Case Report

Dermatology 2007;214:177–182 Received: December 15, 2005

Accepted: September 4, 2006
DOI: 10.1159/000098580

Poikiloderma of Civatte:
A Histopathological and Ultrastructural Study
A.C. Katoulis a N.G. Stavrianeas a J.G. Panayiotides b E. Bozi a E. Vamvasakis a
D. Kalogeromitros a S. Georgala c
a
2nd Department of Dermatology and Venereology and b 2nd Department of Pathology, Attikon University
General Hospital, and c 1st Department of Dermatology and Venereology, A. Sygros Hospital, National and
Kapodistrian University of Athens, Athens, Greece

Key Words phages were often present in the dermis Introduction

Poikiloderma, histopathology
Electron (92%). The most prominent and constant
microscopy
Poikiloderma, differential feature (100%) was solar elastosis of the pap- Idiopathic acquired poikiloderma of
diagnosis illary dermis. The blood vessels were almost the face and neck was first described by A.
invariably dilated (96%) with a mild perivas- Civatte in 1923 [1]. Poikiloderma of Civatte
cular lymphohistiocytic infiltrate (78%), (PC) is a rather common skin condition,
Abstract sometimes with plasmacytes (56%). At the most often affecting the middle-aged or
Background: Poikiloderma of the face and ultrastructural level, the epidermis showed the elderly of the lighter skin phototypes
neck (Civatte) has not been studied in depth only minor changes. The dermoepidermal [2]. It is more often diagnosed in females,
for decades, especially as far as the histopa- junction was intact. The most constant find- particularly at the perimenopausal age, in-
thology is concerned. Material and Meth- ings were swelling and disruption of the col- cluding the iatrogenic menopause [1–3].
ods: We studied 50 consecutive patients lagen fibers as well as focal degeneration of Clinically, PC is manifested by pink to
with poikiloderma of Civatte (PC). Their eval- the collagen bundles. Occasionally, several brownish reticular patches consisting of
uation included: history, physical examina- vacuolar spaces were found just under the linear telangiectasia, mottled hyperpig-
tion, lesional skin biopsy and histological basal lamina. Melanin-laden macrophages mentation and superficial atrophy. It may
examination of sections stained with hema- scattered in the dermis were also detected. involve sun-exposed areas of the neck, the
toxylin-eosin, PAS, Fontana-Masson, acid or- Conclusions: PC shows distinct histological upper chest and the peripheral face in a
cein Giemsa for elastic fibers and toluidine and ultrustructural features, supporting the symmetrical distribution, sparing the ana-
blue for mast cells. In 10 randomly selected theory that it represents a separate entity. tomically shaded areas. PC runs a chronic,
subjects, a second skin biopsy was per- The histology of PC is characteristic but not benign and irreversible course, occasion-
formed and specimens were examined un- pathognomonic. On this basis, the differen- ally producing significant cosmetic disfig-
der the electron microscope. Results: There tial diagnosis from Riehl’s melanosis, poiki- urement [3, 4].
were 34 females (68%) and 16 males. The loderma atrophicans et vasculare and other We studied 50 patients with PC. Our
mean age at diagnosis was 47.8 years for fe- acquired poikilodermas can be made. Ultra- aim was to outline the histopathological
males and 61.7 years for males. Histological structural findings were consistent with the and ultrastructural profile of PC.
examination revealed an atrophic (62%), histological findings. Changes of the dermal
flattened (84%) epidermis with hyperkera- connective tissue (solar elastosis) predomi-
tosis (92%) and occasional follicular plug- nated, providing morphological evidence Material and Methods
ging (34%). In some cases, mild hydropic de- for the role of ultraviolet radiation in the
generation of the basal cell layer was evident pathogenesis of PC. The study was conducted at A. Sygros
Copyright © 2007 S. Karger AG, Basel Hospital, Athens, Greece, from 1996 to
(46%). Melanin was irregularly distributed in
the lower epidermis (94%), and melano- 2000. Fifty consecutive patients with PC
129.173.72.87 - 5/18/2015 12:01:10 PM
Kellogg Health Sciences Libr.

