Received: 26 March 2020 | Revised: 22 May 2020 | Accepted: 27 May 2020

DOI: 10.1111/odi.13469

WW8 PROCEEDINGS

The global changing pattern of the oral manifestations of HIV

Anwar R. Tappuni

Institute of Dentistry, Queen Mary

University of London, London, UK
Correspondence
Anwar R. Tappuni, Institute of Dentistry,
Barts and The London School of Medicine
and Dentistry, Queen Mary University of
London, London, UK.
Email: a.r.tappuni@qmul.ac.uk
Abstract
The significance of the oral manifestations of HIV has been widely recognised since
the start of the epidemic. It is estimated that more than 38 million people are liv-
ing with HIV currently, with more than a third presenting with oral manifestations.
Access to optimum clinical management and effective treatment in resource-rich
countries has led to a remarkable decrease in some of the oral manifestations in the
HIV population but this is not mirrored in developing countries, where most HIV-
positive patients reside. In this paper, a review of the literature since the start of the
HIV infection in different parts of the world is presented to highlight the current
significance of the oral conditions in this population. Oral candidiasis was repeatedly
reported as the most encountered oral manifestation of HIV in different countries,
including in studies on groups on anti-retroviral therapy. Over time salivary gland dis-
ease was reported less in developed countries but was encountered more in develop-
ing countries. There is evidence to show that the prevalence of oral warts increased
with the establishment of anti-retroviral therapy. A review of the worldwide preva-
lence of HIV-related oral conditions indicates that except for oral hairy leucoplakia,
the prevalence of all other nine commonly reported oral conditions remained the
same or increased over time. Oral opportunistic infections in HIV-infected patients
are an ongoing clinical burden mainly in developing countries. Maintaining research
in the subject and improving access to HIV treatment will help address the oral health
inequalities around the world.

KEYWORDS

candidiasis, Global, oral hairy leucoplakia, oral health inequity, oral warts, salivary gland
disease

1 | BAC KG RO U N D significant decrease in the prevalence of the OM of HIV documented

The number of people affected by human Immunodeficiency Virus
(HIV) infection continues to grow globally (UNAIDS, 2019). The oral
manifestations (OM) of HIV are well established markers of disease
progression, and their presence is an indication of a compromised
immune status. They can cause morbidity and affect the quality
of life of patients. The literature indicates that there has been a
in Europe and USA in response to anti-retroviral therapy (ART)
(Nicolatou-Galitis et al., 2004; Patton, McKaig, Strauss, Rogers, &
Eron, 2000; Schmidt-Westhausen, Priepke, Bergmann, & Reichart,
2000; Tappuni & Fleming, 2001). In contrast, in resource-limited
countries where accessibility to health care and anti-retroviral ther-
apy (ART) is limited, OM of HIV continues to place a substantial bur-
den on these countries’ health systems. (Challacombe, 2020).

This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium,
provided the original work is properly cited.
© 2020 The Authors. Oral Diseases published by John Wiley & Sons Ltd

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wileyonlinelibrary.com/journal/odi Oral Diseases. 2020;26(Suppl. 1):22–27.

