10.5826/dpc.1401a39
Introduction: Erythema annulare centrifugum (EAC) is a rare reactive disease that typically presents as annular or polycyclic erythematous lesions. There are few studies about EAC in the literature; therefore, data on the pathogenesis of the disease are limited.
Objectives: We aimed to examine the demographic, clinical, pathological characteristics and associated conditions of the patients with EAC.
Methods: We analyzed records of the patients with EAC who admitted to our clinic in the last four years retrospectively.
Results: A total of 63 patients, 39 women and 24 men, were included in our study. The mean age of the patients was 47.8±11.2 years. The mean disease duration was 15.54±12 months. The trunk and thigh were the most commonly involved sites (49%, 33%). Associated conditions were identified in 52.3% of the patients. Infections (N = 16), malignancies (N = 6), rheumatic diseases (n=4) and drugs (n=4) were the most common precipitating factors respectively. The most common infections were superficial fungal infections and Helicobacter pylori infection. Histopathologically, 10 patients had deep type and 53 patients had superficial type EAC. We determined that the disease duration from the onset of the disease was longer (12.3 versus 16.2 months) and the number of attacks (1.2 versus 2.8 attacks) was higher in the superficial type when compared to the deep type (P = 0.042, P = 0.038).
Conclusions: In our study, infections, malignancies and rheumatic diseases were among the most common etiologic factors. We would also like to draw attention to Helicobacter pylori infection as a precipitating factor which may be a novel finding.
text/xml
2160-9381
3385
en
Funda Erduran
https://creativecommons.org/licenses/by-nc/4.0
Dermatology Practical & Conceptual
associated conditions
Evaluation of Clinicopathological Features and Associated Conditions in Erythema Annulare Centrifugum: A Retrospective Observational Analysis of 63 Patients
Text.Serial.Journal
https://dpcj.org/index.php/dpc
Original Article
2024-01-31
2023-04-03
2024-01-31
2024-04-29
e2024039
Dermatol Pract Concept
Introduction: Erythema annulare centrifugum (EAC) is a rare reactive disease that typically presents as annular or polycyclic erythematous lesions. There are few studies about EAC in the literature; therefore, data on the pathogenesis of the disease are limited.
Objectives: We aimed to examine the demographic, clinical, pathological characteristics and associated conditions of the patients with EAC.
Methods: We analyzed records of the patients with EAC who admitted to our clinic in the last four years retrospectively.
Results: A total of 63 patients, 39 women and 24 men, were included in our study. The mean age of the patients was 47.8±11.2 years. The mean disease duration was 15.54±12 months. The trunk and thigh were the most commonly involved sites (49%, 33%). Associated conditions were identified in 52.3% of the patients. Infections (N = 16), malignancies (N = 6), rheumatic diseases (n=4) and drugs (n=4) were the most common precipitating factors respectively. The most common infections were superficial fungal infections and Helicobacter pylori infection. Histopathologically, 10 patients had deep type and 53 patients had superficial type EAC. We determined that the disease duration from the onset of the disease was longer (12.3 versus 16.2 months) and the number of attacks (1.2 versus 2.8 attacks) was higher in the superficial type when compared to the deep type (P = 0.042, P = 0.038).
Conclusions: In our study, infections, malignancies and rheumatic diseases were among the most common etiologic factors. We would also like to draw attention to Helicobacter pylori infection as a precipitating factor which may be a novel finding.
Funda Erduran
2024/01/31
10.5826/dpc.1401a39
e2024039
Ankara City Hospital, Department of Dermatology, Ankara, Turkey
2160-9381
associated conditions
en
e2024039
Chiang CH, Lai FJ. Pregnancy-associated erythema annulare centrifugum. J Formos Med Assoc. 2015;114(7):670-671. DOI: 10.1016/j.jfma.2014.01.004. PMID: 24548620.
