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1.  Significance and Implications of Patient-reported Xerostomia in Sjögren's Syndrome: Findings From the National Institutes of Health Cohort 
EBioMedicine  2016;12:270-279.
Xerostomia is a chief complaint of patients with Sjögren's syndrome (SS). However, newer proposals for SS classification remove xerostomia and hyposalivation from the criteria list. Given these developments and the importance of patient-centered research outcomes, we sought to evaluate the utility of patient-reported xerostomia with implications for classification criteria, and clinical trials targeting SS treatment modalities.
A nested case-control study was designed within The National Institute of Dental and Craniofacial Research/National Institutes of Health (NIDCR/NIH) SS Cohort - one of the largest SS cohorts in the US. Clinical characteristics of those with and without xerostomia in SS and other salivary gland dysfunctions were compared. Several analytical methods were employed, including multivariable logistic regression modeling.
The NIDCR/NIH Sjögren's Syndrome Clinic has an open cohort with ongoing enrollment since 1984. This open cohort comprised of 2046 participants by August 27, 2015. Baseline data of 701 SS, 355 Sicca, and 247 ISS participants within the source cohort were analyzed. Xerostomia was highest among SS participants (87.4%, 95% CI: 84.8%–89.8%) compared to Sicca (72.4%, 95% CI: 67.4%–77.0%, p < 0.001) and ISS groups (38.1%, 95% CI: 32.0%–44.4%, p < 0.001). Those with xerostomia were more likely to have SS than Sicca/ISS (OR = 4.98, 95% CI: 3.78–6.56). The ability of xerostomia to screen for SS among those with salivary gland dysfunction was higher than screening for Sicca/ISS. Screening diagnostics of xerostomia were of greater utility compared to hyposalivation. After adjusting for confounding in multivariable modeling, SS participants with xerostomia were more likely to be White (Black/African Americans (OR: 0.40, 95% CI: 0.23–0.68, p-value = 0.001) and Asians (OR: 0.49, 95% CI: 0.25–0.96, p-value = 0.038) were less likely to have xerostomia compared to Whites), have dry eye symptoms for > 3 months (OR: 5.80, 95% CI: 3.62–9.28, p-value < 0.001), a lower Van Bijsterveld score (OR: 0.55, 95%CI: 0.34–0.90, p-value = 0.017), a lower stimulated salivary flow rate (OR: 1.67, 95% CI: 1.06–2.65, p-value = 0.028), a focus score of > 2 (OR: 1.92, 95% CI: 1.20–3.09, p-value = 0.007), and salivary gland swelling (OR: 49.39, 95% CI: 2.02–1206.30, p-value = 0.017). Age, gender, fatigue, pain, anxiety, and autoantibodies were not significantly associated with xerostomia.
Findings from this study indicate that patient-reported xerostomia is highly prevalent among SS patients and is associated with several clinical phenotypes of this complex syndrome, thereby making it an important indicator of SS. The evidence also suggests that xerostomia is not limited to low salivary flow but might be reflective of compositional changes of saliva. Consequently, these findings suggest the need to consider xerostomia in the development of SS classification criteria and in patient-centered outcomes research in SS intervention trials.
This research was supported by the Intramural Research Program of the National Institutes of Health (NIH), National Institute of Dental and Craniofacial Research (NIDCR) Grant # DE000704-15. Dr. Baer is supported by RO1-DE-12354-15A1.
•Xerostomia is highly prevalent among SS patients and is associated with several clinical characteristics of SS.•Test diagnostics of xerostomia and other findings indicate that xerostomia is an important indicator of SS.•Findings of the study have implications for SS classification systems and SS intervention trials.
Research in Context
Data on the prevalence of xerostomia/dry mouth in SS are lacking, despite it being a chief complaint of patients. SS is a complex autoimmune disorder that is defined on the basis of classification criteria. There is ongoing debate on the selection of criteria and a consensus has not yet been reached by the scientific community. There is push to eliminate both xerostomia and hyposalivation, an objective sign of low salivary flow, from SS classification. This study offers evidence on the importance of xerostomia with implications for SS classification. Clinical trials to test newer treatment modalities for SS use classification criteria to define an SS case. Therefore, classification criteria are critical for research and advancement of newer therapeutics for SS. Xerostomia should be targeted as a patient-centered research outcome in SS intervention trials.
