Abstract
Background/Objectives:
Limited research is available on the relationship between oral health symptoms and cognitive function among community-dwelling U.S. Chinese older adults. The purpose of this study was to examine the associations between tooth/gums symptoms and changes in cognitive function.
Design:
Two-wave epidemiological study.
Setting:
Population Study of Chinese Elderly in Chicago (PINE).
Participants:
U.S. Chinese older adults (N=2,713; mean age = 72.6 years old, 58.4% - women)
Measurements:
We selected self-reported oral (tooth and gum) symptoms as independent variables. To examine changes in cognitive function (Wave 2 – Baseline), we chose the following three domains: episodic memory (East Boston Memory Test); executive function (Symbol Digit Modalities Test); and working memory (Digit Span Backwards). In addition, we assessed global cognitive function by constructing a composite measure of global cognitive function.
Results:
At baseline, 1,297 (47.8%) reported having teeth symptoms and 513 (18.9%) participants reported having gum symptoms. Adjusting for sociodemographic and health-related characteristics, participants who reported having teeth symptoms at baseline, experienced their global cognition decrease by 0.07 units (estimate = − 0.07; p = 0.003) and their episodic memory decrease by 0.07 units (estimate= − 0.07; p = 0.026). Participants who reported having teeth symptoms at baseline, experienced a faster rate of decline in global cognition for every additional year (estimate = 0.02; p = 0.047). However, this effect disappeared once we adjusted for all covariates (estimate= 0.02; p = 0.069). We found no significant relationship between baseline gum symptoms and change of cognitive function.
Conclusion.
Having teeth symptoms was associated with decline in cognitive function among U.S. Chinese older adults. Developing policy measures aimed at ameliorating health and improving cognition in this high-risk, fast-growing population in the U.S. would need to include oral health preventative and dental care services.
Keywords: oral health, cognition, older adults, Chinese, cognitive change
INTRODUCTION
Oral health is an important part of well-being and overall health in older adults.1 For example, poor oral health in older adults is associated with decreased quality of life,2 depression,3 and hypertension.4 Poor oral health has also been linked to poor cognition5 and cognitive decline.6 When examining the associations between oral health measures and risk for cognitive decline or incident dementia, the methodological limitations of previous studies included inconsistencies in oral health and cognition measures as well as small samples.7 While some studies6,8 reported a positive association between poor oral health and cognitive decline, other did not.9,10
Racial and ethnic minorities are particularly vulnerable to the negative consequences of poor oral health due to lack of access to preventative dental services11 further exacerbated by a language barrier and low socioeconomic status.12 Chinese Americans comprise the largest Asian immigrant and one of the fastest growing minority population in the United States.13 Over the past decade, the population of U.S. community-dwelling Chinese older adults increased by 55% compared to the general growth rate of 15% among U.S. older adults.14 Chinese American older adults may disproportionately experience more oral health symptoms15 and face significant barriers in access to dental care and the use of preventive dental care services.16,17
Previous studies found that a greater number of tooth loss was associated with better cognitive function and slower rate of cognitive decline,5 and higher risk of dementia18 in Chinese older adults. Previous studies did not address cognitive decline associated with oral health symptoms in older American ethnic minorities. Older Chinese Americans may be at a particular risk for having oral health symptoms due to not having dental insurance or not visiting a dental clinic on a regular basis.16 Furthermore, previous research did not explore the relationship between oral health symptoms and specific cognitive domains.7 Given the role of cognitive domains in the dementia diagnosis,19 oral health symptoms may be associated with some, but not all cognitive domains.
The objectives of our study were to: 1) examine the associations between tooth/gum symptoms and change in cognitive function in U.S. community-dwelling Chinese older adults, and 2) examine the association between tooth/gum symptoms and change of individual cognition domains.
METHODS
Study Design and Data Source
In this retrospective, epidemiological study we used data from the Population Study of ChINese Elderly PINE. The New York University IRB designated our study as exempt from human subject review. The PINE study team collected baseline data between 2011 and 2013 using in-home interviews. Detailed description of the baseline PINE data collection is available elsewhere. 20 The second wave of data was completed in 2015. Of 3,157 baseline respondents, follow-up interviews were completed with 2,713 older adults (86% of baseline participants). Compared to those who agreed to participate in Wave 2, those who did not complete the Wave 2 interview were older and had worse cognitive function performance.21
Measures
Oral health symptoms.