TAPPUNI
In this paper, we present a critical appraisal of the worldwide
chronological changes in the prevalence of commonly reported oral
lesions of HIV. The aim was to enhance our knowledge of the present
status of these oral conditions globally and to determine whether
oral health inequity persists in this group of patients.
2 | G E N E R A L O B S E RVATI O N S
A recent comprehensive review of the literature of OM of HIV
worldwide since the beginning of the pandemic highlighted the
discrepancy in the natural progression of the disease in resource-
poor countries compared with developed countries (El Howati &
Tappuni, 2018). Until 1990, most of the papers on the subject origi-
nated from developed countries but this trend slowly reversed and
studies published in the subsequent 10 years between 1990 and
2000 originated evenly from developed and developing countries,
and after 2000 until 2017, about 86% of the studies were conducted
in developing countries. This no doubt reflects the reduction of the
OM of HIV in the Western world (Patton et al., 2000, Tappuni and
Fleming 2001), so not only was there less accessible appropriate
study material but also a perception that there is less need for re-
search, which led to downgrading oral HIV as a research priority.
Despite a proportional increase in papers published from devel-
oping countries in recent times, these are originating from a limited
number of countries and thus may not be fully representative. There
are evident gaps in knowledge in relation to OM of HIV in some coun-
tries in Africa, Asia and South America. The review also highlighted
a stark disparity in the provision of HIV treatment around the world.
In the 1990s approximately 33% of studies conducted in developed
countries included study groups on ART compared with only 10% of
studies in developing countries. The accessibility to ART increased in
the developing world after 2000, but continued to be considerably
less than in developed countries (38% and 87%, respectively).
A WHO article published in September 2010, reported on access
to HIV services in 144 low- and middle-income countries. Universal
access to ART for adults was achieved in eight countries including
Cambodia, Cuba and Rwanda. The report identified several chal-
lenges in achieving efficient management of this condition. Many
patients started their treatment late in the disease process as more
than 60% of HIV-positive people did not know their HIV status.
Additionally, surveys showed that in the first year of initiating treat-
ment, around 18% of patients were lost to follow-up. The report
concludes that continued commitment to HIV research is necessary
if we are to achieve global universal access to HIV treatment and to
reverse the epidemic (WHO; UNAIDS; UNICEF, 2010).
In an attempt to control the HIV epidemic, the United Nation's
programme on HIV/AIDS published the 90–90–90 concept in 2014.
It set three targets to be achieved by 2020:(a) to diagnose 90% of
people who are HIV infected, (b) to treat with ART 90% of people
who are diagnosed and (c) to achieve viral suppression in 90% of
those who are on therapy (UNAIDS, 2014). A report published at the
end of 2019 on the progress of these targets in Europe recognised
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23
the gap in the management of HIV between Eastern Europe and
the rest of the continent. The report stated that in the 36 European
countries that have dependable data, viral suppression in PWHIV is
44%. As a result, HIV incidence is not reducing in this region (EACS
European AIDS Clinical Society, 2019).
The ECC criteria developed in 1993 (EC-Clearinghouse, 1993)
are by far the most commonly applied classification criteria in the
OM of HIV literature, probably because it is easy to understand and
to apply. The pattern of the OM of HIV changed after the estab-
lishment of ART but studies continued to apply the same criteria as
there was no modern alternative. The advantage of this is that re-
sults of studies were easier to compare. However, as our knowledge
of this condition developed and the pattern of oral disease changed
with ART, a data-driven review of these criteria since first estab-
lished in 1993 would have improved its applicability. Newer revised
classification criteria have been shown to perform better (Aggarwal
et al., 2015).
3 | PR E VA LE N C E O F S PEC I FI C O R A L
M A N I FE S TATI O N S O F H I V
There are at least 24 different oral lesions reported in the HIV lit-
erature but only ten of these are encountered consistently. In de-
scending prevalence, these are (a) oral candidiasis (OC), (b) oral
hairy leucoplakia (OHL), (c) herpes simplex virus infection (HSV), (d)
Kaposi's sarcoma (KS), (e) non-specific ulceration, (f) aphthous ul-
cers, (g) periodontal disease, (h) salivary gland disease (SGD), (i) oral
melanotic hyperpigmentation and (j) oral warts (OW). The first eight
were encountered in more than half of the reviewed studies.
OC was the most commonly reported OM of HIV in studies from
around the world, since the beginning of the endemic until the pres-
ent day. The highest reported prevalence was in Africa (51%) and
Asia (39%). The average prevalence in Europe and the USA was com-
parable at 28% and 30%, respectively (Table 1). The majority of the
studies classified OC into subtypes reporting pseudomembranous
as the most prevalent followed by erythematous, angular cheilitis
and hyperplastic candidiasis. The latter was particularly prevalent in
Africa.
As expected, study groups on ART had overall lower prevalence
of OC (26.2%) compared with groups who were not on treatment
(39%) but surprisingly the difference was not considerable (Figure 1).
Perhaps this is because OC is commonly encountered in patients
with underlying health problems generally and is not a condition that
is seen exclusively in HIV. Diabetics, patients using steroid inhalers or
on long-term antibiotic, denture wearers and smokers are groups of
patients at risk for candidiasis. Overall, if the candidiasis is fostered
by an underlying immunodeficiency then the infection would be less
responsive to anti-fungal treatment. However, in studies of the OM
of HIV, other risk factors and the response to treatment were rarely
recorded, so it is difficult to ascertain whether the OC described in
subjects on ART is strictly associated with HIV. Not taking account
of confounding conditions may have led to an overestimation of OC.
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24 TAPPUNI

