Journal of Dental Research

http://jdr.sagepub.com Dental Caries in HIV-seropositive Women

J.A. Phelan, R. Mulligan, E. Nelson, J. Brunelle, M.E.A.F. Alves, M. Navazesh and D. Greenspan J DENT RES 2004; 83; 869 DOI: 10.1177/154405910408301109 The online version of this article can be found at: http://jdr.sagepub.com/cgi/content/abstract/83/11/869

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RESEARCH REPORTS
Clinical

J.A. Phelan1*, R. Mulligan2, E. Nelson1, J. Brunelle3, M.E.A.F. Alves4, M. Navazesh2, and D. Greenspan5
of Oral Pathology (Mail Code 9436), New York University, College of Dentistry, 345 East 24th Street, New York, NY 10010, USA; 2 University of Southern California School of Dentistry, Los Angeles, CA, USA; 3formerly with National Institute of Dental and Craniofacial Research, NIH, Bethesda, MD, USA; 4University of Illinois at Chicago College of Dentistry, Chicago, IL, USA; and 5University of California San Francisco, San Francisco, CA, USA; *corresponding author, joan.phelan@nyu.edu
1Department

Dental Caries in HIV-seropositive Women

J Dent Res 83(11):869-873, 2004

INTRODUCTION
eports of oral findings associated with Human Immunodeficiency Virus R (HIV) infection have focused on oral mucosal lesions and periodontal disease. Studies that include dental caries experience in HIV-seropositive adults are rare (Glick et al., 1998; Jacob et al., 1998; Bretz et al., 2000; Brown et al., 2002). The objective of this study was to determine if there was a relationship between HIV infection and dental caries indices among women enrolled in the Women's Interagency HIV Study (WIHS).

ABSTRACT
Reports that compare dental caries indices in HIVseropositive (HIV+) subjects with HIVseronegative (HIV-) subjects are rare. The objective of this study was to determine if there was an association between HIV infection and dental caries among women enrolled in the Women's Interagency HIV Study. Subjects included 538 HIV+ and 141 HIV- women at baseline and 242 HIV+ and 66 HIV- women at year 5. Caries indices included DMFS and DFS (coronal caries) and DFSrc (root caries). Crosssectional analysis of coronal caries data revealed a 1.2-fold-higher caries prevalence among HIV+ women compared with HIV- women. Longitudinally, DMFS increased with increasing age and lower average stimulated salivary volume. Root caries results were not significant except for an overall increased DFSrc associated with smoking. Anti-retroviral therapy was not identified as a risk factor for dental caries. KEY WORDS: dental caries, HIV, women.

METHODS
The WIHS
The WIHS is an ongoing study investigating HIV disease in women that includes the largest cohort of HIV+ women being studied in the United States (Barkan et al., 1998). The WIHS medical core was initiated in 1994 and an oral substudy added in 1995. The wealth of medical and immunological data available, the inclusion of coronal and root caries examinations, and a comparable HIV- control group provide a unique opportunity for the study of dental caries experience in HIV+ women. WIHS medical core sites are located in the Bronx, Brooklyn, Chicago, Washington, DC, San Francisco, and Los Angeles. A separate, centralized site manages data entry and coordinates analyses. HIV+ and HIV- women were recruited from similar sources, resulting in a cohort of subjects with comparable demographic and HIV risk factors (Barkan et al., 1998). Medical core visits are scheduled every 6 mos. From the WIHS core database, HIV status and HIV risk conditions, socio-demographics, smoking status, medications, and primary markers of HIV infection (e.g., CD4, CD8, and HIV RNA) are available for oral health studies. Laboratory testing for HIV-1 RNA and lymphocyte subsets are documented elsewhere (Anastos et al., 2002).

