BACKGROUND: Scarring alopecias are classified into primary and secondary types according to the initial site of inflammation. In primary scarring alopecias, the hair follicle is the main target of destruction; the term secondary cicatricial alopecia implies that follicular destruction is not the primary pathologic event. AIMS: To review the histopathologic diagnoses of cases of cicatricial alopecia in order to classify them according to the North American Hair Research Society. PATIENTS AND METHODS: Patients with biopsy specimens diagnosed as cicatricial alopecia seen from 2000 to 2005 at the Dermatologic Department of Hospital das Clinicas, São Paulo University Medical School had hematoxylin and eosin, Periodic acid-Schiff and Weigert stained slides reevaluated and sub-typed into different primary cicatricial alopecias. RESULTS: Thirty-eight cases of primary cicatricial alopecias were reclassified as: chronic cutaneous lupus (17), lichen planus pilaris (4), pseudopelade of Brocq (12), folliculitis decalvans (3), dissecting folliculitis (1), and non-specific scarring alopecia (1). In our cases, the methods employed allowed an accurate diagnosis in 12 of 13 cases (92.3%) previously classified as non-specific cicatricial alopecias. CONCLUSIONS: Even in the late, pauci or non-inflammatory phases, an approach with systematic evaluation of a constellation of criteria in routine hematoxylin and eosin stain, Periodic acid-Schiff and Weigert stain allowed for a more accurate diagnosis of cicatricial alopecias

Machado, Maria Cecília da Matta Rivitti

Moure, Emanuella Rosyane Duarte

Romiti, Ricardo

Valente, Neusa Yuriko Sakai

English

PubMed

MOURE, Emanuella Rosyane Duarte

ROMITI, Ricardo

MACHADO, Maria Cecília da Matta Rivitti

VALENTE, Neusa Yuriko Sakai

RCAAP - Repositório Científico de Acesso Aberto de Portugal

Primary cicatricial alopecias: a review of histopathologic findings in 38 patients from a clinical University Hospital in Sao Paulo, Brazil

Universidade de São Paulo

Clinics

Emanuella Rosyane Duarte Moure

Ricardo Romiti

Maria Cecília da Matta Rivitti Machado

Neusa Yuriko Sakai Valente

Directory of Open Access Journals

Crossref

Biblioteca Digital da Produção Intelectual da Universidade de São Paulo (BDPI/USP)

747
CLINICS 2008;63(6):747-52
CLINICAL SCIENCE
Department of Dermatology, Hospital das Clínicas, Faculdade de Medicina, 
Universidade de São Paulo - São Paulo/SP, Brazil.
Email: emanuellamoure@gmail.com
Tel.: 55 11 3564.0112
Received for publication on July 4, 2008
Accepted for publication August 20, 2008
PrImAry CICAtrICIAL ALoPECIAS: A rEvIEw of 
hIStoPAthoLogIC fINdINgS IN 38 PAtIENtS from 
A CLINICAL UNIvErSIty hoSPItAL IN SAo PAULo, 
BrAzIL 
Emanuella Rosyane Duarte Moure, Ricardo Romiti, Maria Cecília da Matta 
Rivitti Machado and Neusa Yuriko Sakai Valente  
 
