A Historical Approach to Hereditary Spastic Paraplegia

r e v u e n e u r o l o g i q u e 1 7 6 ( 2 0 2 0 ) 2 2 5 – 2 3 4 Available online at ScienceDirect www.sciencedirect.com History of Neurology A historical approach to hereditary spastic paraplegia O. Walusinski Private practice, 20, rue de Chartres, 28160 Brou, France i n f o a r t i c l e a b s t r a c t Article history: Hereditary spastic paraplegia (HSP) is a group of rare neurological disorders, characterised Received 12 August 2019 by their extreme heterogeneity in both their clinical manifestations and genetic origins. Received in revised form Although Charles-Prosper Ollivier d’Angers (1796–1845) sketched out a suggestive descrip- 25 November 2019 tion in 1827, it was Heinrich Erb (1840–1921) who described the clinical picture, in 1875, for Accepted 26 November 2019 ‘‘spastic spinal paralysis’’. Jean-Martin Charcot (1825–1893) began teaching the disorder as a Available online 3 January 2020 clinical entity this same year. Adolf von Stru¨mpell (1853–1925) recognised its hereditary nature in 1880 and Maurice Lorrain (1867–1956) gained posthumous fame for adding his Keywords: name to that of Stru¨mpell and forming the eponym after his 1898 thesis, the first review Hereditary spastic paraplegia covering twenty-nine affected families. He benefited from the knowledge accumulated over Weakness a dozen years on this pathology by his teacher, Fulgence Raymond (1844–1910). Here I Motor neuron disease present a history across two centuries, leading to the clinical, anatomopathological, and Neurodegeneration genetic description of hereditary spastic paraplegia which today enables a better unders- Stru¨mpell-Lorrain syndrome tanding of the causative cellular dysfunctions and makes it possible to envisage effective History of neurology treatment. # 2019 Elsevier Masson SAS. All rights reserved. degeneration) causes, or those secondary to nutrient deficien- 1. Introduction cies. We start with a discussion of how a hereditary pathology, referred to as spastic paraplegia, was recognised, notably by Spastic paraplegias are a large group of rare inherited Adolf von Sru¨mpell in 1886. neurological disorders that share the primary symptom of walking difficulties due to muscle weakness and muscle 2. Foundations: 1820–1876 tightness in the legs. As for other diseases of the nervous system, they were described throughout the 19th century, mainly in France, England and Germany. Benefiting from Reading the thesis of Antoine-Barthe´le´my Clot, known as advances in the understanding of medullary physiology, Clot-Bey (1793–1868), defended on 24 July 1820 and entitled clinicians gradually learned to identify the various causes of Recherches et observations sur le spinitis ou inflammation de la spinal cord diseases, including infectious (tuberculosis, syphi- moelle e´pinie`re (Research and observations on spinitis or lis), vascular, carcinogenic, and structural (syringomyelia, inflammation of the spinal cord) [1], one cannot help but E-mail address: [email protected]. https://doi.org/10.1016/j.neurol.2019.11.003 0035-3787/# 2019 Elsevier Masson SAS. All rights reserved. 226 r e v u e n e u r o l o g i q u e 1 7 6 ( 2 0 2 0 ) 2 2 5 – 2 3 4 agree with the comments of Charles-Prosper Ollivier d’Angers For Charcot, this condition points to ‘‘an undeniable (1796–1845) in the introduction to his own thesis, entitled Essai organic substratum, an anatomical lesion at a more or less sur l’anatomie et les vices de conformation de la moelle e´pinie`re chez deep location in the spinal cord. It is also certain that this l’Homme (Essay on the anatomy and conformational defects of lesion specifically affects the lateral spinal tracts’’; he had the spinal cord in humans) [2]. Ollivier d’Angers argued that previously referred to ‘‘symmetrical and primitive sclerosis of ‘‘most spinal cord diseases were observed by physicians in antiquity the lateral tracts of the spinal cord’’ [11]. The clinical [Hippocrates and Galen]; this aspect of pathology has remained manifestations enabled him to eliminate amyotrophic lateral more or less the same since that time’’. In 1818, John Abercrombie sclerosis, ‘‘common transversal myelitis’’, and multiple (1780–1844) in Edinburgh published Observations on the Diseases sclerosis. The absence of searing pain, motor incoordination, of the Spinal Marrow [3]. He also limited himself to describing amblyopia, and so forth also eliminated the diagnosis of ‘‘the inflammation of the spinal marrow’’ and ‘‘the softening of the locomotor ataxia as described by Guillaume Duchenne de spinal cord’’, disturbances which seem to have been infections, Boulogne (1806–1875). Charcot used this lesson to teach his probably syphilitic or vascular conditions. students ‘‘spontaneous or provoked tremor’’: brought about Ollivier d’Angers can be considered a pioneer in his attempt ‘‘by raising the front tip of the foot or the ends of the toes’’. to comprehensively understand the embryology, anatomopa- Unlike Erb, he did not observe any sensory disturbances. With thology, and nosology of spinal