The Oral Substudy

Oral substudy sites are associated with the medical core sites at the Bronx, Chicago, Los Angeles, and San Francisco. Any woman enrolled in the WIHS at these sites was eligible for the oral substudy. Women were enrolled in the oral substudy after providing informed consent to the protocol approved by institutional review boards at each site. The demographics of the oral substudy cohort closely resembled that of the WIHS medical core (Mulligan et al., 2004). Oral substudy examination visits were scheduled every 6 mos, ideally within 2 wks, but no longer than 2 mos after the medical core visit. The oral substudy protocol was developed jointly by the oral investigators and representatives from the NIDCR. The protocol included an oral health questionnaire, measurement of unstimulated and stimulated salivary flow, evaluation of cervical lymph nodes and major salivary glands, an examination for mucosal lesions, and assessment of the number of teeth, dental plaque, gingival banding, status of the interdental papillae, periodontal attachment loss, restorations, coronal caries, and root caries. Procedures for the assessment of

Received August 25, 2003; Last revision August 1, 2004; Accepted August 23, 2004

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salivary flow, salivary glands, and oral mucosal lesions are documented elsewhere (Greenspan et al.,, 2000; Mulligan et al., 2000; Navazesh et al., 2000). Criteria for caries assessment were developed from those used in recent national surveys (NIDR, 1991). We questioned subjects to identify teeth missing due to disease. Caries assessments were performed on all permanent teeth present, excluding third molars and teeth lost to trauma. Examiners were initially trained and calibrated by NIDCR "gold standard" examiners. Subsequent calibration sessions found less than 5% disagreement in tooth-surface coding between examiners and the "gold standard trainer".

Oral Study Variables

Data collected from coronal and exposed root surfaces were transformed into coronal and root caries indices: DMFS (Decayed, Missing, and Filled Surfaces), DFS (Decayed, Filled Surfaces), and DFSrc (Decayed, Filled Surfaces, Root Caries). The number of permanent teeth present was also recorded. The smoking variable was defined as 'currently smoking' or 'not currently smoking'. Salivary flow variables were 'unstimulated' (< 0.1 mL/min vs. > 0.1 mL/min) and stimulated (> 0.4 mL/min < 0.7 mL/min vs. > 0.7 mL/min) salivary flow volume. Age and racial/ethnic groups (non-Hispanic Black, nonHispanic White, and Latina/Hispanic) used were similar to those of the NHANES II reports (Winn et al. , 1996). Remaining racial/ethnic categories were combined into one group. Subject comparisons by age group reflect the baseline age of study subjects. For year 5, the reader should add 5 yrs to each age group. Categories used to assess the effect of anti-retroviral therapy on dental caries indices included: no anti-retroviral therapy, monotherapy, combination therapy, and highly active antiretroviral treatment (HAART). The anti-retroviral therapy data were derived from subjects' self-reported use of these medications and were obtained at each core visit. These anti-retroviral categories are used in other WIHS analyses and are described elsewhere (Anastos et al., 2002).

variables. Other continuous variables that were included by a stepwise process of elimination were: age, number of permanent teeth, CD4 count, CD8 count, and HIV viral load. HIV status (HIV-seropositive, HIV-seronegative), unstimulated salivary flow volume, anti-retroviral therapy type, and smoking status were entered as categorical data. SPSS 11.0 and STATA 7.0 statistical software were used for the data analyses. Differences in the dental caries experience between the HIV-seropositive and -seronegative groups were determined by ANOVA, two-tailed statistics by a comparison of means. We used regression models to perform longitudinal analyses of the same data. We used linear regression models to measure whether the independent variable, HIV status, was a predictor of the dependent outcome variables: DMFS, DFS, DFSrc. Generalized Estimation Equations (GEE) were used for the longitudinal analyses. GEE analysis was used because it is an analysis that takes into account all possible correlations for data with repeated measures. In this manner, the average caries index per subject estimates the development of dental caries during any six-month interval. Throughout all analyses, p-values of < 0.05 were considered to indicate statistically significant findings.

RESULTS
At baseline, oral substudy subjects included 584 HIV+ and 151 HIV- women. By year 5, attrition and deaths reduced the cohort to 242 HIV+ and 66 HIV- women. Subjects who were edentulous at the baseline examination (n = 53) and those who seroconverted from HIV-seronegative to -seropositive during the course of the study (n = 3) were excluded, resulting in a total of 679 subjects at baseline (538 HIV+ and 141 HIV-) and 308 subjects at year 5 (242 HIV+ and 66 HIV-). The HIVseropositive and -seronegative cohorts closely resembled each other in age and race/ethnicity (Table 1).

