Background: Interstitial granulomatous dermatitis (IGD) and palisaded neutrophilic granulomatous dermatitis (PNGD) are uncommon presentations of reactive granulomatous dermatitis. Histologic lesions characterized by IGD/PNGD patterns have been associated with systemic diseases, causing an unmet need for revealing clinical correlates. Objective: The aim of this study was to unravel the systemic diseases beyond dermatitis of IGD/PNGD. Methods: This study analyzed data from case studies, case series, and retrospective cohorts by searching PubMed, Embase, Web of Science, and the Cochrane Library, with no start date or language restrictions on Sep 4, 2021. Results: One hundred ninety-six publications were included (458 cases in total, 216 with details). Systemic diseases associated with IGD/PNGD were classified into 5 groups. Autoimmune disorders (n = 103, 47.6%) including rheumatoid arthritis (n = 51, 23.6%), systemic lupus erythematosus (n = 20, 9.3%), and others were the most common across all underlying diseases, followed by drug eruption (n = 52, 24.1%) such as tumor necrotic factor inhibitor reaction (n = 18, 8.3%) and malignancies (n = 27, 12.5%) such as hematologic malignancy (n = 20, 9.3%). The rest were infectious diseases (n = 12, 5.6%) and accidental conditions (n = 3, 1.4%). Conclusion: IGD/PNGD might be associated with autoimmune disorders, drug eruption, malignancies, infectious diseases, and accidental conditions. Patients with IGD/PNGD need further follow-up.

Interstitial granulomatous dermatitis (IGD) and palisaded neutrophilic granulomatous dermatitis (PNGD) are uncommon histological patterns of reactive granulomatous dermatitis with similar clinical manifestations [1]. Main histologic characteristic includes basophilic degenerated collagen surrounded by palisades of histiocytes, with or without vasculitis and mucin [2]. Although the etiology remains unknown, immune complex deposition, local collagen degeneration, and palisading lymphohistiocytic infiltration are mostly concerned [3].

Typical lesions include annular or linear cords distributed on the lateral trunk (called the “rope sign”), whereas IGD/PNGD could imitate several conditions in clinical manifestations [4] on most occasions. Hence, the diagnosis requires meticulous histological examination. In addition, exclusion of other diseases with granulomatous features is required, especially granuloma annulare, rheumatoid nodules, necrobiosis lipoidica, and early perforating disorders [2]. IGD/PNGD may overlap with the abovementioned diseases, which may be a main obstacle for clinicians [5].

It is suggested that IGD/PNGD might reflect systemic damage; therefore, we aimed to unravel the systemic diseases beyond dermatitis of IGD/PNGD. In this study, we first reviewed cases in the literature, summarized the features of lesions, and revealed underlying diseases of IGD/PNGD.

Search Strategy

Case reports, case series, and retrospective cohorts from PubMed, Web of Science, Embase, and the Cochrane Library were included, with no start date restrictions or language limitations on Sep 4, 2021. Keywords were used as the following: (((interstitial granulomatous dermatitis) OR (palisaded neutrophilic and granulomatous dermatitis)) OR (palisaded neutrophilic granulomatous dermatitis)) OR (reactive granulomatous dermatitis). Other latently relevant papers were also manually checked. Review articles, abstracts, articles unable to translate were excluded.

Data Selection and Quality Assessment

After full-text screening, data were extracted about basic information, medical histories, and follow-up information of patients. Morphological and histologic features of IGD/PNGD lesions were recorded from both text and graphics. Two distinctive reviewers assessed the studies independently, and the disagreements were resolved by consulting or a dermatologist’s determinations. The diagnosis of IGD/PNGD and ultimate clinical diagnosis was established by the authors. Only information from case studies was extracted for statistical analysis.

Temporal relationships between IGD/PNGD and underlying systematic diseases were defined according to chronological orders of lesions and ultimate diagnosis. If IGD/PNGD occurred during the first hospital visit or IGD/PNGD led to medical attention immediately in studies, simultaneity was defined. In addition, if a patient had been diagnosed with a systemic disease or exposed to an explicit physicochemical irritation in the past, which linked with the occurrence of skin lesions this time, the relationship was defined as “after.” When IGD/PNGD occurred separately in the past, the relationship was defined as “before.” Patients with primary dermatitis refer to that they just have cutaneous changes with IGD/PNGD patterns, after exclusion of any underlying disease in reports.

