Tufted folliculitis of the scalp: a distinctive clinicohistological variant of folliculitis decalvans
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1 British Journal of Dermatology 1998; 138: Tufted folliculitis of the scalp: a distinctive clinicohistological variant of folliculitis decalvans G.ANNESSI Department of Dermatology and Dermatopathology, Istituto Dermopatico dell Immacolata, IRCCS, Via Monti di Creta 104, Rome, Italy Accepted for publication 16 December 1997 Summary Tufted folliculitis is an uncommon folliculitis of the scalp that resolves with patches of scarring alopecia within which multiple hair tufts emerge from dilated follicular orifices. The clinicohistological data from a group of 15 patients with tufted folliculitis were reviewed and compared with those of seven patients with folliculitis decalvans, five with acne keloidalis nuchae, four with dissecting cellulitis of the scalp, three with kerion celsi and 20 with follicular lichen planus. It was found that tufted folliculitis could be differentiated from folliculitis decalvans only by finding several hair tufts scattered within patches of scarring alopecia. Histologically, a single tuft consisted of peculiar clustering of adjacent follicular units opening at the bottom of an epidermal depression. Conversely, the presence of keloidal plaques in acne keloidalis nuchae, coalescing nodules discharging purulent material in dissecting cellulitis of the scalp, erythematous plaques covered by pustules replete with fungal elements in kerion celsi, and the absence of follicular pustules in follicular lichen planus distinguished these diseases from tufted folliculitis. On the basis of these findings, it is suggested that tufted folliculitis should be considered as a distinctive clinicohistological variant of folliculitis decalvans. Tufting of hair is caused by clustering of adjacent follicular units due to a fibrosing process and to retention of telogen hairs within the involved follicular units. Tufted folliculitis is a recurrent and progressive folliculitis of the scalp that resolves with irregular areas of scarring alopecia within which numerous hair tufts emerge from dilated follicular openings. 1 8 Histologically, it is characterized by a superficial folliculitis that involves several follicles opening into a common ostium from which multiple hairs come out. 1 8 Some pathogenetic mechanisms have been proposed to explain the development of tufted folliculitis, including naevoid abnormalities, 2,4 retention of telogen hair in the tufts 5 and an infective folliculitis leading to destruction of the upper parts of adjacent follicles that subsequently regrow with formation of a common follicular channel. 1 Some authors, however, believe hair tufting to be a secondary phenomenon that may occur in several different inflammatory disorders of the scalp, rather than a diagnostic feature of a specific disease. 9 The clinicohistological data from a group of 15 patients with tufted folliculitis were studied by us and compared with those of folliculitis decalvans of Quinquaud, acne keloidalis nuchae, dissecting cellulitis of the scalp, kerion celsi and follicular lichen planus. The purpose was to determine whether tufted folliculitis 1998 British Association of Dermatologists could be distinguished from other folliculitides of the scalp on the basis of clinical and histological features and to investigate the mechanism of tuft formation. Patients and methods Fifteen patients with tufted folliculitis were seen at the Istituto Dermopatico dell Immacolata, Rome from January 1993 to June Clinical data and 25 haematoxylin and eosin stained histological sections from 18 biopsy specimens were reviewed. In 12 patients purulent material was sampled for cultural study and, in six, some hair tufts were plucked for light microscopic examination. A clinicohistological study of seven patients with folliculitis decalvans, five with acne keloidalis nuchae, four with dissecting cellulitis of the scalp, three with kerion celsi and 20 with follicular lichen planus was also carried out for comparative purposes. In addition, histological sections of biopsy specimens taken from areas of apparent tufting of hair were examined in one case of acne keloidalis nuchae, one of dissecting cellulitis of the scalp, one of kerion celsi and two of follicular lichen planus. 799
