DOCUMENTO

1. Original article
Investigation of oral atopic diseases: Correlation between
geographic tongue and fungiform papillary glossitis
T. Núñez Amin Dick a
, L. Rocha Santos a
, S. Carneiro b
, D. Moore c
, S. Pestana c
,
J. Laerte Boechat c
, B. Lavinas Sayed Picciani a,
*
a
Postgraduate Program in Pathology, School of Medicine, Fluminense Federal University, 303, Marquês do Paraná, 4th floor, 24033-900 Niterói,
Rio de Janeiro, Brazil
b
Sector of Dermatology, Medical Clinic Department, Rio de Janeiro Federal University, Rio de Janeiro, Brazil
c
Allergy and Clinical Immunology Service, School of Medicine, Fluminense Federal University, Niterói, Rio de Janeiro, Brazil
1. Introduction
Atopic diseases are among the most common chronic diseases
in adolescents and young adults, and their prevalence has
increased significantly over the last decades [1]. By definition,
atopy is the predisposition of the immune system to favor
immunoglobulin E (IgE)-mediated hypersensitivity reactions in
response to common environment antigens internal and external
to the household [1]. The clinical consequence of this is the
propensity to develop allergic bronchial asthma, allergic rhinitis
and atopic dermatitis [2–4]. The International study of asthma and
allergies in childhood (ISAAC) questionnaire points to comparable
prevalence rates of atopic diseases in many countries; however,
studies including clinical examinations and diagnostic criteria
remain scarce [1].
The correlation between oral lesions and atopy is not new, but
few studies have investigated the prevalence of mucosal changes
in diseases within the atopic spectrum, leading to conflicting data
[4,5]. Some studies found a possible relationship between
geographic tongue, transient lingual papillitis and atopic diseases,
leading their authors to conclude that geographic tongue is a
manifestation of atopy [6–8].
Geographic tongue, also known as benign migratory glossitis, is
an oral lesion of unknown etiology, immunologically mediated and
with a chronic inflammatory profile [9,10]. It is usually character-
J Stomatol Oral Maxillofac Surg xxx (2020) xxx–xxx
A R T I C L E I N F O
Article history:
Received 7 September 2019
Accepted 25 May 2020
Keywords:
Asthma
Rhinitis
Atopic dermatitis
Atopic diseases
Geographic tongue
Oral manifestations
A B S T R A C T
Introduction: The correlation between oral lesions and atopy is not new, but few studies have investigated
the prevalence of mucosal changes in diseases within the atopic spectrum, leading to conflicting data.
Some studies found a possible relationship between geographic tongue, transient lingual papillitis and
atopic diseases.
Aim: To investigate the frequency of geographic tongue and fungiform papillary glossitis in patients with
atopic diseases, and its correlation with serum IgE levels and skin test results.
Material and methods: The sample was comprised of participants with atopic diseases paired with
participants who received negative puncture skin tests. All were submitted to stomatological and
medical evaluations, prick test and oral cytopathological.
Results: The female sex was more numerous in both groups. Mean age was 21 years. A total of
60 diagnoses of atopic diseases were obtained, with allergic rhinitis being the most prevalent. Fungiform
papillary glossitis was the most frequent oral lesion in both groups, while geographic tongue was present
in 2 cases (2%) in the test group and 2 (2%) in the control group. Atopic patients with fungiform papillary
glossitis presented high serum IgE levels. In atopic patients with geographic tongue, the prick test
positively identified extracts of Dermatophagoides pteronyssinus (100%) and Dermatophagoides farinae
(100%).
Conclusion: Due to the low frequency of geographic tongue lesions found in the study, it is no possible to
conclude if that could be an oral manifestation of atopy. However fungiform papillary glossitis is a
common alteration in atopic and non-atopic patients and has a relationship with high IgE serum levels.
However, the consolidation of this result requires a larger sample size.
C 2020 Published by Elsevier Masson SAS.
* Corresponding author.
E-mail address: brunapicciani@gmail.com (B. Lavinas Sayed Picciani).
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Please cite this article in press as: Núñez Amin Dick T, et al. Investigation of oral atopic diseases: Correlation between geographic tongue
and fungiform papillary glossitis. J Stomatol Oral Maxillofac Surg (2020), https://doi.org/10.1016/j.jormas.2020.05.025
Available online at
ScienceDirect
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https://doi.org/10.1016/j.jormas.2020.05.025
2468-7855/
C 2020 Published by Elsevier Masson SAS.