The methodological quality or risk of bias of included studies was assessed by The Joanna Briggs Institute (JBI) critical appraisal tool (10 items) especially for case series and retrospective cohorts [6]. As for case reports, 5 items (questions 3, 6, 7, 8, and 5) of 10 should be evaluated [7]. A scoring framework of “yes” (2 points), “unclear” (1 point), “no” (0 points), or “not applicable” were defined. In addition to JBI criteria, reports considered as high quality should be presented with clear general and histological pictures. Quality level of high, medium, and inferior was assessed by the two reviewers. All studies of inferior quality, without illustrations, or with disagreement should be revaluated according to the dermatologist’s recommendations. This study was done in accordance with PRISMA checklist [8] (online Suppl. files; for all online suppl. material, see www.karger.com/doi/10.1159/000527461).

Study Characteristics

Publication selection process is shown in Figure 1. 196 publications were identified that met inclusion criteria (458 cases in total) [1, 2, 4, 9‒201]. The characteristics of eligible retrospective studies and case series are shown in Table 1. JBI scores and methodological quality assessments are described in Table 1 and online supplementary Table S3. We extracted and analyzed information from cases described in detail, including 216 patients from 175 reports.

Table 1.

Characteristics of retrospective studies and case series of IGD/PNGD

 Characteristics of retrospective studies and case series of IGD/PNGD
 Characteristics of retrospective studies and case series of IGD/PNGD
Fig. 1.

Flow diagram of publication selection process.

Fig. 1.

Flow diagram of publication selection process.

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Clinical Results

Demographics of 216 patients were summarized in Table S1. In total, 63.9% were female with a median age of 54 ranging from 6 to 86 years. Diagnostic categories were shown comparatively in online supplementary Figure S1, included cases of autoimmune disorders (47.6%), drug eruption (24.1%), malignancies (12.5%), infectious diseases (5.6%), accidental conditions (1.4%), as well as primary dermatitis (8.8%). More specifically, rheumatoid arthritis, systemic lupus erythematosus, hematologic malignancy, primary dermatitis, and TNF inhibitor reaction were more common across all underlying diseases (Fig. 2).

Fig. 2.

Distribution of IGD/PNGD associated underlying systemic diseases organized by the disease spectrum. HIV, human immunodeficiency virus; MF, mycosis fungoides; MM, multiple myeloma; MGUS, monoclonal gammopathy of undetermined significance; HL, Hodgkin lymphoma; AML, acute myeloid leukemia; APL, acute promyelocytic leukemia; NHL, non-Hodgkin’s lymphoma; CMML, chronic myelomonocytic leukemia; MDS, myelodysplastic syndrome; IBD, inflammatory bowel disease; AOSD, adult-onset Still’s disease; SSc, systematic sclerosis; EAT, autoimmune hypothyroidism; AD, autoimmunity diseases; AIH, autoimmune hepatitis; UCTD, undifferentiated connective tissue disease; SLE, systemic lupus erythematosus; RA, rheumatoid arthritis.

Fig. 2.

Distribution of IGD/PNGD associated underlying systemic diseases organized by the disease spectrum. HIV, human immunodeficiency virus; MF, mycosis fungoides; MM, multiple myeloma; MGUS, monoclonal gammopathy of undetermined significance; HL, Hodgkin lymphoma; AML, acute myeloid leukemia; APL, acute promyelocytic leukemia; NHL, non-Hodgkin’s lymphoma; CMML, chronic myelomonocytic leukemia; MDS, myelodysplastic syndrome; IBD, inflammatory bowel disease; AOSD, adult-onset Still’s disease; SSc, systematic sclerosis; EAT, autoimmune hypothyroidism; AD, autoimmunity diseases; AIH, autoimmune hepatitis; UCTD, undifferentiated connective tissue disease; SLE, systemic lupus erythematosus; RA, rheumatoid arthritis.