We selected self-reported oral health (tooth and gum) symptoms as independent variables. At the time of the interview when reviewing past medical history, the PINE study team asked the participants, “Have you had these symptoms in the past?” We defined “teeth symptoms” if the respondents selected “teeth” as their answer. We defined “gum symptoms” if the participants chose “gums” as their answer.
Cognitive function.
The PINE team administered five cognitive tests at both waves during in-home interviews. Four tests measured three cognitive domains – executive function, episodic and working memory. Detailed description of cognitive measures in this sample have been published elsewhere.21,22 Briefly, executive function was assessed using the Symbol Digit Modalities Test (SDMT) – an 11-item test measuring rapid perceptual comparisons of numbers and symbols in 90 seconds (range 0–80).23 To assess episodic memory, the researchers used the composite score of the East Boston Memory Test (Immediate and Delayed Recall of brief stories; range 0–24).24 Working memory was measured by the Digit Span Backwards.24 In addition, to estimate global cognitive function, the researchers constructed a composite measure of global cognitive function using all five tests (SDMT, East Boston Memory test Immediate and Delayed Recall, Digit Span Backwards, and MMSE).22 To avoid minimal floor and ceiling effects, a composite score was calculated by transforming each participant’s score on the individual cognitive test to a z score based on the mean and standard deviation of the distribution of the scores of all respondents, and then averaging z scores across all cognitive tests.22
Covariates.
The following covariates have previously been shown to be associated with oral health25 and cognition.21 We included two domains of covariates in our analyses: sociodemographic and health-related factors measured at baseline. We used the following sociodemographic variables in our analyses: age (years), gender (male - 0, female - 1), marital status (not married coded as 0, married as 1), living arrangement (defined as a number of household members), language preference (English/Mandarin coded as 0, Cantonese/ Taishanese coded as 1), years in the U.S., years in the community, income, and years of education. Age was measured in chronological years and centered at 72. Health-related factors included the number of medical comorbidities (defined as a count of chronic conditions that a participant told (s)he has by a doctor, nurse, or a therapist), smoking status (never smoked, current or former smoker), and overall social support. We measured the overall social support using the average of six responses on the Health and Retirement Study social support scale (Cronbach’s alpha 0.73).26 Previous research findings indicated an association of social support with cognitive function26 in community-dwelling U.S. Chinese older adults.
Time.
We measured time as the difference between baseline and Wave 2 interviews. The mean was 1.92 (SD = 0.30) years (range 1.75 to 3.72 years).21
Data analysis.
Descriptive chi-squared statistics were used to compare sociodemographic and health-related characteristics between groups with and without oral health symptoms at baseline. Spearman correlations coefficients were used to examine the bivariate associations between baseline oral health symptoms and changes in three cognitive function domains. The change in cognitive function was measured by subtracting baseline cognitive z score test scores from wave 2 responses. Mixed-effect regression models were run to examine the associations between baseline teeth/gum symptoms and the changes in global cognition, executive function, episodic and working memory. Model 1 tested the main effect of oral health symptoms with adjustment for time, baseline oral health symptoms, and oral health symptoms x time. Model 2 added sociodemographic variables. Model 3 further added health-related characteristics. Given the possibility of co-occurring teeth and gum symptoms at baseline, teeth problems were controlled for in the gum model and vice versa. The analyses were completed using SAS, Version 9.2 (SAS Institute Inc, Cary, NC, USA).
RESULTS
Detailed information on cognitive function changes, sociodemographic and health characteristics associated with cognitive function in the PINE sample is available elsewhere.21 Of the 2,713 respondents at baseline, 1,297 (47.8%) reported having teeth symptoms and 513 (18.9%) participants reported having gum symptoms. At baseline 422 (15.6%) reported having both teeth and gum symptoms. Table 1 presents baseline characteristics and their association with oral health symptoms. Compared to participants who had no teeth symptoms, participants with teeth symptoms at baseline were younger, married, lived with more household members, resided in the U.S. and their neighborhood for a shorter period, reported less income, and were currently smoking. Compared to participants who had no gum symptoms at baseline, older adults with gum symptoms at baseline were younger, lived with more household members, resided in the U.S. and their neighborhood for a shorter period, had less income, and more medical conditions.
