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Dental Research
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The Prevalence of Xerostomia and Salivary Gland Hypofunction in a Cohort of HIV-positive and At-risk
Women
M. Navazesh, R. Mulligan, E. Komaroff, M. Redford, D. Greenspan and J. Pkelan
J DENT RES 2000 79: 1502
DOI: 10.1177/00220345000790071201
The online version of this article can be found at:
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M. Navazeshl*, R. Mulligan1, E. Komaroff2,

M. Redford3, D. Greenspan4, and J. Phelan5
'University of Southern California, School of Dentistry,
Department of Dental Medicine & Public Health, Room 4320,
925 W. 34th Street, Los Angeles, CA 90089-0641; 2New
England Research Institutes, Inc.; 3National Institute of Dental
and Craniofacial Research, Division of Extramural Research;
4University of California, San Francisco, Department of
Stomatology; and 5Department of Veterans Affairs, Medical
Center at Northport; *corresponding author,

The Prevalence of Xerostomia

and Salivary Gland Hypofunction
in a Cohort of HIV-positive
and At-risk Women

navazeshghsc.usc.edu
J Dent Res 79(7): 1502-1507, 2000

ABSTRACT
The association of xerostomia and salivary gland
hypofunction with HIV infection has been
established for men but not for women. We
investigated the prevalence of these conditions in a
national cohort (n = 733) of HIV-positive and atrisk HIV-negative women. Participants in this
prospective cross-sectional study were recruited
from the Women's Interagency HIV Study (WIHS)
at five outpatient USA clinics. Xerostomia was
assessed based on "yes" responses to a dry-mouth
questionnaire. Samples of unstimulated whole and
chewing-stimulated whole saliva were collected
under standardized conditions. The major salivary
glands were also evaluated clinically. The
prevalence of dry-mouth complaint, the absence of
saliva upon palpation, and zero unstimulated whole
saliva (flow rate = 0 mL/min) were significantly (p
= 0.001) higher in HIV-positive women. Adjusted
odds of zero unstimulated whole saliva were
significantly (p = 0.02) higher in HIV-positive
women vs. HIV-negative women (OR= 2.86; 95%
CI, 1.23 to 6.63). Significant (p = 0.03) univariate
association was found between zero unstimulated
whole saliva and CD4 counts. Adjusted odds of
zero unstimulated whole saliva were significantly
(p = 0.02) higher for HIV-positive women with
CD4 < 200 compared with those with CD4 > 500
(OR= 2.61; 95% CI, 1.17 to 5.85). Chewingstimulated flow rates were not significantly
different between seropositive and seronegative
women. The prevalence of xerostomia and salivary
gland hypofunction appears to be significantly
higher in HIV-positive women relative to a
comparable group of at-risk seronegative women.
Immunosuppression levels measured by CD4 cell
counts are significantly associated with xerostomia
and salivary gland hypofunction in a population of
HIV-positive women.