PMCID: PMC5078600  PMID: 27639822
Sjogren's syndrome; Xerostomia; Hyposalivation; Autoimmune disorders; Salivary gland dysfunction
2.  Update on Prevalence of Periodontitis in Adults in the United States: NHANES 2009 – 2012 
Journal of periodontology  2015;86(5):611-622.
This report describes prevalence, severity, and extent of periodontitis in the US adult population using combined data from the 2009–2010 and 2011–2012 cycles of the National Health and Nutrition Examination Survey (NHANES).
Estimates were derived for dentate adults 30 years and older from the civilian non-institutionalized population. Periodontitis was defined by combinations of clinical attachment loss (CAL) and periodontal probing depth (PPD) from six sites per tooth on all teeth, except third molars, using standard surveillance case definitions. For the first time in NHANES history, sufficient numbers of Non-Hispanic Asians were sampled in 2011–2012 to provide reliable estimates of their periodontitis prevalence.
In 2009–2012, 46% of US adults representing 64.7 million people had periodontitis, with 8.9% having severe periodontitis. Overall, 3.8% of all periodontal sites (10.6% of all teeth) had PPD≥4 mm and 19.3% of sites (37.4% teeth) had CAL≥3 mm. Periodontitis prevalence was positively associated with increasing age and was higher among males. Periodontitis prevalence was highest in Hispanics (63.5%) and Non-Hispanic blacks (59.1%), followed by Non-Hispanic Asian Americans (50.0%), and lowest in Non-Hispanic whites (40.8%). Prevalence varied two-fold between the lowest and highest levels of socioeconomic status, whether defined by poverty or education.
This study confirms a high prevalence of periodontitis in US adults aged 30 years and older. Prevalence was greater in Non-Hispanic Asians than Non-Hispanic whites, although lower than other minorities. The distribution provides valuable information for population-based action to prevent periodontitis in US adults.
PMCID: PMC4460825  PMID: 25688694
NHANES; Periodontal Disease; Periodontitis; Epidemiology; Surveillance
3.  Association between tobacco use and the upper gastrointestinal microbiome among Chinese men 
Cancer causes & control : CCC  2015;26(4):581-588.
Tobacco causes many adverse health conditions and may alter the upper gastrointestinal (UGI) microbiome. However, the few studies that studied the association between tobacco use and the microbiome were small and underpowered. Therefore, we investigated the association between tobacco use and the UGI microbiome in Chinese men.
We included 278 men who underwent esophageal cancer screening in Henan Province, China. Men were categorized as current, former, or never smokers from questionnaire data. UGI tract bacterial cells were characterized using the Human Oral Microbial Identification Microarray. Counts of unique bacterial species and genera estimated alpha diversity. For beta diversity, principal coordinate (PCoA) vectors were generated from an unweighted UniFrac distance matrix. Polytomous logistic regression models were used for most analyses.
Of the 278 men in this study, 46.8% were current smokers and 12.6% were former smokers. Current smokers tended to have increased alpha diversity (mean: 42.3 species) compared to never smokers (mean: 38.9 species). For a 10 species increase, the odds ratio (OR) for current smoking was 1.29 (95% CI: 1.04–1.62). Beta diversity was also associated with current smoking. The first two PCoA vectors were strongly associated with current smoking (PCoA1 OR 0.66; 95% CI: 0.51–0.87; PCoA2 OR 0.73; 95% CI: 0.56–0.95). Furthermore, Dialister invisus and Megasphaera micronuciformis were more commonly detected in current smokers than in never smokers.
Current smoking was associated with both alpha and beta diversity in the UGI tract. Future work should consider how the UGI microbiome is associated with smoking related diseases.