Table 1:
Baseline characteristics and their association with tooth/gum symptoms N=2,713
Teeth symptoms | Gum symptoms | |||||
---|---|---|---|---|---|---|
Variables | With teeth symptoms (n = 1,297) | Without teeth symptoms (n = 1,416) | t or chi2 (p value) | With gum symptoms (n = 513) | Without gum symptoms (n = 2,200) | t or chi2 (p value) |
Age (mean, SD) | 72.2 (8.2) | 73.0 (8.1) | 2.6 (0.009) | 71.0 (7.9) | 73.0 (8.2) | 5.2 (< 0.001) |
Sex, N (%) | ||||||
Female | 736 (56.8) | 848 (60.0) | 2.7 (0.097) | 310 (60.4) | 1,274 (57.9) | 1.1 (0.297) |
Male | 561 (43.3) | 568 (40.1) | 203 (39.6) | 926 (42.1) | ||
Education (mean, SD) | 8.7 (5.0) | 8.6 (5.1) | −0.97 (0.333) | 8.6 (4.9) | 8.7 (5.1) | 0.2 (0.822) |
Marital Status, N (%) | ||||||
Married | 943 (72.7) | 978 (69.2) | 4.1 (0.043) | 370 (72.1) | 1,551 (70.6) | 0.5 (0.484) |
354 (27.3) | 436 (30.8) | 143 (27.9) | 647 (29.4) | |||
Not married | ||||||
Living arrangement (mean, SD) | 2.0 (2.0) | 1.6 (1.8) | 28.0 (<0.001) | 2.1 (2.0) | 1.8 (1.8) | 7.7 (0.005) |
Language preference, N (%) | ||||||
Cantonese or Taishanese | 992 (76.5) | 1,114 (78.7) | 1.9 (0.172) | 387 (75.4) | 1,719 (78.1) | 1.7 (0.187) |
Mandarin or English | 305 (23.5) | 302 (21.3) | 126 (24.6) | 481 (21.9) | ||
Years in the US (mean, SD) | 18.9 (12.3) | 20.4 (12.7) | 3.2 (0.002) | 16.9 (10.9) | 20.3 (12.8) | 6.1 (<0.001) |
Years in neighborhood (mean, SD) | 11.0 (10.3) | 12.9 (11.0) | 27.0 (<0.001) | 9.5 (8.9) | 12.5 (11.0) | 35.0 (<0.001) |
Income (mean, SD) | 1.8 (1.0) | 2.0 (1.2) | 20.0 (<0.001) | 1.8 (1.0) | 2.0 (1.1) | 8.8 (0.003) |
Medical conditions (mean, SD) | 2.1 (1.5) | 2.1 (1.4) | 0.006 (0.941) | 2.2 (1.5) | 2.0 (1.4) | 6.1 (0.014) |
Smoking status, N (%) | ||||||
Current smoker | 168 (13.0) | 130 (9.2) | 11.2 (0.004) | 57 (11.1) | 241 (11.0) | 0.02 (0.990) |
Former smoker | 241 (18.6) | 250 (17.7) | 92 (17.9) | 399 (18.2) | ||
Non-smoker | 887 (68.4) | 1035 (73.1) | 364 (71.0) | 1558 (70.9) | ||
Overall Social support (mean, SD) | 30.0 (3.1) | 30.2 (3.3) | 1.81 (0.071) | 30.1 (2.9) | 30.1081 (3.3) | −0.2 (0.880) |
Global cognition z score (mean, SD) | −0.04 ( 0.8) | −0.003 (0.8) | 1.5 (0.144) | 0.01 (0.8) | −0.03 (0.8) | −1.1 (0.254) |
Episodic memory z score (mean, SD) | −0.05 (0.9) | −0.01 (1.0) | 1.2 (0.249) | 0.02 (0.9) | −0.05 (1.0) | −1.5 (0.143) |
Executive function z score (mean, SD) | −0.05 (0.9) | −0.06 (0.9) | −0.3 (0.768) | 0.040 (0.9) | −0.07 (0.9) | −2.3 (0.023) |
Working memory z score (mean, SD) | −0.0004 (1.0) | 0.004 (1.0) | 0.1 (0.915) | 0.04 (1.0) | −0.006 (1.0) | −0.9 (0.384) |
Table 2 presents the relationship between baseline teeth symptoms and change of cognitive function. Adjusting for sociodemographic and health-related characteristics, participants who reported having teeth symptoms at baseline, experienced their global cognition decrease by 0.07 units (Global cognition Model 3; estimateteeth symptoms = − 0.07; p = 0.003) and their episodic memory decrease by 0.07 units (Episodic memory Model 3; estimateteeth symptoms = − 0.07; p = 0.026). Participants who reported having teeth symptoms at baseline, experienced a faster rate of decline in global cognition for every additional year (Global cognition Model 1; estimateteeth symptoms X time = 0.02; p = 0.047). However, this effect disappeared once we adjusted for all covariates (Global cognition Model 3; estimateteeth symptoms X time = 0.02; p = 0.069). We found no significant relationship between baseline gum symptoms and change of cognitive function (Table 3).