© 2007 S. Karger AG, Basel Assoc. Prof. N.G. Stavrianeas, MD

1018–8665/07/2142–0177$23.50/0 Attikon University General Hospital, Department of Dermatology and Venereology
Fax +41 61 306 12 34 1, Rimini Str., GR–12462 Haidari, Athens (Greece)
E-Mail [email protected] Accessible online at: Tel. +30 210 583 2396, Fax +30 210 583 2397
Downloaded by:

www.karger.com www.karger.com/drm E-Mail [email protected] or [email protected]

were recruited from the outpatient clinics, metics in the affected area. Among fe-
after they had given their informed con- males, 26 were at the perimenopausal
sent. The study was approved by the ethics stage, including 3 cases of iatrogenic meno-
committee of the hospital. The diagnosis pause. Four patients had a family history
of PC was based on clinical criteria: ac- of PC.
quired poikiloderma involving strictly the The V and the sides of the neck, as well
sun-exposed areas of the neck, the V area as the upper chest, were the most com-
and/or the peripheral face in a symmetric monly affected sites. The peripheral face,
distribution; chronic progressive course in mostly the preauricular region, was in-
adult patients with no associated health volved in 19 patients (38%). Symmetry and
problems. sparing of the area shaded by the chin were
The evaluation included a detailed per- invariably present (fig. 1). The erythema-
sonal and family history and clinical ex- totelangiectatic clinical type predominat-
amination. Epidemiological and clinical ed (58%), followed by the mixed (22%) and
parameters that were recorded included: the pigmented type (20%). Almost half of
age, sex, skin phototype, occupation, lei- the patients (46%) complained of symp-
sure activities, pattern of sun exposure, toms (pruritus, burning sensation or
measures of sun protection, drug history, flushing).
use of perfumes and cosmetics, gyneco- Histological evaluation revealed a flat-
logical history, duration of disease, site of tened epidermis with effacement of the
first appearance, symptoms, clinical form, rete ridges (84%). The epidermis was often
borders, symmetry and distribution of the thin and atrophic (62%). Basket-weave or-
skin lesions. thokeratotic hyperkeratosis was most
A 4-mm punch lesional skin biopsy commonly observed (92%; fig. 2). Some-
was obtained from the V or the side of the times follicular plugging was present Fig. 1. PC – mixed type: reticulate pigmen-
neck of all entered patients. Specimens (34%). In some cases, mild or patchy vacu- tation of the sun-exposed areas of the V
were fixed in formalin 10% and were em- olar degeneration of the basal cell layer was and the sides of the neck in a menopausal
bedded in paraffin. Sections stained with evident (46%). Melanin granules were ir- female.
hematoxylin-eosin, PAS, Fontana-Mas- regularly distributed in the lower epider-
son, acid orcein Giemsa for elastic fibers mis (94%) and melanophages laden with
and toluidine blue for mast cells were ex- melanin were often present in the dermis
amined under the light microscope. The due to melanin incontinence (92%; fig. 3).
evaluation was made by two of the investi- In the papillary dermis, the blood vessels brular texture, containing degenerated or-
gators independently. A quantitative as- were dilated and hyperemic (96%), with a ganelles, most probably mitochondria,
sessment was attempted for solar elastosis. mild perivascular lymphohistiocytic in- could be seen. We also noted inactive fi-
Elastosis was considered severe when ho- flammatory infiltrate (78%; fig. 2, 3). Not broblasts between the collagen bundles. In
mogenization of degenerated elastic fibers unusually, we observed plasmacytes in the 2 cases, several vacuolar spaces of varying
was present. infiltrate (56%). Occasionally, increased size and shape were found just under the
In 10 randomly selected subjects, a sec- numbers of mast cells could be observed basal lamina (fig. 5). In most cases, we de-
ond skin biopsy with a 3-mm punch was around the dilated blood vessels (22%). tected melanin-laden macrophages (mela-
performed. Each specimen was appropri- The most prominent and constant feature nophages) and several electrodense bodies
ately processed and sections were exam- (100%) was solar elastosis of the papillary (pigment granules?) randomly scattered in
ined under the electron microscope. dermis, i.e. fragmentation and curling of the dermis. The endothelial cells of the di-
elastic fibers forming masses of degener- lated dermal blood vessels were normal.
ated fibers that give a false impression of
Results basophil degeneration of collagen (fig. 2,
3). Solar elastosis was separated from the Discussion
Of the 50 entered patients, there were epidermis by a grenz zone.
34 females (68%) and 16 males. They were At the ultrastructural level, the epider- Although a common problem, PC has
all of Greek origin. The mean age at diag- mis showed only minor changes. In the not been studied in depth for decades.
nosis was 47.8 years (range 39–68 years) basal cells, we observed a focal distention Moreover, the histology of PC seems to
for females and 61.7 years (range 48–74 of the perinuclear pool associated with de- have escaped the attention of standard
years) for males. There were 4 skin type I generative changes of the adjacent nuclear textbooks. In the past, even its true nature
subjects, 23 skin type II, 21 skin type III membrane. The dermoepidermal junction was questioned and some authorities be-
and 2 skin type IV. Only 17 (34%) of them was intact. In the papillary dermis, the col- lieved that PC is synonymous with Riehl’s
were outdoor workers, but most patients lagen fibers were swollen and disrupted melanosis or that it may be a more accen-
(72%) reported moderate or excessive and there was focal degeneration of the tuated form of the same process [5–7].
chronic sun exposure during occupational collagen bundles (fig. 4). This was the However, PC shows distinct clinical and
or recreational activities. Thirty-six indi- most constant finding. At these sites, ill- epidemiological features [8]. Moreover,
viduals were applying perfumes or cos- defined foci of microgranular or microfi- our results indicate that PC exhibits a rath-
129.173.72.87 - 5/18/2015 12:01:10 PM