Coronal Caries
Overall, bivariate analysis of the data from the baseline and five-year examinations showed approximately a 1.2-fold higher coronal caries prevalence for HIV+ women as measured by DMFS, at both the baseline and year 5 (p = 0.01 and p = 0.04. respectively) (Table 2). HIV-seropositive subjects had statistically significantly fewer permanent teeth (p = 0.03) than HIV- subjects at the initial baseline examination.

Data Analysis
DMFS, DFS, DFSrc, and number of permanent teeth from the baseline (10/1/95 to 3/31/96) and the tenth (4/1/2000 to 9/30/2000) oral substudy visits were used to make comparisons by HIV status in cross-sectional analyses. Longitudinal regression analysis of DMFS and DFSrc were modeled as continuous dependent
Table 1. Subject Demographics at Baseline and at Year 5

n* Baseline All subjects HIV+ HIVYear 5 All subjects HIV+ HIV* **

Age**

< 18

Age Groups* 18-44

45-64

Black (non-Hisp.)

Race/Ethnicity* White Latina/ (non-Hisp.) Hispanic

All Others

679 538 (79.2%) 141 (20.8%)

36.7 7.8 37.1 7.8 35.4 7.7

2 (0.3%) 2 (0.4%) 0 (0%)

584 (86.0%) 455 (84.6%) 129 (91.5%)

93 (13.7%) 81 (15.1%) 12 ( 8.5%)

354 (52.1%) 103 (15.2%) 281 (52.2%) 82 (15.2%) 73 (51.8%) 21 (14.9%)

211 (31.1%) 11 (1.6%) 168 (31.2%) 7 (1.3%) 43 (30.5%) 4 (2.8%)

308 242 (78.6%) 66 (21.4%)

40.7 7.5 40.8 7.5 40.4 7.8

0 (0%) 0 (0%) 0 (0%)

214 (69.9%) 168 (69.7%) 46 (70.8%)

92 (30.1%) 73 (30.3%) 19 (29.2%)

185 (60.1%) 142 (58.7%) 43 (65.2%)

37 (12.0%) 31 (12.8%) 6 ( 9.1%)

80 (26.0%) 64 (26.4%) 16 (24.2%)

6 (1.9%) 5 (2.1%) 1 (1.5%)

Number and percent (%). Age shown is mean age at time period indicated (mean 1 SD).
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Comparisons considering unstimulated and stimulated estimated instead. When the ratio was used, parameter estimates salivary volume showed a similar statistically significant trend, did not significantly change, and this new variable combination i.e., the DMFS mean index was higher and there were fewer remained statistically significant in the final model, i.e. , total numbers of teeth for HIV+ subjects as compared with remaining negatively associated with DMFS (p = 0.01), as was HIV- subjects (Table 2b). This trend continued at year 5, with the number of teeth. Subjects' age was positively associated with unstimulated salivary volume associated with higher DMFS (p DMFS. There was no significant association with HIV viral = 0.04) and stimulated salivary volume closely approaching load, anti-retroviral therapy type, or salivary flow volume. statistical significance (p = 0.06). For the longitudinal analysis of root caries, the variables At baseline, for the entire cohort, DMFS was significantly were the same as those used for coronal caries. When all higher, and there were significantly fewer Table 2. Mean Caries Index Scores and Number of Teeth at Baseline and Year 5 by HIV permanent teeth in the older age group as Status and then by Unstimulated and Stimulated Salivary Volume compared with the younger age group (p = 0.00) (Table 3). For subjects 18-44 yrs of DMFS DFSrc Number of Teeth age, there was a significantly higher DMFS n Mean SD Mean SD Mean SD among HIV+ subjects compared with HIVsubjects (p = 0.03) at both baseline and year (a) Mean DMFS, DFSrc, and Number of Teeth by HIV Status 5 examinations. None of the other age comparisons showed statistically significant Baseline Exam differences. DFS was analyzed because teeth HIV+ 538 44.0 30.0 1.9 4.6 22.0 6.5 included as missing could have been due to HIV141 37.1 27.3 1.3 4.7 23.3 6.0 either caries or periodontal disease, and the P-value (0.01)* (0.20) (0.03)* components of DFS refer strictly to caries Five-year Exam (Winn et al. , 1996). There were no HIV+ 242 53.7 33.6 1.8 5.5 20.2 7.2 statistically significant findings for DFS by HIV66 44.5 28.2 0.8 2.1 21.9 6.6 HIV status (Table 3).