2 800 G.ANNESSI Table 1. Clinical data of patients with tufted folliculitis of the scalp Patient no. Age/sex Location Duration Bacterial cultures Therapy Response to therapy 1 29/M Parietal 1 year S. aureus Topical erythromycin No improvement 2 25/M Parietal 2 years S. aureus Topical gentamicin No improvement 3 66/F Parietal 9 months S. aureus Topical þ oral erythromycin Transient improvement 4 37/M Parietal 3 years S. aureus Topical þ oral erythromycin Transient improvement 5 21/M Parietal 2 years S. aureus Topical erythromycin þ oral minocycline Transient improvement 6 35/M Parietal 6 months S. aureus Topical erythromycin No improvement 7 36/M Parietal 10 months S. aureus Topical erythromycin þ oral co-trimoxazole Transient improvement 8 42/M Parietal 1 year S. aureus Topical gentamicin þ oral minocycline No improvement 9 25/F Parietal 2 years Topical erythromycin þ oral minocycline Transient improvement 10 27/M Parietal 1 year S. aureus Topical erythromycin þ oral co-trimoxazole No improvement 11 29/M Occipital 4 years S. aureus Topical erythromycin þ oral co-trimoxazole Transient improvement 12 22/M Occipital 4 months S. aureus Topical þ oral erythromycin Transient improvement 13 33/M Parietal and 1 year S. aureus Topical þ oral erythromycin Transient improvement occipital 14 19/M Parietal and 2 years Topical antimycotic No improvement occipital 15 23/M Parietal and 1 year Topical erythromycin No improvement occipital S. aureus, Staphylococcus aureus. Results Clinical findings The clinical data from 15 patients with tufted folliculitis are summarized in Table 1. This series comprised 13 men and two women who ranged in age from 19 to 66 years (average age 31 3 years). Two patients (numbers 14 and 15) were siblings and in one (number 3) the disease developed at the site of previous trauma. The lesions were situated on the parietal (10 patients), occipital (two patients) and both occipital and parietal regions (three patients) of the scalp. Early lesions consisted of small areas of perifollicular erythema and follicular pustules that slowly extended centrifugally leaving central zones of scarring alopecia. Fully developed lesions were characterized by one or more patches of scarring alopecia measuring 2 5 cm in diameter with ill-defined and jagged borders. Several hair tufts were randomly arranged within these patches. Each tuft comprised eight to 14 hairs that emerged from an apparently common and dilated follicular opening. In most cases, this peculiar grouping of hair gave the scalp a dolly hair appearance (Fig. 1). Collarettes of yellowgrey scales encircled some follicular orifices and, at times, pressure on the perifollicular areas produced the discharge of purulent material through the dilated follicular openings. Careful examination of the scalp did not reveal any developmental anomaly of the hair, such as pili multigemini or trichostasis spinulosa. In all patients, the disease ran a chronic and relapsing course with progressive development of new areas of tender erythema and follicular pustules leading to scarring and formation of additional hair tufts. Purulent material or exudate from dilated follicular infundibula was sampled in 10 patients. Staphylococcus aureus was isolated in all cases, whereas fungal cultures were negative. Five patients were treated with topical antiseptics, antibiotics (erythromycin and gentamicin) and antimycotics over a period of 3 5 months. Despite a slight reduction of the inflammatory changes, the disease continued to progress. In other 10 patients, treatment with topical and oral antibiotics including Figure 1. Several hair tufts are present within patches of scarring alopecia giving the scalp a dolly hair appearance.