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Autoimmune Disorders

Autoimmune diseases were reported in 47.6% of all cases (103 patients), mainly rheumatoid arthritis (n = 51, 49.5%) and systemic lupus erythematosus (n = 20, 19.4%), followed by vasculitis (n = 6, 5.9%), undifferentiated connective tissue disease (n = 5, 4.9%), autoimmune hepatitis (n = 5, 4.9%). Autoimmune hypothyroidism, sarcoidosis, systemic sclerosis, inflammatory bowel disease, and others accounted for small part of this group (online supplementary Table S2). In most cases (n = 72, 69.9%), the development of lesions with IGD/PNGD patterns followed the diagnosis, asymptomatic or tender (n = 92, 89.3%) with limited subtype (n = 88, 85.4%). Moreover, “rope sign” was uppermost (n = 11, 10.7%) among all subgroups. Polyarthralgia (n = 70, 68.0%) and positive autoimmune antibodies (n = 58, 56.3%) were noticeable in this group.

Malignancies

Malignancies were observed in 27 cases (12.5%), and hematologic malignancy was the most frequent (n = 20, 74.1%). Myelodysplastic syndrome (n = 5, 18.6%) was the most common followed by chronic myelomonocytic leukemia (n = 4, 14.8%), non-Hodgkin lymphoma (n = 4, 14.8%), acute leukemia (n = 3, 11.1%), solid tumors (n = 3, 11.1%), metastatic adenocarcinoma (n = 3, 11.1%), Hodgkin lymphoma (n = 2, 7.4%), multiple myeloma (n = 2, 7.4%), and mycosis fungoides (n = 1, 3.7%). With a higher percentage of males (51.9%), the distinguishing features included fever (n = 7, 26.0%), fatigue, night sweats, and lose weight (n = 11, 40.7%). For cutaneous reactions, painless (n = 19, 70.4%) or mild pruritus (n = 8, 29.6%) eruptions, which disseminated throughout the body mostly (n = 11, 40.7%) among all groups, were performed before or at the point (n = 20, 74.0%) of the definite diagnosis. Immunological examinations were normal, and the mortality is relatively high (n = 7, 25.9%). Notably, there were more reports about non-Hodgkin lymphoma and mycosis fungoides in retrospective studies and case series (5 reports, Table 1).

Drug Eruption

There were 52 cases (24.1%) specifically related to drugs, typically occurred after months to years of therapy with specific medication. TNF inhibitors (n = 18, 34.6%) were the most common across all. Other biological agents (n = 9, 17.3%), diuretics (n = 6, 11.5%), herbs (n = 5, 9.6%), antiepileptic drugs (n = 4, 7.7%), gout suppressant (n = 3, 5.7%), antiviral agents (n = 2, 3.9%), strontium (n = 2, 3.9%), and statins (n = 2, 3.9%) were also culprit. Eruptions were mostly acute (n = 29, 55.8%), transient (n = 31, 59.6%), limited (n = 43, 82.7%) with pruritus (n = 19, 36.5%). However, systemic symptoms were inapparent.

Primary

Primary IGD/PNGD (n = 19, 8.8%) showed histopathological features of the disease, but without any definite diagnosis at reporting time. Chronic cutaneous lesions (n = 16, 84.2%) with high recurrence rates (n = 7, 36.8%) but without aggravation were mostly found in this group.

Histopathological Features

Considered that PNGD and IGD are on the spectrum of reactive granulomatous dermatitis [202], we summarized integrally including aspects of interface changes, inflammatory cell infiltration (eosinophils and neutrophils), vasculitis manifestations, and mucin deposition. According to our conclusion (Table 2), neutrophil infiltration was widely observed in different groups. Whereas eosinophils invasion in drug reaction and infectious were confirmed in line with the general performance. Nevertheless, Mucin deposition was less shown in autoimmune disorder, drug reaction, and malignancy.

Table 2.