Table 2:
Association between Baseline Teeth symptoms and Changes in Cognitive Function, Estimated from Mixed-Effects Models
Global cognition | Episodic memory | Executive function | Working memory | |||||||||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Model 1 A | Model 2 B | Model 3 C | Model 1 A | Model 2 B | Model 3 C | Model 1 A | Model 2 B | Model 3 C | Model 1 A | Model 2 B | Model 3 C | |||||||||||||
Estimate (SE) | P value | Estimate (SE) | P value | Estimate (SE) | P value | Estimate (SE) | P value | Estimate (SE) | P value | Estimate (SE) | P value | Estimate (SE) | P value | Estimate (SE) | P value | Estimate (SE) | P value | Estimate (SE) | P value | Estimate (SE) | P value | Estimate (SE) | P value | |
Intercept | 0.01 (0.02) | 0.762 | 0.07 (0.05) | 0.133 | −0.28 (0.11) | 0.013 | −0.001 (0.03) | 0.799 | −0.03 (0.06) | 0.603 | −0.46 (0.15) | 0.002 | −0.03 (0.03) | 0.215 | 0.09 (0.06) | 0.167 | −0.31 (0.15) | 0.039 | 0.01 (0.03) | 0.767 | 0.23 (0.06) | < 0.001 | 0.0004 (0.15) | 0.998 |
Time | −0.05 (0.01) | < 0.001 | −0.05 (0.01) | < 0.001 | −0.05 (0.01) | < 0.001 | −0.01 (0.01) | 0.439 | −0.006 (0.01) | 0.635 | −0.01 (0.01) | 0.637 | −0.02 (0.01) | 0.189 | −0.02 (0.01) | 0.192 | −0.02 (0.01) | 0.192 | −0.05 (0.01) | < 0.001 | −0.05 (0.01) | < 0.001 | −0.05 (0.01) | < 0.001 |
Teeth symptoms | −0.07 (0.03) | 0.038 | −0.08 (0.02) | 0.001 | −0.07 (0.02) | 0.003 | −0.06 (0.04) | 0.121 | −0.08 (0.03) | 0.019 | −0.07 (0.03) | 0.026 | −0.04 (0.04) | 0.373 | −0.03 (0.03) | 0.315 | −0.02 (0.03) | 0.437 | −0.01 (0.04) | 0.784 | −0.02 (0.03) | 0.485 | −0.02 (0.03) | 0.612 |
Teeth symptoms × Time | 0.02 (0.01) | 0.047 | 0.02 (0.01) | 0.069 | 0.02 (0.01) | 0.069 | 0.006 (0.02) | 0.768 | 0.001 (0.02) | 0.953 | 0.001 (0.02) | 0.953 | 0.02 (0.02) | 0.323 | 0.02 (0.02) | 0.329 | 0.02 (0.02) | 0.329 | −0.006 (0.02) | 0.725 | −0.004 (0.02) | 0.830 | −0.004 (0.02) | 0.829 |
Gum symptoms | 0.07 (0.04) | 0.080 | 0.04 (0.039) | 0.169 | 0.04 (0.039) | 0.162 | 0.08 (0.04) | 0.062 | 0.04 (0.04) | 0.247 | 0.04 (0.04) | 0.239 | 0.11 (0.05) | 0.025 | 0.03 (0.04) | 0.476 | 0.03 (0.04) | 0.430 | 0.03 (0.05) | 0.475 | 0.03 (0.04) | 0.493 | 0.02 (0.04) | 0.563 |
Estimate (Standard Error)
Model 1: test of main effect of teeth symptoms at baseline with adjustment for time, and teeth symptoms × time
Model 2: Model 1 + sociodemographic characteristics
Model 3: Model 2 + health-related characteristics
Table 3:
Association between Baseline Gum symptoms and Changes in Cognitive Function, Estimated from Mixed-Effects Models
