Systemic lupus erythematosus historical perspective

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Editor-In-Chief: C. Michael Gibson, M.S., M.D. [1]; Associate Editor(s)-in-Chief: Raviteja Guddeti, M.B.B.S. [2]

Overview

5. Osler W. On the visceral complications of erythema exudativum multiforme. Am J Med Sci 1895;110:629-646.
6. Hutchinson J. Lupus erythematosus. Med Times Gaz 1879;1:1-3.
7. Hutchinson J. On lupus and its treatment. Br Med J 1880;1:650-652.
8. Jadassohn J. Lupus erythematodes. In: Mracek F, editor. Handbuch der Hautkrankheiten. Wein, Alfred Holder, 1904, pp 298-404l.
9. Libman E, Sacks B. A hitherto undescribed form of valvular and mural endocarditis. Arch Intern Med 1924;33:701.
10. Klemperer P, Pollack A, Baehr G. Diffuse collagen disease: acute disseminated lupus erythematosus and diffuse scleroderma. JAMA 1984;251:1593-1594.
11. Hargraves MM. Discovery of the LE cell and its morphology. Mayo Clin Proc 1969;44:579-599.
12. Friou GJ. Antinuclear Antibodies: diagnostic significance and methods. Arthritis Rheum 1967;10:151-159.
13. Wasserman A, Neisser A, Bruck C. Eine serodiagnosticsche reaktion bei syphilis. Dtsch Med Wochenschr 1906;32:745-746.
14. Pangborn MC. A new serologically active phospholipid from beef heart. Proc Soc Exp Biol Med 1941;48:484-486.
15. Haserick JR, Long R. Systemic lupus erythematosus preceded by false-positive serologic test for syphilis: presentation of five cases. Ann Intern Med 1952;37:559-565.
16. Moore JE, Lutz WB. The natural history of systemic lupus erythematosus: an approach to its study through chronic biological false positive reactions. J Chron Dis 1955;2:297-316.
17. Arnett FC, Shulman LE. Studies in familial systemic lupus erythematosus. Medicine (Baltimore) 1976;55:313-322.
18. Bielschowsky M, Helyer BJ, Howie JB. Spontaneous hemolytic anemia in mice of the NZB/BL strain. Proc Univ Otago Med School 1959;37:9.

Although the term “lupus” was not confined to a single disorder at that time [3], the peculiarity of the skin lesion was fully recognized, resulting in a variety of descriptive terms (e.g., “butterfly rash” [4]) which are in use until today. It was, however, not until Moritz Kaposi succeeded Hebra to the Chair of the Department of Dermatology at the Vienna University Hospital that the systemic nature of lupus was recognized: Kaposi reported in 1872 that certain patients suffering from lupus presented with a syndrome consisting of fever. arthritis, lymphadenopathy, and anemia [5]. It was this report which led to a clear separation of systemic or disseminated lupus erythemntosus (SLE) from the forms definitely limited to the skin. Publications by Jadassohn from Vienna [6] and by William Osler from Baltimore, Maryland, who discussed visceral complications of “erythema exsudativum multiforme” [7] — which rather would be recognized as SLE today [8] — gave additional evidence for the disseminated nature of the disease, while reports on idiopathic thrombotic thrombocytopenic purpura [9], endocarditis [10], and changes in renal histology [11], culminating in the classic study by Klemperer, Pollack, and Baehr on the pathomorphology of SLE in different organs [12], illustrated its puzzling variety of clinical manifestations.

1. 1. Hebra F (1845) Versuch einer auf pathologischer Anatomie gegründeten Einteilung der Hautkrankheiten. K.k. Gesellschaft der Ärzte in Wien 1: 43–52
2. 2. Cazanave PL, Chausit M (1851) Annales des maladies de la peau et de la syphilis, conference du 4 Juin 1851, Paris. 3: 297–299
3. 3. Holubar K (1980) Terminology and iconography of lupus erythematosus. Am J Dermatopathol. 2: 239–242PubMedCrossRef
4. 4. Hebra F (1846) Bericht über die Leistungen in der Dermatologie. In: Constatt, Eisenmann (eds) Jahresbericht über die Fortschritte der gesamten Medizin, 1845. Enke, Erlangen
5. 5. Kaposi M (1872) Neue Beiträge zur Kenntnis des Lupus erythematosus. Arch Dermatol and Syphilol 4: 36–78CrossRef
6. 6. Jadassohn J (1940) Handbuch der Hautkrankheiten. Mraeck, Berlin
7. 7. Osler W (1900) The visceral lesions of the erythema group of diseases. Br J Dermatol 12: 227–245
8. 8. Talbott J (1974) Historical background of discoid and systemic lupus erythematosus. In: Duboid EL (ed) Lupus erythematosus, 2nd ed. University of Southern California Press, Los Angeles
9. 9. Gitlow S, Goldmark C (1939) Generalized capillary and arteriolar thrombosis: report of two cases with a discussion of the literature. Ann Intern Med 13: 1046–1067
10. 10. Libman E, Sacks B (1924) A hitherto undescribed form of valvular and mural endocarditis. Arch Intern Med 33: 701–737
11. 11. Keith N, Rowntree L (1922) Study of renal complications of disseminated SLE: a report of 4 cases. Trans Assoc Am Physicians 37: 487–502
12. 12. Klemperer P, Pollack A, Baehr G (1941) Pathology of disseminated lupus erythematosus. Arch Pathol Lab Med 32: 569–631