PMCID: PMC4852095  PMID: 25701246
China; microbiome; tobacco; upper gastrointestinal tract
4.  Beta-Diversity Metrics of the Upper Digestive Tract Microbiome are Associated with Body Mass Index 
Obesity (Silver Spring, Md.)  2015;23(4):862-869.
Studies of the fecal microbiome have implicated the gut microbiota in obesity, but few studies examined the microbial diversity at other sites. We explored the association between obesity and the upper gastrointestinal (UGI) microbial diversity.
The UGI microbiome of 659 healthy Chinese adults with a measured body mass index (BMI) range of 15.0 to 35.7 was characterized using the 16S rRNA gene DNA microarray (HOMIM).
In multivariate-adjusted models, alpha diversity was not associated with BMI. However, beta diversity, assessed by principal coordinate vectors generated from an unweighted unifrac distance matrix of pairwise comparisons, was associated with BMI (third and fourth vectors, p=0.0132 and p=0.0280, respectively). Moreover, beta diversity, assessed by cluster membership (3 clusters), was also associated with BMI; individuals in the first cluster (median BMI 22.35, odds ratio (OR)=0.48, 95% confidence interval (CI)=0.05–4.34) and second cluster (median BMI 22.55, OR=0.26, 95% CI=0.09–0.75) were significantly less likely to be obese (BMI ≥27.5) than those in the third cluster (median BMI 23.59).
A beta-diversity metric of the UGI microbiome is associated with a four-fold difference in obesity risk in this Asian population. Future studies should address whether the UGI microbiome plays a causal role in obesity.
PMCID: PMC4380747  PMID: 25755147
beta-diversity; body mass index; Chinese; microbiome; obesity; upper gastrointestinal tract
5.  Performance of a quality assurance program for assessing dental health in methamphetamine users 
BMC Oral Health  2015;15:76.
Systematic characterization of the dental consequences of methamphetamine (MA) abuse presupposes a rigorous quality assurance (QA) program to ensure the credibility of the data collected and the scientific integrity and validity of the clinical study. In this report we describe and evaluate the performance of a quality assurance program implemented in a large cross-sectional study of the dental consequences of MA use.
A large community sample of MA users was recruited over a 30 month period during 2011–13 and received comprehensive oral examinations and psychosocial assessments by site examiners based at two large community health centers in Los Angeles. National Health and Nutrition Examination Survey (NHANES) protocols for oral health assessments were utilized to characterize dental disease. Using NHANES oral health quality assurance guidelines, examiner reliability statistics such as Cohen’s Kappa coefficients and inter-class correlation coefficients were calculated to assess the magnitude of agreement between the site examiners and a reference examiner to ensure conformance and comparability with NHANES practices.
Approximately 9 % (n = 49) of the enrolled 574 MA users received a repeat dental caries and periodontal examination conducted by the reference examiner. There was high concordance between the reference examiner and the site examiners for identification of untreated dental disease (Kappa statistic values: 0.57–0.75, percent agreement 83–88 %). For identification of untreated caries on at least 5 surfaces of anterior teeth, the Kappas ranged from 0.77 to 0.87, and percent agreement from 94 to 97 %. The intra-class coefficients (ICCs) ranged from 0.87 to 89 for attachment loss across all periodontal sites assessed and the ICCs ranged from 0.79 to 0.81 for pocket depth. For overall gingival recession, the ICCs ranged from 0.88 to 0.91. When Kappa was calculated based on the CDC/AAP case definitions for severe periodontitis, inter-examiner reliability for site examiners was low (Kappa 0.27–0.67).
Overall, the quality assurance program confirmed the procedural adherence of the quality of the data collected on the distribution of dental caries and periodontal disease in MA-users. Examiner concordance was higher for dental caries but lower for specific periodontal assessments.