178 Dermatology 2007;214:177–182 Katoulis /Stavrianeas /Panayiotides /Bozi /

Kellogg Health Sciences Libr.

Vamvasakis /Kalogeromitros /Georgala

Downloaded by:
Fig. 2. The epidermis is flattened with mild atrophy and hyper- Fig. 3. Severe solar elastosis of the upper dermis associated with
keratosis. In the papillary dermis, connective tissue changes (so- grossly dilated blood vessels. Melanophages scattered in the der-
lar elastosis), dilated blood vessels and a mild perivascular lym- mis are also evident. Hematoxylin-eosin. !100.
phohistiocytic inflammatory infiltrate can be observed. Hema-
toxylin-eosin. !100.

er uniform histological picture supporting ial cases, as well as the occurrence of PC in closed atrophy of the epidermis and the
the theory that it represents a real entity. patients in whom all suspected causal fac- papillary dermis, loss of papillae, hyaline
The etiopathogenesis of PC is still un- tors are absent, can lead to the speculation masses at the dermoepidermal junction
clear [4]. Predilection for sun-exposed ar- that a genetic predisposition to the disease and disappearance of the elastic network
eas dictates a crucial role for chronic sun may exist [11]. Recently, based on epide- in the upper dermis. In fully developed le-
exposure. The age and sex distribution of miological, clinical and histological simi- sions, he observed cavities in the connec-
the patients suggests that hormonal fac- larities, it has been suggested that PC and tive tissue, filled with epidermic cells, pig-
tors in combination with the normal age- rosacea may represent variants in the same ment and lymphocytes.
ing process may be involved [3, 9]. It has nosological spectrum [12]. Histological findings of individual PC
been speculated that photodynamic sub- Civatte [1] in his original description cases examined by other authors included:
stances in perfumes and cosmetics possi- correlated histological findings with clini- thinning of the epidermis with patchy hy-
bly induce a photoallergic or a phototoxic cal lesions. Examination of an erythroder- perkeratosis; a well-marked stratum gran-
reaction that triggers the disease process mic pigmented patch revealed a lympho- ulosum; thinning of the stratum malpighi;
[3, 5]. On the basis of patch testing and cytic infiltration of the papillary body, ag- much degeneration of the lower epidermis
photo patch testing, it has been suggested gregations of chromatophores filled with with hyaline bodies; vacuolization of some
that a contact delayed hypersensitivity re- melanin and lymphoid nodules in the of the basal cells; pigment granules irregu-
action, most possibly to fragrances, may neighborhood of the pilosebaceous folli- larly distributed in the basal layer cells;
underlie PC [10]. The recognition of famil- cles. Sections from an atrophic macule dis- absence of papillary processes; dilated su-
129.173.72.87 - 5/18/2015 12:01:10 PM