3 TUFTED FOLLICULITIS OF THE SCALP 801 Table 2. Clinical data from patients with folliculitis decalvans, acne keloidalis nuchae, dissecting cellulitis of the scalp, kerion celsi and follicular lichen planus Patients Age range Hair tufts n ¼ (years) Sex Site of involvement Types of lesion n ¼ Folliculitis decalvans M (6), F (1) Occipital, parietal regions Scarring alopecia, follicular pustules Acne keloidalis nuchae M (5) Occipital region Keloidal plaques, pustules 1 Dissecting cellulitis of the scalp M (4) Occipital, parietal regions Purulent coalescing nodules 1 Follicular lichen planus M (8), F (12) Occipital, parietal, frontal regions Scarring alopecia, 2 follicular horny plugs Kerion celsi M (3) Parietal region Plaques, pustules, alopecia 1 erythromycin (four patients), minocycline (three patients) and co-trimoxazole (three patients) was started. In two cases, no response was obtained, while eight patients noted an improvement of the lesions. In these, however, relapses were observed within few weeks after treatment interruption. The seven patients with folliculitis decalvans had round or irregular shaped patches of scarring alopecia with small follicular pustules at the advancing edge of the lesions. The patches of alopecia were mostly located on the parietal and occipital regions of the scalp (Table 2). No hair tufts were seen within the lesional areas. Acne keloidalis nuchae consisted of several follicular pustules surrounded by keloidal papules and plaques on the occipital region. The four cases of dissecting cellulitis of the scalp were characterized by groups of deep-seated, partially alopecic, coalescing nodules often discharging purulent material from interconnecting sinuses and abscesses. Patients with kerion celsi displayed painful, boggy plaques covered by pustules and thick crusts of scale with decreased follicular density and broken hair shafts. Conversely, the vast majority of patients with follicular lichen planus showed irregular patches of cicatricial alopecia accompanied by perifollicular erythema and follicular keratotic papules. Occasional tufts of three to five unaffected hairs were seen within scarring areas in one patient with acne keloidalis nuchae, one with dissecting cellulitis of the scalp, one with kerion celsi and two with follicular lichen planus. Histological findings Five biopsy specimens taken from the erythematous and pustular borders of tufted folliculitis showed a superficial folliculitis that involved either single follicles or groups of two to four follicles whose infundibula merged into a common ostium. A dense infiltrate of neutrophils and lymphocytes was seen around and within follicular infundibula while the lower follicular segments were spared by the pathological changes. Neutrophilic pustules and scale-crusts were present at the top of some follicular orifices. An infiltrate of lymphocytes and plasma cells surrounded the vessels of the superficial and mid-dermis. Two biopsies from scarring areas disclosed several fibrotic tracts at the sites of extinct follicles, focal aggregates of histiocytes and foreignbody giant cells containing small hair fragments and a scarring process involving the superficial and middermis. Eleven biopsy specimens included one or more hair tufts. Every tuft consisted of a peculiar cluster of two to four groups of inflamed follicles. Each group, in turn, was composed of two to three follicles that opened into a common ostium from which multiple hairs were seen to emerge. A superficial perifollicular and interfollicular fibrosing process trapped the involved follicular groups causing clustering and also a depression of the interfollicular epidermis (Figs 2 and 3). In six patients, some hair tufts were plucked for light microscopic examination. The number of hairs from each tuft ranged from eight to 14. In all cases, more than one-third of the hairs were found from their club roots and absence of the outer root sheaths to be in the telogen phase of the hair cycle. The remaining showed the features of anagen or dystrophic anagen hair. Pustules of folliculitis decalvans displayed large aggregates of neutrophils within the infundibulum of single follicles or groups of two to three follicles opening into a common ostium. Older lesions showed follicular remnants within scarred areas surrounded by an infiltrate of lymphocytes, neutrophils, histiocytes and numerous plasma cells. Acne keloidalis nuchae consisted of focal aggregates of lymphocytes, neutrophils, histiocytes, many plasma cells and hair fragments trapped into large keloidal areas in the reticular dermis.
4 802 G.ANNESSI Figure 2. A hair tuft is the result of clustering of several adjacent follicular units that open at the base of an epidermal dell due to a superficial scarring process (haematoxylin and eosin; original magnification 20). Nodular lesions of dissecting cellulitis of the scalp were mainly characterized by dermal and subcutaneous neutrophilic abscesses with the disruption of follicles and other cutaneous appendages. Occasionally, the abscesses were partially outlined with squamous epithelium derived from epidermis or the adjacent follicular epithelium. Extensive dermal fibrosis was seen in areas of healing. Plaques of kerion celsi disclosed follicular hyperkeratosis, dense, nodular aggregates of neutrophils around and within the upper and lower segments of adjacent follicles, and marked dermal fibroplasia. Numerous fungal elements were detected around and within most hair shafts. Early lesions of follicular lichen planus exhibited follicular hyperkeratosis, vacuolar changes and necrotic keratinocytes at the junction between follicular epithelium and dermis, and a lichenoid lymphohistiocytic infiltrate around the upper part of several adjacent follicles. Older lesions displayed Figure 3. Superficial interfollicular and perifollicular fibrosis traps adjacent follicular units (haematoxylin and eosin; original magnification 80).