doi: 10.1590/S1807-59322008000600007
Moure ERD, Romiti R, Machado MCMR, Valente NYS. Primary cicatricial alopecias: a review of histopathologic findings 
in 38 patients from a clinical university hospital in São Paulo, Brazil. Clinics. 2008;63:747-52.
BACKGROUND: Scarring alopecias are classified into primary and secondary types according to the initial site of inflammation. 
In primary scarring alopecias, the hair follicle is the main target of destruction; the term secondary cicatricial alopecia implies that 
follicular destruction is not the primary pathologic event. 
AIMS: To review the histopathologic diagnoses of cases of cicatricial alopecia in order to classify them according to the North 
American Hair Research Society.
PATIENTS AND METHODS: Patients with biopsy specimens diagnosed as cicatricial alopecia seen from 2000 to 2005 at the 
Dermatologic Department of Hospital das Clinicas, São Paulo University Medical School had hematoxylin and eosin, Periodic 
acid-Schiff and Weigert stained slides reevaluated and sub-typed into different primary cicatricial alopecias. 
RESULTS: Thirty-eight cases of primary cicatricial alopecias were reclassified as: chronic cutaneous lupus (17), lichen planus 
pilaris (4), pseudopelade of Brocq (12), folliculitis decalvans (3), dissecting folliculitis (1), and non-specific scarring alopecia (1). 
In our cases, the methods employed allowed an accurate diagnosis in 12 of 13 cases (92.3%) previously classified as non-specific 
cicatricial alopecias.
CONCLUSIONS: Even in the late, pauci or non-inflammatory phases, an approach with systematic evaluation of a constellation 
of criteria in routine hematoxylin and eosin stain, Periodic acid-Schiff and Weigert stain allowed for a more accurate diagnosis of 
cicatricial alopecias.
KEYWORDS: Cutaneous lupus erythematosus; Lichen planus pilaris; Pseudopelade of Brocq; Folliculitis decalvans; Dissecting 
folliculitis.
INTRODUCTION
Alopecias can be broadly classified into non-scarring 
or non-cicatricial and scarring or cicatricial forms. 
Pathologically, a scar constitutes the end point of reparative 
fibrosis with permanent destruction of the preexisting 
tissue.1 
Scarring alopecias are further subdivided into primary 
and secondary types. In primary scarring alopecias, the 
hair follicle is the primary target of destruction, which is 
microscopically evident as “preferential destruction of 
follicular epithelium and/or its associated advential dermis 
with relative sparing of the reticular dermis.2” This group 
includes the following clinical entities: chronic cutaneous 
lupus erythematosus (CCLE), lichen planopilaris (LPP), 
pseudopelade of Brocq (PB), folliculitis decalvans (FD), 
dissecting cellulitis/folliculitis (DF). If the follicular 
destruction is secondary to the scarring and occurs outside 
the follicular unit, e.g., the reticular dermis, epidermis, or sub 
cutis, it can eventually impinge upon and even eradicate the 
whole follicle. The term secondary scarring alopecia implies 
that follicular destruction is not the primary pathologic 
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CLINICS 2008;63(6):747-52Primary cicatricial alopecias: a review of histopathologic findings in 38 patients
Moure ERD et al.
event. Exogenous factors, such as burns, and endogenous 
infiltrative and inflammatory diseases, such as sarcoidosis, 
pemphigus vulgaris and reticular dermal sclerosis, can result 
in secondary alopecias.
In 2001, a group of hair clinicians, pathologists and 
researchers, under the rubric of the North American Hair 
Research Society (NAHRS),3 issued a consensus opinion on 
the classification of primary cicatricial alopecias. The proposed 
classification subdivides primary scarring alopecias on the 
basis of the predominant type of inflammatory cell component, 
an approach that had already published1,4,5-7 and was further 
refined by the workshop. In addition to the lymphocyte- and 
neutrophil-associated subgroups, a mixed and nonspecific group 
was differentiated and newly defined (Table 1). 
In the late phase of cicatricial alopecias, a histopathologic 
diagnosis is more difficult because the main criteria of 
classification, i.e., the type of inflammatory infiltrate, cannot 
always be evaluated. In these cases, additional criteria, such 
as the evaluation of the perifollicular elastic sheet and the 
fibrosis, can be useful.
The goal of this study was to review clinical and 
histopathologic findings of 38 patients diagnosed with late, 
pauci or non-inflammatory phase of cicatricial alopecias at 
the Dermatologic Department of the Hospital das Clinicas, 
São Paulo University Medical School, over a six-year period 
