J Oral Pathol Med (2009) 38: 126–131

ª 2009 John Wiley & Sons A/S Æ All rights reserved doi: 10.1111/j.1600-0714.2008.00716.x

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Oral manifestations of HIV infection in adult patients

from the province of Sancti Spiritus, Cuba
Emilio Carpio1, Vania López2, Vicente Fardales1, Iralys Benı́tez1
1
Facultad de Ciencias Me´dicas ‘‘Dr. Faustino Pe´rez Hernández’’, Sancti Spiritus, Cuba; 2Hospital General Universitario ‘‘Camilo
Cienfuegos’’, Sancti Spiritus, Cuba

BACKGROUND: Studies on the prevalence of HIV- Introduction

related oral lesions (HIV-OL) have shown great variations
among different countries. The aim of this study was to
Oral manifestations of HIV infection represent an
describe the prevalence of HIV-OL in adults infected with
important issue in the AIDS epidemic (1). Many HIV-
HIV in the province of Sancti Spiritus, Cuba, and to
infected individuals suffer from any HIV-related oral
determine the factors associated with the presence of
lesions (HIV-OL) during the course of the disease, with
HIV-OL.
the corresponding impact on their quality of life (2).
METHODS: A cross-sectional observational study was
These lesions are readily accessible and can be diag-
performed between November 2006 and August 2007 at
nosed, with high degree of reliability, from the clinical
the Hospital General Universitario Camilo Cienfuegos’,
features alone. Diagnostic criteria based on these clinical
Sancti Spiritus. One hundred and fifty-four HIV-infected
features are well established (3). The presence of some of
patients were included. Patients were examined and
these lesions such as oral hairy leucoplakia (OHL) or
interviewed by a periodontal specialist. Diagnosis of HIV-
oral candidiasis (OC) correlates with the decrease of
OL was based on clinical criteria. Demographical, clinical
CD4+ lymphocytes and increase in plasma viral load,
and laboratory data were obtained. Independent associ-
indicating disease progression (4). Oral examination by
ation of each factor with HIV-OL was assessed by logistic
healthcare workers of all individuals at risk of infection
regression modelling.
or diagnosed HIV-infected is mandatory. With the
RESULTS: The prevalence of HIV-OL was 40.9%. The
introduction of highly active antiretroviral therapy
commonest manifestation was oral hairy leucoplakia
(HAART), the prevalence of many of these lesions has
(n = 19; 12.3%); oral candidiasis (n = 17; 11%); herpes
decreased but their recurrence in a patient under
simplex virus infection (n = 11; 7.4%); and aphthous ulcer
HAART indicates a multi-drug resistance or HAART
(n = 9; 5.8%). Principal factors associated with the pres-
failure (4–6). Studies on the prevalence of HIV-OL from
ence of HIV-OL were CD4+ lymphocytes <500 cells ⁄ mm3
different regions of the world are important as they can
(OR: 2.06; 95% CI: 1.019–4.195) and smoking (OR: 2.03
provide a more complete description of the epidemic
CI: 1.037–3.982).
and a scientific basis for the appropriate management of
CONCLUSION: This study described the prevalence of
this problem by health providers.
HIV-OL in 154 HIV-infected patients which represent
Many studies have addressed the epidemiology of
about 80% of those known to be infected in the province
HIV-OL throughout the world (4–7). The prevalence of
of Sancti Spiritus. The prevalence of HIV-OL was lower
HIV-OL have shown great variations from country to
than those reported from developing countries. Oral
country thought the greatest differences are between rich
hairy leucoplakia and oral candidiasis were the most
and poor nations (5, 7). Several factors such as study
prevalent HIV-OL. Smoking and CD4+ cells count
design, diagnostic criteria, accessibility to appropriate
<500 cells ⁄ mm3 were the two factors independently
health care, economical, cultural and biological issues,
associated with the presence of HIV-OL.
among others, may influence on such variations. Vari-
J Oral Pathol Med (2009) 38: 126–131
ables that had shown a strong and more consistent
association with the presence of HIV-OL are those
Keywords: acquired immunodeficiency syndrome; Candida;
related with the state of immunosuppression: CD4+
human immunodeficiency virus infection; leucoplakia; oral mucosa
cells count, HAART and viral load (1). However, other
social or demographical factors, which may be highly
variable between countries, may also be important and
Correspondence: Dr Emilio Carpio, Facultad de Ciencias Médicas they have not been studied in deep. In a recent review
‘‘Dr. Faustino Pérez Hernández’’, Sancti Spiritus, CP 60 100, Cuba.
Tel: 53-41 328139, Fax: 53-41 328539, E-mail: ecarpio60@yahoo.es (7), Ranganathan et al. analysed the most relevant
Accepted for publication August 18, 2008 epidemiological studies from developing countries and