Evaluation of Clinicopathological Features and Associated Conditions in Erythema Annulare Centrifugum: A Retrospective Observational Analysis of 63 Patients
https://dpcj.org/index.php/dpc/article/download/3385/2413
      Evaluation of Clinicopathological Features and
       Associated Conditions in Erythema Annulare
       Centrifugum: A Retrospective Observational
                  Analysis of 63 Patients
                                                         Funda Erduran1


1 Ankara City Hospital, Department of Dermatology, Ankara, Turkey



Key words: Erythema annulare centrifugum, clinicopathological features, associated conditions
Citation: Erduran F. Evaluation of Clinicopathological Features and Associated Conditions in Erythema Annulare Centrifugum:
A Retrospective Observational Analysis of 63 Patients. Dermatol Pract Concept. 2024;14(1):e2024039. DOI: https://doi.org/10.5826
/dpc.1401a39
Accepted: September 25, 2023; Published: January 2024
Copyright: ©2024 Erduran. This is an open-access article distributed under the terms of the Creative Commons Attribution-
NonCommercial License (BY-NC-4.0), https://creativecommons.org/licenses/by-nc/4.0/, which permits unrestricted noncommercial use,
distribution, and reproduction in any medium, provided the original authors and source are credited.
Funding: None.
Competing Interests: None.
Corresponding Author: Funda Erduran, Ankara City Hospital, Department of Dermatology. Üniversiteler Mah, Çankaya, Ankara, 06800,
Turkey. Tel: +90 505 228 1615 Email: fnderdrn@mail.com




  ABSTRACT             Introduction: Erythema annulare centrifugum (EAC) is a rare reactive disease that typically presents
                       as annular or polycyclic erythematous lesions. There are few studies about EAC in the literature;
                       ­therefore, data on the pathogenesis of the disease are limited.
                       Objectives: We aimed to examine the demographic, clinical, pathological characteristics and ­associated
                       conditions of the patients with EAC.
                       Methods: We analyzed records of the patients with EAC who admitted to our clinic in the last
                       four years retrospectively.
                       Results: A total of 63 patients, 39 women and 24 men, were included in our study. The mean age of
                       the patients was 47.8±11.2 years. The mean disease duration was 15.54±12 months. The trunk and
                       thigh were the most commonly involved sites (49%, 33%). Associated conditions were identified in
                       52.3% of the patients. Infections (N = 16), malignancies (N = 6), rheumatic diseases (n=4) and drugs
                       (n=4) were the most common precipitating factors respectively. The most common infections were su-
                       perficial fungal infections and Helicobacter pylori infection. Histopathologically, 10 patients had deep
                       type and 53 patients had superficial type EAC. We determined that the disease duration from the onset
                       of the disease was longer (12.3 versus 16.2 months) and the number of attacks (1.2 versus 2.8 attacks)
                       was higher in the superficial type when compared to the deep type (P = 0.042, P = 0.038).
                       Conclusions: In our study, infections, malignancies and rheumatic diseases were among the most
                       common etiologic factors. We would also like to draw attention to Helicobacter pylori infection as a
                       precipitating factor which may be a novel finding.



Original Article | Dermatol Pract Concept. 2024;14(1):e2024039                                                                      1
Introduction                                                         Objectives
Erythema annulare centrifugum (EAC) is a slowly progressive          The aim of our study was to evaluate the demographic, clin-
eruption characterized by annular or polycyclic erythematous         ical and histopathologic characteristics of patients with EAC
papules and plaques [1]. EAC is considered a type 4 hypersen-        and to examine the associated diseases.