Over the years, the reported prevalence of OHL decreased
from 26% in the 1980s to about 18% in the 1990s and to 12% in
2000–2017 (Figure 1). The overall reduction is probably due to the
inclusion of study groups on ART in later studies. Unlike OC, OHL is
almost exclusively associated with an immunodeficiency status and
its presence reflects the health status of the subject. OHL was first
reported in association with HIV by Greenspan et al., 1984, but it has
also been described in transplant patients (Greenspan, Greenspan,
Souza, Levy, & Ungar, 1989). Since then, the frequency of reporting
this condition increased after 1990 (Figure 1). The overall prevalence
of OHL decreased considerably in groups on ART (10%) when com-
pared with groups who were treatment naïve (18%) (Figure 2).
It is worth noting that there has been reports of OHL in non-HIV
OHL was reported in diverse countries and continents in relation
to HIV, with no significant difference between developed (16%) and
developing countries (14%) (Table 2). However, it was more prevalent
in America (17%) where the studies were mostly on MSM compared
with Africa (11%) (Table 1), where the vast majority of the studies
were on heterosexual subjects. This is in line with the suggestion
that OHL is more prevalent in men who have sex with men (MSM)
(Reichart et al., 1989). The mode of transmission of HIV may also
explain the reason for the higher prevalence of OHL in developed
countries compared with developing countries despite the avail-
ability of ART (Barone, Ficarra, Gaglioti, Orsi, & Mazzotta, 1990;
Frezzini, Leao, & Porter, 2005).
HSV infection was reported in most studies on OM of HIV pub-
lished since 1980s, as either herpes labialis, herpetic ulceration or
herpes simplex infection. In general, the reported prevalence in-
creased with time but remained very low in all continents with Asia
having the highest occurrence (Table 1).
The reported prevalence of KS worldwide was surprisingly
higher in later decades, probably as a reflection of increased
awareness and better reporting of this condition in the develop-
ing world where KS is 3 times more prevalent (6.6%) compared
with developed countries (2.2%) (Figure 1, Table 2). KS was of
Necrozing ulcerave gingivis
Hepes simplex

Kaposi sarcoma

TA B L E 1 A comparison of the prevalence of the Oral Non-specific ulcers

manifestations of HIV in different continents Oral warts

Aphthous ulcers
America Europe Africa Asia
Type of oral condition (%) (%) (%) (%) Periodons

Salivary Gland Disease

OC 30 29 52 39
Hyper-pigmentaon
OHL 17 16 11 12
Oral Hairy Leukplakia
Periodontitis and 4.4 9.3 8 14
Candidiasis
gingivitis
0 5 10 15 20 25 30 35 40 45
Necrotising ulcerative 2 3 4 2.7
lesions On therapy Not on therapy

Herpes simplex 3 3 4 10 F I G U R E 2 Mean prevalence of HIV-OM in study groups with

Aphthous ulcer 5 10 7 9 and without anti-viral therapy
Non-specific 4 5 6 7
ulceration
KS 2 3 14 4
TA B L E 2 A comparison of the mean prevalence of commonly
SGD 5 10 8 15
reported oral manifestation of HIV in developed and developing
Warts 2 5 4 0 countries
Oral Melanotic 8 4 9 21
hyperpigmentation Developed Developing
OM-HIV countries (%) countries(%)

OC 31 39
45 OHL 16 14
40
35
30 Periodontitis and gingivitis 6.9 9.5
25
20
15
Necrotising ulcerative lesions 2 3
10
5 Herpes simplex 4 5
0
Aphthous ulcer 7 7
Non-specific ulceration 5 5
KS 3 7
SGD 6 10
1980s 1990s 2000s Warts 5 2