there were no reports from Cuba. They stated that
Well-designed and documented studies are necessary
for the correct assessment of the nature and magnitude
of the problem in developing countries’.
There are several reasons to believe that the preva-
lence of HIV-OL in Cuba could be different to other
regions of the world. Cuba is a Third World country
but some of its public health statistics are comparable
to many rich nations. Furthermore, the characteristics
of the cuban HIV epidemic and the way it is confronted
by the national health authorities are peculiar (8–13).
The epidemiological pattern of oral lesions in HIV-
infected cubans and the principal risk factors associated
with its prevalence are largely unknown since no report
is found in the MEDLINE database. Only few studies
related with oral health in HIV-infected cuban patients
are available but they have been published in journals
out of the principal mainstream of science (14–18). Two
of these papers (16, 17) are from the pre-HAART era
and other (18) analysed the HIV-OL prevalence in 48
HIV-infected patients from the province of Camaguey.
The other two papers deal only with periodontal
disease in HIV-infected individuals (14, 15). In this
article, we described the prevalence of HIV-OL in
the majority of adult populations infected with HIV
in the province of Sancti Spiritus and we analysed the
principal risk factors associated with the presence of
HIV-OL.
Methods
Study population and study design
This was a cross-sectional observational study. Sancti
Spiritus province is located in the central region of the
island and comprises 463 758 inhabitants according
to the national statistics (http://www.one.cu/aec2006/
anuariopdf2006/capitulo2/II.4.pdf; viewed July 5, 2008).
By January 2007, 186 adults were living with HIV infec-
tion in this province. As part of their clinical follow-up,
a periodical oral examination, with a 6-month interval,
is provided by an oral health professional. All adults
infected with HIV residing in the province of Sancti
Spiritus who attended to this periodical oral health
examination between November 2006 and August 2007
and who volunteered to participate in the study after
given their signed informed consent were included.
Exclusion criteria were: age <15 years, pregnancy, and
antifungal drugs or antibiotics used for oral infections
1 month prior the examination. This study was
approved by the Ethical Committee of the Hospital
General Universitario Camilo Cienfuegos’, Sancti
Spiritus.
Data collection
All patients were examined and interviewed by an
experienced periodontal specialist (VL, author of this
paper), at the principal University General Hospital of
the province (Hospital General Universitario Camilo
Cienfuegos’, Sancti Spiritus). The examination was
carried out in a dental chair with artificial light using
dental mirrors and probes. The HIV-OL were recorded
HIV-related oral lesions in Cuba
Carpio et al.
127
as present or absent on a presumptive diagnosis
according to the revised classification of the EC-Clear-
inghouse on Oral Problems related to HIV infection
criteria (3). Gender, age, possible route of infection,
smoking, CD4+ cells count, plasma viral load, oral
hygiene and unprotected oral sexual practices (UOSP)
were recorded by the interviewer or from the medical
records. The laboratory data such as CD4+ cells count
and plasma viral load were taken from the clinical
records (CD4+ cells count and viral load determina-
tions is offered to all cuban HIV-infected patients with
6-months interval, we took the data from the last
determination near the day of the examination). The
HIV-1 viral load and CD4+ cells count were measured
by means of reverse transcriptase-polymerase chain
reaction (RT-PCR, Amplicor; Roche Diagnostics,
Branchburg, NJ, USA) and by means of flow cyto-
metry (FacScan; Becton Dickinson, Mountain View, CA,
USA) with monoclonal antibodies (Orthodiagnostic-
System, Raritan, NJ, USA) respectively. The detection
limits of the viral load assay was 50 RNA copies ⁄ ml and
the data were recorded as detectable (>50 copies ⁄ ml) or
undetectable (<50 copies ⁄ ml).The data on USOP were
recorded in the interview by asking for oral contact with
genitals or genital fluids without barriers such as
condom in the month prior the examination. Oral
hygiene was assessed according to the simplified Greene
and Vermillion index (19). Smoking was assessed by
asking the patient whether he (she) was a current smoker
or not-current smoker. All patients requiring treatment
for their lesions were treated and followed up by a
competent specialist.
Statistical analysis
All analyses were done with SPSS software (version
11.0.1, SPSS Inc, Chicago, IL, USA). Frequencies
distribution table to show oral lesions prevalence were
used. Univariate logistic regression analysis was used
to calculate odds ratio (OR) and its 95% confidence
interval, as an estimate of the strength of association
between the presence of HIV-OL with gender, UOSP,
oral hygiene, smoking, viral load and CD4+ cells count.
Those variables that were shown to be significantly
associated with the presence of any oral lesion
(P < 0.05) were included in a multivariate model to
assess their independent effect. For comparison of
both mean and variance of CD4+ cells count in people
with or without oral lesions the independent samples
Student’s t-test was used. Other descriptive statistics
used to describe the data were mean, standard deviation,
lower and upper values and median. The significance
test P-values below 0.05 were regarded as significant.
Results
By January 2007, 186 adults residing in the province of
Sancti Spiritus were known to be infected with HIV-1,
confirmed by ELISA and Western Blot; one patient was
excluded from the study due to his bad health, unable to
give his informed consent. A woman was also excluded
due to pregnancy. A total of 154 patients gave their
J Oral Pathol Med
 HIV-related oral lesions in Cuba
Carpio et al.