5 TUFTED FOLLICULITIS OF THE SCALP 803 Figure 4. A hair tuft from follicular lichen planus consists of one follicular unit whose follicles are surrounded by perifollicular fibrosis and a scant inflammatory infiltrate (haematoxylin and eosin; original magnification 20). perifollicular fibrosis, fibrotic tracts at the sites of extinct follicles and a scant perivascular lymphocytic infiltrate in the adventitial dermis. Histological examination of the hair tufts taken from acne keloidalis nuchae, dissecting cellulitis of the scalp, kerion celsi and follicular lichen planus showed similar findings. Each tuft, in fact, consisted of three to five follicles opening into a common ostium surrounded by perifollicular fibrosis, extensive cicatricial or keloidal areas in the reticular dermis and a perifollicular mixed cell infiltrate of lymphocytes and histiocytes with a variable amount of neutrophils and plasma cells (Fig. 4). Discussion Tufted folliculitis is an inflammatory disorder of the scalp characterized by a peculiar tufting of hair within areas of scarring alopecia. The differential diagnosis mainly includes folliculitis decalvans, acne keloidalis nuchae, dissecting cellulitis of the scalp, kerion celsi and follicular lichen planus. On the basis of this clinicohistological study, the presence of keloidal papules and/or plaques in acne keloidalis nuchae and of fluctuant, coalescing nodules composed of dermal and subcutaneous neutrophilic abscesses in dissecting cellulitis of the scalp, easily distinguishes these diseases from tufted folliculitis. Kerion celsi, unlike tufted folliculitis, consists of erythematous plaques studded with pustules that are characterized histologically by dense neutrophilic infiltrates around and within follicles that house fungal elements. Follicular lichen planus does not show follicular pustules and is constituted by perifollicular lichenoid infiltrates of lymphocytes. In contrast, the findings in this study illustrate that tufted folliculitis shares several clinical, histological and microbiological features with the type of folliculitis decalvans described by Quinquaud in Both the conditions mainly occur in young adult men and involve mostly the parietal and occipital regions of the scalp. 1 8,10,11 Clinically, tufted folliculitis and folliculitis decalvans begin with areas of perifollicular erythema and small follicular pustules that spread peripherally leaving central patches of scarring alopecia. Recurrent exacerbations over a period of months to years result in the development of new lesions or in slow but progressive enlargement of previous alopecic patches. 1 8,10,11 In our patients, histological examination of tufted folliculitis and folliculitis decalvans pustules showed a superficial neutrophilic folliculitis that involved either single follicles or groups of follicles opening into a common ostium. Dense infiltrates of neutrophils and plasma cells were seen around the vessels of the superficial and middermis. Furthermore, S. aureus has been cultured from most lesions of folliculitis decalvans and of tufted folliculitis 1 8,10,11 (i.e. 12 in this series). Lastly, both the conditions follow a chronic and relapsing course that is scarcely responsive to topical and systemic antibiotic treatment. In this study, a combined therapy with topical and oral antibiotics produced an improvement in eight patients with tufted folliculitis. The disease, however, rapidly worsened after discontinuation of the treatment. On the whole, these findings suggest that tufted folliculitis should be regarded as a peculiar form of folliculitis
6 804 G.ANNESSI Figure 5. (A) Hair follicles on the human scalp are normally arranged in follicular units. (B) A superficial folliculitis involves adjacent follicular units. (C) Fibrous tissue contraction causes an epidermal depression and clustering of the inflamed follicular units. A hair tuft results from the grouping of the hairs that come out from the follicular units opening at the base of the epidermal dell. decalvans characterized by multiple hair tufts scattered within the patches of scarring alopecia that give the scalp a typical dolly hair appearance. Usually, each tuft consists of five to 20 hairs 4,6 8 that seem to emerge from a widely dilated follicular opening. With subsequent relapses, new tufts appear at the periphery of the lesions while others disappear in the centre because of progressive scarring. In 1984, Headington demonstrated that hair follicles on the human scalp are mostly arranged in small groups that he termed follicular units. 