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Allergic rhinitis and periodontitis among Korean adults: results from a nationwide population-based study (2013–2015)

  • Eun-Jeong Kim
  • Yong-Keum Choi
Open Access
Research article
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Part of the following topical collections:
  1. Head and neck disorders

Abstract

Background

The purpose of this study was to examine whether allergic rhinitis is associated with periodontal disease in a representative sample of elderly Korean people that was adjusted for socio-demographic factors, oral and general health behaviors, and systemic health status.

Methods

A total of 10,643 subjects who were between 20 and 59 years of age participated in the Korean National Health and Nutrition Examination Survey and underwent cross-sectional examination. Medical history of allergic rhinitis was collected from participants by questionnaire; additionally, periodontal status was assessed using a Community Periodontal Index score of 3 or 4. Multivariate logistic regression analysis was conducted to adjust for socio-demographic variables, oral health status and behaviors, and general health status and behaviors. All analyses were performed using a complex sampling design.

Results

Allergic rhinitis and periodontitis showed a significant inverse association. After adjusting for all confounders, a trend of decreasing periodontitis risk was observed as allergic rhinitis increased. The adjusted odds ratio of periodontitis was 0.79 (0.66–0.95) for patients with allergic rhinitis.

Conclusion

A significant inverse association between allergic rhinitis and periodontal status was demonstrated in this patient population.

Keywords

Adults Allergic rhinitis Epidemiology Periodontitis 

Abbreviations

AR

Allergic rhinitis

CI

Confidence interval

CPI

Community periodontal index

CPITN

Community Periodontal Index of Treatment Needs

FDI

Federation Dentaire Internationale

KCDCP

Korean Center for Disease Control and Prevention

KNHANES

Korean National Health and Nutrition Examination Survey

OR

Odds ratio

PD

Pocket depth

PSU

Primary sampling units

Th1

T-helper type 1

Th2

T-helper type 2

WHO

World Health Organization

Background

Periodontal disease is a major bacterial infection that causes periodontal tissue destruction and bone resorption; it may result in tooth loss [1].

Chronic periodontal disease is reported in more than 90% of the American population [2]. In Korea, the prevalence of periodontal disease in adults over 19 years of age is 29.2%; furthermore, 3 out of 10 adults have periodontal disease that requires treatment, and the number of outpatients with periodontal disease continues to increase [3].

The most significant risk factor for periodontal disease is the composition of subgingival bacteria. Actinobacillus actinomycetemcomitans is considered to be a pathogen implicated in several forms of aggressive periodontitis, while Porphyromonas gingivalis and Tan-nerella forsythia are considered to be important etiological agents of chronic periodontitis [4]. In addition, age, sex, stress, socioeconomic status, systemic disease, inadequate host immune response, personal oral hygiene and smoking are factors that affect the development of periodontal disease [5].

Studies on the association between periodontal and systemic diseases have been recently reported [6, 7]. The most common systemic illnesses that are associated with periodontal disease include the following: diabetes mellitus, hyperglycemia, atherosclerosis, atheromatous disease, abnormal pregnancy, respiratory disease, osteoporosis, rheumatoid arthritis, cancer, and cardiovascular disease [8]. In addition, studies have suggested that there is an association of between periodontal disease and allergic rhinitis [9].

Allergic rhinitis (AR) is a common allergic disease in which the nasal mucosa becomes hypersensitive to a variety of causative agents; it results in sinusitis, nasal congestion, otitis media, sleep disorders, and asthma [10]. AR is known to produce periodontal disease by causing chronic facial nasal obstruction and impaired breathing, leading to facial osteoarthritis, dental malocclusion, and dry mouth [11, 12].

On the other hand, the “hygiene hypothesis” suggests that infections in early infancy have preventive effects against the pathogenesis of allergies. Likewise, a low prevalence of periodontal disease has been reported in patients with allergic diseases [13].

Periodontal disease is a complex process in which pathogens interact with the host’s immune response; this process persists within the periodontal pockets and produces an acquired immune response that defends against microorganisms and pathogens [14]. Accordingly, the “hygiene hypothesis” posits that, in arthritic rhinitis and other immune diseases, exposure to various microorganisms activates and strengthens the immune system, thereby decreasing the incidence of periodontal disease. Studies investigating the association between allergic (e.g., rhinitis) and periodontal diseases are underway but are currently inadequate.