Discovery

• The history of lupus erythematosus can be divided into three periods: the classical, neoclassical, and modern.
• The word lupus means wolf in Latin, as the destructive injuries the disease caused, brought to mind the bites of this animal. The ancient people used to believe that lupus patients could turn into wolfs especially during the exposure to sunlight. Probably this is as a result of lupus photo-sensitivity.
• Hippocrates firstly used the word "herpes esthiomenos" which was a definition for lupus lesions and thus Hippocrates is considered the first to have described cutaneous ulceration of the disease.
• Rogerius Frugardi (1230 ad) used the term lupus to describe erosive facial lesions for the first time scientifically.
• Then Giovanni Manardi (1530 ad) used the same pattern of ulceration to describe the lower extremity lesions and called it lupus as well.
• A British dermatologist, Robert Willan (1757-1808), described destructive lesions of the face and nose under the heading of lupus. Lupus willani which is the cutaneous tuberculosis or lupus vulgaris is named after him.
• Ferdinand von Hebra described an aggressive skin lesion with tissue destructive characteristics in 1845. Later in 1866, Ferdinand von Hebra used the "butterfly" to describe what is known as malar rash. He named the condition initially as seborrhea congestiva.
• In 1833, Laurent Theodore Biett was the first one to describe lupus erythematosus, although he called it erythema centrifugum. Later his student, Pierre Louis Alphee Cazenave, published Biett's work.
• Cazenave described discoid lupus completely and called it "lupus erythematosus" disease, as a rare condition in 1851.
• In 1872, Kaposi was the first to describe the systemic signs of the disorder including arthritis, fever, anemia, lymphadenopathy, and weight loss.
• Kaposi and Cazenave were the first ones that clearly distinguished lupus erythematosus from lupus vulgaris or cutaneous tuberculosis, although both disease coexistance in some patients had led to a lot of confusion that time.
• Sir William Osler was the first to coin the term systemic lupus erythematosus. He discussed visceral complications of “erythema exsudativum multiforme” include cardiac, pulmonary, and renal problems as well as cutaneous lesions.
• Jonathan Hutchinson^{[[null 11],[null 12]]} was the first to describe the photosensitive nature of the malar rash.
• In 1902, Sequira and Balean were the first to describe acroasphyxia, or Raynaud phenomenon, and lupus nephritis.
• In 1908, Alfred Kraus and Carl Bohac were the first to describe pulmonary involvement in lupus.
• In 1923, Emanuel Libman and Benjamin Sacks were the first to describe noninfectious endocarditis due to lupus.
• George Belote and H.S. Ratner were the first to describe endocarditis of Libman-Sacks was a manifestation of the disease even without cutaneous involvement. They changed the common idea of the necessity of cutaneous involvement for the diagnosis of lupus.
• In 1935, Paul Klemperer, George Baehr, and A.D. Pollack were the first to describe wire loop nephritis.
• In 1959, Leonardt, Arnett, and Schulman were the first to describe the familial aggregation of lupus and concordance in monozygotic twins.

Landmark Events in the Development of Treatment Strategies

• In [year], [scientist] was the first to discover the association between [risk factor] and development of [disease].
• In 1906, Wasserman was the first to describe a complement-fixing antibody that reacted with extracts from bovine hearts while trying to develop a serologic test for syphilis. The corresponding antigen which later was identified as cardiolipin.
• In 1948, Malcolm Hargraves discovered the LE cell. He observed two unusual phenomena in several bone marrow preparations while adding the serum from patients with lupus erythematosus to bone marrow preparations from normal subjects.
• In 1954, Miescher and Fauconnet observed that absorption of lupus serum with nuclei prevented its ability to induce the LE cell phenomenon, suggesting that a globulin in the serum was reacting with, or destroying, the nuclei.
• in 1958, George Friou discovered that the substance in the serum of patients with lupus erythematosus that reacted to the nuclei of cells was gamma globulin. He also discovered that the target in the nucleus was DNA complexed to histones. He described the indirect immunoflourescence test to detect antinuclear antibodies. Autoantibodies like nuclear ribonucleoprotein (nRNP), Sm, Ro, La, and anticardiolipin antibodies were discovered based on his primary works.
• In 1954, researchers at the Cleveland Clinic were the first to describe drug-induced lupus erythematosus with the antihypertensive drug, hydralazine.
• In 1971, the first classification criteria for systemic lupus erythematosus were established that required 4 of 14 criteria.
• In 1982, the criteria were revised by the American College of Rheumatology (ACR) to add the new advances in serologic testing (ANA and anti-dsDNA) and improved biostatistical techniques.
• In 2012, the Systemic Lupus Collaborating Clinics (SLICC) revised and validated the American College of Rheumatology (ACR) SLE classification criteria in order to improve clinical relevance, meet stringent methodology requirements and incorporate new knowledge in SLE immunology.

Impact on Cultural History

In 1959, a breakthrough in the understanding of lupus was happened by the discovery of a lethal kidney disease in Otago Medical School in New Zealand. It provided many insights of disease mechanisms in imunopathogenesis of autoantibody formation, immunologic tolerance, and the development of glomerulonephritis in lupus as well. It also led to better evaluation of newer therapeutic agents in lupus erythematosus.