pathologies on the whole [4]. his gift of expression, he described the difference between this Among other coinages, we owe him the word ‘‘syringomye- tabes and ataxia as follows: ‘‘In spasmodic tabes there are not lia’’, even though he did not really describe the disease [5]. these excessively flexible limbs, sometimes seeming disloca- After defending his thesis on 12 June 1823, he published an ted, which give the ataxic’s gait its special hallmark’’. Finally, expanded version in 1827, a true treatise on spinal cord the inexorable ascending progression, with muscular trophi- diseases [6] that was further expanded and published in a new city maintained, completed the clinical picture described by edition in 1837 [7], making the French translation of Charcot, who, in December 1875, did not indicate the age of Abercrombie’s book by Augustin-Nicolas Gendrin (1796– onset or the role of heredity, even though heredity was, 1890) obsolete when it was released in 1832. according to him, the cause of most diseases affecting the In the section on chronic myelitis, Ollivier d’Angers nervous system. presented a clinical picture suggestive of spastic paraplegia: As was his habit for subjects under exploration but not ‘‘These patients have a characteristic gait: they struggle to lift totally elucidated, Charcot suggested to one of his students, their foot from the ground, and in their effort to lift it entirely Isidore Be´tous (1852–?), who was from Caupenne d’Armagnac and move it forward, their trunks straighten and are thrown in southwest France and would go on to work in the Bare`ges back, as if to offset the weight of the lower limb, which shakes thermal treatment centre [12], that he use this topic for his involuntarily before it is returned to the ground. In this thesis. On 18 May 1876, Charcot presided over the defence of progression, the front tip of the foot can be either lowered, the thesis [13], entitled E´ tude sur le tabes dorsal spasmodique. dragging more or less against the ground before lifting from it, Based on four detailed observations, Be´tous presented the or raised suddenly at the same time the foot bends toward the clinical information exactly as Charcot did in his lesson, outside [. .]. When the paralysis has existed for some time, highlighting the differential diagnostic criteria for locomotor ordinarily the affected limbs stiffen and retract little by little, ataxia and multiple sclerosis. His view of the prognosis was remaining in a permanent contraction that it is difficult to rather positive, given the very slow and long progression. As overcome’’. none of the four patients had died, Be´tous made no In a December 1875 lesson, Jean-Martin Charcot (1825– anatomopathological argument to support Charcot’s hypo- 1893) reviewed this initial clinical description that he taught thesis of lateral column damage. The following year, Erb under the term ‘‘spasmodic dorsal tabes’’ [8]. The word ‘‘tabes,’’ added nineteen other purely clinical observations, still meaning ‘‘disintegrate’’ in Latin and a synonym of ‘‘phthisis’’ awaiting anatomopathological confirmation of localisation in Greek, was purely descriptive of the macroscopic appea- in the lateral column [14]. After these publications and until rance of the spinal cord and gave no indication of aetiology. World War I, the eponym ‘‘Erb-Charcot paralysis’’ was in Charcot credited his German alter-ego in Heidelberg, Heinrich current use, replacing spastic spinal paralysis, but was most Erb (1840–1921), with the initial term ‘‘spinalen Symptomencom- often used incorrectly to refer to a rare form of neurosyphilis. plex’’ and with the complete description shortly before Charcot had nonetheless clearly indicated that spasmodic Charcot’s lesson [9]. Based on sixteen observations he had dorsal tabes was ‘‘fundamentally distinct from all other forms of compiled, Erb baptised as ‘‘spastischen Spinalparalyse’’, or chronic myelitis’’. ‘‘spastic spinal paralysis’’, a gradually progressing association of symptoms with ‘‘growing weakness in the lower limbs, later 3. Doubts and uncertainties: 1880–1885 invading the upper limbs [. .]. There are multiple spasmodic phenomena which consist in more or less pronounced rigidity of the limbs with spontaneous jerking, tonic contractions, initially In 1883, Adrien Proust (1834–1903) identified ‘‘spasmodic spinal temporary, and clonic shaking in the lower limbs [. .]. Their gait is lathyrism’’, after having observed, while travelling, an hesitating and slightly vacillating. The soles of the feet stick to the epidemic of spasmodic paraplegia ‘‘in an indigenous popula- ground and the patient drags his leg as he walks, which he does with tion’’ that he linked to the consumption of a supposedly toxic small steps, keeping the legs held closely together. The front tip of the plant (lathyrus cicera) following a famine in Kabylia. His foot collides with the slightest obstacle [. .]. The tendon reflexes are colleague at the Acade´mie de Me´decine, Alfred Le Roy de almost always exaggerated’’ [10].

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