2. ized by a keratotic line, which delimits an erythematous region
relative to the hypotrophic area of the filiform papillae [9,10]. It
most frequently affects the back, lateral margins and apex of the
tongue. The lesion migrates, and goes through periods of
exacerbation and mollification [9,10]. Its course is usually
asymptomatic; however, some patients may report pain or a
burning sensation, especially after ingesting acidic, overly sea-
soned or spicy foods [9,10].
This study investigated the prevalence of oral lesions among
patients with atopic diseases, focusing on geographic tongue and
fungiform papillary glossitis. In addition, this study is an attempt to
assess the correlation between these lesions, IgE serum levels, and
the main allergens detected by the prick test.
2. Materials and methods
This study was an analytical and cross-sectional. Participation
was not age or sex-restricted. All participants were selected from
the Clinical Immunology Outpatient Clinic of the Antônio Pedro
School of Medicine, associated with the Fluminense Federal
University. Participants with some kind of atopic disease (asthma,
rhinitis, and/or atopic dermatitis) as well as non-atopic partici-
pants were selected. In order to be diagnosed as having an atopic
disease, participants had to test positive for at least one of the
antigens under consideration (an aeroallergen or food), in addition
to fitting the anamnesis and physical examination results
characteristic of one or more atopic diseases. To be diagnosed as
non-atopic, participants had to prick test negative for all antigens
under consideration, however, they had symptoms of allergies.
Excluded were participants with a history of autoimmune,
immune-mediated and metabolic diseases; hepatitis B or C virus
or HIV infections; inflammatory bowel disease; neurological or
psychiatric diseases, and pregnant women. All participants were
submitted to demographic and clinical data collection, extra and
intraoral physical examination, blood collection for total IgE serum
dosing, and puncture test (prick test).
All participants had prick tests performed in the volar surface
of the forearm, to which one drop of negative control, one drop of
positive control (histamine), and one drop of the suspect extract
were applied, followed by puncturing the skin through the drop
of suspect extract or controls. The puncture was made using a
lancet appropriate for the immediate reading of the skin tests.
After 15 minutes, the transverse diameter of the papule’s
elevation was read. The obtained papules were delimited using
a ballpoint pen with a thin tip; tests in which the papules had a
diameter equal to or greater than 3 mm (after discounting the
diameter of the negative control, when applicable) were
considered positive. The puncture was performed on all
suspected allergens at the same time.
Version 22 of the statistical package for the social sciences
(SPSS) was used for statistical tests. Statistical description of
categorical variables was performed according to proportions. For
numerical variables, means, standard deviations, minimum-
maximum values, mode and medians were calculated. Fisher’s
exact test was used to evaluate the difference between two or more
categorical variables. For numerical variables, the groups were
collectively compared using the Mann–Whitney test. The level of
statistical significance established for all analyses was 5%
(P < 0.05).
This study was approved by the university’s Ethics and Research
Committee (68432217.4.0000.5243) and it is in compliance with
the Helsinki Declaration, that each subject in the project signed a
detailed informed consent form.
3. Results
The sample consisted of 66 participants, 33 (50%) with atopic
diseases and 33 (50%) without. The female sex prevailed in both
groups (65%). Brown skin color occurred in 42% of atopics and
white skin color in 45% of non-atopics. Age ranged from 3 to
82 years in both groups. In atopic patients, allergic rhinitis was the
most prevalent disease with 27 (45%) cases, followed by allergic
asthma with 20 (33%), and atopic dermatitis with 13 (22%). Total
IgE serum level measured in 23 atopic and 27 non-atopic
participants ranged from 7.87 to 6950 IU/mL (mean: 1129 IU/
mL) in the atopic group and 6.17 to 1660 IU/mL (mean: 257.07 IU/
mL) in the non-atopic group (P = 0.001).
Concerning the prick test, performed on all participants, to
identify negative response in 33 cases (50% – non-atopic
participants) and 33 cases (50% - atopic participants) positive
response. Positive extracts in atopic participants, there were 28
(85%) positive identifications of Dermatophagoides pteronyssinus
extract, 26 (79%) of Dermatophagoides farinae, 21 (64%) of Blomia
tropicalis, 1 (3%) of Blatella germanica, 1 (3%) of Periplaneta
americana, 1 (3%) of Canis familiar, and 2 (6%) of Felis domesticus.