Thus, the aim of this study was to investigate the association between allergic rhinitis and periodontal disease by examining a representative sample of elderly Korean patients who were adjusted for socio-demographic factors, oral and general health behaviors, and systemic health status.

Methods

Study design and subject selection

The data were derived from the Sixth Korean National Health and Nutrition Examination Survey (KNHANES), which was conducted by the Korean Center for Disease Control and Prevention (KCDCP) from 2013 to 2015. The Korean Ministry of Health and Welfare performed the survey. The sampling protocol for the KNHANES was designed to employ a complex, stratified, multistage, and probability-based sampling design with proportional allocation in Korea. The KNHANES was approved by the institutional review board of the KCDC (2013-07CON-03-4C, 2013-12EXP-03-5C, and 2015–01-02-6C). The target population of the survey included all non-institutionalized civilian Korean individuals who were 1 year of age or older. The survey used stratified multistage probability sampling units that were based on geographic area, gender, and age; these sampling units were based on the households reported in the 2005 National Census Registry. The 2005 census data was used and 200 primary sampling units (PSU) were selected across Korea. The final sample for the KNHANES included 4600 households. In the KNHANES, physical and oral examinations, as well as blood sampling, were performed at mobile examination centers where trained staff members took all clinical measurements. The KNHANES included highly structured health-related questionnaires. Each participant signed an informed consent form during the survey. Previous publications of the KNHANES have described the sampling methods and survey contents in detail [15]. Out of the 22,948 participants of the KNHANES, only individuals who were between 20 and 59 years of age and had complete datasets were included in our analysis; consequently, we analyzed a total of 10,643 participants (4469 males and 6179 females) (Table 1). The following two exclusion criteria utilized: (1) participants who did not complete an oral examination and (2) subjects with one or more missing answers in their questionnaire.
Table 1

Association with sociodemographic characteristics, oral health behaviors, and systemic health status based on Allergic Rhinitis (n = 10,643)

Variables

Number

Non-AR

AR

p value

N

% (95% CI)a

N

% (95% CI)a

Age

     

< 0.001

 20–29

1777

1371

77.1 (74.8–79.2)

406

22.9 (20.8–25.2)

 

 30–39

2643

2144

81.2 (79.4–82.8)

499

18.8 (17.2–20.6)

 

 40–49

2989

2556

86.2 (84.8–87.5)

433

13.8 (12.5–15.2)

 

 50–59

3239

2937

90.6 (89.5–91.7)

302

9.4 (8.3–10.5)

 

Sex

     

< 0.001

 Male

4469

3914

86.5 (85.2–87.6)

555

13.5 (12.4–14.8)

 

 Female

6179

5094

81.6 (80.6–82.7)

1085

18.4 (17.3–19.4)

 

Monthly Household income

     

0.459

 < 25%

905

782

86.2 (83.1–88.8)

123

13.8 (11.2–16.9)

 

 25–50%

2542

2153

83.8 (82.0–85.5)

389

16.2 (14.5–18.0)

 

 50–75%

3382

2862

84.1 (82.6–85.5)

520

15.9 (14.5–17.4)

 

 > 75%

3768

3167

83.7 (82.2–85.0)

601

16.3 (15.0–17.8)

 

Education

     

< 0.001

 Primary school

711

639

89.5 (86.5–91.9)

72

10.5 (8.1–13.5)

 

 Middle school

873

777

87.9 (85.1–90.2)

96

12.1 (9.8–14.9)

 

 High school

4063

3448

84.2 (82.9–85.5)

615

15.8 (14.5–17.1)

 

 College

4366

3514

80.0 (78.7–81.4)

852

20.0 (18.6–21.3)

 

Smoking status

     

< 0.001

 No

8314

6959

83.0 (82.0–83.9)

1355

17.0 (16.1–18.0)

 

 Yes

2334

2049

87.2 (85.6–88.7)

285

12.8 (11.3–14.4)

 

Hypertension

     

< 0.001

 No

9578

8049

83.5 (82.6–84.4)

1529

16.5 (15.6–17.4)

 

 Yes

1061

950

89.5 (87.2–91.4)

111

10.5 (8.6–12.8)

 

Diabetes mellitus

     

< 0.001

 No

10,252

8646

83.8 (83.0–84.6)

1606

16.2 (15.4–17.0)

 