Root Caries
The differences in DFSrc between HIV+ and HIV- subjects were not statistically significant (Table 2a). Age range comparisons for DFSrc were inconsistent and not statistically significant (Table 3). At baseline, HIV+ subjects in the 18- to 44-year age group had a 1.6-fold higher prevalence of root caries than the HIV- subjects, while the opposite was true for those in the 45-to 64year age group, in which the HIV- controls had a root caries rate 1.4-fold higher than that in the HIV+ subjects. By year 5, HIV+ subjects in both age groups had a 2.3-fold higher caries prevalence than HIV- subjects. Baseline and year 5 comparisons for DFSrc, with unstimulated and stimulated salivary volume considered, showed no statistically significant findings (Table 2b).

P-value

(0.04)*

(0.20)

(0.09)

(b) Mean DMFS, DFSrc, and Number of Teeth by HIV Status and Salivary Volume Baseline Exam Unstimulated HIV+ < 0.1 mL/min > 0.1 mL/min HIV- < 0.1 mL/min > 0.1 mL/min P-value Five-Year Exam Unstimulated HIV+ < 0.1 mL/min > 0.1 mL/min HIV- < 0.1 mL/min > 0.1 mL/min P-value

150 383 29 110

50.3 32.4 41.3 28.6 48.0 26.9 34.1 26.8 (0.01)*

2.4 5.5 1.7 4.2 3.7 9.7 0.6 1.4 (0.20)

20.2 7.3 22.7 5.9 21.7 6.8 23.8 5.8 (0.03)*

86 153 17 48

65.0 33.3 47.6 32.4 56.3 31.8 40.4 26.2 (0.04)*

1.5 2.8 1.9 6.6 1.8 3.5 0.5 1.2 (0.18)

18.0 7.6 21.4 6.7 18.7 7.2 23.0 6.2 (0.10)

Longitudinal Analysis
The results of the longitudinal analysis are shown for all subjects and then for HIV+ subjects separately (Table 4a). From the baseline measure, for the entire cohort, there was no significant difference associated with HIV status. DMFS increased with increasing age and with decreasing number of teeth, CD4 count, and volume of stimulated saliva. For HIV+ subjects alone, the variables remaining in the final regression model for coronal caries included age, CD4 count, CD8 count, and number of teeth. Since there was a resulting statistical confounding effect with CD4 and CD8 lymphocyte counts, the ratio, e.g. , CD4/CD8, of the 2 variables was

Baseline Exam Stimulated HIV+ > 0.4 < 0.7 mL/min 185 > 0.7 mL/min 321 HIV- > 0.4 < 0.7 mL/min 50 > 0.7 mL/min 88 P-value Five-year Exam Stimulated HIV+ > 0.4 < 0.7 mL/min 150 > 0.7 mL/min 83 HIV- > 0.4 < 0.7 mL/min 34 > 0.7 mL/min 31 P-value *

46.4 31.7 41.6 28.4 32.9 24.9 38.2 27.4 (0.01)*

2.2 4.8 1.7 4.6 0.5 1.1 1.7 5.9 (0.19)

21.1 7.0 22.8 5.8 24.7 5.2 22.9 6.0 (0.02)*

53.1 32.2 53.5 35.7 44.3 28.9 45.2 28.2 (0.06)

1.3 3.9 1.9 6.2 1.3 2.7 0.2 0.7 (0.22)

20.5 6.8 20.0 7.8 22.3 6.8 21.4 6.6 (0.13)

Statistically significant difference between HIV status groups, ANOVA (p < 0.05).