Poikiloderma of Civatte Dermatology 2007;214:177–182 179

Kellogg Health Sciences Libr.
Downloaded by:
Fig. 4. Swollen and disrupted collagen fibers (*) as well as focal Fig. 5. Vacuolar cavities (*) can be observed under the dermoepi-
degeneration of collagen bundles in the papillary dermis. The dermal junction (d). !1,200.
dermoepidermal junction (d) is intact. !2,500.

perficial vessels; interstitial edema in the through the liberation of vasoactive agents. second most important finding, and it is
upper cutis; mild to marked chronic in- Mast cells are involved in the early stages possibly related to a delayed hypersensitiv-
flammatory infiltrate of round cells with of delayed hypersensitivity reactions and ity reaction (contact sensitization to per-
perivascular and periappendageal distri- are found among the inflammatory infil- fume or cosmetic ingredients) that pro-
bution; band-like lymphonuclear infiltrate trate in dermatoheliosis. There were also duces mild changes of the basal layer. It is
in the upper dermis; pigment granules two other interesting findings: subtle hy- clinically evident as reticulate hyperpig-
and/or melanophages in the inflammato- dropic changes of basal keratinocytes and mentation [10]. It is of interest that the vac-
ry infiltrate; a large cyst lined partly with several melanophages in the papillary der- uolar spaces observed by us in 2 of our cas-
epidermal cells and apparently derived mis. Our results are in agreement with the es may be related to the vacuolar cavities
from a hair follicle, and destruction of findings from true PC cases reported by under the basal membrane described by
elastic tissue in the upper cutis [4, 7, 13– most other authors. In contrast, we ob- Civatte in his original description [1].
16]. served neither a lichenoid pattern nor a The differential diagnosis of acquired
On the basis of our findings, the histo- vacuolar interface dermatitis reported by reticulate, patchy and mottled pigmenta-
logical picture of PC was characteristic but some authors [13, 14]. Ultrastructural tion of the neck, including PC, has been
not pathognomonic. Solar elastosis of the findings are consistent with the histologi- extensively studied by Lautenschlager and
upper dermis was the sine qua non feature. cal picture. Connective tissue changes of Itin [18]. The clinical and histological dif-
This is morphological evidence in support the papillary dermis predominated, indi- ferential diagnosis for PC is summarized
of the pathogenetic role of chronic sun ex- cating that this may represent the primary in table 1.
posure in the development of PC. Changes step of the pathogenetic cascade. Apart In conclusion, this is the first histo-
of the dermal connective tissue result in from ultraviolet radiation, the low estro- pathological and electron microscopy
telangiectasia due to loss of vascular sup- gen levels of the menopause have been study of PC to appear in the literature. We
port. It is of interest that vasodilatation associated with changes of the dermal con- observed a series of constant alterations
was more prominent, where solar elastosis nective tissue (rapid reduction of skin col- that give PC a proper physiognomy. In ad-
was more intense. The presence of mast lagen) [17]. This may explain the well- dition, histopathological and ultrastruc-
cells with perivascular distribution may established association of PC with the tural findings provide new insights into
contribute to erythema and telangiectasia menopause. Melanin incontinence is the the debated etiopathogenesis of PC.
129.173.72.87 - 5/18/2015 12:01:10 PM

180 Dermatology 2007;214:177–182 Katoulis /Stavrianeas /Panayiotides /Bozi /

Kellogg Health Sciences Libr.

