ORIGINAL ARTICLE

A Study of Correlation Between Clinical and Histopathological Findings of in North Bengal Population Sabyasachi Banerjee, Swarup Ghosh1, Rajesh Kumar Mandal2

Abstract From the Department of Background: Erythroderma is a reaction pattern characterized by erythema and Dermatology, STD and Leprosy desquamation of 90% or more body surface area along with some metabolic alterations. Malda Medical College, 1 Materials and Methods: Here we studied 32 patients of erythroderma at of North Bengal Medical Department of Pathology, Asansol SD Hospital, Burdwan, 2Department College for a period of 1 year to find the etiology, clinical features and histological changes. of Dermatology, STD, and Leprosy, Detailed history was taken from all the patients followed by relevant biochemical investigations North Bengal Medical College, and histological examination. To correlate the clinical and histopathological findings chi square Darjeeling, West Bengal, India test was used. Results: Male preponderance was present and most of them were in the 4th or 5th decade. Etiologically the patients were divided into secondary erythroderma developing over pre‑existing dermatoses, and idiopathic erythroderma. Secondary erythroderma (n = 24) Address for correspondence: cases outnumbered the idiopathic cases (n = 8). Among the pre‑existing dermatoses, Dr. Rajesh Kumar Mandal, was found to be the most common etiologic agent. Apart from erythema the other common Department of Dermatology, STD, presenting features were scaling and itching. Histopathological categorization was possible in and Leprosy, North Bengal Medical 59.3% cases, rest of the cases showed non‑specific dermatitis. The most common histopathologic College, Darjeeling, West Bengal, diagnosis was psoriasis (21.8% of cases). Conclusions: Our study of clinicopathological India. E‑mail: drrajeshkumar. correlation of erythroderma patients among north bengal population corroborates with most [email protected] of the previous studies done in other areas. As ours is a cross-sectional study in a undefined population so we could not determine the true incidence of erythroderma in north bengal population. We might have missed lymphoma as a cause of erythroderma in idiopathic cases due to lack of long follow-up, so we understand that further studies over a defined population with long follow-up is needed to determine the true incidence and causes of idiopathic erythroderma.

Key Words: Clinical, correlation, erythroderma, histopathology

What was known? Erythroderma is a reaction pattern characterized by erythema and desquamation of 90% or more body surface area along with some metabolic alterations. It mostly occurs secondary to psoriasis but can be primary also. As it is a serious disease and the treatment is mainly based on the etiology, diagnosing the cause is very important which relies mostly on histopathology.

Introduction necessary for cells to mature and travel through the epidermis is decreased. This compressed maturation Erythroderma, first described by Hebra in 1868, is process results in an overall greater loss of epidermal a reaction pattern characterized by generalized and material, which is manifested clinically as severe scaling confluent erythema with desquamation affecting more and shedding. than 90% of body surface area [Figure 1a and 1b] and Exfoliative dermatitis accounts for about 1% of all is usually accompanied by other systemic manifestations hospital admissions for dermatologic conditions.[3] Overall resulting in hemodynamic and metabolic incidence is 1 to 2 patients per 100,000 populations.[5] [1‑4] derangements. In Indian subcontinent, one large prospective study has Erythroderma is the result of a dramatic increase in the epidermal turnover rate. In patients with this disorder, the mitotic rate and the absolute number of germinative skin cells are higher than normal. Moreover, the time

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DOI: 10.4103/0019-5154.169124 a b Figure 1: (a) Erythroderma (psoriatic). (b) Erythroderma (non-specific)