sitivity reaction to an antigenic stimulus [2]. The term EAC
was first used by Jean Darier in 1916 [3]. Darier referred to
                                                                     Methods
EAC also by a synonym “érythème papulo-circiné migrateur
et chronique” [3]. There are few studies on EAC in the lit-          Our study was designed as a retrospective study in a tertiary
erature which are retrospective studies with small number            referral hospital. We analyzed data of the patients over the
of patients [4-6]. The exact prevalence is unknown [1]. EAC          age of 18 years who were followed up with a diagnosis of
is seen in two clinical forms, superficial and deep [2,7]. In        EAC between January 2019 and January 2023. We stipu-
both forms, the lesions start as a hard erythematous papule          lated a clinicopathologic correlation in our study to exclude
with centrifugal spread, which begins to heal from the center.       other annular erythemas resembling EAC. Ethics committee
The superficial type appears as erythematous, non-indurated          approval numbered E1-23-3287 was obtained before the
plaques. On the inner side of the advancing margin, trailing         study (08.02.2023). Statistical analysis calculations were
scale is typical. In the deep type, there is typically no scale,     made with Statistical Package for Social Sciences (SPSS) ver-
and the advancing borders are raised and indurated. Lesions          sion 24.0 for Windows program. Continuous variables (age,
may sometimes persist for weeks and months, regressing and           duration of disease) are expressed as mean and standard de-
disappearing without leaving a scar [2,7]. Paraneoplastic EAC        viation, while categorical variables (localizations of lesions,
associated with malignancy is called PEACE (paraneoplastic           number of attacks, histopathological subtype, associated
erythema annulare centrifugum eruption) [8]. EAC may start           conditions, concomitant diseases, treatments received) are
years before, simultaneously or later than malignancy [9]. The       expressed as number and percentage. Chi-Square test statis-
first approach in the treatment of EAC is to treat the under-        tics was used to compare categorical measurements. Statisti-
lying disease if one is detected. Since it usually regresses spon-   cal significance level was accepted as 0.05 in all tests.
taneously without treatment and is largely asymptomatic, it
can be followed up without treatment in mild cases [1,10].
                                                                     Results
Some authorities recommend empirical use of antibiotics and
antifungal agents even if the cause cannot be identified. Al-        We included a total of 63 patients, 39 (62%) females and 24
though systemic steroids provide clinical remission, they are        (38%) males, aged between 19 and 84 years in our study.
not preferred since the findings tend to recur after discontinu-     We had excluded five patients with missing or incongruous
ation of the drug [10,11]. Local tacrolimus, calcipotriol, oral      histopathological data on the eve of the study. The mean age
metronidazole, subcutaneous interferon and apremilast were           of the patients was 47.8±11.2 years. The duration of disease
reported to be beneficial in some patients [12-15]. However,         ranged from 1 week to 10 years with a mean of 15.54±12
it has been reported that the treatments did not change the          months. In 19 patients, the duration of disease was longer
chronic and recurrent course of the disease [6].                     than 1 year and the disease persisted for an average of 45.8
    The histopathology of EAC varies according to its type.          months. Trunk, thighs and arms were the most frequently
In the superficial type nonspecific findings such as mild            affected sites (Figures 1 and 2). Localizations of the lesions
spongiosis, microvesiculation, focal parakeratosis, epidermal        are shown in Table 1. Involvement in multiple localizations
hyperplasia, minimal superficial perivascular lymphohistio-          was observed in eight patients. The number of attacks of the
cytic infiltration are seen. Furthermore, edema of the pap-          patients varied between 1-20 attacks. Multiple attacks de-
illary dermis is more common in the superficial type [1,4].          veloped in 43% (N = 27) of the patients and it was the first
In the deep form, epidermal changes are not prominent and            attack in 57% (N = 36). In patients with multiple episodes,
mononuclear cell infiltration with dense perivascular aggre-         the episodes recurred in an average of 9.1 months. Histo-
gation is evident in the mid and lower dermis which leads            pathologically, 10 (15.9%) and 53 (84.1%) patients had
to elevated and more indurated lesions in the deep form of           findings compatible with deep (Figures 3 and 4) and super-
EAC clinically [1,4]. In addition, inflammatory cells typically      ficial type EAC, respectively. It was consistent with clinical
accumulate densely around the vessels in a so-called “sleeve”        deep and superficial types. We evaluated all patients diag-
fashion [1,4]. This typical infiltration may be considered as        nosed with EAC in our study in terms of underlying diseases.
a marker for the differentiation of EAC from other figurate          Factors that may be involved in the etiology were found in
erythemas. Since fibrin extravasation is not expected in EAC,        52.3% of the patients. Associated conditions are shown in
it can be considered as pseudovasculitis [1,4].                      Table 2. Eight patients had fungal infections (tinea pedis



2                                                                        Original Article | Dermatol Pract Concept. 2024;14(1):e2024039
Figure 1. Our patient with deep type of EAC. Non-scaly erythema-
tous annular plaques with central clearence.                       Figure 3. Our patient with histopathologically deep type of EAC
                                                                   (who was also clinically consistent with deep type of EAC). Tight
                                                                   perivascular mononuclear cellular infiltrate in both upper and lower
                                                                   dermis without prominent epidermal changes and edema of the pap-
                                                                   illary dermis (H&E, X40). From the archive of Dr. Nuran Süngü,
                                                                   Ankara City Hospital, Department of Pathology.