FIGURE 1 Prevalence of HIV-OM over time Oral Melanotic hyperpigmentation 4 14


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significantly higher rate in Africa (14%) compared with Asia (4.3%),
Europe (3.4%) and America (2.3%) (Table 1). Before the HIV epi-
demic, KS was an endemic tumour in Africa, and the HIV epidemic
caused a marked increase in its prevalence (Hengge et al., 2002).
Surprisingly, although KS was less prevalent in patients on ART
(2.7%) compared with those who are not on ART (3.5%), the dif-
ference was not significant (Figure 2). As KS, like other OM of HIV,
is an opportunistic infection, its presence is directly related to the
immunological status of the study subject and their response to
ART. Therefore, it would have been more accurate to report the
presence of KS in relation to immunological recovery/parameters
rather than as a straightforward observation of whether patients
are on ART.
Recurrent aphthous ulceration (RAU) is a distinct condition of
unknown aetiology (Tappuni, Kovacevic, Shirlaw, & Challacombe,
2013). By definition therefore, oral ulcers reported as an OM of HIV
should not be categorised as RAU and would be more precisely re-
ferred to as HIV-related oral ulcers. However, RAU was reported in
approximately half of the OM of HIV studies published after 1990,
with a mean prevalence of 7%. Interestingly in studies reporting
RAU, the prevalence was double in patients on ART (10%) compared
with those not on treatment (5%), but the prevalence of ulceration
did not differ in these two groups in studies reporting the ulcers as
“non-specific” (Figure 2). It is likely that genetic and environmental
factors such as poor oral health and malnutrition play a role in pre-
cipitating oral ulcers but very few studies if any, were concerned
with confounding causative factors when reporting the oral ulcers
as an OM of HIV.
The ECC classification criteria identified, linear gingival er-
ythema (LGE), periodontitis and necrotising ulcerative gingivitis
(NUG) as periodontal conditions that are strongly associated with
HIV. (EC-Clearinghouse, 1993). Collectively, conditions of the peri-
odontium were reported about 30% more often in studies from
developed countries (Table 2). However, evaluating individual con-
ditions revealed that NUG was more commonly encountered in de-
veloping countries and where participants were not on ART Table 2,
Figure 2). NUG and periodontitis were more predominant in Africa,
presumed to be exacerbated by poor oral hygiene and lack of oral
care (Freeman, Liberali, Coates, & Logan, 2012; Glick, Muzyka, Lurie,
& Salkin, 1994; Sharma, Pai, Setty, Ramapuram, & Nagpal, 2009)
(Table 1). Periodontal disease was about 25% more likely to be en-
countered in groups on ART compared with those who were not
on treatment (Figure 2). It has been suggested that this condition
is associated with aging rather than HIV (Berberi & Noujeim, 2015;
Ceballos-Salobrena, Aguirre-Urizar, & Bagan-Sebastian, 1996;
Ranganathan et al., 2004). Additionally, being a common condition
casts doubt on whether periodontal conditions should be included
as strongly indicative of HIV. Another periodontal condition, LGE,
also classified in the EC-clearinghouse criteria as strongly associated
with HIV, is not commonly reported in this group of patients.
SGD was one of the first conditions recognised as a manifesta-
tion of HIV infection. Generally, the frequency of reporting SGD in-
creased after 1990 where it was reported in more than half of the
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25
reviewed papers (16/29), with a mean prevalence of 8% in studies be-
fore 2000, increasing to 10% in more recent publications (Figure 1).
Studies conducted in developed countries reported a mean preva-
lence of 6%, lower than in developing countries (10%) (Table 2). The
mean prevalence of SGD in Asia was 15%, significantly higher than
in other continents; Europe (9.4%), Africa (8%) and America (4.6%)
(Table 1). The literature suggests that HIV-related SGD decreased
after 2000 in both developing and developed countries. The rele-
vant literature associates SGD with AIDS and advanced HIV (Phelan,
Saltzman, Friedland, & Klein, 1987; Roberts, Brahim, & Rinne, 1988;
Silverman, Migliorati, Lozada-Nur, Greenspan, & Conant, 1986) or
as a side effect of ART. (Nittayananta & Chungpanich, 1997; Sharma
et al., 2009).
The frequency of reporting oral hyperpigmentation has increased
with time and was reported in 30% of papers published 2000–2017
(n = 50), with increasing prevalence from 4% in the 1980s and 7% in