Regarding the prevalence of oral lesions, more than 90%
patients in both groups presented one or more lesions (Fig. 1).
Fungiform papillary glossitis was the most frequent lesion,
observed in 25 (31%) cases in atopic patients and 20 (23%) in
non-atopic patients (Table 1 and Fig. 2). Atopic patients with
fungiform papillary glossitis presented high serum IgE levels when
compared to non-atopic patients (Mean: 1020 IU/mL vs. 337 IU/
mL; P = 0.005; Table 2).
Geographic tongue (Fig. 3) was present in only 4 cases, 2 (2%) in
each group. Among atopics with geographic tongue, there were
positive skin-test identifications for D. pteronyssinus (100%), D.
farinae (100%) and B. tropicalis (50%) (Table 3). Because blood was
not collected, total serum IgE was only evaluated in two
Fig. 1. Most prevalent oral lesions in atopic and non-atopic participants.
T. Núñez Amin Dick et al. / J Stomatol Oral Maxillofac Surg xxx (2020) xxx–xxx
2
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JORMAS-867; No. of Pages 6
Please cite this article in press as: Núñez Amin Dick T, et al. Investigation of oral atopic diseases: Correlation between geographic tongue
and fungiform papillary glossitis. J Stomatol Oral Maxillofac Surg (2020), https://doi.org/10.1016/j.jormas.2020.05.025

3. Table 1
Description of oral manifestations in the sample.
Manifestation Atopic disease Control Total Pa
n = 33 % = 100 n = 33 % = 100 n = 66 % = 100
Oral lesion present 81 98 87 99 168 98 0.757
Oral lesion absent 2 2 1 1 3 2
Fungiform papillary glossitis 25 31 20 23 45 27 0.191
Caries 17 21 23 26 40 24 0.443
Fissured tongue 19 23 20 23 39 23 1
Melanosis 7 9 7 8 14 8 0.764
Malocclusion 5 6 6 7 11 7 1
Candidiasis 1 1 4 5 5 3 1
Geographic tongue 2 2 2 2 4 2 1
Torus palatinus 2 2 2 2 4 2 1
Proteic stomatitis 0 0 1 1 1 1 NAb
Fistula 0 0 1 1 1 1 NA
Torus mandibularis 1 1 0 0 1 1 NA
Gingivitis 1 1 0 0 1 1 NA
Aphthous stomatitis 1 1 0 0 1 1 NA
Herpes labialis 0 0 1 1 1 1 NA
Total 81 100 87 100 168 100
a
Fischer’s exact test.
b
NA: non-applicable.
Fig. 2. Clinical aspects of fungiform papillary glossitis.
Table 2
Correlation between atopic patients and controls with fungiform papillary glossitis, according to family history, prick test and serum IgE levels.
Variable Category Atopic disease Control Total P
n = 25 % n = 20 % n = 45 %
Family history of atopic diseasesa
Present 17 68% 13 65% 30 67 1.000
Absent 8 32% 7 35% 15 33
Serum IgE levelb
Mean (sd) 1020 (955) 337 (436) 730 (841) 0.005
Minimum 7.87 6.17 6.17
Maximum 3.529 1.660 3529
Standard Deviation 955 436 841
Dermatophagoides pteronyssinus 21 84% – – 21 47 –
Dermatophagoides farinae 21 84% – – 21 47
Blomia tropicalis 18 72% – – 18 40
Prick Test Blatella germanica (cockroach) 1 4% – – 1 2
Periplaneta americana (cockroach) 1 4% – – 1 2
Canis familiares (dog) 0 0% – – 0 0
Felis domesticus (cat) 1 4% – – 1 2
a
Fischer’s exact test.
b
Mann–Whitney test.
T. Núñez Amin Dick et al. / J Stomatol Oral Maxillofac Surg xxx (2020) xxx–xxx 3
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Please cite this article in press as: Núñez Amin Dick T, et al. Investigation of oral atopic diseases: Correlation between geographic tongue
and fungiform papillary glossitis. J Stomatol Oral Maxillofac Surg (2020), https://doi.org/10.1016/j.jormas.2020.05.025

4. participants, 1 from the atopic group (389 IU/mL) and 1 from the
non-atopic group (62.83 IU/mL).