Figure 2. Our patient with superficial EAC. Erythematous and an-
nular plaques with a trailing scale.




         Table 1. Localizations of the lesions                     Figure 4. Perivascular mononuclear infiltrate, tightly adherent to
                   in the patients.                                vascular plexus in “coat sleeve pattern” (H&E, X100). From the
                                                                   archive of Dr. Nuran Süngü, Ankara City Hospital, Department of
     Localizations of the lesions                  N (%)           Pathology.
 Trunk                                            31 (49.2)
 Thigh                                            21 (33.3)
 Arm                                              14 (22.2)        cancer: 2, breast cancer: 1, thyroid cancer: 1). The diagnosis
 Gluteal area                                      7 (11.1)        of malignancy was made before the onset of EAC in 5 of the
 Neck                                               1 (1.6)        patients while in one patient it was made concurrently with
                                                                   EAC. Of these patients, 3 were in remission or cured, while
                                                                   in 3 patients the disease was active and they were receiving
and/or tinea unguium in 7 patients, vaginal candidiasis in         chemotherapy. Four patients were diagnosed with rheumatic
1 patient), 4 patients had gastritis and Helicobacter pylori       diseases (juvenile rheumatoid arthritis, palindromic rheuma-
infection. There was one case each of urinary tract infection,     tism, rheumatoid arthritis, granulomatosis with polyangiitis,
upper respiratory tract infection, Coronavirus disease 2019        1 case of each of them). The most common concomitant
(COVID-19), HIV infection and pregnancy. Four patients             diseases were gastritis (N = 10), diabetes (N = 7), hypothy-
had a history of drug use (analgesics, oral contraceptives,        roidism (N = 6), malignancy (N = 6) and rheumatic disease
antibiotics, escitalopram, 1 case of each of them). Two pa-        (N = 4) respectively. Concomitant diseases are shown in
tients had Hashimoto thyroiditis. Malignancy was detected          ­Table 3. In our study, when superficial and deep types were
in 6 patients (gastric cancer: 1, cervical cancer: 1, prostate     compared based on the clinical and histological classification,



Original Article | Dermatol Pract Concept. 2024;14(1):e2024039                                                                       3
     Table 2. Associated conditions which were                       Table 4. Treatments received by the patients.
      blamed for triggering erythema annulare                                    Treatments                         N (%)
            centrifugum in the patients.                           Topical corticosteroids                        30 (47.6)
        Associated                                                 Topical calcineurin inhibitors                  8 (12.6)
     conditions, N (%)                      N
                                                                   Terbinafine                                       6 (9.5)
 Infections, 16 (25.3)       tinea pedis/unguium: 7
                                                                   Calcipotriol                                      4 (6.3)
                             vaginal candidiasis: 1
                             Helicobacter pylori infection: 4      Azithromycin                                      3 (4.7)
                             urinary tract infection:1             Systemic steroid                                  2 (3.2)
                             upper respiratory tract               Dapsone                                           1 (1.6)
                             infection: 1                          Fluconazole                                       1 (1.6)
                             COVID-19:1
                                                                   None                                           17 (26.9)
                             HIV infection:1
 Malignancies, 6 (9.5)       prostate cancer:2
                             gastric cancer:1
                             cervix cancer:1                      Topical steroid (N = 30), topical calcineurin inhibitor
                             breast cancer:1                      (N = 8), terbinafine (N = 6) and calcipotriol (N = 4) were
                             thyroid cancer:1                     the most commonly received treatments by our patients
 Rheumatic diseases,         juvenile romatoid arthritis:1        (Table 4). We determined that 26.9% (N = 17) of the pa-
 4 (6.3)                     romatoid arthritis:1                 tients did not receive any treatment. The lesions resolved in
                             romatoid arthritis:1
                                                                  some of these patients while waiting for the results of skin
                             granulomatosis with
                                                                  biopsy or the laboratory tests made for revealing precipitat-
                             polyangiitis:1
                                                                  ing factors. Also, some of the patients did not apply their
 Medications, 4 (6.3)        oral contraceptives:1
                             analgesics:1                         treatments. Treatment responses could not be evaluated in
                             antibiotics:1                        our study because of the self-healing tendency of EAC and
                             escitalopram:1                       dropout of some patients from treatment.