INTRODUCTION
erostomia (subjective complaint of dry mouth) and salivary gland
ypofunction (objective evidence of reduced salivary output) have often been
associated with the Human Immunodeficiency Virus (HIV) infection.
Xerostomia has been reported in 10% of 375 American homosexual males with
or at risk for HIV infection (Silverman et al., 1986), 9% of 74 HIV-infected
Dutch patients (Schulten et al., 1989), 26% of 160 Greek male and female HIVinfected individuals (Laskaris et al., 1992), and 80% of 20 Peruvian HIVpositive patients (Gillespie and Marino, 1993).
Salivary gland hypofunction has been investigated mostly in HIV-infected
men. Stimulated parotid and submandibular/sublingual saliva flow rates are
reported by some investigators to be lower in this population compared with
rates in non-infected controls (Yeh et al., 1988). Other investigators have
reported no significant difference in stimulated parotid or whole saliva flow rates
in HIV-infected patients (Marder et al., 1985). Only one study has examined the
impact of HIV infection on salivary gland function on a longitudinal basis
(Atkinson et al., 1989). The results of this limited (n = 12) study revealed that
submandibular/sublingual function is affected earlier than parotid function, and
that parotid glands become increasingly affected over time.
Our review of the literature revealed that: (1) most of the data were based
on HIV-infected men, not women; (2) there was a paucity of reports for the
HIV-positive women; (3) the terms "xerostomia" and "salivary gland
hypofunction" were used interchangeably; (4) there was no standardized
protocol for the assessment of xerostomia and salivary gland hypofunction; and
(5) no attention was paid to the concurrent use of xerogenic medications and
their impact on salivary gland function. Therefore, we attempted to determine
the prevalence of xerostomia and salivary gland hypofunction in a cohort of
women with or at risk for HIV infection who were participating in the Women's
Interagency HIV Study (WIHS). The WIHS is an unprecedented study of
human immunodeficiency virus among 2626 US women. This study is being
conducted at five clinical sites across the United States, with standardized
protocols. As part of the study protocol, comprehensive interviews, physical
evaluation, and biological sampling procedures are conducted at baseline and
six-month follow-up visits on all WIHS participants. The design and objectives
of the Women's Interagency HIV Study have been described in depth elsewhere
(Barkan et al., 1998).
In conjunction with their routine study visits, a subsample of WIHS
participants undergoes a comprehensive oral examination including
assessments of the salivary glands, soft tissue, periodontia, and teeth-conducted
by trained oral examiners. Findings reported here are based on the assessment of
xerostomia and salivary gland hypofunction data obtained at the baseline visit.

KEY WORDS: xerostomia, salivary gland hypofunction, HIV infection, women.

MATERIALS & METHODS

Received March 25, 1999; Last revision September 9, 1999;

Accepted December 29, 1999

Of the 2626 women participating in the WIHS Core project, approximately 28%
(n = 733) were enrolled in the WIHS Oral Component. All participants provided

1502

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J Dent Res 79(7) 2000 Xerostomia and Salivary Gland Hypofunction in HIV-positive Women
consent to the research protocol that had been reviewed and approved
by the appropriate institutional review boards at the participating
clinical sites. Five hundred eighty-one women were HIV-positive,
and 152 were negative but at risk for HIV infection. The participants'
ages ranged from 17 to 61 years. Xerostomia was assessed based on
the participants' responses to an abbreviated version of a dry-mouth
questionnaire developed by Fox et al. (1987). The abbreviated
questionnaire consisted of the following three questions: (1) Does the
amount of saliva in your mouth seem to be too little, too much, or
you do not notice it? (2) Do you need to sip liquids to aid you in
swallowing dry foods? (3) Does your mouth feel dry when eating a
meal? Salivary gland hypofunction was assessed based on the
following three parameters: (1) the presence or absence of saliva
upon palpation of parotid and submandibular/sublingual glands; (2)
the unstimulated whole saliva flow rate; and (3) the chewingstimulated whole saliva flow rate. All examiners received the same
formal training in performing the study protocols.
Parotid and submandibular/sublingual glands were examined
visually and by palpation according to our previously published
method (Navazesh et al., 1992b). Unstimulated whole saliva was
measured by the draining method (Navazesh and Christensen, 1982).
Participants were asked to fast (with the exception of water) for 90
min prior to the test session. After participants practiced for 1 min,
saliva was collected for 5 min. Participants were asked to lean the
head forward, keep the eyes open, minimize the movement of the
tongue and lips, and allow saliva to drip off the lower lip into a
graduated test tube fitted with a funnel. At the end of 5 min,
participants were asked to expectorate into the test tube. Chewingstimulated whole saliva was collected by the spitting method
(Navazesh and Christensen, 1982). Participants practiced chewing
on a standard-sized gum base for 2 min. These samples were
discarded. The flow rate was then measured over 3 min. Participants
were instructed to void the mouth of saliva at one-minute intervals.
The frequency of chewing was controlled by a metronome set at
approximately 70 beats per min. The majority of the saliva
specimens were collected between 9:00 am and 3:00 pm. Flow rates
were determined as mL per min.