4. Discussion
Atopic diseases have a high prevalence in the pediatric
population, likely manifesting themselves in the first months of
life [10–12]. Despite affecting both sexes, some studies point to
greater prevalence among women [11–15]. However, this may be
linked to participants’ ages, insofar as it affects the appearance of
diseases in women and men differently [12,13]. In our study, the
female sex prevailed (65%), while the brown skin color occurred in
42% of atopics. The average age of atopic patients was 21 years,
corroborating the notion that atopic diseases occur frequently in
younger people [1]. It is worth noting that, as the participants were
recruited in a specialized care service, the data may not represent
the characteristics of the general population.
Regarding oral alterations in atopic patients, Ghapanchi et al.
[4] recently observed an increase in the presence of atrophic
candidiasis (13%) among asthmatic patients when compared to
the control group (2%), but found no relationship between the
disease and other alterations such as fissured tongue, caries and
anterior open bite [4]. This may be explained by the use of
medication via inhalation, favoring the emergence of oral
candidiasis and also causing salivary alterations, preventing
saliva from properly performing its protective function [4]. While
studying patients with atopic dermatitis, Gonzaga et al. [5]
concluded that the prevalence of geographic tongue (GT),
persistent thrush and fissured tongue in these patients was not
higher [5]. Marks et al. [14], on the other hand, observed a 52%
frequency of fungiform papillary glossitis in atopic patients,
suggesting atopy as responsible for this type of inflammatory
alteration in the tongue [14]. In our study, intraoral examination
allowed for the diagnosis of several alterations, with a high
frequency (> 90%) in both groups.
Fig. 3. Clinical aspects of geographic tongue.
Table 3
Rates of positive prick tests among atopics with fungiform papillary glossitis (FPG), geographic tongue, or none of the alternatives.
Variable Category FPG Geographic tongue No FPG or geographic
tongue
n = 25 % n = 2 % n = 8 %
Prick test Dermatophagoides pteronyssinus 21 84 2 100 7 87
Dermatophagoides farinae 21 84 2 100 7 87
Blomia tropicalis 18 72 1 50 4 50
Blatella germanica (cockroach) 1 4 0 0 0 0
Periplaneta americana (cockroach) 1 4 0 0 0 0
Canis familiares (dog) 0 0 0 0 1 12
Felis domesticus (cat) 1 4 0 0 0 0
T. Núñez Amin Dick et al. / J Stomatol Oral Maxillofac Surg xxx (2020) xxx–xxx
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Please cite this article in press as: Núñez Amin Dick T, et al. Investigation of oral atopic diseases: Correlation between geographic tongue
and fungiform papillary glossitis. J Stomatol Oral Maxillofac Surg (2020), https://doi.org/10.1016/j.jormas.2020.05.025

5. Fungiform papillary glossitis was the most frequently diag-
nosed alteration in both groups, being observed in 31% of atopics
and 23% of non-atopics. Although no studies have related
fungiform papillary glossitis to skin tests, it is known that the
most frequently identified inhalable antigens are the mites D.
pteronyssinus, D. farinae and B. tropicalis [15,16]. In our study,
those were also more frequently identified in patients with
fungiform papillary glossitis, as expected.
Despite not being a specific lesion of atopic diseases, some
authors report GT as associated with these disorders [7,17–19] The
association between GT and atopy was described by Marks et al.
[6], who found an increased frequency of atopy (asthma, rhinitis
and dermatitis) in patients with GT [6]. Since then, belief in this
association has been commonplace [19–22]. One possible expla-
nation for this relationship is that both are inflammatory and
recurrent conditions, and thus the manifestation of atopic diseases
could stimulate the appearance of GT and vice-versa [6]. However,
in our study, GT was present in only 4 (2%) cases, 2 (2%) in the test
group and 2 (2%) in the control group. This association is not very
well understood and some authors do not believe in such a
relationship, claiming that previous studies have methodological
flaws in the diagnosis of oral and systemic lesions. Shulman et al.
[10] evaluated the presence of atopy with emphasis on skin
manifestations in 279 cases of GT and 16.554 control individuals.
No relationship was found [10]. Jainkittivong et al. [21] evaluated
188 patients with GT paired against healthy individuals, and found
that there was no significant difference in the frequency of atopies
between the groups (55% versus 45%). In that study, a low
frequency of GT was found [21] Most studies associate GT with
diseases such as psoriasis, but not with atopic diseases.