the 1990s to 16% after 2000 (Figure 1). It had significantly higher
rate of detection in developing countries (14%) compared with de-
veloped countries (4%) (Table 2). There was higher prevalence of
hyperpigmentation reported in Asia (21%) compared with other
continents (Africa 9%, America 8% and Europe 4%) (Table 1). Whilst
some cases of oral hyperpigmentation are recognised as second-
ary to medication, others appearing in HIV-infected patients are
idiopathic and have been associated with the systemic condition.
The two categories differ histologically in that pigmentation asso-
ciated with medication show melanin concentration in phagocytes
and extracellularly in the connective tissue. In pigmented lesions of
unknown cause, melanin is restricted to keratinocytes of the basal
cell layer or extracellularly in the lamina propria. (Langford, Pohle,
Gelderblom, Zhang, & Reichart, 1989). Generally, studies reporting
hyperpigmentation in HIV population did not differentiate between
the types of oral pigmentation.
OW was significantly more in the developed world (4.6%) when
compared with developing countries where there were three re-
ports only of a high prevalence of OW since the 1980s; in 1997,
2006 and 2009, and none suggested a specific association with
ART. (Arendorf, Bredekamp, Cloete, Wood, & O’Keefe, 1997; Bravo
et al., 2006; Cavasin Filho & Giovani, 2009). OW prevalence in
1990 was reported as 2%, increasing to more than 5% after 2000
(Figure 1), but did not differ significantly in patients on ART (4%)
and in subjects not on ART (5%) (Figure 2). In a retrospective study
of 1,280 HIV-infected patients by Greenspan, Canchola, Macphail,
Cheikh, and Greenspan (2001), the prevalence of OW was higher in
patients on ART (Greenspan et al., 2001). Recently, the increase in
the prevalence of HPV-related oral conditions has been attributed to
the immune reconstitution status (King et al., 2002) or age-related
immune insufficiency, rather than as direct consequence of using
ART (Anaya-Saavedra et al., 2013).
In addition to the ten OM of HIV described above, a lower
prevalence of other oral lesions was reported. Non-Hodgkin's
lymphoma was included in 14 studies in developing countries, at
a higher prevalence in Africa (4.5%) compared with other conti-
nents (Europe 2%, Asia 1.8% and America 0.6%). NHL was seldom
 |
26
reported in the head and neck area but if present, it was a clear
indicator of a compromised immune system and highly associated
with HIV, justifying its description as such in the ECC criteria (EC-
Clearinghouse, 1993). Additionally, there were conditions that
were reported in the literature sporadically including squamous
cell carcinoma (seven studies; five in developing countries and
two in developed countries), varicella zoster, facial palsy, exfoli-
ative cheilitis, histoplasmosis, erythema multiform and molluscum
contagiosum.
In conclusion, when reviewing the relevant literature, it becomes
clear that there is a difference in the prevalence of OM of HIV
around the world, dictated mainly by the developmental status of
the country. This is probably indicative of the standard of health care
and the accessibility to effective treatment. Data strongly suggest
that ART is important when justifying the difference in the pattern
of OM between developed and developing countries, but other fac-
tors including, oral and life style habits, gender, HIV stage, smoking
and alcohol consumption also play a role.
The pattern of the OM-HIV may have changed over the de-
cades and is no longer problematic in developed countries, but
they remain a significant clinical challenge in the developing world.
This emphasises the persistent inequity in oral health around the
world. When the relevant published literature was scrutinised,
data on the evolution of OM of HIV worldwide since the start of
the HIV epidemic in 1980 showed that OM-HIV continues to be a
current health challenge highlighting the importance of continuing
the research in the field. The World Workshops of Oral Health and
Disease in HIV/ADIS have provided a setting for oral HIV clinicians
and researches from around the world to debate and work col-
laboratively to address topical problems, since they were started
30 years ago (Greenspan & Challacombe, 2020). The latest work-
shop in Bali, Indonesian in September 2019, advocated improved
education underpinned by research in oral HIV to support achiev-
ing the UNAIDS objectives (WW8 The BALI Declaration on Oral
Health in HIV/AIDS, 2019).
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