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subjects were analyzed together, the variables remaining in the final working model included age, number of teeth, unstimulated salivary volume, and current smokers (Table 4b). There was no association with HIV status or CD4 or CD8 lymphocyte counts. The direction of association for age, number of teeth, and salivary flow was not different from that for coronal caries in this group, except that it was unstimulated rather than stimulated salivary volume that was negatively associated with root caries. In this model, there was a positive association between root caries and smoking (p = 0.01). For HIV+ subjects alone, the variables remaining in the final regression model included age, number of teeth, and average stimulated salivary volume. Root caries increased with increasing age (p = 0.02), decreasing number of teeth, and stimulated salivary volume (p = 0.03 and p = 0.03, respectively). There was no association with CD4 or CD8 lymphocyte counts, HIV viral load, or anti-retroviral therapy.

Table 3. Coronal and Root Caries and Number of Teeth by HIV Status Within Age Groups DMFS** Mean SD DFS Mean SD DFSrc Mean SD No. Teeth** Mean SD

Subgroups*

Prevalence at Baseline <18 HIV+ 2 HIV0 18-44 HIV+ 455 HIV129 45-64 HIV+ 81 HIV12 Prevalence at Year 5* < 18 HIV+ 0 HIV0 18-44 HIV+ 168 HIV46 45-64 HIV+ 73 HIV19 *

12 8.5 40.6 29.0*** 34.6 26.1*** 64.0 27.9 64.3 27.2

12.0 8.5 16.9 11.8 16.5 11.6 17.3 14.4 17.6 13.1

1.0 0.0 1.8 4.7 1.1 4.8 2.3 4.1 3.2 3.2

28.0 0.0 22.7 6.1 24.0 5.7 17.6 6.7 18.3 7.0

47.0 33.0*** 40.0 28.4*** 69.1 30.2 55.6 25.7

18.3 11.9 16.5 10.2 19.5 13.4 19.8 17.0

1.6 5.2 0.7 1.9 2.3 6.3 1.0 2.4

21.5 6.8 22.8 6.6 17.3 7.2 19.7 6.6

Baseline age: The reader should add 5 yrs to the age groups shown, to reflect time from baseline. ** Overall, statistically significant difference across age groups, ANOVA, p = 0.00. *** Age-specific statistically significant difference by HIV status within specified age group, ANOVA, p = 0.03.

Table 4. Longitudinal Analysis: Parameter Estimates from Regression Models over a Five-year Period Variables* (a) Coronal Caries (DMFS) All subjects Age Number of teeth CD4n CD8n Stimulated saliva Age Number of teeth CD4/CD8 ratio 0.58 ( 0.47, 0.69) -3.23 (-3.36, -3.11) -0.00 (-0.00, -0.00) 0.00 (-0.00, 0.00) -0.35 (-0.68, -0.02) 0.69 ( 0.43, 0.94) -2.92 (-3.24, -2.60) -2.34 (-3.97, -0.72) 0.00 0.00 0.04 0.13 0.04 0.00 0.00 0.01 Estimate (95% CI) P-value**

DISCUSSION
The results of this study show a cross-sectional increase in mean DMFS among HIV+ women compared with HIVwomen at both baseline and year 5, with no significant difference in DFSrc. The reasons for the increased DMFS prevalence among HIV+ subjects were not explained by either the cross-sectional or the longitudinal analyses and remain unclear. Interpretation of the DMFS is complicated by the fact that missing teeth included in the index could be due to either caries or periodontal disease. Examination of mean DFS did not help to clarify this problem. Analysis of gingival/periodontal findings among WIHS subjects has not found significant differences between HIV+ and HIVwomen (Mulligan et al. , 2004), suggesting that the differences in the numbers of teeth, and thus the 'missing' component of the DMFS in this cohort, are more likely associated with caries than with periodontal disease. To date, only one HIV study has reported dental caries findings transformed to DMFS (Bretz et al., 2000). In that study, all subjects were HIV+ and were predominantly men. The overall DMFS prevalence was 42.9 28.9, a finding very similar to that of our study, in that, among HIV+ women, the overall DMFS at baseline was 44.0 30. The results for the root caries index are not as clear as those for coronal caries. Although there appeared to be a trend toward an increased prevalence of root caries in HIV+ women, this did not reach significance. Subsequent longitudinal analyses with data from additional WIHS visits may reveal clearer results. The association between smoking and an increased incidence of root caries was seen across the entire cohort. Smoking has been reported to be a significant