Global cognition | Episodic memory | Executive function | Working memory | |||||||||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Model 1 A | Model 2 B | Model 3 C | Model 1 A | Model 2 B | Model 3 C | Model 1 A | Model 2 B | Model 3 C | Model 1 A | Model 2 B | Model 3 C | |||||||||||||
Estimate (SE) | P value | Estimate (SE) | P value | Estimate (SE) | P value | Estimate (SE) | P value | Estimate (SE) | P value | Estimate (SE) | P value | Estimate (SE) | P value | Estimate (SE) | P value | Estimate (SE) | P value | Estimate (SE) | P value | Estimate (SE) | P value | Estimate (SE) | P value | |
Intercept | −0.002 (0.02) | 0.920 | 0.06 (0.05) | 0.186 | −0.29 (0.11) | 0.001 | −0.01 (0.02) | 0.594 | −0.04 (0.06) | 0.544 | −0.47 (0.15) | 0.001 | −0.04 (0.03) | 0.163 | 0.08 (0.06) | 0.188 | −0.32 (0.15) | 0.036 | 0.007 (0.03) | 0.796 | 0.23 (0.06) | < 0.001 | 0.002 (0.15) | 0.991 |
Time | −0.04 (0.01) | < 0.001 | −0.04 (0.01) | < 0.001 | −0.04 (0.01) | < 0.001 | −0.003 (0.01) | 0.764 | −0.0006 (0.01) | 0.952 | −0.0006 (0.01) | 0.955 | −0.01 (0.01) | 0.312 | −0.01 (0.01) | 0.319 | −0.01 (0.01) | 0.319 | −0.05 (0.01) | < 0.001 | −0.05 (0.01) | < 0.001 | −0.05 (0.01) | < 0.001 |
Gum symptoms | 0.07 (0.04) | 0.082 | 0.04 (0.03) | 0.165 | 0.04 (0.03) | 0.159 | 0.10 (0.05) | 0.036 | 0.07 (0.04) | 0.118 | 0.07 (0.04) | 0.115 | 0.11 (0.05) | 0.040 | 0.02 (0.04) | 0.623 | 0.02 (0.04) | 0.574 | 0.05 (0.05) | 0.293 | 0.05 (0.04) | 0.282 | 0.04 (0.04) | 0.329 |
Gum symptoms × Time | −0.003 (0.01) | 0.834 | −0.004 (0.01) | 0.762 | −0.004 (0.01) | 0.763 | −0.02 (0.02) | 0.344 | −0.03 (0.02) | 0.265 | −0.03 (0.02) | 0.267 | 0.01 (0.02) | 0.596 | 0.01 (0.02) | 0.622 | 0.01 (0.02) | 0.622 | −0.02 (0.02) | 0.309 | −0.02 (0.02) | 0.318 | −0.02 (0.02) | 0.322 |
Teeth symptoms | −0.05 (0.03) | 0.107 | −0.06 (0.02) | 0.0006 | −0.06 (0.02) | 0.014 | −0.05 (0.03) | 0.111 | −0.08 (0.03) | 0.007 | −0.07 (0.03) | 0.011 | −0.03 (0.04) | 0.502 | −0.02 (0.03) | 0.482 | −0.01 (0.03) | 0.646 | −0.02 (0.04) | 0.656 | −0.03 (0.03) | 0.365 | −0.02 (0.03) | 0.490 |
Model 1: test of main effect of gum symptoms at baseline with adjustment for time, and gum symptoms × time
Model 2: Model 1 + sociodemographic characteristics
Model 3: Model 2 + health-related characteristics
DISCUSSION
In our study, we found that participants who reported having teeth symptoms at baseline, experienced change in their cognition. Specifically, for having baseline teeth symptoms, global cognition and episodic memory both declined. We found that sociodemographic and health-related covariates accounted for most of the relationship between baseline teeth symptoms and the rate of cognitive decline in global cognition. Having gum symptoms at baseline showed no significant relationship with any of the cognitive domains.