 Yes

387

353

91.2 (87.6–93.9)

34

8.8 (6.1–12.4)

 

Obesity

     

< 0.001

 Underweight

500

384

76.1 (71.3–80.3)

116

23.9 (19.7–28.7)

 

 Normal

6756

5667

83.5 (82.5–84.5)

1089

16.5 (15.5–17.5)

 

 Obese

3289

2868

86.4 (85.0–87.8)

421

13.6 (12.2–15.0)

 

Asthma

     

< 0.001

 No

10,414

8881

84.8 (83.9–85.6)

1533

15.2 (14.4–16.1)

 

 Yes

234

127

54.8 (47.6–61.9)

107

45.2 (38.1–52.4)

 

Atopic dermatitis

     

< 0.001

 No

10,338

8811

84.7 (83.8–85.5)

1527

15.3 (14.5–16.2)

 

 Yes

310

197

65.2 (58.8–71.1)

113

34.8 (28.9–41.2)

 

Periodontitis

     

< 0.001

 No

7211

5938

81.9 (80.9–82.9)

1273

18.1 (17.1–19.1)

 

 Yes

2448

2201

89.6 (88.1–91.0)

247

10.4 (9.0–11.9)

 

Tooth-brushing frequencies

     

< 0.001

 Never

366

351

94.2 (90.5–96.6)

15

5.8 (3.4–9.5)

 

 Once daily

739

642

85.3 (82.1–88.0)

97

14.7 (12.0–17.9)

 

 Twice daily

3592

3058

84.3 (82.8–85.7)

534

15.7 (14.3–17.2)

 

 More than 3 times

5946

4952

83.0 (81.9–84.1)

994

17.0 (15.9–18.1)

 

Use of floss

     

< 0.001

 No

7917

6826

85.6 (84.6–86.5)

1091

14.4 (13.5–15.4)

 

 Yes

2726

2177

79.5 (77.7–81.1)

549

20.5 (18.9–22.3)

 

Use of interproximal brush

     

0.001

 No

8234

7027

84.8 (83.9–85.7)

1207

15.2 (14.3–16.1)

 

 Yes

2409

1976

81.4 (79.5–83.2)

433

18.6 (16.8–20.5)

 

Use of mouthwash

      

 No

8407

7105

83.8 (82.8–84.8)

1302

16.2 (15.2–17.2)

0.219

 Yes

2236

1898

85.1 (83.4–86.6)

338

14.9 (13.4–16.6)

 

Dental visit during the past one year

    

0.051

 No

7258

6190

84.6 (83.6–85.5)

1068

15.4 (14.5–16.4)

 

 Yes

3385

2813

82.9 (81.5–84.3)

572

17.1 (15.7–18.5)

 

AR allergic rhinitis

Values are presented as number (%)

Monthly Household income: monthly average family equivalent income (−monthly average household income/ status based on Allergic Rhinitis

Obesity; Normal; Body Mass Index (BMI) 18.5 to < 25, Underweight: BMI < 18.5, and Obesity: BMI ≥25.0 kg/m2

Bold values denotes statistical significance at p < 0.05

aWeighted percent, 95% Confidence Interval (CI), and p-value obtained by Chi-square test

Assessment of periodontitis

Trained dentists performed the oral health examination. The clinical examinations were performed with the subject seated in a dental chair while dentists utilized a light, mouth mirror, and World Health Organization (WHO) periodontal probe. The WHO community periodontal index (CPI) was used to assess the extent of periodontitis. According to the WHO guidelines, a CPI probe with a 0.5-mm ball tip was utilized with a probing force of approximately 20 g. Periodontitis was defined as a CPI greater than or equal to “code 3,” which indicates that at least one site had a pocket depth (PD) > 3.5 mm (“code 4” indicates a pocket > 5.5 mm). The index tooth numbers were 11, 16, 17, 26, 27, 31, 36, 37, 46 and 47 according to the Federation Dentaire Internationale (FDI) system. A sextant was examined only if two or more teeth were present that were not scheduled for extraction. If no index teeth were present in a sextant that was examined, all remaining teeth were probed and the highest score was recorded as the score for that sextant. The CPI was scored form 0 to 4 as follows: 0 (normal), 1 (gingivitis with bleeding on probing), 2 (presence of calculus), 3 (PD ≥ 3.5 mm) and 4 (PD ≥ 5.5 mm). The interexaminer reliability (mean of kappa value) was 0.84.