HIV+ subjects

(b) Root Caries (DFSrc) All subjects Age Number of teeth Unstimulated saliva Current smoker Age Number of teeth Stimulated saliva 0.05 ( 0.01, 0.08) -0.09 (-0.13, -0.05) -0.50 (-0.96, -0.02) 0.54 ( 0.14, 0.94) 0.08 ( 0.01, 0.14) -0.09 (-0.17, -0.01) -0.43 (-0.83, -0.03) 0.01 0.00 0.04 0.01 0.02 0.03 0.03

HIV+ subjects

**

Variables used for longitudinal analyses were HIV status, age, number of teeth, anti-retroviral therapy types, CD4+ and CD8+ lymphocyte counts, stimulated and unstimulated salivary volume, HIV viral load, and smoking status (current or not current smoker). GEE population-averaged model, STATA, 7.0, statistical significance p < 0.05, controlled for race.

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risk indicator for dental caries and strongly associated with periodontal disease (Axelsson et al., 1998; Pihlstrom, 2001; Calsina et al., 2002; Jansson and Lavstedt, 2002). Examination of the relationship among smoking, gingival recession, and root caries in WIHS subjects may clarify this finding. Access to dental care, salivary flow, and medications are areas that require further study. In the overall WIHS cohort at baseline, more HIV+ than HIV- women reported that they had received dental care in the preceding 6 mos (Barkan et al., 1998), and, similarly, in the oral substudy at baseline, HIV+ women were more likely than HIV- women to have seen a dentist in the preceding 6 mos (Mulligan et al. , 2004). Differences in DMFS could be related to access to dental care and variations in dental professional practices. The prevalence of salivary gland disease and decreased salivary flow has been reported to be increasing in HIV-infected individuals (Patton et al., 2000). Previously reported studies from the WIHS have also reported increased prevalences of decreased unstimulated salivary flow (Navazesh et al., 2000) and increased salivary gland enlargement (Mulligan et al. , 2000) among HIV+ women. In this study, salivary flow was associated, albeit inconsistently, with increased DMFS in both the cross-sectional and longitudinal results. The associations in the longitudinal analysis between DMFS and decreased CD4/CD8 ratio suggest another area to be explored. After many iterations of estimation equations, there was no significant difference in coronal or root caries by HIV status, nor did the results of this study support a relationship between anti-retroviral therapy and increased dental caries risk. This is consistent with the results of the study reported by Bretz et al. (2000). Anecdotal reports have suggested a relationship between anti-retroviral therapy and dental caries (Glick et al., 1998), and an association between decreased salivary flow and HAART in the WIHS oral cohort has been reported (Navazesh et al. , 2003). Combination anti-retroviral therapy emerged during the time of this study. At baseline, more than half of the HIV+ subjects in the oral cohort were not yet taking any antiretroviral therapy (356/679), and by year 5, less than half of the remaining HIV+ subjects were taking HAART (121/308). This study may not have been long enough for us to see the effect of anti-retroviral therapy on dental caries indices.

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ACKNOWLEDGMENTS
Data in this manuscript were collected by the Oral Substudy of the Women's Interagency HIV Study (WIHS) Collaborative Study Group with centers (Principal Investigators) at New York City/Bronx Consortium (Joan Phelan); The Connie Wofsy Study Consortium of Northern California (Deborah Greenspan. John S. Greenspan); Los Angeles County/Southern California Consortium (Roseann Mulligan); Chicago Consortium (Mario Alves); and Data Coordinating Center (Alvaro Muoz, Stephen J. Gange). The authors acknowledge the support and encouragement of Dr. Maryann Redford. The WIHS is funded by the National Institute of Allergy and Infectious Diseases, with supplemental funding from the National Cancer Institute, the National Institute of Child Health & Human Development, the National Institute on Drug Abuse, and the National Institute of Dental and Craniofacial Research (U01-AI-35004, U01-AI-31834, U01-AI-34994, U01-AI34989, U01-HD-32632, U01-AI-34993, U01-AI-42590, M01RR00071, and M01-RR00083).

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