Since GT and atopic diseases are recurrent and inflammatory
conditions that can be initiated by contact with external
environmental irritants, we sought to relate them and found that
female atopic participants with GT also had allergic asthma. In one
of those cases, there was an association between asthma and
allergic rhinitis. This finding corroborated a study with asthmatics
by Ghapanchi et al. [4], who concluded that the frequency of GT in
100 asthmatics was 10%, considerably higher than that of the
control group (2%) [4]. However, the authors did not describe how
the diagnosis of asthma and GT was performed. Thus, it is not
possible to confirm GT as an oral manifestation associated with
asthma, [22] mainly because there may be lesions diagnosed as GT
that are actually cases of candidiasis which regresses after
treatment by antifungal agents. [23]. In this sense, the assessment
of candidiasis in some cases of GT could be important for a correct
diagnosis and treatment. Another difficulty in the way of this
assessment concerns accuracy: in addition to the possibility of the
lesion being absent at the time of examination, the patient may
never have performed a detailed oral assessment, being unaware
that the lesion is present. For this reason, while evaluating the
prevalence of GT in some diseases such as psoriasis, Gonzaga et al.
[24] concluded that patients are not routinely submitted to full oral
examination and that the results of this examination would be very
useful for resolving the divergences between data from different
researches [24].
Some studies also sought to demonstrate a correlation between
GT and atopy using total IgE serum levels and prick test results.
Maks et al. [6] reported that out of 100 participants with GT, 28%
had total IgE serum levels 200 IU/mL, compared to 18% in the
control group [6]. In 1987, Marks and Tait evaluated 95 participants
with GT, demonstrating that 24% had high serum IgE levels [18]. In
our study, due to two patients’ refusal to allow blood collection,
serum IgE levels were only evaluated in 2 participants with GT, one
from the test group (389 IU/mL) and one from the control group
(63 IU/mL). From these results and considering that, for the overall
sample, average IgE concentrations were 1129 IU/mL in the test
group and 257 IU/mL in the control group we can infer that there is
no significant association between GT and high serum IgE levels:
participants with GT presented below-average levels.
Concerning the prick test, a 1984 study by Marks and Czarny
investigated 102 participants who tested positive for atopic
diseases. Among these, 46 (45%) had GT, compared to 12 (31%)
among the 164 non-atopic participants [20]. Based on these results
and some other parameters, the authors concluded there is a
correlation between atopy and GT [20]. In another, more recent
study, the skin test was performed in 40 participants with GT and
40 controls [25]. The prick test came back positive for 10 parti-
cipants (25%) in the test group and 4 (10%) in the control group
[25]. These findings led the authors to conclude that there is a
predisposition to allergy in patients with GT [25]. Similarly to what
was seen in this latter study, here the most frequent positively
identified extracts among atopic patients were D. pteronyssinus
(100%) and D. farinae (100%), followed by B. tropicalis (50%).
Although the correlation between GT and atopy remains unproven,
there may be a relationship between sensitization to the most
common aeroallergens (mites) and GT.
Moreover, although atopic diseases and GT are recurrent and
inflammatory conditions, their immunopathogenesis differs. This
is not the case for psoriasis and GT, which present clinical,
histopathological and genetic similarities. While atopic diseases
are associated with the Th2 pathway, involving the IL-4 and IL-13
cytokines and IgE production, geographic tongue presents a
response mediated by CD3/CD4/CD8 T lymphocytes. Thus, the
relationship between GT and atopic diseases remains uncertain
[26,27].
5. Conclusion
Due to the low frequency of geographic tongue lesions found in
the study, it is no possible to conclude if that could be an oral
manifestation of atopy. However fungiform papillary glossitis is a
common alteration in atopic and non-atopic patients and has a
relationship with high IgE serum levels. To consolidate this result, a
greater sample size is required.
Funding
None.
Disclosure of interest
The authors declare that they have no competing interest.
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and fungiform papillary glossitis. J Stomatol Oral Maxillofac Surg (2020), https://doi.org/10.1016/j.jormas.2020.05.025

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Please cite this article in press as: Núñez Amin Dick T, et al. Investigation of oral atopic diseases: Correlation between geographic tongue
and fungiform papillary glossitis. J Stomatol Oral Maxillofac Surg (2020), https://doi.org/10.1016/j.jormas.2020.05.025