 Endocrinopathies, 2(3.1) Hashimoto thyroidit:2
 Other, 1(1.5)               pregnancy:1
                                                                  Conclusions
                                                                  In our study, 62% of the patients were female and 38% were
    Table 3. Concomitant diseases in the patients.                male. The mean age of the patients in our study was 47.8±11.2
                                                                  years and the mean disease duration was 15.54±12 months. In
         Concomitant diseases                        N
                                                                  a study by Kim et al evaluating the demographic and clinical
 Gastritis, dyspepsia                                10
                                                                  characteristics of 39 patients with EAC, 64% of the patients
 Esophagitis                                         2
                                                                  were female and 36% were male [5]. In another study, 24
 Diabetes                                            7
                                                                  (36%) of 66 patients with EAC were male and 42 (64%) were
 Hypothyroidism                                      6            female. In the same study, the mean age was 39.7 years and the
 Malignancy                                          6            mean disease duration was 2.8 years [6]. The mean age and
 Rheumatic disease                                   4            gender distribution in these studies were similar to our study.
 Hypertension                                        3               We observed that the most commonly involved areas in
 Asthma, allergic rhinitis                           3            our patients were the trunk and thigh, respectively. In the
 Fibromyalgia, depression                            2            study by Kim et al the lower extremities, especially the thigh,
 Chronic renal impairment                            1            were reported as the most commonly affected region [6]. In
 HIV infection                                       1            the study by Weyers et al it was found that the main predi-
 Hepatitis B carrier                                 1            lection site was the trunk in both types similar to our study,
                                                                  whereas the extremities and buttocks were more commonly
                                                                  involved in the superficial type and the face and neck in the
no difference was found in terms of age, gender, lesion lo-       deep type [4]. In our study, the number of attacks varied be-
calization, triggering factors and comorbidities (P > 0.05),      tween 1-20 attacks and the attacks recurred in a mean of
whereas the total duration of the disease from the onset of the   9.1 months. In the study by Kim et al the mean duration of
disease was longer (12.3 versus 16.2 months) and the number       persistent lesion was found to be 4.7 months [5].
of attacks (1.2 versus 2.8 attacks) was higher in the superfi-       In our study, 15.9% and 84.1% of the patients had
cial type compared to the deep type (P = 0.042, P = 0.038).       findings compatible with deep and superficial type EAC,



4                                                                     Original Article | Dermatol Pract Concept. 2024;14(1):e2024039
respectively. Similar to our study, 82.1% of the cases were       activation and lymph node metastasis was found [9]. In that
evaluated as superficial type and 17.9% as deep type in the       case, it was emphasized that if EAC occurred due to an un-
study by Kim et al [5]. In another study, it was also found       derlying disease, EAC may be correlated with exacerbations
that 78% of the patients with available data had superficial      of this disease [9]. The possible activation of cancer was also
type EAS and 22% had deep type EAC [6].                           investigated in our patients who were in remission but no
    We identified associated conditions in 52.3% of the pa-       recurrence of malignancy was detected. We had 2 cases of
tients in our study, while we evaluated that 47.6% were idio-     Hashimoto thyroiditis. A case that started 3 months before
pathic. In the study of Kim et al 33.3% of the patients were      Hashimoto thyroiditis and was associated with Hashimoto
found to have potentially related factors (cutaneous fungal       thyroiditis has been reported previously [16]. We had one
infections, pregnancy, malignancy, autoimmune diseases            case associated with pregnancy. Similar to our case, EAC as-
and drugs) [5]. In the study by Weyers et al infections, rheu-    sociated with pregnancy has been reported. In that patient,
matoid arthritis, thrombocythemia, malignancies, allergic         EAC developed in pregnancy and completely disappeared
asthma and drug reactions were blamed in 36 percent of the        1 week after delivery without treatment and did not recur in
patients [4]. In the study by Kim et al 72% of patients had       1-year follow-up [17]. Although 11.1% of the patients in our
comorbidities. Associated diseases were categorized as cuta-      study had a history of diabetes mellitus, no direct association
neous fungal infections (48%), other skin diseases (18%),         with the disease was established and no such association has
malignancies (13%) and other systemic diseases (21%) [6].         been found in the literature.