Statistical Analysis
Unstimulated and chewing-stimulated salivary flow rates were
analyzed as continuous and dichotomous outcome measures. The
Wilcoxon rank-sum test was used to evaluate HIV differences for

1503

continuous measures because of considerable skewness of both

unstimulated and stimulated flow rate distributions. For both flow
rates as dichotomous variables, the cutpoint was zero (0 mL/min) vs.
greater than zero flow rates. Univariate associations were tested with
either the Pearson's chi-square or Fisher's exact test, when the
assumptions of the Pearson test were violated, and multivariate
logistic regression was used to determine adjusted odds ratios. All
analyses were done with SAS version 6.12 (SAS Institute, Inc., 1989).

RESULTS
The prevalence of "yes" responses to all three questions on the
dry-mouth questionnaire was significantly higher in the HIVpositive as compared with the HIV-negative women (Table 1).
The prevalence of no saliva upon palpation of both parotid and
submandibular/sublingual glands was significantly higher in
HIV-positive women (Table 2). The mean chewing-stimulated
flow rate was 1.26 mL/min (SD = 1.11; median = 1.0) for the
HIV-positive women and 1.33 mL/min (SD = 1.07; median =
1.0) for HIV-negative women. The chewing-stimulated flow
rates were not significantly different based on the Wilcoxon
rank-sum test. Three percent (18/530) of the HIV-positive
women had zero chewing-stimulated flow rates compared with
2% (3/140) of the HIV-negatives; this is a non-significant
difference.
The mean unstimulated flow rate for HIV-positives was
0.29 mL/min (SD = 0.34; median = 0.20), and for HIVnegatives it was 0.35 (SD = 0.34; median = 0.23). The
Wilcoxon rank-sum test revealed that HIV-positive women had
significantly (p = 0.006) lower unstimulated flow rates as
compared with HIV-negatives. Seventeen percent (95/556) of
HIV-positive women had a zero unstimulated flow rate as
compared with 6% (9/142) of the HIV-negatives. This
difference was significant (p = 0.001). After the individuals
with a zero unstimulated flow rate were removed from the
analysis, the unstimulated flow rates for HIV-positives and negatives were no longer significantly different (p = 0.34).
Therefore, further analyses were based on the identification of
covariates of unstimulated flow rates as only a dichotomous
variable (0 mL/min vs. > 0 mL/min). The participants'
demographic, medical, and social histories were reviewed for
the identification of possible risk factors for zero unstimulated

Table 1. Prevalence of "Yes" Responses to the Dry Mouth Questionnaire: Comparing HIV-positive with HIV-negative Women
HIV-

HIV+

Question

(1) Does the amount of saliva in your mouth seem to be too

little, too much, or you do not notice it?
(2) Do you need to sip liquids to aid you in swallowing
dry food?
(3) Does your mouth feel dry when eating a meal?

129

22.4

15

9.9

0.001

124
255

21.7
44.7

14
49

9.3
32.7

0.001
0.008

Table 2. Prevalence of No Saliva upon Palpation of Parotid and Submandibular/Sublingual Glands in HIV-positive and -negative Women
HIV-

HIV+

Salivary Gland
Parotid
Submandibular/sublingual

132
77

22.9
13.4

16
8

10.6
5.3

0.001
0.006

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Navazesh et al.

150A

Table 3. Univariate Covariates of Zero Unstimulated Whole Saliva Flow

Rates for HIV-positive and -negative Women
Covariates

Serostatus
HIV+
HIVRace/Ethnicity
Hispanic
Black
White
Age (yrs)
*29
30-39
40-49
*50
Dry Mouth Complaint
Too little saliva
Do not notice/too much
High Blood Pressure
Yes
No
Diabetes
Yes
No

Zero Flow Rate

%

95
9

17.1
6.3

0.001

20
56
23

11.6
13.6
23.7

0.018

12
31
46
11

8.8
10.7
20.1
30.6

0.001

35
68

25.4
12.2

0.001

30
72

24.6

0.001

9
93

32.1
14.1

0.014a

26
77

26.3
13.1

0.001

10
94

25.6
14.3

0.053

12.7

Heroin/Methadone
Yes
No

Psychotropics
Yes
No

Fisher's exact test; otherwise, Pearson chi-square.