549 Indian Journal of Dermatology 2015; 60(6) Banerjee, et al.: Clinicopathological correlation of erythroderma patients shown that overall incidence of erythroderma is 35 per wherever indicated. A punch biopsy was done under 100,000 dermatological patients.[6] sterile environment for histological examination. Primary erythroderma develops in normal skin and Data were analyzed using standard statistical tools. etiological factors are drug reactions, lymphomas and Patients with bleeding disorders (contraindicated for hematological malignancies or may be idiopathic (25%).[7,8] punch biopsy) and seriously ill moribund patients were On the other hand, secondary erythroderma develops excluded from the study due to non‑availability of through generalization of existing dermatoses such as informed consent. Ethical approval was taken from the eczema, psoriasis, rubra pilaris, , Institutional Ethics Committee. etc.[7] Correlation of clinical diagnosis with histological findings Since erythroderma is a serious disease due to its ability was thoroughly studied. Data were analyzed using to cause metabolic derangement, optimal therapy is very standard statistical tools. important, which again depends upon the establishment Results and Analysis of the causes.[9] Most of the erythroderma patients were in the age group Laboratory findings are typically unhelpful in of 4th and 5th decades (31.25% each, n = 10) [Table 1]. The [10] establishing etiology of erythroderma. A skin biopsy is minimum age of the patient with clinical presentation of the only relevant investigation as the histopathological erythroderma was 16 years and the maximum age was features of the underlying disorders are recognizable 69 years with a mean age of 41.81 years and median [11,12] in more than half of the cases. A comprehensive value was 42 years. The ratio between male and female clinicopathological correlation is of substantial in this study was 1.66:1. importance to render the diagnosis of the cause.[13] Psoriatic erythroderma was more common in 4th and Etiological factors depend largely on the population 5th decades of life [Table 1]. Seborrheic dermatitis as studied, though clinical presentations may essentially a cause of erythroderma was seen in the age group of [14] be the same. As no earlier published study was 3rd and 4th decade. Erythroderma due to atopic dermatitis found even after diligent search regarding frequency was seen in younger populations (before 5th decade of of underlying causes of erythroderma in North Bengal life). Idiopathic erythroderma cases seen in this study population, this study might be helpful to asses any were in the age group of 5th and 6th decades of life. variation in clinical, etiological and histopathological profiles among these patients. The majority (68.75%, n = 22) of erythroderma cases had chronic onset whereas 31.25% (n = 10) cases had acute The aims of the study were to do histopathological onset. Out of 20 erythroderma cases due to pre‑existing categorization of clinically diagnosed erythroderma dermatoses, 17 cases (85%) presented with chronic onset. patients among North Bengal population and to observe All 4 cases with drug‑induced erythroderma presented correlation between clinical and histopathological with acute onset, whereas 37.5% (3 out of 8) cases with diagnosis. idiopathic erythroderma presented with acute onset and Materials and Methods remaining 62.5% cases presented with chronic onset. Cases with more than 6 weeks of duration were considered Clinically diagnosed cases of erythroderma attending as chronic erythroderma as an operational definition. OPD and IPD of dermatology and medicine department of North Bengal Medical College for a period of Apart from erythema and scaling which was seen 1 year were evaluated by detailed history taking and in all erythroderma patients, itching was found in clinical examinations after informed consent. All the 22 (68.7%) out of 32 cases [Table 2]. Nail changes findings were recorded in case data sheet. All required were evident only in cases secondary to psoriasis, biochemical tests were performed. HIV screening was with 7 (63.6%) out of 11 cases of psoriasis presented done in all patients. Radiological tests like X‑ray, with nail changes. Eight (25%) cases presented with echocardiography and ultrasonography were performed hair changes including crusting within hair shaft

Table 1: Age wise distribution of erythroderma cases with different clinical etiologies Etiological diagnosis 10-19 years 20-29 years 30-39 years 40-49 years 50-59 years 60-69 years Total (%) Psoriasis ‑ ‑ 05 03 03 ‑ 11 (34.37) Seborrheic dermatitis ‑ 01 02 ‑ ‑ ‑ 03 (9.37) Atopic dermatitis 01 02 01 ‑ ‑ ‑ 04 (12.5) Contact dermatitis ‑ ‑ 01 ‑ 01 ‑ 02 (6.25) Drug induced ‑ ‑ 01 03 ‑ ‑ 04 (12.5) Idiopathic ‑ ‑ ‑ 04 03 01 08 (25)

Indian Journal of Dermatology 2015; 60(6) 550 Banerjee, et al.: Clinicopathological correlation of erythroderma patients

