorarium from Colgate-Palmolive.

The authors would like to thank Dr. Wang Lin and Dr. Xu Yan at Nanjing Medical University and Dr. Zhang Guirong in Shenyang for their assistance.

Jincai Zhang, DDS, PhD
Professor and President
Guangdong Provincial Stomatological Hospital
Guangzhou, China

Dongying Xuan, DDS, PhD
Assistant Professor
Department of Periodontology
Guangdong Provincial Stomatological Hospital
Guangzhou, China

Weihua Fan, DDS
Professor and Chair
Department of Preventive Dentistry
Guangdong Provincial Stomatological Hospital
Guangzhou, China

Xiong Zhang, DDS
Professor and Chair
Department of Periodontology
Guangdong Provincial Stomatological Hospital
Guangzhou, China

Serge Dibart, DMD
Professor
Department of Periodontology and Oral Biology
Boston University Henry M. Goldman School of Dental Medicine
Boston, Massachusetts

William De Vizio, DMD
Vice President, Clinical Dental Research Department
Colgate-Palmolive Company
Piscataway, New Jersey

Foti Panagakos, DMD, PhD
Director, Clinical Dental Research Department
Colgate-Palmolive Company
Piscataway, New Jersey

Yun-Po Zhang, MSc, PhD
Director, Clinical Dental Research Department
Colgate-Palmolive Company
Piscataway, New Jersey