flow rates in positive and negative women combined. It should

be noted that all licit and illicit drug variables were based on
self-reported use within 6 months of the oral baseline visit.
Table 3 summarizes the variables that were significantly
associated with zero unstimulated flow rates for HIV-positives
and -negatives combined. For the multivariate logistic
regression model, all the variables from Table 3 were initially
entered into the analysis, but the variables that remained in the
final model (Table 4) were determined by the backward
elimination procedure in SAS. Variables were sequentially
removed from the model when they did not meet the
significance criterion of p < 0.05 (Wald chi-square) to stay in
the model. We started by removing the least significant
variable from the model first and then re-calculating the pvalue for the variables remaining in the model. Once a variable
was removed from the model, it remained excluded. The
procedure cycled through this process until all variables met the
criteria to remain in the model.
The final models (Tables 4 and 5) are comprised of
categorical variables predicting the odds of zero unstimulated
flow rates. The odds are the proportion of, for example, HIVpositive women with zero unstimulated flow rates divided by
the proportion of HIV-positive women without zero
unstimulated flow rates. The odds ratio is the odds of zero

J Dent Res 79(7) 2000

unstimulated flow rates for HIV-positive women divided by the

odds of zero unstimulated flow rates for HIV-negative women.
Specifically, the OR = 2.86 (i.e., 2.86:1) states that the odds
of zero unstimulated flow rates were almost three times higher
for HIV-positive women compared with the odds of zero
unstimulated flow rates for HIV-negative women (indicated in
Table 4 by "1"). In summary, HIV-positive women had a
significant and almost three times higher likelihood of zero
unstimulated flow rates compared with HIV-negative women
after controlling for other factors which were also significantly
associated with zero unstimulated flow rates.
To assess the potential association of HIV-related
immunosuppressive factors with zero unstimulated flow rates,
we repeated univariate and multivariate analyses for HIVpositives only. Significant univariate association was found for
CD4 cell count (p = 0.03) but not for viral load (HIV RNA),
self-reported class C AIDS-defining conditions, and antiretroviral medication usage. Other significant covariates
included race/ethnicity (p = 0.023), age (p = 0.003), complaint
of dry mouth (p = 0.001), hypertension (p = 0.002), diabetes (p
= 0.001), heroin/methadone (p = 0.001), and psychotropic drug
(p = 0.038) usage. The adjusted odds of a zero unstimulated
flow rate were 2.6 times higher for HIV-positive patients with
CD4 cell counts < 200 compared with those with counts > 500
after controlling for age, race/ethnicity, complaint of dry
mouth, diabetes, and history of alcohol, heroin/methadone,
anti-retrovirals, and psychotropic drug usage (Table 5).

DISCUSSION
This is the first time that the prevalence of xerostomia and
salivary gland hypofunction has been investigated in a large
national cohort of HIV-infected women. The complaint of dry
mouth, based on responses to the three-item dry-mouth
questionnaire, was found to be more prevalent in the HIVpositives than -negatives. Previous studies have associated the
first question (about the amount of saliva seeming to be too
little) with the unstimulated and the second and third questions
(about the need to sip liquids when swallowing and the feeling
of dry mouth when eating) with the stimulated salivary status
(Fox et al., 1987). Although "yes" responses to the second and
third questions were more common among HIV-positives than
-negatives, chewing-stimulated whole saliva flow rates did not
differ among these two groups. Previous investigators (Sreebny
and Broich, 1987; Narhi, 1994) have documented a lack of
correlation between the complaint of dry mouth and salivary
gland hypofunction, except for extreme levels of hypoactivity.
Unstimulated whole flow rates, however, were found to be
significantly lower in the HIV-positive women.
Whole saliva is a combination of secretions produced by the
parotid, submandibular/sublingual, and minor salivary glands.
Under unstimulated conditions, the submandibular/sublingual
glands contribute about 67% and the parotid glands about 25%
of whole saliva (Schneyer, 1956). At high levels of stimulation,
parotid glands may contribute up to 49% of whole saliva
(Shannon, 1962).
The unstimulated salivary flow rate is affected by a variety
of local, systemic, and pharmacotherapeutic factors. Advancing
age (Navazesh et al., 1992a), diabetes (Thorstensson et al.,
1989; Newrick et al., 1991), hypertension (Streckfus et al.,
1994), and medications with anticholinergic effects, such as