in order to classify them by sub-types according to NAHRS 
and evaluate the dermal elastic system and thickness of the 
epidermal basement membrane, using Weigert and PAS 
stains, respectively.
PATIENTS AND METHODS 
Biopsy specimens obtained using 5-mm punches from 
patients seen between 2000 and 2005 at the Dermatologic 
Department of Hospital das Clinicas, São Paulo University 
Medical School with cicatricial alopecias in the late, pauci or 
non-inflammatory phase were reevaluted. Essential criteria 
included histopathologic diagnosis of cicatricial alopecia and 
accessibility of the patient’s clinical records. Slides stained 
with hematoxylin and eosin, PAS and stain for elastic tissues 
(Weigert with previous oxidation by peracetic acid) were 
reviewed, evaluating the presence or absence of criteria listed 
in the Table 2. This table shows the histopathologic criteria 
for different causes of cicatricial alopecia. 
RESULTS
A total of 38 cases with a histopathologic diagnosis of 
cicatricial alopecia were included in the study. These cases 
had been previously diagnosed as follows: eight cases of 
CCLE, two cases of LPP, 13 cases of PB, two cases of 
FD, one case of scleroderma and 13 cases of non-specific 
cicatricial alopecia.
The cases were reclassified into primary or secondary 
alopecias. The ratio of primary versus secondary alopecias 
was 37:1. One case was classified as non-specific alopecia. 
Twelve of 13 cases (92.3%) that were initially classified 
as non-specific cicatricial alopecias could be specifically 
reclassified.
Chronic cutaneous lupus erythematosus was diagnosed 
in 17 cases, representing 43.6% of the total number of 
scarring alopecias. The female to male ratio was 4.7: 1 (14 
females and three males). The age at onset ranged from 29 
to 75 years, with a mean age of 46.5 years. Characteristic 
histopathologic findings of the late phase included 
hyperkeratosis, horn plugs, atrophy of the Malpighian layer, 
slight vacuolar degeneration of the basal layer, and fibrous 
tract replacing the follicles. A thickened basal membrane 
could be seen in 58.8% of the cases on PAS –stained 
sections, and an incomplete elastic sheet occurred around 
the fibrous tracts. in all cases on Weigert- stained sections. 
Elastolytic foci were also found in areas of fibrosis outside 
the perifollicular zone (Figure 1d-f). 
Table1 - Primary Scarring (Permanent) Alopecias (ac-
cording to the Proposed Working Classification of Primary 
Cicatricial Alopecia by the North American Hair Research 
Society; 1999)3
Lymphocyte-associated primary scarring alopecias
Chronic cutaneous lupus erythematosus
Lichen planopilaris
Classic lichen planopilaris
Frontal fibrosing alopecia
Graham Little syndrome
Classic pseudopelade (Brocq)
Central centrifugal cicatricial alopecia
Alopecia mucinosa
Keratosis follicularis spinulosa decalvans
Neutrophil-associated primary scarring alopecias
Folliculitis decalvans
Dissecting cellulitis/folliculitis (perifolliculitis abscedens et suf-
fodiens)
Mixed inflammatory primary scarring alopecias
Folliculitis (acne) keloidalis
Folliculitis (acne) necrotica
Erosive pustular dermatosis
Nonspecific primary scarring alopecias*
* Non-specific scarring primary alopecia is defined as an idiopathic scarring 
alopecia with inconclusive clinical and histopathologic findings and may 
include the end stage of a variety of inflammatory primary scarring alopecias, 
such as lichen planopilaris and folliculitis decalvans. 
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CLINICS 2008;63(6):747-52 Primary cicatricial alopecias: a review of histopathologic findings in 38 patients
Moure ERD et al.
Table 2 - Histopathologic characteristics of primary scarring alopecias
@
 LPP * CCLE # PB  $ FD ## DF
Hyperqueratosis extrafollicular – + – +/- +/-
Horn plug  + + – +/- +/-
Epidermal atrophy – + – +/- +/-
Vacuolar degeneration of epidermal basal cells – + – +/- +/-
Neutrophilic folliculitis – – – + +
Lichenoid Perifolliculitis + + – – –
Dermal lymphocytic periecrine infiltrate – + – – –
Fibrous tract replacing follicle + colloid bodies 
within
+ + + +
Extrafollicular extensive dermo-hipodermal fibrosis – +/- – + dermal + dermo-
hipodermal
Sinus tract – – – – +
Preserved perifollicular elastic sheet – – + – –
Thickened basement membrane (epidermal or follicular) – + – – –
@ Lichen Planus Pilaris (LPP); * Chronic Cutaneous Lupus (CCLE); # Pseudopelade of Brocq (PB); $ Folliculitis decalvans (FD); ## Dissecting folliculitis (DF)
Figure 1 - Cicatricial alopecias of the lymphocytic group in the late phase: Pseudopelade of Brocq : (a) – cicatricial alopecia, HE, OM: x 40 (b) – absence 