Table 2: Correlation of clinical features and etiological types Etiological types Scaling Plaque/ Itching Nail Hair Oozing Mucosal Lymph Associated papules changes changes lesion nodes systemic features Psoriasis 11 02 08 07 05 07 ‑ 01 09 Atopic dermatitis 04 02 04 ‑ ‑ 02 ‑ 01 Seborrheic dermatitis 03 01 02 ‑ 03 01 ‑ 02 02 Contact dermatitis 02 02 02 ‑ ‑ ‑ ‑ 01 ‑ Drug induced 04 01 01 ‑ ‑ ‑ 03 ‑ Idiopathic 08 03 05 ‑ ‑ 01 ‑ 03 Total 32 11 22 07 08 11 03 04 15 100% 34.3% 68.7% 21.8% 25% 34.3% 9.3% 12.5% 46.8% and alopecia, among whom five cases were psoriatic erythroderma and three cases were erythroderma secondary to seborrheic dermatitis. 34.3% of cases (11 out of 32) presented with oozing from the skin surfaces. Mucosal lesions were seen in 9.3% of cases. Four (12.5%) cases of erythroderma presented with dermopathic lymphadenopathy. Fifteen cases (46.8%) presented with systemic complications, most commonly associated with psoriasis [Table 2], while three out of eight patients of idiopathic erythroderma had systemic complications. The most common systemic complain was fever. Other than fever we also found tachycardia, pedal edema, anemia, chilly sensation and weight loss. This difference was statistically significant (P = 0.048, i.e. <0.05). Drug‑induced erythroderma cases and erythroderma due Figure 2: Photomicrograph showing psoriatic erythroderma (H and E, ×100) to contact dermatitis cases were not associated with systemic complications in our series. Histopathology was done in all 32 cases to find out the underlying etiology, but histopathological diagnoses was possible only in 19 cases out of 32 cases (59.37%) [Table 3]. Remaining 40.63% cases were diagnosed as non‑specific dermatitis. About 21.87% of total cases and 63.63% of clinically diagnosed erythrodermic psoriasis cases were histopathologically diagnosed as psoriasis [Figure 2]. 6.25% of total cases and 66.66% of clinically diagnosed erythroderma cases secondary to seborrheic dermatitis were confirmed as seborrheic dermatitis by histopathology. Subacute spongiotic dermatitis, chronic spongiotic dermatitis and lichenoid dermatitis each comprised of 9.36% of total cases. Figure 3: Photomicrograph showing subacute spongiotic dermatitis (H and E, ×400) Out of four cases clinically diagnosed as erythroderma percent of drug‑induced erythroderma cases were due to atopic dermatitis two (50%) cases were diagnosed as lichenoid dermatitis [Figure 4] and 25% cases histopathologically diagnosed as subacute spongiotic were diagnosed as non‑specific dermatitis [Figure 5]. dermatitis [Figure 3], one (25%) as chronic spongiotic dermatitis and another (25%) as non‑specific dermatitis. Among the idiopathic erythroderma cases, Out of two cases of erythroderma clinically suspected histopathological diagnosis was made as acute spongiotic due to contact dermatitis, one case (50%) was diagnosed dermatitis in one (12.5%)) case, chronic spongiotic histopathologically as subacute spongiotic dermatitis and dermatitis in another cases and non‑specific dermatitis remaining one as non‑specific dermatitis. Seventy‑five in remaining six (75%) cases.

551 Indian Journal of Dermatology 2015; 60(6) Banerjee, et al.: Clinicopathological correlation of erythroderma patients

Histologically [Table 4] acanthosis was the most common Parakeratosis and acanthosis were present in all (100%) feature found in 87.5% (28 out of 32) cases, followed histopathologically diagnosed cases of psoriatic by parakeratosis and mixed cellular infiltrates in dermis, erythroderma (n = 7). Hypo/absent granulosis and 62.5% (20 out of 32 cases) each. Hyperkeratosis was spongiotic vessels in dermis seen in 85.71% (six out seen in 53.12% (17 out of 32) cases, spongiosis in of seven) histopathologically diagnosed psoriatic 31.25% (10 out of 32 cases). erythroderma cases. Supra papillary thinning, Munro’s