PMCID: PMC4491420  PMID: 26143495
Dental caries; Methamphetamine use; Reliability; Quality assurance; NHANES
6.  Association between upper digestive tract microbiota and cancer predisposing states in the esophagus and stomach 
The human upper digestive tract microbial community (microbiota) is not well characterized and few studies have explored how it relates to human health. We examined the relationship between upper digestive tract microbiota and two cancer predisposing states, serum pepsinogen I/pepsinogen II ratio (PGI/II) (predictor of gastric cancer risk), and esophageal squamous dysplasia (ESD) (the precursor lesion of esophageal squamous cell carcinoma (ESCC)) in a cross-sectional design.
The Human Oral Microbe Identification Microarray was used to test for the presence of 272 bacterial species in 333 upper digestive tract samples from a Chinese cancer screening cohort. Serum PGI and PGII were determined by enzyme-linked immunosorbent assays. ESD was determined by chromoendoscopy with biopsy.
Lower microbial richness (number of bacterial genera per sample) was significantly associated with lower PGI/II ratio (P=0.034) and the presence of ESD (P=0.018). We conducted principal component (PC) analysis on a β-diversity matrix (pairwise difference in microbiota), and observed significant correlations between PC1, PC3 and PGI/II (P=0.004, 0.009 respectively), and between PC1 and ESD (P=0.003).
lower microbial richness in upper digestive tract was independently associated with both cancer predisposing states in the esophagus and stomach (presence of ESD and lower PGI/II).
PMCID: PMC4011942  PMID: 24700175
microbiota; gastric cancer; esophageal squamous cell carcinoma; esophageal squamous dysplasia; serum pepsinogen I/pepsinogen II ratio
7.  The association between the upper digestive tract microbiota by HOMIM and oral health in a population-based study in Linxian, China 
BMC Public Health  2014;14:1110.
Bacteria affect oral health, but few studies have systematically examined the role of bacterial communities in oral diseases. We examined this relationship in a large population-based Chinese cancer screening cohort.
Human Oral Microbe Identification Microarrays were used to test for the presence of 272 human oral bacterial species (97 genera) in upper digestive tract (UDT) samples collected from 659 participants. Oral health was assessed using US NHANES (National Health and Nutrition Examination Survey) protocols. We assessed both dental health (total teeth missing; tooth decay; and the decayed, missing, and filled teeth (DMFT) score) and periodontal health (bleeding on probing (BoP) extent score, loss of attachment extent score, and a periodontitis summary estimate).
Microbial richness, estimated by number of genera per sample, was positively correlated with BoP score (P = 0.015), but negatively correlated with tooth decay and DMFT score (P = 0.008 and 0.022 respectively). Regarding β-diversity, as estimated by the UniFrac distance matrix for pairwise differences among samples, at least one of the first three principal components of the UniFrac distance matrix was correlated with the number of missing teeth, tooth decay, DMFT, BoP, or periodontitis. Of the examined genera, Parvimonas was positively associated with BoP and periodontitis. Veillonellacease [G-1] was associated with a high DMFT score, and Filifactor and Peptostreptococcus were associated with a low DMFT score.
Our results suggest distinct relationships between UDT microbiota and dental and periodontal health. Poor dental health was associated with a less microbial diversity, whereas poor periodontal health was associated with more diversity and the presence of potentially pathogenic species.
Electronic supplementary material
The online version of this article (doi:10.1186/1471-2458-14-1110) contains supplementary material, which is available to authorized users.
PMCID: PMC4223728  PMID: 25348940
Microbiota; Oral health; Dental caries; Periodontitis; Bleeding on probe; Attachment loss
8.  Quantitative Light Fluorescence (QLF) and Polarized White Light (PWL) assessments of dental fluorosis in an epidemiological setting 
BMC Public Health  2012;12:366.
To determine if a novel dual camera imaging system employing both polarized white light (PWL) and quantitative light induced fluorescence imaging (QLF) is appropriate for measuring enamel fluorosis in an epidemiological setting. The use of remote and objective scoring systems is of importance in fluorosis assessments due to the potential risk of examiner bias using clinical methods.