128
written informed consent and were examined and Table 2 Association between the presence of HIV-OL with potential
interviewed in this study. risk factors expressed as odds ratio (OR) with 95% confidence
intervals
Some demographical and clinical characteristics of
this series of patients were: The majority were male, 121
(78.6%) and the age range was between 16 and 64 years Presence of any type
of lesion
old (mean 29.3). In all cases, the possible route of
infection was sexual contact. More than 80% of man Variable No (%) Yes (%) P OR CI 95%
declared having sex with other men. Sixty-five patients Gender
(42.2%) were current smokers and 64 (41.6%) stated Female 15 (16.5) 18 (28.6) 0.07 2.02 (0.93–4.41)
having unprotected receptive oral sex within the month Male 76 (83.5) 45 (71.4)
OUSP*
prior the interview. One hundred and twenty-nine No 8 (8.8) 0 0.03 12.92 (0.73–227.87)
patients (83.7%) had a viral load lower than the assay’s Yes 83 (91.2) 63 (100)
detection limit. The mean of CD4+ cells count was Smoking
487.1 (±263.3) cells ⁄ mm3. Sixty-seven (43.5%) patients No 60 (65.9) 29 (46) 0.01 2.26 (1.17–4.38)
presented good oral hygiene. Yes 31 (34.1) 34 (54)
Oral hygiene
The prevalence of HIV-OL is presented in Table 1. Good 41 (45.1) 26 (41.3) 0.64 1.16 (0.60–2.23)
Sixty-three patients (40.9%) showed at least one oral Bad 50 (54.9) 37 (58.7)
lesion. The commonest manifestation was OHL Viral load (copies ⁄ ml)
(n = 19, 12.8 %) followed by OC (n = 17, 11.0%); £50 80 (87.9) 49 (77.8) 0.09 2.07 (0.87–4.94)
>50 11 (12.1) 14 (22.2)
herpes simplex virus infection (n = 11, 7.4%); and CD4+ cells count (cells ⁄ mm3)
aphthous ulcer (n = 9, 5.8%). Only three patients >500 42 (42.2) 17 (27) 0.01 2.31 (1.16–4.63)
presented HIV associated periodontitis and four showed £500 49 (53.8) 46 (73)
linear gingival erythema. Kaposi¢s sarcoma or other
malignancies were not detected. *A value of 0.5 was added to each cell frequency to calculate OR. Two
cells contained expected value <5.
The association between the presence of HIV-OL with OUSP, Oral unprotected sexual practice.
several potential risk factors is shown in Table 2. The
presence of HIV-OL did not showed association with
gender, oral hygiene, UOSP or viral load. Smoking and Table 3 CD4+ cells count in people with or without HIV-related oral
lesions
CD4+ cells count <500 cells ⁄ mm3 was associated with
the presence of HIV-OL (Table 2). CD4+ cells count
was also analysed as a continuous variable and the Presence of lesions
CD4+ cells count in patients with HIV-OL and patients CD4+ cells count All cases No Yes
without HIV-OL are shown in Table 3. CD4+ cells Lower value 62 62 132
count were significantly lower in patients with HIV-OL Upper value 1190 1190 1138
than in patients without HIV-OL. The analysis of UOSP Median 453 483 408.38
was hampered by the fact that there was a zero (0) in the Mean 487.11 527.72 428.44
SD 263.37 280.41 226.10
cell of people without lesions and no OUSP thus, for the CI (95%) 445.18–529.03 469.32–586.12 371.50–485.38
estimation of odds ratio, 0.5 was added to each cell
frequencies. Given that in the univariate analysis model Student’s t-test for CD4+
two cells contained expected values <5, UOSP was not Levene’s test for CD4+ cells count means
analysed further in a multivariate model. cells count variances comparison
As CD4+ cells count and smoking were the two F P T P
factors that showed significant association with the
8.36 0.04 2.33 0.02
presence of HIV-OL in the univariate analysis, they
were studied further using a logistic regression model for F, Fisher’s statistic for varience comparison; T, Student’s statistic for
a multivariate analysis. When step by step regression independent samples.