Assessment of allergic rhinitis

AR was defined according to patients’ self-reported answers to the question, “Has your doctor ever diagnosed you with AR?” Only patients who had received at least one AR diagnosis from a certified otolaryngologist were considered.

Assessment of potential confounders

We analyzed socio-demographic factors such as age, sex, household income, and education, as well as oral (e.g., tooth brushing frequency, prior history of periodontitis, dental visit within the past year, and the use of floss, interproximal brush, and mouthwash) and general health behaviors (e.g., smoking status and systemic illnesses such as hypertension, diabetes mellitus, obesity, asthma and atopic dermatitis). Socio-demographic, oral and general health behaviors were assessed by using the questionnaires in an interview format. General health-related factors were assessed using questionnaires, clinical examination and laboratory procedures. Monthly house hold income was categorized into quartiles and adjusted for the number of family members. Educational level was classified into the following four groups: primary school or less, middle school, high school and college. Hypertension, diabetes mellitus, asthma and atopic dermatitis by were diagnosed by a physician. Obesity was assessed using a self-administered questionnaire survey. Dentists carefully assessed each patient’s periodontal status utilizing the Community Periodontal Index of Treatment Needs (CPITN) to quantify the extent of periodontitis. The selected index tooth numbers were 11, 16, 17, 26, 27, 31, 36, 37, 46 and 47. The CPITN Index was scored from 0 to 4 as follows: 0 (normal), 1 (gingivitis with bleeding on probing), 2 (presence of calculus), 3 (pocket depth ≥ 3.5 mm) and 4 (pocket depth ≥ 5.5 mm). Periodontal status was grouped into the following two categories: absence (CPI of 1 to 2) and presence (CPI of 3 to 4) of periodontitis. The frequency of tooth brushing was divided into the following four groups: never, once daily, twice daily and more than three times daily. The use of floss, interproximal brush and mouthwash, as well as dental visits during the past year, were grouped into binomial yes or no categories.

Statistical analysis

The complex sampling design of the survey was utilized to obtain the variances and individual weight of each analyzed factor. To investigate the characteristics of AR and periodontitis patients, a chi-squared test of complex sample analysis with weight application was performed to estimate the weighted proportions (95% confidence interval [CI]) of the total sample population. Multivariate logistic regression analyses were sequentially applied to assess the association between AR and other variables after adjusting for age, sex, household income, education, smoking status, hypertension, diabetes mellitus, asthma, atopic dermatitis, tooth brushing frequency, dental visit during the past year, and the use of floss, interproximal brush, and mouthwash.

A multiple logistic regression analysis of complex samples was carried out to evaluate the weight-adjusted association between AR and periodontitis. Model 1 represents a crude association. Model 2 is adjusted for sociodemographic factors. Model 3 is adjusted for all the variables in Model 2, including oral health status and behaviors. Model 4 is adjusted for all the variables in Model 3, including general health status and behaviors.

To enable the complex survey design involving stratified, random and cluster sampling, the SPSS Complex Samples Procedures were used for all statistical analyses (IBM SPSS Statistics Version 21, IBM Inc., Chicago, IL, USA). A p-value < 0.05 was considered statistically significant.

Results

Characteristics of the study participants

The characteristics of the study participants were categorized by AR. Of the 10,643 participants that were included in the analyses, 1640 (15.4%) had AR (Table 1). In our analysis, chi-squared tests were used to investigate the univariate association between confounding variables and AR. AR was more prevalent among younger participants, females, participants with higher education, and non-smokers. Among individuals with AR, asthma, atopic dermatitis, hypertension, obesity and periodontitis were observed to be more prevalent. Participants with AR were also observed to have greater tooth-brushing frequency and an increased use of both floss and interproximal brushes.