Subjects were recruited from a panel previously characterized for fluorosis and caries to ensure a range of fluorosis presentation. A total of 164 children, aged 11 years (±1.3) participated following consent. Each child was examined using the novel imaging system, a traditional digital SLR camera, and clinically using the Dean’s and Thylstrup and Fejerskov (TF) Indices on the upper central and lateral incisors. Polarized white light and SLR images were scored for both Dean’s and TF indices by raters and fluorescence images were automatically scored using software.
Data from 164 children were available with a good distribution of fluorosis severity. The automated software analysis of QLF images demonstrated significant correlations with the clinical examinations for both Dean’s and TF index. Agreement (measured by weighted Kappa’s) between examiners scoring clinically, from polarized photographs and from SLR images ranged from 0.56 to 0.92.
The study suggests that the use of a digital imaging system to capture images for either automated software analysis, or remote assessment by raters is suitable for epidemiological work. The use of recorded images enables study archiving, assessment by multiple examiners, remote assessment and objectivity due to the blinding of subject status.
PMCID: PMC3490889  PMID: 22607363
9.  Trends in Oral Health by Poverty Status as Measured by Healthy People 2010 Objectives 
Public Health Reports  2010;125(6):817-830.
Poverty is a significant social determinant for oral health, yet Healthy People 2010 (HP 2010) does not monitor changes in oral health status by poverty. We assessed recent trends for six HP 2010 oral health objectives by poverty status.
We used data from the 1988–1994 and 1999–2004 National Health and Nutrition Examination Surveys to analyze trends for HP 2010 age-specific objectives relating to caries experience, untreated tooth decay, dental sealants, periodontal disease, tooth retention, and complete tooth loss by poverty status.
Dental caries significantly increased from 19% to 24% for children aged 2–4 years, but when stratified by poverty, caries only increased significantly for non-poor 2- to 4-year-old children (10% to 15%) (Objective 21-1a). The largest percentage point increase in dental caries was for non-poor boys (9% to 18%). The use of dental sealants continues to grow in the U.S. The largest percentage point increase in sealant use (Objective 21-8) between the two survey periods was for all poor children aged 8 years (3% to 21%). Among adults aged 35–44 years, periodontal disease significantly declined in the U.S. from 22% to 16% (Objective 21-5b) and more adults retained all of their natural teeth (30% to 38%) (Objective 21-3). However, the increase in tooth retention was significant only for non-poor adults, particularly non-poor men (34% to 48%).
Overall, the oral health status of Americans as measured by HP 2010 objectives mostly showed improvement or remained unchanged between 1998–1994 and 1999–2004. However, some changes in oral health status for some traditionally low-risk groups, such as non-poor children, may be reversing improvements in oral health that have consistently been observed in previous decades. These results suggest that poverty status is an important factor for planning and monitoring future national oral health goals.
PMCID: PMC2966663  PMID: 21121227
10.  Using NHANES oral health examination protocols as part of an esophageal cancer screening study conducted in a high-risk region of China 
BMC Oral Health  2007;7:10.
The oral health status of rural residents in the People's Republic of China has not been extensively studied and the relationship between poor oral health and esophageal cancer (EC) is unclear. We aim to report the oral health status of adults participating in an EC screening study conducted in a rural high-risk EC area of China and to explore the relationship between oral health and esophageal dysplasia.
National Health and Nutrition Examination Survey (NHANES) oral health examination procedures and the Modified Gingival Index (MGI) were used in a clinical study designed to examine risk factors for esophageal cancer and to test a new esophageal cytology sampling device. This study was conducted in three rural villages in China with high rates of EC in 2002 and was a collaborative effort involving investigators from the National Institutes of Health and the Cancer Institute of the Chinese Academy of Medical Sciences.