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J Dent Res 79(7) 2000 Xerostomia and Salivary Gland Hypofunction in HIV-positive Women
Table 4. Multivariate Logistic Regression Covariates and Adjusted Odds
Ratios for Zero Unstimulated Whole-saliva Flow Rates for HIV-positive
and -negative Women

Serostatus
HIV+
HIV-

OR

Zero Flow Rate

95% Cl

pa

2.86

1.23-6.34

0.015

Race/Ethnicity
Hispanic

Black
White
Age (yrs)
.50
40-49
30-39
* 29
Dry Mouth Complaint
Too little saliva
Do not notice/too much

0.43
0.46

0.20-0.91
0.24-0.86

0.028
0.015

1.47-12.61
1.16- 5.54
0.54-2.63

0.008
0.019
0.666

2.55
1b

1.50-4.33

0.001

0.35
lb

0.16-0.79

2.78

1.48-5.22

4.31
2.54
1.19
lb

0.011

Heroin/Methadone Use
Yes
No
a

Table 5. Multivariate Logistic Regression Covariates and Adjusted Odds

Ratios for Zero Unstimulated Whole Saliva Flow Rates for HIV-positive
Women Only

CD4 Count
< 200
200-500
* 500

OR

Zero Flow Rate

95% Cl

2.61
1.76

0.84-3.68

0.020
0.134

0.27-0.91

0.024

3.78
1.95
1.21
1b

1.14-12.55
0.82- 4.66
0.51- 2.88

0.030
0.134
0.671

0.37
0.45

0.16-0.86
0.22-0.91

0.020
0.025

2.90
1b

1.63-5.18

0.000

3.61

1.13-11.59

0.031

0. 14-0.84

0.019

1.57-6.61

0.001

1.05-8.19

0.040

1.17-5.85

pa

Anti-retrovirals
Yes
No
Age (yrs)
*50
40-49
30-39
* 29

0.491
b

Race/Ethnicity

Alcohol Abuse
Yes
No

1 505

0.001

Hispanic

Black
White
Dry Mouth Complaint
Too little
Did not notice/too much
History of Diabetes

Yes
No

lb

Alcohol Abuse

Wald chi-square p-values.

"1" is the reference category.

Yes
No

0.35
b

Heroin/Methadone Use
psychotropics and narcotics (Sreebny and Schwartz, 1986;
Persson et al., 1991), have been associated with reduced
salivary output. Our investigation confirmed these associations.
It was not possible for us to control for all medical/biological
factors that could have accounted for differences in saliva flow
rates between HIV-positive and -negative women. However,
after controlling for the factors that were both known to us and
measurable, we found that HIV infection remained significantly
and independently associated with the zero unstimulated flow
rate. As previously stated, unstimulated whole saliva is
predominantly produced by submandibular/sublingual glands.
Therefore, our findings may support previous reports (Yeh et
al., 1988) associating reduced submandibular/sublingual saliva
output with HIV infection.
It is difficult to calibrate examiners to collect individual
gland saliva in a large multi-center trial. Unlike Yeh et al., who
collected saliva from submandibular and sublingual glands, our
findings are based on whole, not individual gland, saliva
collection. The results reported here are based on a crosssectional design. We are currently evaluating the impact of
HIV infection on salivary gland function based on a
longitudinal design. It would be interesting to see if stimulated
whole saliva will be affected by the HIV infection over time.
The parotid glands are reported to be affected at a later stage of
HIV disease progression (Atkinson et al., 1989). Because
parotid glands contribute more to the stimulated rather than to
the unstimulated whole saliva, their involvement (if any) may
be reflected in the chewing-stimulated saliva data collected at

Yes
No

3.22
b

Psychotropics Use
Yes
No
a

2.93
l

Wald chi-square p-values.

"1" is the reference category.

the consecutive follow-up visits.