Due to the paucity of data in the literature on EAC, the un-         When we compared superficial and deep types based on
derlying causes are not fully known and are of great interest.    both clinical and histological classification, we found that
The associations detected after the diagnosis of the disease      the total disease duration from the onset of the disease was
have been generally reported as cases to date, and a clear        longer and the number of attacks was higher in the super-
relationship is usually not established. In our study, the most   ficial type compared to the deep type. In the study by Kim
frequently associated conditions with EAC were infections,        et al the detection of higher recurrence rate in the superficial
malignancies, rheumatologic diseases and drugs, respec-           type supports our findings [5]; however, it should be kept in
tively. This result was similar to aforementioned studies. Also   mind that the number of deep-type EAC cases was very low
the most common infection was superficial fungal infections       in both studies.
in concordance with previous studies. Helicobacter pylori            The most important limitations of our study are the small
infection was the second most common infection detected           number of patients and the retrospective design of our study
in our study. Since our study allowed a 4-year follow-up of       which led to missing data about treatment responses. There
medical records, we observed that most of our patients had        is an obligatory overlap between some of associated condi-
complaints of dyspepsia and heartburn. They were evaluated        tions and concomitant diseases in our study. Associated con-
for gastritis in internal medicine and gastroenterology de-       dition may be a concomitant disease and vice versa is also
partments close to or immediately after the onset of the dis-     possible. We favored to group associated conditions accord-
ease, and endoscopic examinations were performed in some          ing to priorly defined causes of EAC in the literature. Four
patients. As a matter of fact, gastritis was the most common      of the patients with gastritis had also Helicobacter pylori
disease found in the patients history. Indeed we discovered       infection. After Helicobacter pylori eradication EAC lesions
that EAC disappeared after antibiotic treatment for Heli-         regressed, so we blamed it as a triggering factor and these
cobacter pylori infection in our patients and did not recur       four patients were included in both of associated conditions/
as far as we could follow up. We think that there may be          infections and concomitant diseases/gastritis category. Sim-
a causal relationship between EAC and Helicobacter pylori         ilarly two patients with Hashimoto thyroiditis were diag-
infection, which we observed in our study.                        nosed concurrently with EAC and they were included in
    In our study, all of the patients with associated ma-         both of the categories as associated conditions/endocrinop-
lignancy had solid tumors. In a case series of 40 patients        athies and concomitant diseases/hypothyroidism. Remaining
followed up with a diagnosis of PEACE, association with           four patients with hypothyroidism suffered from the disease
lymphoproliferative diseases (most frequently leukemia and        for many years and they were stable under treatment. We
lymphoma) was observed in 62.5% of the patients and with          could not establish a cause-and-effect relationship and put
solid tumors in 37.5% [8]. In the study of Kim et al 2 of 39      them only in concomitant diseases group.
patients had thyroid cancer [5]. In the study by Weyers et al        We described the demographic and clinical character-
the number of patients with associated malignancy was 6           istics of patients with EAC in our study. We would like to
(13.33% of those with an associated disease) and the disease      point out that the association with Helicobacter pylori in-
was active in only one of these patients [4]. In a patient di-    fection, which we observed in our study may be significant.
agnosed with breast cancer EAC was associated with disease        We also found that the superficial type had a longer disease



Original Article | Dermatol Pract Concept. 2024;14(1):e2024039                                                                  5
duration and a higher number of attacks compared to the                        2012;13(4):239-246. DOI: 10.2165/11596580-000000000-00000.
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