Association between periodontitis and potential confounding variables

The characteristics of the study subjects were categorized by periodontal status after controlling for all possible confounders (Table 2). The demographic characteristics of the participants were noteworthy for a higher percentage of males with periodontitis (30.5%) compared to females (18.7%); the odds ratio (OR) was 1.44 (95% CI: 1.27–1.63) for males with periodontitis. Periodontitis was present in 26.5% of the non-AR group and 15.8% of the AR group; the crude OR was 1.53 (95% CI: 1.28–1.82) for participants with both AR and periodontitis.
Table 2

Univariate association with sociodemographic characteristics, oral health and general health behaviors, and systemic health status based on periodontitis (n = 9659)

Variables

Number

Periodontitis

OR (95% CI)

No

Yes

N

% (95% CI)a

N

% (95% CI)a

Age

 20–29

1657

1582

95.3 (93.9–96.4)

75

4.7 (3.6–6.1)

0.07 (0.05–0.09)

 30–39

2497

2128

84.4 (82.1–86.4)

369

15.6 (13.6–17.9)

0.27 (0.22–0.33)

 40–49

2774

1978

69.4 (67.1–71.6)

796

30.6 (28.4–32.9)

0.61 (0.53–0.70)

 50–59

2982

1712

55.2 (52.7–57.6)

1270

44.8 (42.4–47.3)

Reference

Sex

 Male

4191

2819

69.5 (67.6–71.3)

1372

30.5 (28.7–32.4)

1.44 (1.27–1.63)

 Female

5719

4581

81.3 (79.9–82.7)

1138

18.7 (17.3–20.1)

Reference

Monthly Household income

  < 25%

853

562

66.1 (62.0–70.1)

291

33.9 (29.9–38.0)

1.08 (0.86–1.37)

 25–50%

2357

1700

73.4 (71.1–75.6)

657

26.6 (24.4–28.9)

0.99 (0.84–1.18)

 50–75%

3136

2379

76.3 (74.2–78.2)

757

23.7 (21.8–25.8)

0.92 (0.78–1.08)

  > 75%

3516

2724

78.0 (75.9–79.9)

792

22.0 (20.1–24.1)

Reference

Education

 Primary school

639

355

54.9 (49.8–59.9)

284

45.1 (40.1–50.2)

2.76 (2.13–3.57)

 Middle school

801

474

57.7 (53.8–61.5)

327

42.3 (38.5–46.2)

2.82 (2.30–3.47)

 High school

3728

2781

75.5 (73.6–77.2)

947

24.5 (22.8–26.4)

1.34 (1.16–1.54)

 College

4036

3291

81.5 (79.7–83.2)

745

18.5 (16.8–20.3)

Reference

Smoking status

 No

2084

1301

64.2 (61.5–66.8)

783

35.8 (33.2–38.5)

1.69 (1.47–1.95)

 Yes

7575

5910

79.0 (77.5–80.3)

1665

21.0 (19.7–22.5)

Reference

Hypertension

 No

8931

6837

77.2 (75.8–78.6)

2094

22.8 (21.4–24.2)

0.56 (0.46–0.68)

 Yes

979

563

55.8 (51.9–59.7)

416

44.2 (40.3–48.1)

Reference

Diabetes mellitus

 No

9557

7221

76.2 (74.8–77.6)

2336

23.8 (22.4–25.2)

0.53 (0.40–0.71)

 Yes

353

179

49.4 (43.9–55.0)

174

50.6 (45.0–56.1)

Reference

Obesity

 Underweight

454

393

86.9 (83.0–90.0)

61

13.1 (10.0–17.0)

0.45 (0.32–0.64)

 Normal

6282

4858

77.9 (76.3–79.4)

1424

22.1 (20.6–23.7)

0.75 (0.66–0.85)

 Obese

3088

2069

68.0 (65.8–70.1)

1019

32.0 (29.9–34.2)

Reference

Asthma

 No

9438

7035

75.2 (73.7–76.6)

2403

24.8 (23.4–26.3)

1.14 (0.77–1.69)

 Yes

221

176

79.7 (72.8–85.2)

45

20.3 (14.8–27.2)

Reference

Atopic dermatitis

 No

9365

6946

74.8 (73.3–76.2)

2419

25.2 (23.8–26.7)

2.58 (1.58–4.22)

 Yes

294

265

90.2 (85.1–93.7)

29

9.8 (6.3–14.9)

Reference

Allergic rhinitis

 No

8139

5938

73.5 (72.0–75.0)

2201

26.5 (25.0–28.0)

1.53 (1.28–1.82)

 Yes

1520

1273

84.2 (81.8–86.3)

247

15.8 (13.7–18.2)

Reference

Tooth-brushing frequencies

 Never

270

184

66.7 (59.4–73.3)

86

33.3 (26.7–40.6)

1.16 (0.71–1.88)