The level of immunosuppression measured by CD4 cell
counts was significantly associated with a higher prevalence of
zero unstimulated flow rates in the HIV-infected women. The
viral load (HIV RNA), class C AIDS-defining conditions, and
anti-retroviral medication usage were not found to be
significant covariates in the univariate analysis. However, antiretroviral medication usage was significantly associated with
zero unstimulated flow rates based on the multivariate model.
The likelihood of having a zero unstimulated flow rate was
significantly higher in individuals with a CD4 cell count of <
200.
The CD4 cell count reflects the extent of damage that has
already occurred in the immune system of an HIV-infected
individual. Viral load (HIV RNA level) indicates the magnitude
of HIV replication in a given time. The association between the
CD4 counts and a zero unstimulated flow rate may indicate the
chronic nature of salivary glandular changes associated with

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1506

Navazesh et al.

the progression of HIV infection. The higher likelihood of a

zero unstimulated flow rate for those women who were not
using anti-retroviral medications may also indicate the role that
anti-retrovirals play in the prevention of salivary gland
hypofunction by controlling the HIV active replication.
The exact mechanism of action of HIV infection on the
salivary glands that results in xerostomia and salivary gland
hypofunction is not known. Some investigators (Greenberg et
al., 1997, 1995) have suggested a relationship to the presence
of cytomegalovirus co-infection in HIV-infected patients. The
results of our investigation revealed an association between
HIV infection and salivary gland function, and that the level of
immunosuppresion (CD4 cell count) is associated with the
degree of salivary gland hypofunction.
Saliva plays a significant role in oral homeostasis (Mandel,
1989). Recurrent dental caries and oral candidiasis are the most
common complications associated with salivary gland
hypofunction (Scully et al., 1994; Navazesh et al., 1995;
Epstein et al., 1996). The predictive value of salivary gland
hypofunction for recurrent oral candidiasis in HIV-infected
patients has been reported to be higher than the predictive value
of the CD4 cell count (McCarthy et al., 1991). Therefore, it is
imperative to screen HIV-infected patients routinely for
xerostomia and salivary gland hypofunction. If these conditions
are present, appropriate measures should be taken to prevent
commonly associated complications that may diminish the
quality of life for HIV-infected individuals.

ACKNOWLEDGMENTS
The Oral Substudy of the Women's Interagency HIV Study
(WIHS) Collaborative Study Group includes the following:
* New York City/Bronx Consortium: VA Medical Center,
Northport, NY (Joan Phelan, DDS);
* The Connie Wofsy Study Consortium of Northern
California: University of California, San Francisco
(Deborah Greenspan, BDS, DSc; John S. Greenspan,
BDS, PhD, FRC Path);
* Los Angeles County/Southern California Consortium:
University of Southern California, Los Angeles (Roseann
Mulligan, DDS, MS; Mahvash Navazesh, DMD; Joyce
Galligan, RN, DDS; Nancy Kiehl-Hillman, RDH, MS;
Kristi Ellis, RDH; Sharon Bautista-King; Claudia
Vargas);
* Chicago Consortium: University of Illinois at Chicago
(Mario Alves, DDS, MS, DSc);
* Data Coordinating Center: Johns Hopkins School of
Hygiene and Public Health, Baltimore, MD (Alvaro
Mufioz, PhD; Stephen J. Gange, PhD; Jean Anderson,
MD; Cheryl Enger, PhD; Lisa P. Jacobson, ScD; Lynn
Kirstein, MS; Cynthia Kleeberger, MAS; Robert Lyles,
PhD; Joseph B. Margolick, MD, PhD; Sol Su, ScD);
* NIH: The National Institute of Dental and Craniofacial
Research (Maryann Redford, DDS, MPH); and
* Statistical and Clinical Coordinating Center, 1995-1998:
New England Research Institutes, Watertown,
Massachusetts (Susan Barkan, PhD; Leslie Kalish, ScD;
Sonja McKinlay, PhD; Irene Doherty, BS; Kirstin
Nelson, MS; Eugene Komaroff, PhD).
The WIHS is funded by the National Institute of Allergy and

J Dent Res 79(7) 2000

Infectious Diseases, with supplemental funding from the

National Cancer Institute, the National Institute of Child Health
& Human Development, the National Institute on Drug Abuse,
the National Institute of Dental and Craniofacial Research, the
Agency for Health Care Policy and Research, and the Centers
for Disease Control and Prevention. UO1-AI-35004, UOJ-Al31834, UO1-AI-34994, AI-34989, UO1-HD-32632 (NICHD),
UO1-AI-34993, UO1-AI-42590.

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