Figure 4: Photomicrograph showing non-specific dermatitis (H and E, ×40) Figure 5: Photomicrograph showing lichenoid dermatitis (H andE, ×400)

Table 3: Comparison between clinical diagnosis and histopathological diagnosis Clinical diagnosis (Etiology) No. of cases (%) Histopathological Diagnosis No. of cases (%) Psoriasis 11 (34.3) Psoriasis 07 (63.63) Nonspecific dermatitis 04 (36.36) Seborrheic dermatitis 03 (9.3) Seborrheic dermatitis 02 (66.66) Chronic spongiotic dermatitis 01 (33.33) Atopic dermatitis 04 (12.5) Subacute spongiotic dermatitis 02 (50) Chronic spongiotic dermatitis 01 (25) Nonspecific dermatitis 01 (25) Contact dermatitis 02 (6.2) Subacute spongiotic dermatitis 01 (50) Nonspecific dermatitis 01 (50) Drug induced erythroderma 04 (12.5) Lichenoid interface dermatitis 03 (75) Nonspecific dermatitis 01 (25) Idiopathic erythroderma 08 (25) Acute spongiotic dermatitis 01 (12.5) Chronic spongiotic dermatitis 01 (12.5) Nonspecific dermatitis 06 (75)

Table 4: Histopathological features seen in different erythroderma cases Epidermal changes No. of cases (%) Dermal changes No. of cases (%) Hyper keratosis 17 (53.12) Edema 13 (40.62) Parakeratosis 20 (62.5) Spongiotic vessels 14 (43.75) Acanthosis 28 (87.5) Mixed infiltrate 20 (62.5) Spongiosis 10 (31.25) Eosinophil infiltrate 04 (12.5) Hypo/absent granulosis 06 (18.72) Spongiotic pustules 04 (12.5) Cellular infiltration 17 (53.12) Acantholysis 02 (6.25) Munro’s microabscess 04 (12.5) Neutrophilic crust 02 (6.25) Supra papillary thinning 04 (12.5) Broad rete ridge 01 (3.12)

Indian Journal of Dermatology 2015; 60(6) 552 Banerjee, et al.: Clinicopathological correlation of erythroderma patients microabscesses and spongiform pustules of Kogoz were patients and to observe correlation between clinical and seen in 57.14% of cases each. histopathological diagnosis. Chi square test was used to find the clinical and histological correlation. The p-value Mixed inflammatory cell infiltration was seen in was 0.968928. The result was not significant at P <0.05. all cases of non‑specific dermatitis, followed in a decreasing order by acanthosis (76.92% cases), The mean age of the patients with erythroderma was hyperkeratosis (61.53%), dermal edema (53.84%) and found to be 41.81 years in this study group, with a range parakeratosis (46.15%) [Table 5]. of minimum 16 years to maximum 69 years. The median age of the study group was 42 years which corroborates Discussion with the previous published studies.[17‑19] The male and Erythroderma can develop over pre‑existing dermatoses, female ratio in the present study was 1.66:1 and also [18‑20] as a drug reaction, as a manifestation of malignancy matches the previous studies. or systemic diseases. In a fair number of cases no In our study, apart from erythema and scaling which etiology is found.[15] There are some congenital causes of was present in all cases, the most common presenting erythroderma as well – bullous congenital ichthyosiform feature was itching (68.7%). Hair changes were seen erythroderma (autosomal dominant) and congenital in 25% of erythroderma patients and nail changes ichthyosiform erythroderma (autosomal recessive).[16] ranging from onycholysis, subungual hyperkeratosis and In daily practice diagnosis of erythroderma usually shiny nails were evident in 21.8% cases. Dermatopathic revolves around the history of pre‑existing dermatosis but lymphadenopathy was seen in 12.5% cases. Moreover, on many occasions there was no such history and then 46.8% cases had systemic complications like fever, it becomes a diagnostic challenge to find out the cause. tachycardia, pedal edema, anemia and weight loss. The clinical features of erythroderma are non‑specific Most of the patients with secondary complications were psoriatic erythroderma cases. with erythema and scaling along with pruritus are the main presenting features. So a comprehensive A majority of the presenting symptoms were clinicopathological correlation is of substantial corroborating with the findings described in studies done importance to render the diagnosis of the cause.[13] previously.[17,21] In one study by Pal et al., shiny nails and Beau’s lines were most common nail changes.[20] The present study was done for histopathological categorization of clinically diagnosed erythroderma Most of the previously published studies showed that erythroderma mostly occurs on pre‑existing dermatoses (minimum 50% to maximum 74.4%). The Table 5: Histopathological features seen in comparisons of the different etiologies of erythroderma non‑specific dermatitis in the study population (n=13) in previous studies are given in Table 6.[6,17-20,22-25] Histopathological features No. of cases (%) Drug‑induced erythroderma were seen in 5% to 29.4% Hyperkeratosis 08 (61.53) of total cases, idiopathic erythroderma cases were seen Parakeratosis 06 (46.15) in 6.5% to 29.2% of cases, and malignancies were found Acanthosis 10 (76.92) to be the underlying cause in a maximum of 12.5% Hyper granulosis 03 (23.07) cases. However, in our study we did not find any case Dermal edema 07 (53.84) of erythroderma having any underlying malignancy as Spongiotic vessels 04 (30.76) a cause. Studies by Mittal et al.[26] and Sehgal et al.[25] Mixed cellular infiltrate in dermis 13 (100) also did not found any case of malignancy‑associated