of criteria for lupus erithematosus and for lichen planus, HE, OM: x 100 (c) – perifollicular elastic sheet well preserved Weigert, OM: x 100; – lupus er-
ithematosus: (d) – cicatricial alopecia with dermal collagen sclerosis, HE, OM: x 40 (e) – hyperkeratosis with horn plugs and epidermal atrophy, HE, OM: 
x 100 (f) – even in this late, non-inflammatory phase, thickening of the basement membrane, PAS, OM: x 200; lichen planus: (g) – besides fibrous tracts, 
a lichenoid perifolliculis and no other epidermal or dermal alterations, HE, OM: x 40; (h) – numerous colloid bodies within the fibrous tract that succeded 
the lichenoid perifolliculitis, PAS, OM: x 400; (i) – perifollicular elastic sheet partially destroyed, Weigert, OM: x 100. Original magnification: OM
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CLINICS 2008;63(6):747-52Primary cicatricial alopecias: a review of histopathologic findings in 38 patients
Moure ERD et al.
Lichen planus pilaris: This category of cicatricial 
alopecia represented 10.2% of the total number of biopsies, 
totaling four cases. The genders were equally represented. 
The ages at onset were 21, 25, 28 and 48 years. In one case, 
there was a lichenoid infiltrate around the infundibuloisthmic 
segment of one follicle in addition to fibrous tracts replacing 
follicles. In all the others, absence of inflammation, absence 
of sebaceous epithelium, and atrophy of the bulge area 
occurred, resulting in hourglass figures. Fibrous tracts 
replacing the follicle, with or without the presence of colloid 
bodies, were also observed. The basal membrane was not 
thickened on PAS-stained sections, and the perifollicular 
elastic sheet was partially destroyed, as observed with the 
Weigert stain (Figure 1g-i).
Pseudopelade of Brocq was diagnosed in 12 cases, 
representing 30.8% of the total number of biopsies. The 
female to male ratio was 10:2. Age of onset ranged from 23 
to 69 years, with a mean age of 54.4 years. Characteristic 
histopathologic findings were the absence of criteria seen in 
CCLE and LPP and preservation of the elastic sheet around 
the follicles (Figure 1a-c).
Folliculitis decalvans was diagnosed in three cases, 
representing 7.7% of the total number of biopsies. The 
female to male ratio was 1:2. The age of onset was 17, 29 
and 36 years. 
The histopathologic hallmark was the presence of 
superficial suppurative folliculitis and fibrosis replacing the 
follicle and the perifollicular area, with elastolysis visible 
with the Weigert stain (Figure 2a-c).
Dissecting folliculitis: This category of cicatricial 
alopecia represented 2.6% of the total number of cicatrizing 
biopsies, totaling one case in a female 19 year-old patient. 
In this case, the inflammation was slight, and there was 
an extensive and deeper dermal fibrosis extending to the 
hypodermis, with elastolysis (Figure 2d-f).
Idiopathic alopecias: One case of non-specific alopecia 
was diagnosed due to the destruction of the follicles being 
the only histopathologic finding. No additional criteria 
pointed to a more specific diagnosis.
DISCUSSION
Considering the group of primary lymphocytic cicatricial 
alopecias in the inflammatory phase, a differential diagnostic 
Figure 2 - Cicatricial alopecias of the neutrophic group in the late phase. Folliculitis decalvans; (a) – neutrophic folliculitis with intense perifolliculitis, HE 
OM: x 100; (b) – degenerated neutrophils inside the infundibulum and mixed perifollicular inflammatory infiltrate, HE OM: x 400;(c) – some perifollicular 
multinucleated histiocytes and plasma cells; Dissecting foliculitis, HE OM: x 400; (d) – perifolliculitis and extensive and deeper perifollicular cicatricial 
fibrosis than in folliculitis decalvans, HE OM: x 40; (e) – perifollicular mixed inflammatory infiltrate, HE OM: x 400; (f) – Extensive elastolysis near and 
outside the follicle, Weigert OM: x 100. Original magnification: OM
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CLINICS 2008;63(6):747-52 Primary cicatricial alopecias: a review of histopathologic findings in 38 patients
Moure ERD et al.
consideration for CCLE is LPP. However, the interface 
alteration is primarily vacuolar rather than lichenoid in 
CCLE. The superficial and deep perivascular and periecrine 
patterns of inflammation further aid in differentiating CCLE 
from LPP. In the late pauci or non-inflammatory phase, as 
observed in our cases of CCLE, interfollicular epidermis 
alterations were evident (hyperkeratosis and atrophy), in 
an area usually spared in LPP cases. Commonly, in the 
dermis in LPP, the only disturbance was the fibrous tract 
replacing the follicle, while in CCLE, there was frequent 
extra follicular fibrosis and elastolysis; even in this late 