Brief summary of histopathological features for cases of IGD/PNGD

 Brief summary of histopathological features for cases of IGD/PNGD
 Brief summary of histopathological features for cases of IGD/PNGD

Treatment

Treatment of IGD/PNGD is listed in Table 3. Alleviation of lesions under topical or systemic steroids treatment was performed. Monotherapy of dapsone, disease-modifying antirheumatic drugs, and biological agents showed varying degrees of improvement. Controlling of the underlying disease led to resolution of existing lesions and prevents recurrences.

Table 3.

Summary of treatment strategies of IGD/PNGD with various underlying diseases

 Summary of treatment strategies of IGD/PNGD with various underlying diseases
 Summary of treatment strategies of IGD/PNGD with various underlying diseases

With a wide diversity of underlying diseases, skin lesions performing pathological forms of IGD/PNGD patterns are confusing and remain unclear. This study is the first to identify disease spectrum of IGD/PNGD patterns systematically. We found that except for autoimmunity disorders in concordance with the prior literature [1], tumors, especially hematologic malignancies, drug eruption, and infectious diseases are worthy of note as well. We also hope to raise the awareness of the follow-up of primary dermatitis.

Whereas IGD/PNGD patterns are more common in rheumatoid arthritis and systemic lupus erythematosus, evidence suggests that the occurrence of skin rash has close correlation with disease progression. Cutaneous changes with IGD/PNGD patterns can precede the hematologic malignancy, being asymptomatic, recurrent, and extremely similar to the autoimmunity disorder and drug eruption.

Calcium channel blockers and HMG-CoA reductase inhibitors were previously unrecognized as main causes of interstitial granulomatous drug reaction. Here, we demonstrate that TNF inhibitors occupy a larger proportion, which, remarkably, indicates underlying mechanism.

The presence of interface changes, inflammatory cell infiltration (eosinophils and neutrophils), vasculitis manifestations, and mucin deposition are intimately linked to systematic disease, extraneous with IGD/PNGD patterns per se. For example, eosinophil infiltration and keratinocyte necrosis have been considered as drug eruption in general.

Treatment remains challenging lack of high efficacy. Indeed, treating underling diseases is reasonable in most cases. However, giving that IGD/PNGD patterns can precede disease development, pretreatment strategies such as monotherapy of steroid or non-steroid systemic agents are alternative. In some cases, surprisingly, TNF inhibitors showed promise in eliminating severe and persistent lesions. Nevertheless, considering their pathogenicity, further research is needed to clarify the roles of pathogenesis and therapeutic mechanism.

This study is limited by reporting bias of references and finite statistical power. Case series and retrospective cohorts lack detailed individual information and were listed without statistical analysis, which may lead to an insufficient number of cases. Also, our finding is limited by the fact that primary dermatitis of IGD/PNGD patterns may be variable during the course. The border of IGD/PNGD and IGD/PNGD patterns is difficult to define.

The evidence cited in this review supports the views that cutaneous changes with IGD/PNGD patterns should be aware of for the roles in different systemic diseases. On this condition, tissue damage with denaturation of collagen and palisades of histiocytes may indicate a common pathway for pathology. Consequently, we suggest a multifaceted assessment for a more accuracy diagnosis and more targeted managements.

IGD/PNGD might be associated with autoimmune disorders, drug eruption, malignancies, infectious diseases, and accidental conditions. Patients with IGD/PNGD need further follow-up.

An ethics statement is not applicable because this study is based exclusively on published literature.

The authors have no conflicts of interest to declare.

This study was supported by the National Natural Science Foundation of China (82173400).

Changyi Yang is the lead author and analyzed and interpreted the data from case studies, case series, and retrospective cohorts, and was a major contributor in writing the manuscript. Shunli Tang visualized statistical data of studies and proofread all references. Sheng Li and Shuni Ying contributed to the language polish and corrected the grammatical errors. Dingxian Zhu, Taoming Liu, and Yuqi Chu helped perform the analysis with constructive discussions. Jianjun Qiao contributed to the conception of the study and helped perform the analysis with constructive discussions. Hong Fang contributed significantly to improve the review structure.

All data generated or analyzed during this study are included in this article and its online supplementary material. Further inquiries can be directed to the corresponding author.

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