Table 6: Etiology of erythroderma (exfoliative dermatitis) cases in different previous studies Authors Cases Pre‑existing Drug Malignancies Idiopathic (No.) dermatosis (%) reaction (%) (%) (%) Sehgal and Srivastava, 1986[6] 80 52.5 24.7 0 22.5 Akhyani M, et al., 2005[17] 97 59.7 21.6 11.3 7.2 Jowker et al., 2006[18] 102 55.9 29.4 2.9 11.8 Sigurdsson, Toonstra, and Boer, 1996[19] 102 53 5 16 26 Pal and Haroon, 1998[20] 90 74.4 5.5 5.5 14.6 Bharatiya and Joshi, 1995[22] 46 67.4 21.74 4.35 6.5 Vanconcellos, Domigues and Aoki, 1995[23] 247 59.5 7.3 4 29.2 Botella Estrada R, Sanmartino and Oliver, 1994[25] 56 62.5 16 12.5 9 Mittal, Walia, and Gill, 1996[26] 50 50 28 0 22 Our study, 2014 32 62.25 12.5 0 25

553 Indian Journal of Dermatology 2015; 60(6) Banerjee, et al.: Clinicopathological correlation of erythroderma patients erythroderma. It may be a fact that the idiopathic cases erythroderma in 66.4% of cases and subacute and chronic of erythroderma diagnosed in our study might have dermatitis was the most common histopathological been diagnosed as neoplastic erythroderma if proper finding (35.18%), followed by drug reaction (16.66%) and long follow up could be instituted as cutaneous and psoriasis (14.81%). Most consistent histopathology lymphoid neoplasia may present with erythroderma was seen in drug reaction cases followed by psoriasis.[18] as a sole clinical feature so long‑term follow up with In their study of 20 erythroderma cases, Sudho et al. repeated skin biopsies is needed to establish underlying also found that 36% cases were psoriasis, 24% cases malignancy as a cause of erythroderma. were dermatitis and 8% each were erythema multiforme and pemphigus foliaceus.[27] Among the pre‑existing dermatoses, we found psoriasis as the most common (34.3%, n = 32) etiology in our Over all prognoses was good in our study with study corroborating previous studies.[17,19,20,26] In the drug‑induced cases responded very well to treatment drug‑induced group, drugs like phenytoin, sulphonamide, and we did not came across any death in our study thus dapsone and NSAIDs were responsible for causing supporting that prognosis of erythroderma is good.[17] erythroderma in our study. Interestingly we did not find However, the mortality rate is shown to be up to 64% in any case of carbamazepine‑induced erythroderma in our a study by Sehgal et al.[25] study which is in an unusual finding as per previous studies.[17,27] King et al.[14] and Sigurdsson et al.[19] Conclusion also found carbamazepine as a less common cause of In our study, secondary erythroderma (n = 24) cases drug‑induced erythroderma in their studies. Similarly, outnumbered the idiopathic cases (n = 8) with psoriasis we did not found any case of allopurinol‑induced being the most common cause of secondary erythroderma erythroderma. The cause may be less frequency of followed by drugs. Histopathological categorization was prescription of these drugs in North Bengal or less possible in 59.3% cases, and the remaining cases showed genetic susceptibility of the studied population but as non‑specific dermatitis. Most common histopathologic in our study there were only four cases of drug‑induced diagnosis