 Once daily

670

418

63.3 (58.9–67.6)

252

36.7 (32.4–41.1)

1.36 (1.10–1.67)

 Twice daily

3283

2377

72.8 (70.7–74.7)

906

27.2 (25.3–29.3)

1.11 (0.99–1.23)

 1 (0.99–1.23)re

5433

4230

78.9 (77.3–80.4)

1203

21.1 (19.6–22.7)

Reference

Use of floss

 No

7136

5073

71.9 (70.2–73.5)

2063

28.1 (26.5–29.8)

1.70 (1.48–1.97)

 Yes

2520

2136

85.3 (83.5–86.9)

384

14.7 (13.1–16.5)

Reference

Use of interproximal brush

 No

7448

5522

74.8 (73.3–76.3)

1926

25.2 (23.7–26.7)

0.92 (0.78–1.07)

 Yes

2208

1687

76.9 (74.2–79.3)

521

23.1 (20.7–25.8)

Reference

Use of mouthwash

 No

7602

5701

75.8 (74.3–77.3)

1901

24.2 (22.7–25.7)

0.73 (0.63–0.84)

 Yes

2054

1508

73.2 (70.6–75.6)

546

26.8 (24.4–29.4)

Reference

Dental visit during the past one year

 No

6563

4878

75.1 (73.5–76.6)

1685

24.9 (23.4–26.5)

0.88 (0.78–1.00)

 Yes

3093

2331

75.7 (73.6–77.7)

762

24.3 (22.3–26.4)

Reference

AR, allergic rhinitis

Values are presented as number (%)

Monthly Household income: monthly average family equivalent income (−monthly average household income/behaviors, and systemic health stat

Obesity; Normal; Body Mass Index (BMI) 18.5 to < 25, Underweight: BMI < 18.5, and Obesity: BMI ≥25.0 kg/m2

Bold values denotes statistical significance at p < 0.05

aWeighted percent, 95% Confidence Interval (CI), and p-value obtained by Chi-square test

Association between AR and periodontitis

The associations between periodontitis and AR was analyzed using multivariable logistic regression models. These analyses revealed that the AR was inversely associated with the risk for periodontitis throughout the adjustment processes utilized in Models 1, 2, 3, and 4 (Table 3). After adjusting for socio-demographic factors, oral and general health behaviors, and general health factors, the inverse associations between AR and periodontitis remained significant.
Table 3

Adjusted odds rations (OR) and 95% confidence intervals (CI) between the periodontitis and allergic rhinitis in multiple models (9659)

Variable

Number

OR (95% CI)

Model 1a

Model 2b

Model 3c

Model 4d

Allergic rhinitis

 Yes

2448

0.52 (0.44–0.62)

0.74 (0.62–0.89)

0.76 (0.63–0.91)

0.79 (0.66–0.95)

 No

7211

1

1

1

1

OR odds ratio, CI confidence interval

Bold values denotes statistical significance at p < 0.05

aModel 1 was unadjusted association

bModel 2 was adjusted for sex, age, household income and education

dModel 3 was adjusted for all variables in model 2 and use of floss, use of interproximal brush, use of mouthwash, tooth-brushing frenquencies and dental visit during the past one year

dModel 4 was adjusted for all variables in model 3 and smoking status, hypertension, diabete mellitus, obesity, asthma and atopic dermatitis

Discussion

Our results demonstrated that AR is inversely associated with periodontitis among Korean adults (aged 20–59 years) and that this association remained significant even after adjusting for age, sex, household income, smoking, hypertension, diabetes mellitus, obesity, asthma, atopic dermatitis, periodontitis, tooth brushing frequency, dental visits during the past year, and the use of floss, interproximal brush, and mouthwash. These results were based on a national Korean population sample consisting of 10,643 participants and supported evidence from previous studies showing an inverse association between allergic disease and periodontitis [13]. To the best of our knowledge, this study provides the first evidence showing that AR is inversely associated with the prevalence of periodontitis in middle-aged adults.

We found that AR was more prevalent in women compared to men, which is similar to the results of another study conducted in the US [16]. Our results also showed that participants with lower age had a higher prevalence of AR; accordingly, Skoner reported that AR symptoms develop before the age of 20 years in approximately 80% of cases [17]. In addition, participants who had allergic diseases, such as asthma and atopic dermatitis, showed a higher prevalence of AR. Once a patient has become sensitized to allergens, subsequent exposures appears to trigger a cascade of events that result in AR symptoms [17].

