Neurological examination: pioneering authorsand their booksExame neurológico: autores pioneiros e seus livros
Péricles Maranhão-Filho1,2, Maurice Borges Vincent1, Marcos Martins da Silva1
ABSTRACTThe objective of this article is to highlight some of the most important pioneering books specifically focused on the neurologicalexamination and their authors. During the XIX Century, Alexander Hammond, William Gowers and Charles Mills pioneered the neurologicalliterature, followed in the XX Century by Aloysio de Castro, Monrad-Krohn, Derek Denny-Brown, Robert Wartenberg, Gordon Holmes, andRussel DeJong. With determination and a marked sense of observation and research, they competently developed and spread thetechnique and art of the neurological exam.
Keywords: neurologic examination, textbooks, semiology.
RESUMOO objetivo deste artigo é destacar alguns dos primeiros e mais importantes livros-texto interessados em difundir o ensino do exameneurológico e seus autores. Durante o século XIX, Alexander Hammond, William Gowers e Charles Mills foram pioneiros na literaturaneurológica, seguidos por Aloysio de Castro, Monrad-Krohn, Derek Denny-Brown, Robert Wartenberg, Gordon Holmes e Russel DeJong noséculo XX. Com determinação, grande senso de observação e pesquisa, eles competentemente disseminaram a técnica e a arte de serealizar o exame neurológico.
Palavras-chave: exame neurológico, livros-texto, semiologia.
Although the case history generally remains as the mainsource of data for a proper diagnosis, the neurological exam-ination (NE) as we know today is a critical element in clin-ical practice. The NE is based on a systematic sequence ofmaneuvers specifically conceived to highlight dysfunctionsin various parts of the nervous system. The XIX and thebeginning of the XX Centuries were particularly fruitful forthe settlement of the NE, when seminal textbooks on thesubject were published. We herein highlight some of thesepioneer books and comment on their authors.
J. M. Charcot (1825-1893), the father of modern neuro-logy1, applied the clinical-pathological method by correlatingsigns and symptoms to morbid anatomy, but there is sparseliterature about how he would perform the NE. The lack ofdocumentation is probably related to the fact that the NEwas not systematized at the time2 and rather based onobservational analysis of selected phenomena3. The NEdeveloped significantly after him as the following generation
of physicians incorporated his findings and progressivelydeveloped a systematic approach.
The written neurologic teaching emerged during the XIXCentury. Four books, three published in London and one inGermany, were seminal in the initial development of neuro-logy: "A Treatise on the Nervous Diseases" by John Cooke in1820, "The Nervous System of the Human Body" by CharlesBell in 1830, "Lectures on the Nervous System and itsDiseases" by Marshall Hall in 18364,5 and Lehrbook derNervenkrankheiten des Menschen (“A Manual of NervousDiseases of Man”) by Moritz Romberg in 1840. Romberg’swork was the first neurology textbook to be considered pro-foundly influential, not only in Germany but also in UnitedKingdom, after its translation, in 1853, by E. H. Sieveking6,one of the first physicians at Queen Square. TwoAmericans, Alexander Hammond and Charles Mills, and aBritish author, William Gowers, should also be honored aspioneers in publishing neurology books.
1Universidade Federal do Rio de Janeiro, Faculdade de Medicina, Hospital Universitário Clementino Fraga Filho, Departamento de Clínica Médica, Rio deJaneiro RJ, Brazil;2Instituto Nacional de Câncer do Rio de Janeiro, Hospital do Câncer, Rio de Janeiro RJ, Brazil.
Correspondence: Péricles Maranhão-Filho; Av. Prefeito Dulcídio Cardoso, 1680/1802; 22620-311 Rio de Janeiro RJ, Brasil;E-mail: [emailprotected]
Conflict of interest: There is no conflict of interest to declare.
Received 07 January 2014; Received in final form 07 October 2014; Accepted 27 October 2014.
DOI: 10.1590/0004-282X20140215
VIEWS AND REVIEWS
140
William Alexander Hammond (1828-1900), a generalsurgeon at the United States Army, was the first Americanto devote himself full-time to neurology. Hammond wasdescribed as, “a dominant personality in any field heentered, attracting a following and developing active enem-ies”7, 8. His theatrical behavior, large build and powerfulspeaking ability attracted much attention. Originally fromMaryland, he moved with his parents to Pennsylvania atage of five, where he lived until starting medical school. Hereceived his MD from the University of the City of NewYork at the age of twenty. In 1849, he entered the U.S.Army as an assistant surgeon where he worked for elevenyears. He participated in several campaigns against Indiansin New Mexico and Kansas. In 1860, Hammond resignedhis military post to become in charge of the anatomy andphysiology departments at the University of Maryland’smedical school. However, he would rejoin the army in1861 to participate in the civil war. After the war, his careerremained active and he became a professor of nervous andmental diseases at several medical schools. Neurology was anew specialty, and Hammond became a pioneer in the field8.