Chinese older adults face barriers, which may contribute to our findings. For example, in a sample of 1,288 Asian Americans living in New York City, 41.5% reported not receiving annual oral health examinations.27 Furthermore, factors that contributed to the lack of annual oral health examinations included poor English fluency, low educational attainment, and lack of dental insurance. Lack of English proficiency compared to English fluency was associated with a two-fold increase of not receiving oral health examinations.27 Similarly, in another study of older Asian Americans, older adults with limited English fluency were 3.5 more times likely to lack dental health insurance. Furthermore, older Asian Americans who lacked dental insurance were 6.4 times less likely to use preventive dental care services.16
Our study did not find an association between gum symptoms and cognitive function. Cultural factors may have partially contributed to our findings. Chinese older adults may view teeth symptoms as more acute dental problems compared to chronic gum symptoms, such as bleeding or swollen gums, making gum problems less likely to be reported. Moreover, they may rely on self-treatment (i.e. Vitamin C supplementation, drinking tea or rinsing with salt water) and delay seeking dental care treatment.28 Periodontitis starts out symptomless; therefore, older adults are less likely to seek oral health treatments. Periodontitis, however, is a major contributor to tooth loss, tooth migration, and ultimately, masticatory dysfunction.29
In our study, we found significant associations between baseline teeth symptoms and change in episodic memory. Deficits in episodic memory (i.e. ability to retain new information) are most common in older adults with mild cognitive impairment making them more likely to progress to Alzheimer’s disease dementia.30 Furthermore, changes in episodic memory are often reported in older adults several years before the onset of dementia. Therefore, in a short follow-up period we are more likely to capture changes in the episodic memory, compared to other cognitive domains (i.e. executive function, working memory).
Our study has several limitations. First, the average follow-up time of less than 2 years may not be long enough to detect cognitive changes in our sample. Second, we used self-reported general oral health symptoms as predictors for changes in cognitive function. We were not able to examine potential associations between a more precise objective measure of poor oral health (i.e. toothaches, tooth decay, bleeding or swollen gums) and cognitive function. Subjective self-reported oral health symptoms may not correlate highly with the direct clinical evaluations; thus, we cannot ascertain the effect of tooth loss and periodontal disease on cognition. Third, we were not able to ascertain the timing of oral health symptoms. Fourth, due to 14% sample attrition and the fact that those who did not complete the Wave 2 interview were older and had worse cognitive function performance,21 our findings may be more pertinent to older adults with better cognitive function. Additionally, we were not able to include factors related to the use of preventative oral health services, such as dental health insurance. Asian older adults who do not have dental insurance or lack English proficiency are less likely to receive oral health care.27 This study, however, was the first step toward gaining a better understanding of the relationship between oral health symptoms and changes in cognitive function in a large U.S. Chinese older adult population.
Despite these limitations, this study has important policy and practice implications. Our findings point to the importance of assessing oral health symptoms in this population. Developing policy measures aimed at ameliorating health and improving cognition in this high-risk, fast-growing population in the U.S. would need to include oral health preventative and dental care services. Medical and dental care providers can identify problematic oral health symptoms as risk factors of cognitive decline. Outreach programs that target older adults to improve the awareness of these problems can then be developed. Dental care community outreach programs should focus their information on practical ways to prevent oral health problems and provide information on accessible treatment options.
Our study has important implications for future research. Future studies should include objective oral health assessments, when examining the association between oral health symptoms and cognitive function in this population. Second, studies with a longer follow-up period may be needed to observe more clinically meaningful changes in cognition. Additionally, future studies should consider how the timing of oral health symptoms is related to changes across multiple cognitive domains.
ACKNOWLEDGMENTS:
Sponsor’s Role: NIH/NIDCR 1 U01 DE027512-01 (PI: Bei, WU)
Footnotes
Financial Disclosure: None
Conflict of Interest: None
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