12 Each follicular unit consists of two to four terminal follicles and one or two vellus follicles whose infundibula merge into a common ostium from which several hairs come out. Therefore, on the normal scalp, most hair emerges in small clusters from single follicular orifices. On the basis of the histological findings in this study, it is suggested that the first event in the development of tufted folliculitis is a superficial suppurative folliculitis that involves several adjacent follicular groups (follicular units) accompanied with marked perifollicular and interfollicular fibroplasia. In time, fibrous tissue contraction may cause a depression of the interfollicular epidermis and clustering of the involved follicular units. Thus, a hair tuft results from the grouping of several hairs that emerge from the clustered follicular units opening at the bottom of an epidermal dell (Fig. 5). As the disease progresses, the hair tufts are gradually destroyed by the inflammatory process whereas others may form at the periphery of the lesions. In six patients, plucked hair analysis demonstrated the presence of a high proportion of telogen hairs in each tuft. This unusual finding suggests that local inflammatory processes around follicular units may result in protracted retention of telogen hairs. This mechanism could further contribute to enhance the number of hairs in each tuft. Some authors have reported the occasional presence of hair tufts in acne keloidalis nuchae and dissecting cellulitis of the scalp suggesting that hair tufting may occur in several exudative inflammatory diseases of the scalp and should be considered as a secondary phenomenon rather than a diagnostic feature of a specific disease. 9 This hypothesis, however, has not been supported by histological confirmation. It was found that every tuft obtained from lesions of acne keloidalis nuchae, dissecting cellulitis of the scalp, kerion celsi and follicular lichen planus consisted histologically of one follicular unit trapped in a cicatricial area instead of a cluster of some adjacent follicular units opening at the bottom of an epidermal dell, as seen in tufted folliculitis. This indicates that the mechanism of tuft formation in tufted folliculitis is different from that detected in acne keloidalis nuchae, dissecting cellulitis of the scalp, kerion celsi and follicular lichen planus. In conclusion, the findings suggest that tufted folliculitis should be considered as a distinctive clinicohistological variant of folliculitis decalvans characterized by multiple hair tufts within patches of scarring alopecia. The mechanism of tuft formation is peculiar and consists of clustering of several adjacent follicular units caused by a fibrosing process and retention of telogen hairs within the involved follicular units. Acknowledgments I am grateful to MariaPia Accetturi, Biagio Didona, Cesare Secci, Claudia Di Pietro, Giuseppe Aleo, Anna- Maria Bucci and Luciana Martini for their assistance in the preparation of this manuscript.
7 TUFTED FOLLICULITIS OF THE SCALP 805 References 1 Smith NP, Sanderson KV. Tufted folliculitis of the scalp. J R Soc Med 1978; 71: Metz J, Metz G. Navoide Bundelhaare beim Menschen. Hautarzt 1878; 29: Oakley A, Scollay D. Hair bundles: a presentation of folliculitis. Australas J Dermatol 1985; 26: Tong AKF, Baden HP. Tufted hair folliculitis. J Am Acad Dermatol 1989; 21: Dalziel KL, Telfer NR, Wilson CL, Dawber RPR. Tufted folliculitis. A specific bacterial disease? Am J Dermatopathol 1990; 12: Pujol RM, Matias-Guiu X, Garcia-Patos V, De Moragas JM. Tufted hair folliculitis. Clin Exp Dermatol 1991; 16: Luelmo-Aguilar J, Gonzales-Castro U, Castells-Rodellas A. Tufted hair folliculitis. A study of four cases. Br J Dermatol 1993; 128: Secchi T, Balme B, Thomas P et al. Folliculites en touffes du cuir chevelu. Ann Dermatol Venereol 1994; 121: Pujol RM, Garcia-Patos V, Ravella-Mateu A et al. Tufted hair folliculitis. A specific disease? Br J Dermatol 1994; 130: Quinquaud E. Folliculite epilante et destructive des regions velues. Bull Mem Soc Med Hop Paris 1888; 5: Bogg A. Folliculitis decalvans. Acta Derm Venereol (Stockh) 1963; 43: Headington JT. Transverse microscopic anatomy of the human scalp. Arch Dermatol 1984; 120:
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