Mainly based on his observations, clinical investigations,and Charcot texts, he published his “Treatise on Diseases ofthe Nervous System” in 1872. A sixth edition was publishedin 18769 (Figure 1). With 750 pages divided into 42 chapters,Hammond created the first concise and explicit neurologicaltextbook in the English language. He introduced his treatisewith a thorough description of instruments used for the dia-gnosis and treatment of neurological diseases and aspects ofthe NE directly related to these tools. At a cost of $4.00,Hammond’s textbook was enthusiastically received by mostof his peers, but unfortunately he did not discuss the neuro-logical examination in a systematic way4.
Sir William Richard Gowers (1845-1915), was born inHackney, England, now a suburb of London, in his father’scobbler shop. Gowers lived in dire poverty as a child dueto the death of his father when he was 1110. He was awardedthe MD degree with a Gold Medal from the University ofLondon in 1870 and spent nearly his entire career at theNational Hospital for the Paralyzed and Epileptic in QueenSquare, London. Gowers not only helped define the modern
neurological examination, but also made epochal contribu-tions to our knowledge of many diseases11. In 1888 Gowerssimultaneously published American and English editions of“A Manual of Diseases of the Nervous System”12 (Figure2), containing descriptions of neurological diseases as wellas methods to examine muscular strength, coordination,sensory perception, tone, tremor, reflexes, actions of indi-vidual muscles, and cranial nerves. His book was publishedin two volumes - the first, dedicated to the study of spinalcord diseases, was immediately acclaimed as the “Bible ofNeurology”13. Spillane (1891) suggested that it should beconsidered as the neurology “new testament”14. In thissuperb text regarding an extensive range of topics, Gowersused a highly descriptive prose and included definitive linedrawings made by himself.
Charles Karsner Mills (1845-1931), was born at the Fallsof the Schuylkill River, a suburb of Philadelphia. He gradu-ated from the Central High School in 1861. After interruptinghis education by volunteering to fight for the Union in thedeadly Civil War battles at Bull Run and Gettysburg, he grad-uated from the University of Pennsylvania medical school in1869. Mills was appointed Professor of Nervous and MentalDisease at the same University in 1893 and Professor ofNeurology in 19019. In 1898, just after he had published“The Nervous System and Its Diseases, a Practical Treatiseon Neurology for the use of Physicians and Students”14
(Figure 3) – 1056 pages which became known as the lastimportant American textbook on neurology of the XIXCentury and the first formal and comprehensive review ofthe NE – Mills was struck by a bicyclist and had the retinaedetached. Despite his poor vision, he had an extraordinaryauditory memory that he used to recall almost verbatimthe contents of journals and books that his friends read tohim. Mills died of acute pulmonary edema on the day hewas to present a paper at the American NeurologicalAssociation.
During the XX Century, six main authors disseminatedand expanded the knowledge on the NE through carefullydrafted textbooks (Table).
A Brazilian author deserve consideration. Born in Rio deJaneiro, Aloysio de Castro (1881-1959) was a physician,teacher, writer, literary critic, poet and musician. He joined
Figure 1. William Alexander Hammond and the first page of his1872 book.
Figure 2. Sir William Richard Gowers and the first page of thesecond volume of the first edition of his 1888 book.
Péricles Maranhão-Filho et al. Pioneering authors and their books 141
the Faculdade de Medicina da Universidade Federal do Rio deJaneiro in 1898 and until the 4th year was a student of hisfather, Francisco Castro, also a physician and professor,known as the "Divine Master." Aloysio graduated at age2215. His 232 pages graduation thesis entitled DasDesordens da Marcha e seu Valor Clínico (1904)16 (“GaitDisorders and Their Clinical Value”) (Figure 4), revealedhis talent as a great scientist and exceptional writer, repre-senting a real innovation in both form and content as com-pared to contemporary medical texts.
For emerging as the best student in his class and com-pleting medical school with honors, the College ofMedicine council awarded him a trip abroad in order toimprove their knowledge. In May 1906 he arrived in Parisand was presented to Pierre Marie, at that time consideredthe best neurologist alive. His training took place mainly inHôpital Bicêtre and involved neurology, pathology, and clin-ical practice17,18,19.
Upon his return to Brazil, de Castro worked in the SantaCasa de Misericórdia do Rio de Janeiro and as Chief ofInternal Medicine at Policlínica Geral do Rio de Janeiro,where he created the first outpatient clinic where studentscould observe his work. He also innovated in the studyand dissemination of medical education by filming patients.De Castro produced 130 movies of neurological diseaseswith a primary focus on gait and movement disorders18.
In 1914 he published the "Tractado de Semiotica Nervosa"19
(Figure 4), the first Brazilian book completely focused on NE.He thus introduced the local medical iconography using
photography (not drawings) and excerpts from movies. In thesame year he was elected dean of the school of medicine. In1935 he re-edited his book, revised and enlarged under thetitle "Semiotica Nervosa"20. Although Professor Aloysio deCastro dominates other languages including French andEnglish, his thesis and the books were published only inPortuguese. Therefore, his work did not produce internationalimpact it deserved.