phase, the basement membrane was thickened in 58.8% 
of cases. CCLE is differentiated from PB by the presence 
of predominately vacuolar interface changes at the level of 
follicular infundibulum in the former and lack of interface 
alterations in the latter.1 In our cases, the perifollicular elastic 
sheet was preserved in PB cases, while it was partially 
destroyed in LPP and CCLE, confirming the previous 
findings of Pinkus et al.7
Some authors believe that PB is not a distinct clinical-
pathologic entity but a variant of certain primary cicatricial 
alopecias or, alternatively, a form of end-stage alopecia 
caused by other scarring alopecias, such as CCLE, LPP and 
FD.7-9 
According to Stephen (1993)1 and other authors, with 
whom we agree, PB does indeed have sufficient distinct 
pathologic features to merit a separate classification.5,10-12 
Klaus and Wilma (2006)1 believe that the close 
clinicopathlogic correlation in the histologic absence of 
significant follicular plugging, as well as the use of elastic 
fiber stain in addition to evaluation of conventional HE-
stained sections, should enable the differentiation of classic 
PB from late stage lesions of LPP and CCLE in most cases 
and further justify the classification of the condition as an 
entity sui generis. 
In relation to the neutrophilic cicatricial alopecias, it is 
remarkable that even in the late phases of this disorder, it 
seems that the inflammatory process persists in our cases,, 
and a neutrophilic folliculitis can frequently be seen, which 
helps make the correct histopathologic diagnosis. We could 
also see that the fibrotic process that is secondary to this 
neutrophilic folliculitis was more intense and proceeded by a 
granulation tissue, as is expected after a suppurative process. 
This fibrosis is deeper in DF than in FD. Sinus tracts are the 
histopathologic hallmark of dissecting cellulites and are not 
seen in either folliculitis decalvans or acne keloidalis and 
were not observed in our late phase cases. Bacterial or fungal 
folliculitis (kerion and favus) may have to be excluded in 
the group of neutrophilic cicatricial alopecias, with the use 
of special stains. Acne keloidalis cases were not seen in our 
series because they are histopathologically reported in our 
laboratory as a superficial and deep suppurative and giant 
cellular granulomatous folliculitis with extensive fibrosis 
compatible with acne keloidalis, not as a cicatricial alopecia. 
Besides, the clinical aspect of this disorder is so typical that 
histopathologic exam is seldom required.
CONCLUSION
A scalp biopsy is mandatory in all cases of cicatricial 
alopecias, representing the clinically inflammatory area. If 
there is no evidence of inflammation, a biopsy at the border 
of the cicatricial zone should be performed. Multiple biopsies 
are sometimes required to achieve a definitive diagnosis. A 
precise diagnosis is possible, even in the late, pauci or non-
inflammatory phase of cicatricial alopecias if a systematic 
evaluation of a constellation of criteria is employed, using 
routine HE, PAS and a stain for elastic tissue. In our cases, this 
method allowed a precise diagnosis in 97.4% of cases, even in 
those initially considered non-specific cicatricial alopecia. 
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3. Olsen EA, Bergfeld WF, Cotsarelis G, Price VH, Shapiro J, Sinclair R, 
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Arch Dermatol

Cicatricial alopecia: clinico-pathological findings and treatment. Clin Dermatol. 2001;19:211-25.752 CLINICS 2008;63(6):747-52 Primary cicatricial alopecias: a review of histopathologic findings

Differential patterns of elastic fibers in scarring and nonscarring alopecias.

Histopathologic Evaluation of Alopecias.

Massive lymphocyte-mediated apoptosis during the early stage of pseudopelade.

Pseudopelade of Brocq secondary to lichen planus.

Scarring alopecia: a classification based on microscopic criteria.

The follicular degeneration syndrome in black patients: “hot comb alopecia” revisited and revised. Arch Dermatol

The transversely sectioned scalp biopsy specimen: the technique and an algorithm for its use in the diagnosis of alopecia.

Vernarbende Alopezien: Diagnostik und Therapie. Schweiz Rundsch Med Prax.

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Primary Cicatricial Alopecias: A Review of Histopathologic Findings in 38 Patients from a Clinical University Hospital in Sao Paulo, Brazil

Primary Cicatricial Alopecias: A Review of Histopathologic Findings in 38 Patients from a Clinical University Hospital in Sao Paulo, Brazil

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