Vamvasakis /Kalogeromitros /Georgala

Downloaded by:
Table 1. Clinical and histopathological differential diagnosis for PC

Etiology Clinical characteristics Histopathology

Riehl’s melanosis Pigmented dermatitis possibly Spotted brown pigmentation, Liquefaction of the basal cell layer, basal
caused by perfumes or telangiectasia is minimal or absent [20] membrane changes, melanin incontinence;
cosmetics [19] Distribution: face, most intense on the solar elastosis and atrophic changes of the
forehead and temples epidermis are absent
Ultrastructural changes: intra- and/or
intercellular edema of the lower epidermis with
disruption of desmosomes, activated melano-
cytes with increased number of melanosomes,
multilayered basal membrane [21]
Erythromelanosis Unknown; Young males Dilated hair follicles and hypertrophic
follicularis faciei et genetic predisposition Brownish red hyperpigmentation, sebaceous glands; solar elastosis and atrophic
colli telangiectasia and minute follicular papules changes are absent
(follicular keratosis) of the peripheral face
and/or neck [22]; shaded areas not spared
Poikiloderma Flattened, atrophic epidermis, hydropic
degeneration of the basal layer, band-like
infiltrate of the papillary dermis admixed with
melanophages, which in places invades the
epidermis [23]
Associated with Autoimmune disorder, Dermatomyositis: heliotrope erythema and Basal membrane is thick and/or interrupted,
collagen vascular sun-exacerbated edema (periorbital) of the face, neck and and the upper dermis is atrophic and
disease chest, Gottron’s sign, periungual edematous with deposition of an alcianophilic
telangiectasia, polymyositis, vasculitis mucoid substance and only slight dermal
Subacute lupus erythematosus: psoriasiform infiltration [23]
papulosquamous eruption on sun-exposed Immunofluorescence of the skin: lupus band
neck, trunk, upper extremities,
telangiectasia, no atrophy, periungual
telangiectasia
Systemic lupus erythematosus: butterfly
rash, discoid lupus plaques, palpable
purpura, urticarial vasculitis, fever, arthritis,
systemic involvement (renal disease,
pneumonitis, pericarditis, CNS disease etc.)
Associated with Malignant transformation; Telangiectasia, reticulate pigmentation, Epidermotropic large lymphoid cells with
cutaneous T cell precursor of mycosis ungoides superficial atrophy with asymmetrical convoluted or cerebriform nuclei [23]
lymphoma distribution on non-sun-exposed trunk
(poikiloderma Parapsoriasis en grandes plaques Patch
atrophicans et stage mycosis fungoides
vasculare)
Chronic graft- Immune reaction of Lichenoid papules, sclerodermoid changes, Hyperkeratosis, acanthosis, basal vacuolization,
versus-host disease histoincompatible poikiloderma; trunk, buttocks and mild perivascular inflammatory infiltrate,
immunocompetent donor extremities; mucosal involvement melanin incontinence. Late sclerodermoid
cells against immuno- changes with loss of appendages [23]
competent host tissues
Chronic radiation Exposure to ionizing radiation History of exposure. Epidermal atrophy; loss of appendages;
dermatitis as a result of therapy, Atrophy, hypopigmenation, telangiectasia, hyalinization, fusion of collagen and elastic
occupational or accidental poikiloderma, loss of appendages, tissue; vascular dilatation with fibrous
ulceration, necrosis at a portal of thickening of the arterial wall
radiotherapy
Melasma Genetic factors, ultraviolet Young adult females, macular brown, Increased melanin in the epidermis
radiation, female sex geographic hyperpigmentation, mostly on
hormones, drugs the central face
Berloque dermatitis Phototoxic reaction to 5- Brown pigmentation following the pattern Hyperpigmentation of the basal layer, dermal
methoxypsoralen in bergamot formed by the trickle of perfume over the melanophages [24]
oil contained in perfumes skin
129.173.72.87 - 5/18/2015 12:01:10 PM