was psoriasis (21.8% of cases). We recognized two erythroderma which is very less to draw any conclusion. limitations of our study. True incidence of erythroderma We found that majority (68.75%, n = 22) of in North Bengal population could not be determined as erythroderma cases had chronic onset, whereas this was a cross‑sectional study and no defined population 31.25% (n = 10) cases had acute onset. As there is no group was available. Moreover, we might have missed available standard demarcation of chronic and acute the cases of erythroderma secondary to the cutaneous onset erythroderma, we considered the cases with lymphoma group due to lack of follow‑up studies. clinical features started in preceding 6 weeks as acute What is new? onset erythroderma. All the four cases of drug‑induced No known study of erythroderma patients are there in north bengal population erythroderma had acute onset which is in accordance and this is the first attempt to study the clinocopathological correlation among them. with previous studies.[10,25] Interestingly we did not found any case of erythroderma References associated with HIV as there is increased chance of 1. Burton JL. Erythroderma: Rook, Wilkinson, Ebling Textbook of erythroderma either due to the drugs used HAART Dermatology. In: Champion RH, Burton JL, Ebling FJ, editors. th or exaggeration of certain dermatosis in HIV positive 5 ed, Vol. 1. United States: Oxford Blackwell Scientific Publications; 1992. p. 584‑8. individuals but studies by Pal et al. and Akhyani et al. 2. Nicolis GD, Helwig EB. Exfoliative dermatitis: also showed similar results. Morar et al. in their study A clinicopathologic study of 135 cases. Arch Dermatol found HIV positive in many of their cases and they 1973;108:788‑97. concluded that erythroderma can be a marker of HIV in 3. Herman LE, Kurban AK. Erythroderma as a manifestation of young black males.[28] AIDS related complex. J Am Acad Dermatol 1987;17:507‑8. 4. Shelley WB, Shelley ED. Advanced dermatologic therapy. In our study, histopathological diagnosis was most Philadelphia: WB Saunders; 1987. p. 185‑9. consistent with clinical diagnosis in drug‑induced 5. Sigurdsson V, Stegmans PH, Vloten WA van. The incidence erythroderma (75%) cases. Histopathological findings of erythroderma: A survey among all dermatologists in the were consistent in 66.66% of seborrheic dermatitis cases Netherland. J Am Acad Dermatol 2001;45:675-8. and 63.63% of psoriatic erythroderma cases. 6. Shegal VN, Srivastava G. Exfoliative Dermatitis: A prospective study of 80 patients. Dermatologica 1986;173:278‑84. The study conducted by Akhyani et al. showed that 7. Braun‑Falco O, Pleerig G, Wolf H, Winkelman RK. Dermatology. histology was helpful to correlate clinical diagnosis in Verlag: Berlin Springer; 1991. p. 444‑7. 50% of cases. They found psoriasis to be the predominant 8. Bolognia JL, Jorizzo JL, Rapini RP. Dermatology. 2nd ed. etiologic agent causing erythroderma.[17] According to Toronto (ON): Mosby Elsevior; 2008. p. 149. Jowker et al., there was clinicopathological correlation of 9. Rothemj, Bernsteil ML, Grant‑Kels JM. Life threatening

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