Nearly 17% of the study participants aged 40–67 years old were edentulous. Overall, the mean number of adjusted missing teeth (including third molars and retained dental roots) was 13.8 and 35% had 7 contacts or less. Women were more likely to experience greater tooth loss than men. The average age at the time of first tooth loss for those with no posterior functional contacts was approximately 41 years for men and 36 years for women. The mean DMFT (decayed, missing, and filled teeth) score for the study population was 8.5. Older persons, females, and individuals having lower educational attainment had higher DMFT scores. The prevalence of periodontal disease (defined as at least one site with 3 mm of attachment loss and 4 mm of pocket depth) was 44.7%, and 36.7% of the study participants had at least one site with 6 mm or more of attachment loss. Results from a parsimonious multivariate model indicate that participants with poor oral health wemore likely to have esophageal dysplasia (OR = 1.59; 95% CI 1.06, 2.39).
This report describes the first use of NHANES oral health protocols employed in a clinical study conducted outside of the United States. The extent and severity of poor oral health in this Chinese study group may be an important health problem and contributing factor to the prevalence of EC.
PMCID: PMC1993835  PMID: 17640341
11.  Influence of cigarette smoking on the overall perception of dental health among adults aged 20-79 years, United States, 1988-1994. 
Public Health Reports  2005;120(2):124-132.
OBJECTIVE: Investigation into the relationship between lifestyle factors (particularly cigarette smoking) and perceived oral health has been limited. Data from the third National Health and Nutrition Examination Survey (NHANES II), 1988-1994, were used to explore this relationship in a large sample of U.S. adults. METHODS: This study used data on 13,357 dentate participants in NHANES III aged 20-79 years. In NHANES III, information on perceived dental health, sociodemographic attributes, smoking status, frequency of dental visits, dental insurance, and general health perception were collected during a home interview, and oral health status was assessed at a mobile examination center. RESULTS: Overall, 34.4% of individuals in the study sample reported having an unfavorable perception of their dental health by qualifying it as "fair" or "poor." Furthermore, 46.6% of smokers had an unfavorable dental health perception, compared to 28.3% of non-smokers. An interaction between smoking and race/ethnicity was found in logistic regression modeling. Stratified results show that cigarette smoking was not a significant predictor for an unfavorable dental health perception among individuals who self-identified as Mexican American, but smoking was a significant predictor for an unfavorable dental health perception among those who identified as non-Hispanic black or non-Hispanic white. CONCLUSIONS: This is the first study to describe the effects of smoking on dental health perception while controlling for examined oral health status. Because perceived dental health is a potential indicator for dental care utilization, a better knowledge of the factors that influence dental health perception is not only important for dental services planning, but also for understanding oral health-related quality of life issues. Additionally, given that smoking may negatively affect dental health perception, these findings have potential implications for smoking cessation activities conducted by dental care providers.
PMCID: PMC1497695  PMID: 15842113
12.  The relationship between blood lead levels and periodontal bone loss in the United States, 1988-1994. 
Environmental Health Perspectives  2002;110(10):997-1002.
An association between bone disease and bone lead has been reported. Studies have suggested that lead stored in bone may adversely affect bone mineral metabolism and blood lead (PbB) levels. However, the relationship between PbB levels and bone loss attributed to periodontal disease has never been reported. In this study we examined the relationship between clinical parameters that characterize bone loss due to periodontal disease and PbB levels in the U.S. population. We used data from the Third National Health and Nutritional Examination Survey (NHANES III), 1988-1994, for the analyses. A total of 10,033 participants 20-69 years of age who completed a periodontal examination and had whole blood tested for lead were examined. Four types of periodontal disease measures were used to indicate oral bone loss: periodontal pocket depth, attachment loss extent, attachment loss severity, and the presence of dental furcations. We found that dental furcations were the best periodontal bone loss indicator for PbB levels (p = 0.005) in a multivariate linear regression model adjusting for sex, age, race/ethnicity, educational attainment, poverty status, smoking, and age of home. Furthermore, after additional modeling, we found a smoking and dental furcation interaction (p = 0.034). Subsequent stratified analyses indicated that current and past smoking is an effect modifier for dental furcations on PbB levels. These findings indicate that increased PbB levels may be associated with advanced periodontal bone loss, particularly among people with a history of smoking.
PMCID: PMC1241025  PMID: 12361924

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