Poikiloderma of Civatte Dermatology 2007;214:177–182 181

Kellogg Health Sciences Libr.
Downloaded by:
 References

1 Civatte A: Poïkilodermie réticulée pigmen- 9 Leveque JL, Goubanova E: Influence of age 16 Brain RT: Civatte’s poikilodermia. Proc R Soc
taire du visage et du cou. Ann Dermatol on the lips and perioral skin. Dermatology Med 1930;23:1481–1482 (Sect Derm, 43–44).
Syphiligr 1923;6:605–620. 2004;208:307–313. 17 Dunn LB, Damesyn M, Moore A, et al: Does
2 Graham R: What is poikiloderma of Civatte? 10 Katoulis AC, Stavrianeas NG, Katsarou A, estrogen prevent skin aging? Arch Dermatol
Practitioner 1989;233:1210. Antoniou C, Georgala S, Rigopoulos D, et al: 1997;133:339–342.
3 Bleehen SS: Disorders of skin colour; in Evaluation of the role of contact sensitization 18 Lautenschlager S, Itin PH: Reticulate, patchy
Champion RH, Burton JL, Burns DA, Breath- and photosensitivity in the pathogenesis of and mottled pigmentation of the neck: ac-
nach SM (eds): Rook/Wilkinson/Ebling poikiloderma of Civatte. Br J Dermatol 2002; quired forms. Dermatology 1998; 197: 291–
Textbook of Dermatology, ed 6. Oxford, 147:493–497. 296.
Blackwell Scientific Publications, 1998, pp 11 Katoulis AC, Stavrianeas NG, Georgala S, 19 Serrano F, Pujol C, Chandra J, Gallo S, Ali-
1790–1791. Katsarou-Katsari A, Koumantaki-Mathiou- aga A: Riehl’s melanosis: pigmented contact
4 Katoulis AC: A Contribution to the Study of daki E, Antoniou C, Stratigos JD: Familial dermatitis caused by fragrances. J Am Acad
the Histopathology and Aetiopathogenesis cases of poikiloderma of Civatte: genetic im- Dermatol 1989;21:1057–1060.
of Civatte’s Poikiloderma; Thesis, National plications in its pathogenesis? Clin Exp Der- 20 Rorsman H: Riehl’s melanosis. Int J Derma-
and Kapodistrian University of Athens, matol 1999;24:385–387. tol 1982;21:75–80.
2000. 12 Katoulis AC, Georgala S, Stavrianeas NG: 21 Nagao S, Iijima S: Light and electron micro-
5 Canizares O: Poikiloderma of Civatte. Arch Poikiloderma of Civatte and rosacea: vari- scopic study of Riehl’s melanosis. J Cutan
Dermatol 1968;98:429–431. ants in the same nosological spectrum. Der- Pathol 1974; 1:165–175.
6 Braun-Falco O, Plewig G, Wolff HH, Win- matology 2005; 211:386–387. 22 Whittaker SJ, Griffiths WAD: Erythromela-
kelmann RK (eds): Dermatology. Berlin, 13 Graham Little EG: Poikilodermie-Civatte. nosis follicularis faciei et colli. Clin Exp Der-
Springer, 1991, p 692. Br J Dermatol 1928;40:231–241. matol 1987;12:33–35.
7 Pierini LE, Bosq P: Maladie de Civatte. Ann 14 Sahoo B, Kumar B: Role of methylchloro- 23 Grosshans E, Rongioletti F: Diagnostic d’un
Dermatol Syphiligr 1938;9:381–420. isothiazolinone/methylisothiazolinone état poïkilodermique. Pathologica 1990; 82:
8 Katoulis AC, Stavrianeas NG, Georgala S, (Kathon CG) in poikiloderma of Civatte. 351–358.
Bozi E, Kalogeromitros D, Koumantaki E, Contact Dermatitis 2001;44:249. 24 Zaynoun ST, Aftimos BA, Tenekjian KK,
Katsambas AD: Poikiloderma of Civatte: a 15 Nomland R: Poïkilodermie réticulée pig- Kurban AK: Berloque dermatitis: a continu-
clinical and epidemiological study. J Eur mentaire du visage et du cou (Civatte). Arch ing cosmetic problem. Contact Dermatitis
Acad Dermatol Venereol 2005; 19:444–448. Dermatol Syphiligr 1930;32:184–185. 1981;7:11–116.

129.173.72.87 - 5/18/2015 12:01:10 PM

182 Dermatology 2007;214:177–182 Katoulis /Stavrianeas /Panayiotides /Bozi /

Kellogg Health Sciences Libr.

Vamvasakis /Kalogeromitros /Georgala

Downloaded by: