© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
J Cutan Pathol 2014: 41: 340–346 doi: 10.1111/cup.12294 John Wiley & Sons. Printed in Singapore
Journal of Cutaneous Pathology
Perspectives in Dermatopathology
Who Described Civatte Bodies? Eosinophilic apoptotic (necrotic) keratinocytes in the lower epidermis and at the dermoepidermal junction are a feature of many interface dermatoses but are most reliably found in lichen planus. These structures are universally known as Civatte bodies. Nonetheless, they were first described by Raymond Sabouraud in 1912. Even after Achille Civatte discussed and beautifully illustrated them a decade later, it took until the late 1960s for the term Civatte body to win acceptance. Keywords: basement membrane zone, keratinocytes, lichen planus, pathology dermatopathology Burgdorf WHC, Plewig G. Who Described Civatte Bodies? J Cutan Pathol 2014; 41: 340–346. © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Probably every dermatologist and dermatopathologist reading this paper learned that the eosinophilic globules seen at the dermoepidermal junction in lichen planus are known as Civatte bodies (Fig. 1). These apoptotic keratinocytes are also called colloid, cytoid or hyaline bodies – all derived from the original French descriptions – but the noneponymic names are much less often encountered. It seems obvious that these bodies must have been described by either Achille or Jean Civatte. Few
Fig. 1. Photomicrograph of lichen planus showing an interface dermatitis with Civatte bodies at the dermoepidermal junction [hematoxylin and eosin (H&E ×200)] [Courtesy of Dr. Werner Kempf, Zurich, Switzerland].
340
Walter H. C. Burgdorf and Gerd Plewig Department of Dermatology, Ludwig Maximilian University, Munich, Germany
Walter H. C. Burgdorf, MD, Department of Dermatology, Ludwig Maximilian University, Traubinger, Str. 45A, 82327 Tutzing, Munich, Germany Tel: +11 49 8158 7159 Fax: +11 49 89 5160 6022 e-mail: [email protected] Accepted for publication January 14, 2014
people know that they were first described by Raymond Sabouraud, whose name everyone generally associates with mycology, not dermatopathology. Raymond (or Raimond) Jacques Adrien Sabouraud (1864–1938) (Fig. 2)1 studied medicine
Fig. 2. Raymond Sabouraud [Reprinted from Pantheon of Dermatology. Outstanding Historical Figures. (Fig. 1, p. 973) with the permission of Springer, Heidelberg, Germany].
Who Described Civatte Bodies?
Fig. 3. Sabouraud’s original illustration of cells with colloid degeneration (c) in the Malpighian layer in lichen planus [Fig. 9 in Ref. 4 ].
in Paris, initially working in microbiology at ´ Metchnikoff Institut Pasteur with two pioneers – Elie (1845–1916) a Nobel Prize winner who described ´ phagocytosis and Emile Roux (1853–1933) who discovered diphtheria toxin and mycoplasma. When he started his dermatological training at Hˆopital Saint-Louis, he initially worked in syphilis research but Ernest Besnier (1831–1909) suggested that he turned his attention to tinea. By 1894 he had identified two main types of tinea caused by what we today know as Trichophyton and Microsporon species. He later identified over 50 different dermatophytes, wrote a classic book Les Teignes (The Dermatophytes)2 , developed his still well-known fungal culture agar, and became Chef de laboratoire de l’Ecole des Teigneux at Hˆopital Saint-Louis. Sabouraud was also a gifted artist, illustrating many of his own works and winning fame as a sculptor. Sabouraud was also a skilled histopathologist who in 1910 turned his attention to lichen planus. Erasmus Wilson had initially described lichen planus in 1869.3 Writing about lichen plan de Wilson, Sabouraud described and depicted colloid degeneration of the cells of the Malpighian layer, providing what was almost certainly the first description of what we today call Civatte bodies (Fig. 3).4 Both Oscar Gans5 and Karl Herxheimer6,7 wrote at length about
‘Sabouraud cells’ which they correctly felt were degenerating keratinocytes. Neither emphasized their diagnostic importance in lichen planus. Achille Civatte (1877–1956) (Fig. 4)8 was from a family of doctors in Sisteron in the north of
Fig. 4. Achille Civatte [Reprinted from Pantheon of Dermatology. Outstanding Historical Figures. (Fig. 1, p. 162) with the permission of Springer, Heidelberg, Germany].
341
Burgdorf & Plewig
Fig. 5. First depiction of hyaline bodies by Achille Civatte [Fig. 5 in Ref. 9 ]. The hyaline bodies may be single (h) or grouped (ah).
Fig. 7. Photomicrograph of lichen planus from Atlas d’histopathologie cutan´ee (Fig. 136, p. 166).
Fig. 6. Title page of Atlas d’histopathologie cutan´ee.
the Provence. He started his training at Hˆopital Saint-Louis in 1899, just 7 years after Sabouraud, so the two giants probably spent hours over the microscope together. Civatte spent considerable time learning dermatopathology in Germany, visiting
342
Breslau, Berlin and working with Paul Gerson Unna (1850–1929) in Hamburg. In 1922, he established the Mus´ee d’ histologie de L’ Hˆopital Saint-Louis, an immense collection of microscope slides which unfortunately has not been maintained. Civatte never applied for a professorship but instead spent his mornings doing all the dermatopathology for the six divisions of Hˆopital Saint-Louis and working in his private practice in the afternoons. He continued this routine until 1954, 2 years before his death. Achille Civatte described poikilodermie r´eticul´ee pigmentaire du visage et du cou (reticular poikiloderma of the face and neck)9 in 1922; today the disease is known as poikiloderma of Civatte. In this paper, he clearly illustrated corps hyalins (Fig. 5). Five years later in a paper contrasting lichen nitidus and lichen planus, he emphasized that the corps colloides were a helpful way to confirm the diagnosis of lichen planus.10 In 1953, he and Henri Gougerot wrote a long paper on the clinical and microscopic diagnostic criteria for lichen planus in which they emphasized the corps
Who Described Civatte Bodies?
Fig. 8. Drawing of hyaline bodies in Atlas d’histopathologie cutan´ee (Fig. 137, p. 167).
Fig. 9. Jean Civatte [Courtesy of Dr. Daniel Wallach, Paris, France].
hyalins of the lower epidermis and interface.11 He also wrote one of the first descriptions of dermatofibroma as fibrome en pastille in 1928.12 Unquestionably his greatest scientific contribution was the identification in 1943 of acantholytic cells in pemphigus vulgaris whose properties he accurately described without the benefit of immunofluorescence studies, paving the way to the now seemingly obvious distinction
Fig. 10. Title page of first edition of Histopathologie cutan´ee.
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Burgdorf & Plewig
Fig. 11. Illustration of hyaline bodies from Histopathologie cutan´ee (Fig. 25, p. 99).
between pemphigus vulgaris, bullous pemphigoid and dermatitis herpetiformis.13 Achille Civatte started writing his Atlas d’histopathologie cutan´ee (Fig. 6) in the 1950s but only the first volume was completed and it was published posthumously in 1957. This volume covered eczema, seborrheic and senile keratoses, psoriasis, lupus erythematosus, lichen planus, lichen sclerosus and his first love, parapsoriasis. In the 40-plus pages devoted to lichen planus, he clearly illustrates the corps hyalins or boules hyalins at the dermoepidermal junction both with photomicrographs and drawings (Figs. 7 and 8).14 Achille Civatte’s son, Jean Civatte (born in 1922) (Fig. 9),15 also became a leader in French dermatology and dermatopathology. He succeeded Robert Degos and headed the main Dermatology
344
Department in Hˆopital Saint-Louis from 1975 to 1989. He was also Secretary of the French Society of Dermatology (1976–1991) and editor-in-chief of the Annales de dermatologie. He played the first role in the development of the Journ´ees dermatologiques de Paris, the main French dermatology meeting. In 1990, he became a member of the distinguished Acad´emie de medicine. His main interest has always been dermatopathology. He helped his father finalize Atlas d’histopathologie cutan´ee and then wrote Histopathologie cutan´ee which went through two editions in 1967 and 1982. He wrote a multitude of important dermatopathology papers and was a highly regarded consultant among French-speaking dermatopathologists. Exactly how the term Civatte body crept into the daily vocabulary of dermatopathologists and
Who Described Civatte Bodies? dermatologists is a mystery. Obviously Achille Civatte was very aware of the significance of hyaline bodies in lichen planus and took considerable pains to precisely picture them. He also mentioned in his 1957 book that he had also identified them in drug eruptions. In Robert Degos’ classic loose-leaf textbook16 which was ‘The Bible’ at Hˆopital SaintLouis, the bodies are illustrated and described as the result of d´eg´en´erescence colloïde, but no eponym is attached. Jose Mascaro from Barcelona, who trained at Hˆopital Saint-Louis from 1958 to 1967, remembers hearing the term ‘Civatte body’. Jean-Hilaire Saurat from Geneva, who followed Mascaro by a few years, recalls that corps cytoïdes was the usual designation and continues to employ this term in his textbook.17 The first written use of Civatte body that we found was by Hamilton Montgomery in his classic textbook in 1967.18 Hermann Pinkus and Amir Mehregan also employed the term 2 years later in the first edition of A Guide to Dermatohistopathology.19 Walter Lever first mentioned Civatte bodies in the index of 5th edition of Histopathology of the Skin20 but did not discuss them in the text until the 6th edition.21 A detailed review of histopathology of lichen planus in the Journal of Investigative Dermatology in 1967 mentioned neither Civatte nor his bodies.22 The first reference to Civatte bodies in PubMed is a paper in 1970 by Peter Copeman, Arnold Schroeter and Robert Kierland on four patients with an overlap between lupus erythematosus and lichen planus.23 The person who obviously knows best – Jean Civatte – did not employ the term in the first edition of Histopathologie cutan´ee (Fig. 10) in1967; instead he discussed corps hyalins ou colloides anucl´e´es (Fig. 11).24 In the second edition in 1982, he once again demonstrated the structures, added an immunofluorescence photomicrograph, and now wrote of corps hyalins ou colloides (corps de A. Civatte).25 When contacted on the occasion of his 90th birthday
in 2012, he graciously pointed out once again that his father had not described the bodies. Today the term Civatte body is ubiquitous, found in virtually every dermatopathology book. During teaching conferences, when confronted with a biopsy from lichen planus, residents are taught early in their careers to respond with the term Civatte body, just as we were. However, we have learned quite a bit about the nature of these structures in the last 40 years. In the 1970s, several groups used primarily electronic microscopy to prove that Civatte bodies are damaged or degenerating keratinocytes undergoing apoptosis.26 – 28 Later the structures were shown to react with a variety of monoclonal antibodies directed against various keratins,29 once again confirming their origin. It is not our intention to in any way diminish the role of Achille Civatte in popularizing the corps hyalins of lichen planus. One simply should remember that they were first identified by his colleague Sabouraud. There is perhaps a bit of justice, as Achille Civatte did not get the recognition he richly deserved for separating pemphigus vulgaris from bullous pemphigoid; Civatte bodies are another way of recognizing this great dermatopathologist. Acknowledgements Daniel Wallach helped us find old French sources, corrected our translation efforts, provided a picture of Jean Civatte and helped in many other ways. Dan Lipsker refreshed our knowledge of French terminology for the epidermal layers. David Elder helped us find old dermatopathology texts. Jean Civatte, Jose Mascaro and Jean-Hilaire Saurat patiently answered our questions.
Author contribution Drs. Burgdorf and Plewig were both involved in manuscript design, first draft and critical revision.
References 1. Effendy I. Raymond Sabouraud. In: L¨oser C, Plewig G, Burgdorf WHC, eds. Pantheon of Dermatology. Outstanding Historical Figures. Heidelberg: Springer, 2013; 973. 2. Sabouraud R. Les maladies cryptogamiques. Les teignes. Avec 433 figures dans le texte et 28 planches hors texte. Paris: Masson, 1910. 3. Wilson E. On lichen planus. J Cutan Med Dis Skin 1869; 3: 117. 4. Sabouraud R. Sur quelques points de l’anatomie pathologique du lichen plan de Wilson. Ann Dermatol Syph 1910; 5e s´erie (Tome I): 491. 5. Gans O. Histologie der Hautkrankheiten, Erster Band. Berlin: Springer, 1925.
¨ 6. Herxheimer K. Uber die Darstellung der ‘‘Sabouraud”-Zellen”. Arch Dermatol Syph 1932; 166: 172. ¨ 7. Herxheimer K. Uber die Deutung der Sabouraud-Zellen. Arch Dermatol Syph 1932; 166: 416. 8. Civatte J. Achille Civatte. In: L¨oser C, Plewig G, Burgdorf WHC, eds. Pantheon of Dermatology. Outstanding Historical Figures. Heidelberg: Springer, 2013; 162. 9. Civatte A. Poikilodermie r´eticul´ee pigmentaire du visage et du cou. Ann Dermatol Syph 1923; 6i`eme s´erie (Tome IV): 605. 10. Civatte A. «Lichen nitidus» et lichen plan. Bull Soc Fr Dermatol Syphiligr 1927; 34: 232.
11. Gougerot H, Civatte A. Crit´eres cliniques et histologues des lichens plans cutan´es et muqueux: D´elimitation. Ann Dermatol Syph 1953; 80: 5. 12. Civatte A. Fibrome en pastille. Marseille Med 1928; 65: 365. 13. Civatte A. Diagnostic histopathologique de la dermatite polymorphe douloureuse ou maladie de Duhring-Brocq. Ann Dermatol Syph 1943; 8ieme s´erie (Tome 3): 1. 14. Civatte A. Atlas d’histopathologie cutan´ee. Paris: Masson, 1957. 15. Schnitzler L. Dermatology at the Hˆopital Saint-Louis from 1945 to the present day. In Wallach D, Tilles G, eds. Dermatology in France. Toulouse: Editions Privat, 2002; 477.
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Burgdorf & Plewig 16. Degos R. Dermatologie, 9th ed. Paris: Maloine, 1976; 280(Loose-leaf revision). 17. Saurat J-H, Grosshans E, Laugier P, LaChapelle J-M (eds). Dermatologie et v´en´er´eologie, 2e ed ed. Paris: Masson, 1990; 339. 18. Montgomery H. Dermatopathology. Vol. 1. New York: Hoeber-Harper & Row, 1967; 285. 19. Pinkus H, Mehregan A. A Guide to Dermatohistopathology. New York: AppletonCentury-Crofts, 1969; 120. 20. Lever W, Schaumburg-Lever G. Histopathology of the Skin, 5th ed. Philadelphia: Lippincott, 1975; 777.
346
21. Lever W, Schaumburg-Lever G. Histopathology of the Skin, 6th ed. Lippincott: Philadelphia, 1983; 153. 22. Ellis FA. Histopathology of lichen planus based on analysis of one hundred biopsy specimens. J Invest Dermatol 1967; 48: 143. 23. Copeman PWM, Schroeter AL, Kierland RR. An unusual variant of lupus erythematosus or lichen planus. Br J Dermatol 1970; 83: 269. 24. Civatte J. Histopathologie cutan´ee. Paris: Flammarion, 1967; 98. 25. Civatte J. Histopathologie cutan´ee, 2nd ed. Paris: Flammarion, 1982; 162.
26. Ebner H, Gebhart W. Light and electron microscopic studies on colloid and other cytoid bodies. Clin Exp Dermatol 1977; 2: 311. 27. Hashimoto K. Apoptosis in lichen planus and several other dermatoses. Intra-epidermal cell death with filamentous degeneration. Acta Derm Venereol 1976; 56: 187. 28. Weedon D, Searle J, Kerr JF. Apoptosis. Its nature and implications for dermatopathology. Am J Dermatopathol 1979; 1: 133. 29. Biermann H, Rauterberg EW. Expression of fetal cytokeratins in epidermal cells and colloid bodies in lichen planus. J Cutan Pathol 1998; 25: 35.
J Cutan Pathol 2014: 41: 340–346 doi: 10.1111/cup.12294 John Wiley & Sons. Printed in Singapore
Journal of Cutaneous Pathology
Perspectives in Dermatopathology
Who Described Civatte Bodies? Eosinophilic apoptotic (necrotic) keratinocytes in the lower epidermis and at the dermoepidermal junction are a feature of many interface dermatoses but are most reliably found in lichen planus. These structures are universally known as Civatte bodies. Nonetheless, they were first described by Raymond Sabouraud in 1912. Even after Achille Civatte discussed and beautifully illustrated them a decade later, it took until the late 1960s for the term Civatte body to win acceptance. Keywords: basement membrane zone, keratinocytes, lichen planus, pathology dermatopathology Burgdorf WHC, Plewig G. Who Described Civatte Bodies? J Cutan Pathol 2014; 41: 340–346. © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Probably every dermatologist and dermatopathologist reading this paper learned that the eosinophilic globules seen at the dermoepidermal junction in lichen planus are known as Civatte bodies (Fig. 1). These apoptotic keratinocytes are also called colloid, cytoid or hyaline bodies – all derived from the original French descriptions – but the noneponymic names are much less often encountered. It seems obvious that these bodies must have been described by either Achille or Jean Civatte. Few
Fig. 1. Photomicrograph of lichen planus showing an interface dermatitis with Civatte bodies at the dermoepidermal junction [hematoxylin and eosin (H&E ×200)] [Courtesy of Dr. Werner Kempf, Zurich, Switzerland].
340
Walter H. C. Burgdorf and Gerd Plewig Department of Dermatology, Ludwig Maximilian University, Munich, Germany
Walter H. C. Burgdorf, MD, Department of Dermatology, Ludwig Maximilian University, Traubinger, Str. 45A, 82327 Tutzing, Munich, Germany Tel: +11 49 8158 7159 Fax: +11 49 89 5160 6022 e-mail: [email protected] Accepted for publication January 14, 2014
people know that they were first described by Raymond Sabouraud, whose name everyone generally associates with mycology, not dermatopathology. Raymond (or Raimond) Jacques Adrien Sabouraud (1864–1938) (Fig. 2)1 studied medicine
Fig. 2. Raymond Sabouraud [Reprinted from Pantheon of Dermatology. Outstanding Historical Figures. (Fig. 1, p. 973) with the permission of Springer, Heidelberg, Germany].
Who Described Civatte Bodies?
Fig. 3. Sabouraud’s original illustration of cells with colloid degeneration (c) in the Malpighian layer in lichen planus [Fig. 9 in Ref. 4 ].
in Paris, initially working in microbiology at ´ Metchnikoff Institut Pasteur with two pioneers – Elie (1845–1916) a Nobel Prize winner who described ´ phagocytosis and Emile Roux (1853–1933) who discovered diphtheria toxin and mycoplasma. When he started his dermatological training at Hˆopital Saint-Louis, he initially worked in syphilis research but Ernest Besnier (1831–1909) suggested that he turned his attention to tinea. By 1894 he had identified two main types of tinea caused by what we today know as Trichophyton and Microsporon species. He later identified over 50 different dermatophytes, wrote a classic book Les Teignes (The Dermatophytes)2 , developed his still well-known fungal culture agar, and became Chef de laboratoire de l’Ecole des Teigneux at Hˆopital Saint-Louis. Sabouraud was also a gifted artist, illustrating many of his own works and winning fame as a sculptor. Sabouraud was also a skilled histopathologist who in 1910 turned his attention to lichen planus. Erasmus Wilson had initially described lichen planus in 1869.3 Writing about lichen plan de Wilson, Sabouraud described and depicted colloid degeneration of the cells of the Malpighian layer, providing what was almost certainly the first description of what we today call Civatte bodies (Fig. 3).4 Both Oscar Gans5 and Karl Herxheimer6,7 wrote at length about
‘Sabouraud cells’ which they correctly felt were degenerating keratinocytes. Neither emphasized their diagnostic importance in lichen planus. Achille Civatte (1877–1956) (Fig. 4)8 was from a family of doctors in Sisteron in the north of
Fig. 4. Achille Civatte [Reprinted from Pantheon of Dermatology. Outstanding Historical Figures. (Fig. 1, p. 162) with the permission of Springer, Heidelberg, Germany].
341
Burgdorf & Plewig
Fig. 5. First depiction of hyaline bodies by Achille Civatte [Fig. 5 in Ref. 9 ]. The hyaline bodies may be single (h) or grouped (ah).
Fig. 7. Photomicrograph of lichen planus from Atlas d’histopathologie cutan´ee (Fig. 136, p. 166).
Fig. 6. Title page of Atlas d’histopathologie cutan´ee.
the Provence. He started his training at Hˆopital Saint-Louis in 1899, just 7 years after Sabouraud, so the two giants probably spent hours over the microscope together. Civatte spent considerable time learning dermatopathology in Germany, visiting
342
Breslau, Berlin and working with Paul Gerson Unna (1850–1929) in Hamburg. In 1922, he established the Mus´ee d’ histologie de L’ Hˆopital Saint-Louis, an immense collection of microscope slides which unfortunately has not been maintained. Civatte never applied for a professorship but instead spent his mornings doing all the dermatopathology for the six divisions of Hˆopital Saint-Louis and working in his private practice in the afternoons. He continued this routine until 1954, 2 years before his death. Achille Civatte described poikilodermie r´eticul´ee pigmentaire du visage et du cou (reticular poikiloderma of the face and neck)9 in 1922; today the disease is known as poikiloderma of Civatte. In this paper, he clearly illustrated corps hyalins (Fig. 5). Five years later in a paper contrasting lichen nitidus and lichen planus, he emphasized that the corps colloides were a helpful way to confirm the diagnosis of lichen planus.10 In 1953, he and Henri Gougerot wrote a long paper on the clinical and microscopic diagnostic criteria for lichen planus in which they emphasized the corps
Who Described Civatte Bodies?
Fig. 8. Drawing of hyaline bodies in Atlas d’histopathologie cutan´ee (Fig. 137, p. 167).
Fig. 9. Jean Civatte [Courtesy of Dr. Daniel Wallach, Paris, France].
hyalins of the lower epidermis and interface.11 He also wrote one of the first descriptions of dermatofibroma as fibrome en pastille in 1928.12 Unquestionably his greatest scientific contribution was the identification in 1943 of acantholytic cells in pemphigus vulgaris whose properties he accurately described without the benefit of immunofluorescence studies, paving the way to the now seemingly obvious distinction
Fig. 10. Title page of first edition of Histopathologie cutan´ee.
343
Burgdorf & Plewig
Fig. 11. Illustration of hyaline bodies from Histopathologie cutan´ee (Fig. 25, p. 99).
between pemphigus vulgaris, bullous pemphigoid and dermatitis herpetiformis.13 Achille Civatte started writing his Atlas d’histopathologie cutan´ee (Fig. 6) in the 1950s but only the first volume was completed and it was published posthumously in 1957. This volume covered eczema, seborrheic and senile keratoses, psoriasis, lupus erythematosus, lichen planus, lichen sclerosus and his first love, parapsoriasis. In the 40-plus pages devoted to lichen planus, he clearly illustrates the corps hyalins or boules hyalins at the dermoepidermal junction both with photomicrographs and drawings (Figs. 7 and 8).14 Achille Civatte’s son, Jean Civatte (born in 1922) (Fig. 9),15 also became a leader in French dermatology and dermatopathology. He succeeded Robert Degos and headed the main Dermatology
344
Department in Hˆopital Saint-Louis from 1975 to 1989. He was also Secretary of the French Society of Dermatology (1976–1991) and editor-in-chief of the Annales de dermatologie. He played the first role in the development of the Journ´ees dermatologiques de Paris, the main French dermatology meeting. In 1990, he became a member of the distinguished Acad´emie de medicine. His main interest has always been dermatopathology. He helped his father finalize Atlas d’histopathologie cutan´ee and then wrote Histopathologie cutan´ee which went through two editions in 1967 and 1982. He wrote a multitude of important dermatopathology papers and was a highly regarded consultant among French-speaking dermatopathologists. Exactly how the term Civatte body crept into the daily vocabulary of dermatopathologists and
Who Described Civatte Bodies? dermatologists is a mystery. Obviously Achille Civatte was very aware of the significance of hyaline bodies in lichen planus and took considerable pains to precisely picture them. He also mentioned in his 1957 book that he had also identified them in drug eruptions. In Robert Degos’ classic loose-leaf textbook16 which was ‘The Bible’ at Hˆopital SaintLouis, the bodies are illustrated and described as the result of d´eg´en´erescence colloïde, but no eponym is attached. Jose Mascaro from Barcelona, who trained at Hˆopital Saint-Louis from 1958 to 1967, remembers hearing the term ‘Civatte body’. Jean-Hilaire Saurat from Geneva, who followed Mascaro by a few years, recalls that corps cytoïdes was the usual designation and continues to employ this term in his textbook.17 The first written use of Civatte body that we found was by Hamilton Montgomery in his classic textbook in 1967.18 Hermann Pinkus and Amir Mehregan also employed the term 2 years later in the first edition of A Guide to Dermatohistopathology.19 Walter Lever first mentioned Civatte bodies in the index of 5th edition of Histopathology of the Skin20 but did not discuss them in the text until the 6th edition.21 A detailed review of histopathology of lichen planus in the Journal of Investigative Dermatology in 1967 mentioned neither Civatte nor his bodies.22 The first reference to Civatte bodies in PubMed is a paper in 1970 by Peter Copeman, Arnold Schroeter and Robert Kierland on four patients with an overlap between lupus erythematosus and lichen planus.23 The person who obviously knows best – Jean Civatte – did not employ the term in the first edition of Histopathologie cutan´ee (Fig. 10) in1967; instead he discussed corps hyalins ou colloides anucl´e´es (Fig. 11).24 In the second edition in 1982, he once again demonstrated the structures, added an immunofluorescence photomicrograph, and now wrote of corps hyalins ou colloides (corps de A. Civatte).25 When contacted on the occasion of his 90th birthday
in 2012, he graciously pointed out once again that his father had not described the bodies. Today the term Civatte body is ubiquitous, found in virtually every dermatopathology book. During teaching conferences, when confronted with a biopsy from lichen planus, residents are taught early in their careers to respond with the term Civatte body, just as we were. However, we have learned quite a bit about the nature of these structures in the last 40 years. In the 1970s, several groups used primarily electronic microscopy to prove that Civatte bodies are damaged or degenerating keratinocytes undergoing apoptosis.26 – 28 Later the structures were shown to react with a variety of monoclonal antibodies directed against various keratins,29 once again confirming their origin. It is not our intention to in any way diminish the role of Achille Civatte in popularizing the corps hyalins of lichen planus. One simply should remember that they were first identified by his colleague Sabouraud. There is perhaps a bit of justice, as Achille Civatte did not get the recognition he richly deserved for separating pemphigus vulgaris from bullous pemphigoid; Civatte bodies are another way of recognizing this great dermatopathologist. Acknowledgements Daniel Wallach helped us find old French sources, corrected our translation efforts, provided a picture of Jean Civatte and helped in many other ways. Dan Lipsker refreshed our knowledge of French terminology for the epidermal layers. David Elder helped us find old dermatopathology texts. Jean Civatte, Jose Mascaro and Jean-Hilaire Saurat patiently answered our questions.
Author contribution Drs. Burgdorf and Plewig were both involved in manuscript design, first draft and critical revision.
References 1. Effendy I. Raymond Sabouraud. In: L¨oser C, Plewig G, Burgdorf WHC, eds. Pantheon of Dermatology. Outstanding Historical Figures. Heidelberg: Springer, 2013; 973. 2. Sabouraud R. Les maladies cryptogamiques. Les teignes. Avec 433 figures dans le texte et 28 planches hors texte. Paris: Masson, 1910. 3. Wilson E. On lichen planus. J Cutan Med Dis Skin 1869; 3: 117. 4. Sabouraud R. Sur quelques points de l’anatomie pathologique du lichen plan de Wilson. Ann Dermatol Syph 1910; 5e s´erie (Tome I): 491. 5. Gans O. Histologie der Hautkrankheiten, Erster Band. Berlin: Springer, 1925.
¨ 6. Herxheimer K. Uber die Darstellung der ‘‘Sabouraud”-Zellen”. Arch Dermatol Syph 1932; 166: 172. ¨ 7. Herxheimer K. Uber die Deutung der Sabouraud-Zellen. Arch Dermatol Syph 1932; 166: 416. 8. Civatte J. Achille Civatte. In: L¨oser C, Plewig G, Burgdorf WHC, eds. Pantheon of Dermatology. Outstanding Historical Figures. Heidelberg: Springer, 2013; 162. 9. Civatte A. Poikilodermie r´eticul´ee pigmentaire du visage et du cou. Ann Dermatol Syph 1923; 6i`eme s´erie (Tome IV): 605. 10. Civatte A. «Lichen nitidus» et lichen plan. Bull Soc Fr Dermatol Syphiligr 1927; 34: 232.
11. Gougerot H, Civatte A. Crit´eres cliniques et histologues des lichens plans cutan´es et muqueux: D´elimitation. Ann Dermatol Syph 1953; 80: 5. 12. Civatte A. Fibrome en pastille. Marseille Med 1928; 65: 365. 13. Civatte A. Diagnostic histopathologique de la dermatite polymorphe douloureuse ou maladie de Duhring-Brocq. Ann Dermatol Syph 1943; 8ieme s´erie (Tome 3): 1. 14. Civatte A. Atlas d’histopathologie cutan´ee. Paris: Masson, 1957. 15. Schnitzler L. Dermatology at the Hˆopital Saint-Louis from 1945 to the present day. In Wallach D, Tilles G, eds. Dermatology in France. Toulouse: Editions Privat, 2002; 477.
345
Burgdorf & Plewig 16. Degos R. Dermatologie, 9th ed. Paris: Maloine, 1976; 280(Loose-leaf revision). 17. Saurat J-H, Grosshans E, Laugier P, LaChapelle J-M (eds). Dermatologie et v´en´er´eologie, 2e ed ed. Paris: Masson, 1990; 339. 18. Montgomery H. Dermatopathology. Vol. 1. New York: Hoeber-Harper & Row, 1967; 285. 19. Pinkus H, Mehregan A. A Guide to Dermatohistopathology. New York: AppletonCentury-Crofts, 1969; 120. 20. Lever W, Schaumburg-Lever G. Histopathology of the Skin, 5th ed. Philadelphia: Lippincott, 1975; 777.
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21. Lever W, Schaumburg-Lever G. Histopathology of the Skin, 6th ed. Lippincott: Philadelphia, 1983; 153. 22. Ellis FA. Histopathology of lichen planus based on analysis of one hundred biopsy specimens. J Invest Dermatol 1967; 48: 143. 23. Copeman PWM, Schroeter AL, Kierland RR. An unusual variant of lupus erythematosus or lichen planus. Br J Dermatol 1970; 83: 269. 24. Civatte J. Histopathologie cutan´ee. Paris: Flammarion, 1967; 98. 25. Civatte J. Histopathologie cutan´ee, 2nd ed. Paris: Flammarion, 1982; 162.
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