Table 4 Association of smoking and CD4+ lymphocytes count

Table 1 Prevalence of oral lesions in HIV-infected patients from the £500 cells ⁄ mm3 with the presence of HIV-OL in the equation of
province of Sancti Spiritus, Cuba logistic regression model

Oral lesions No (n = 154) % Variable P OR CI 95%

+
Any lesion 63 40.9 CD4 cells count 0.044 2.067 (1.019–4.195)
Oral hairy leucoplakia 19 12.4 £500 cells ⁄ mm3
Oral candidiasis 17 11.0 Smoking 0.039 2.032 (1.037–3.982)
Pseudomembranous candidiasis 10 6.5 Intercept 0.000 0.319
Angular cheilitis 7 4.5
Herpes simplex virus infection 11 7.1
Aphthous ulcers 9 5.9 model was applied we found that the variable that
Linear gingival erythema 4 2.6 showed the strongest association with the presence of
HIV-associated periodontitis 3 1.9
HIOV-OL was smoking (Table 4). CD4+ cells count

J Oral Pathol Med


<500 cells ⁄ mm3 was the second predictor for the
presence of HIV-OL. According to our data (intercept
0.319 in Table 4), non smokers patients with lympho-
cytes counts higher that 500 cells ⁄ mm3 have a very small
probability to have any HIV-OL.
Discussion
This study described the prevalence of oral lesions
associated with HIV disease in a series of patients from
the province of Sancti Spiritus, Cuba. To our knowledge,
this is the first report on the epidemiology of HIV-OL
that analysed both the prevalence and the principal risk
factors associated with the presence of HIV-OL in a
series of cuban patients. Ranganathan et al. (7) analysed
the published papers on the prevalence or incidence of
oral lesions in HIV-infected patients from developing
countries in a period of 14 years (1990–2004); several
countries from Latin America were represented in their
study but there were no reports from Cuba. This
prevalence study of HIV-OL from Cuba represents a
contribution to the aim of giving a more global picture
of the epidemic, particularly in the Third World where
the majority of HIV-infected people live.
The most relevant characteristics that distinguish the
series of HIV-infected patients presented here from
those described in previous studies are that they were
composed mainly by men that had sex with men; almost
half of the patients were current smokers and unpro-
tected receptive oral sexual practice were common. In all
cases the HIV infection was acquired by sexual contact
and there were no intravenously drug users. All these
patients have free access to health cares and received
oral and clinical attention closest to the best interna-
tional standards, including antiretroviral therapy.
The prevalence of HIV-OL (40.9%) was slightly lower
than those reported in the majority of papers from
developing countries (7) but this figure was little higher
than those obtained in many studies from rich nations,
specially after the introduction of HAART (4, 5). Italy
has described a prevalence of 35.6% (20) and 47% (21);
United Kingdom, 32.3% (22) and Greece, 36.4% (23).
Ranganathan et al. (7) analysed the average prevalence
of HIV-OL by regions in developing countries and they
found the highest prevalence in India (89.3%) and
Africa (71%), followed by Latin America (59 %) and
Thailand (54.5%); all these figures are higher than the
prevalence reported in our study. Our prevalence data
were very similar to those reported from Mexico. One
paper compared the prevalence of HIV-OL in two
health centres for HIV in Mexico City and the figures
was around 40% (24).
The most prevalent type of HIV-OL in our study was
OHL fallowed by OC and herpes simplex virus infec-
tion. This is in contrast with the majority of reports
from developing countries (7) that documented OC as
the most prevalent lesion. One possible explanation for
this finding is that more than 50% of patients from this
series were men that had sex with men and Epstein–Barr
virus, the aetiological agent of OHL, are highly
prevalent in this population (25–27). The prevalence of
HIV-related oral lesions in Cuba
Carpio et al.
129
OHL found in our series was comparable but a little
lower than those obtained in the study from Mexico
City where they reported a prevalence of 14% and
20.5% in two different health centres (24).
Oral candidiasis was expressed mainly as angular
cheilitis or pseudomembranous candidiasis. Reported
prevalence of OC in developing countries range from
11% to 81 %, according to the previously mentioned
review (7), but the average prevalence for Latin America
was 41.8 %, almost four times higher than the one
reported here.
One intriguing finding is that, based on the few
published articles, the prevalence of OHL and OC have
not shown a great declining after the availability of
HAART in Cuba. Santana-Garay et al. (16) studied 243
HIV-infected patients in 1991 and they found a preva-
lence of 14.8% and 13.9% for OHL and OC respec-
tively. Other study from Camaguey (18), after the
introduction of HAART, reported a prevalence of
27% and 25% for OC and OHL respectively.
The prevalence of herpes simplex virus infection in
our series of patients was higher than those reported in
the majority of studies from developing countries; we do
not have a rational explanation for this finding, but we
may speculate that as this series are composed mainly by
men that had sex with men and many of them declared
to practice unprotected oral receptive sex, they were
involved in risky behaviours for the transmission of
herpes simplex virus (28).
The prevalence of periodontal lesions was low for
both linear gingival erythema and HIV-related peri-
odontitis. The low prevalence of periodontal disorders
could be related with the good oral hygiene that showed
almost half of the patients and with the fact that all of
them have free access to oral health cares.
The association of several factors with the presence of
HIV-OL was assessed by univariate analysis. Gender,
oral hygiene, UOSP and viral load were not associated
with the presence of any lesion while CD4+ cells count
and smoking showed association with the presence of
HIV-OL. This association was also corroborated in the
multivariate regression model. This is in agreement with
several studies that have confirmed the association of low
CD4+ cells count with the presence of HIV-OL (29–33).
The appearance of several types of lesions such as OC
and OHL increases with the decline of CD4+ cells count
below 200 cells ⁄ mm3 (29–33).
Patients who were current smokers were twice as
likely to present an HIV-OL compared to not-current
smokers. While CD4+ cells count represent intuitive,
biologically plausible, and previously documented risk
factor, tobacco use are more controversial and some
studies have not found association between HIV-OL
and smoking (24). However, the majority of papers have
found association of smoking with HIV-OL (33–36). In
a prospective study of OHL and OC with a cohort of
283 HIV-infected adults from North Carolina, Chatto-
padhyay et al. (33) concluded that current smokers are
twice as likely to develop OHL or OC compared to not-
current smokers. A cross-sectional study that included
1 058 HIV-infected male patients who received clinical
J Oral Pathol Med
 HIV-related oral lesions in Cuba
Carpio et al.
130
care at the University of California, San Francisco,
found a strong association between cigarette smoking
and the presence of specific HIV-OL (34). Sroussi et al.
(35) analysed the association of smoking with the
presence of HIV-OL in 415 patients and they concluded
that tobacco use was a major and often underestimated
risk factor for oral lesions. Whether smoking itself or
other smoking-associated factors explain the association
found in our study could be explored further but as
several studies have shown a consistent correlation of
smoking with the appearance of HIV-OL, tobacco
cessation should be included as part of routine oral
health cares in HIV-infected individuals. According to
our data from the logistic regression analysis, patients
who do not smoke and have CD4+ cells count higher
than 500 cells ⁄ mm3 have a very small probability to
develop any HIV-related oral lesion.
In contrast to our data, the majority of previous
studies have found an association of HIV-OL with high
viral load (1, 4–6). One possible explanation for this
discrepancy is that we did not measure the viral load
at the moment of oral examination; we took the data from
the medical records and viral load was measured within
the previous 6 months. As CD4+ cells count showed
association with HIV-OL, it could be possible that rising
of viral load and the declining of CD4+ lymphocytes
did not perfectly match in time. Other unknown factors
could be related with this lack of association.
One of the strength of this study is related with the
fact that we have described the prevalence of HIV-OL in
a series of HIV-infected patients that represent >80%
of all people which are known to be infected with HIV in
a cuban province, Sancti Spiritus. Most of the previous
studies on the prevalence of HIV-OL included patients
who came to a secondary health centre and this fact
precludes an estimation of the prevalence in the com-
munity. Several studies have addressed the question of
what percent of the cuban HIV epidemic is actually
known (9, 11). One study (9) concluded that the
efficiency of the Cuban HIV detection system is between
75% and 87%. Another paper (11), using data up to
2002, estimated that it takes a mean of 2.7 years to
detect a person infected with HIV. Thus, we might say
that we have reported the prevalence of HIV-OL in
almost 80% of people infected with HIV in the province
of Sancti Spiritus. Taking into consideration that the
ways HIV-infected patients are followed and treated are
similar in the whole national territory, according to
national guidelines, the data presented here might offer
an approximate estimation of the prevalence in the
country as a whole; although, further studies are needed
to confirm this assumption. According to the cuban
national health statistics (http://www.sld.cu/servicios/
sida/temas.php?idv=2240; viewed July 5, 2008), by the
end of 2006, 9 039 HIV-positive patients had been
detected since the beginning of the epidemic and 81%
were males. The majority of infected people were men
that had sex with men (67%); this figure represents
86.1% of infected males. The group of HIV-infected
patients studied in this paper showed similar propor-
tions with respect to gender and sexual preferences.
J Oral Pathol Med
Limitations of our study comprise the cross-sectional
design that did not allowed us to correlate the time of
appearance of HIV-OL with any potential risk factors
and the low number of patients that preclude some
statistical analysis. The use of presumptive clinical
criteria for the diagnosis of each lesion could also raise
concern for potential misclassification. The accepted
consensus criteria for definitive diagnosis of many of
these lesions included other procedures in addition to
clinical features. In spite of this, the majority of
previously published articles on the prevalence of oral
manifestations of HIV disease (3, 7) make use of the
same clinical criteria that we have employed here for the
diagnosis. Other important drawback is related with
the fact that laboratory data such as viral load and CD4+
cells count were taken from the clinical records and
those variables were measured several months (6 months
maximum) prior to oral examination and interview.
As this is the first epidemiological report on the
prevalence of HIV-OL in this province, several issues
have not been deeply assessed and should be clarified in
future studies. The association of risk factors such as
CD4+ cells count, duration of infection, viral load,
HAART and smoking with the appearance of any oral
lesion should be assessed in a prospective design with a
cohort of patients without lesions at baseline. The
number of patients should also be increased in the
studies yet to come. For this purpose, patients from
other provinces or from the whole national territory
must be included.
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