There were a few studies on allergic disease and periodontitis in the literature. Friedrich et al. [13] conducted a study in a large Germany population sample to investigate whether allergic diseases such as hayfever, house dust mite allergy, and asthma were associated with periodontal disease; their study found that an inverse association between periodontitis and respiratory allergies. The present study, also showed an inverse association between periodontitis and allergic rhinitis as well as other allergic disease such as asthma and atopic dermatitis.

Several biological mechanisms have been suggested to explain how periodontopathic bacteria influence allergic rhinitis. Periodontal disease represents early infection, which may elicit an immune response, and the primitive conditions for the onset of periodontal disease may emerge in childhood [17]. Strachan [18] posited the “hygiene hypothesis,” which provides a potential explanation for the T-helper type 1 (Th1)/T-helper type 2 (Th2) paradigm [19, 20]. Allergic disease is Th2-mediated and characterized by the release of IgE; however, bacterial and viral infections are more likely to be Th1-mediated. Th2-derived cytokines inhibit the development of Th1 cells and vice versa. The infection-induced Th1-specific cytokine inhibits the development of allergen-specific Th2 cells. Several studies also supported the hygiene hypothesis [21, 22], suggesting that bacterial colonization elicit a systemic reaction that prevents the onset of allergic diseases.

Little is known about possible relationship between rhinitis and periodontitis. One study by Hung et al. has reported that rhinitis is associated with periodontitis, which is a finding that is different from the current study [9]. It should be noted that Hung et al. did not fully adjust for systemic factors. And another study by Choi et al. has also reported that asthma diagnosis is associated with tooth loss, however, this study focused on asthma not on allergic rhinitis [23].

There are four major strengths of our study. First, the KNHANES data utilized for this study was a large national survey that is representative of the Korean population. Seconds, professional examiners documented the general health examination and laboratory analyses. Third, trained dentists performed periodontal examinations and assessed oral health status. These results provide the first evidence linking periodontitis and AR among middle-aged adults. Finally, confounding factors showed a statistically significant independent association with periodontitis in our data, thus corroborating the reliability of our data.

This study has some limitations. Because the KNHANES is a cross-sectional survey, it is not possible to identify a causal relationship between AR and periodontitis; however, the biological plausibility of this association may indicate this relationship. Furthermore, the periodontal status was assessed using the CPI; therefore, the prevalence of periodontitis may have been overestimated or underestimated because the CPI’s use of representative teeth may include pseudo pockets [24]. Additionally, the method for defining AR was self-questionnaire, which runs the risk of recall bias, even if the question involves a physician’s diagnosis. Case control and cohort studies are needed to investigate the relationship between periodontal disease and AR.

Notwithstanding these limitations, the results of our study are reliable enough to test the hypothesis that AR is inversely associated with periodontitis.

Conclusion

In conclusion, this study found an inverse association between AR. Further case control and cohort studies are needed to confirm the hypothesis and mechanism of this inverse association between AR and periodontitis.

Notes

Acknowledgements

This study was suppoprted by research fund from the National Research Foundation of Korea (NRF-2017R1C1B5017185).

Availability of data and materials

The data used for this study are owned KCDCP and were used under a confidentiality agreement to allow access to individual level data for the current study. Researchers can request the data from KCDCP.

Authors’ contributions

YKC designed the study, interpreted the data and revised the draft; EJK analyzed the data, wrote the draft, and English proof. All authors approved the final manuscript.

Ethics approval and consent to participate

Not applicable. The data for the research was obtained from an existing database containing details of Korean National Nutritional and Health Survey from 2012 to 2015. The sixth KNHANES was a cross-sectional survey conducted by the Korea Center for Disease Control and Prevention (KCDCP) from 2012 to 2015. The KNHANES was approved by the KCDC Institutional Review Board (2013-07CON-03-4C, 2013-12EXP-03-5C, and 2015–01-02-6C).

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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© The Author(s). 2018

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors and Affiliations

  1. 1.Department of Preventive and Social DentistrySchool of Dentistry, Seoul National UniversitySeoulSouth Korea
  2. 2.Present Address: Department of Dental Hygiene, College of Health Science and Genome-based BioT Convergence InstituteSun Moon UniversityAsan-siSouth Korea

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