Georg Herman Monrad-Krohn (1884-1964) was a Nor-wegian neurologist trained at the Queen Square Hospital inLondon. He wrote the first book on clinical examination ofthe nervous system in Norway, published in Oslo in 1914.The English-language edition – "The Clinical Examination ofthe Nervous System" – edited by H.K. Lewis & Co, LTD., wasreleased in London in 192121.
The idea of the book was to present a comprehensiveapproach to the NE through a method based on examina-tion of the functional status followed by anatomic and aeti-ological diagnosis. The book, known as the "Blue Bible" or"Blue Book of Neurology," as Norwegian students called it,was reprinted 12 times and translated into many languages.The translation of the eleventh edition22 (Figure 5), co-authored with Professor Sigvald Bernhard Refsum, whor*placed Monrad-Krohn as Chair in the direction ofNeurology University of Oslo, has 16 chapters spread over500 pages containing dozens of interesting footnotes andan appendix in which he addresses various forms of specificclinical approaches such as aphasia, diplopia, vestibulartests, loss of consciousness, etc., and electric exams. Thebook concludes with discussion over simulator neurologicalexaminations22. Refsum developed a reputation as talentedlecturer able to improvise virtually any speech, a skillactually trained to exhaustion in a detailed way (OttarSjaastad, personal communication to MBV).
The Blue Bible offers a detailed description of a detailedNE and highlights important topics such as the dissociationof emotional mimicry in central facial paresis and cutaneousabdominal reflexes (while training in Queen Square Hospital,Monrad-Krohn completed a thesis on the abdominal reflex).
Figure 3. Charles K. Mills and the first page of his 1898 book.
Figure 4. Aloysio de Castro, the first pages of his MDconclusion Thesis (1904) (left), and the 1st Edition of his book1914 (right).
Figure 5. Monrad-Krohn, the “Blue bible”. Front page (left), andthe first page of this eleventh edition book translation 1967(right).
142 Arq Neuropsiquiatr 2015;73(2):140-146
In addition, the author calls attention to an unusualresponse not previously cited in the static equilibrium test:"Some neurotic patients, mostly very thin women with atendency to hypochondria, imbued by an absurd horror oflosing their balance, generally fall during the currentRomberg test towards the physician performing the test inorder to lean on them for support (though sometimes for dif-ferent reasons!)". Monrad-Krohn consider the examination ofsensory perception as the hardest part of the NE and suggesta technique difficult to be applied today: “(...) to get a generalidea at first glance, then conducting a closer examination ona second opportunity, for example, the next day when thepatient is quiet (...)”.
Derek Ernest Denny-Brown (1901-1980) was born andwent to medical school in New Zealand. During his medicalschool years from 1919 until 1924 he was particularly stimu-lated by anatomy and physiology. After graduation hereceived an appointment as Beit Memorial Fellow forMedical Research, which permitted him to spend three yearsin Sir Charles S. Sherrington laboratory’s in Oxford, England25.In December 1928, Denny-Brown became a Resident MedicalOfficer at the National Hospital, Queen Square, London, wherehe completed his neurology training. Dr. Denny-Brownfound himself amid a number of superb clinicians and tea-chers, including Kinnier Wilson, Gordon Holmes, CharlesSymonds, James Collier, and Francis Walshe. He learned hisapproach to clinical neurology from many of these indivi-duals, but particularly from Charles Symonds and GordonHolmes25. Next he moved to America and became directorof the Neurological Unit at Boston City Hospital andJames Jackson Putnam professor of neurology at Harvard.With the support and advice of Raymond Adams andHarry Kozol he published the “Handbook of NeurologicalExamination and Case Recording” in March 1942, a privateprinting for the Neurological Unit. This small wire-boundbooklet went through three editions. The 1942 edition wasreprinted in 195226 (Figure 6). This extremely useful text, con-taining 11 chapters in 108 pages but less than 10 references,has been used widely throughout the United States andabroad as a beginner’s guidebook to the neurologic examina-tion. Seventy years ago, in Friday October 22, 1943, Denny-Brown was in the Medical School Faculty Room, as a reader
of the PhD Thesis entitled "Spreading Depression of Activity inthe Cerebral Cortex” by the Brazilian scientist AristidesAzevedo Pacheco Leão (personal communication from A.A.P. Leão to PM-F).
Denny-Brown was president of the American Neurol-ogical Association. In 1967, he retired from his positionas director of the Neurological Unit at the BostonCity Hospital and took up a post as chief in charge ofthe Section of Neurophysiology and associate director ofthe New England Regional Primate Center25. He studiedthe effects of sectioning dorsal roots in apes27 and continuedhis interest in dystonia, describing abnormal postures fromlesions of the basal ganglia and cerebral cortex in infant pri-mates. In 1972, he became a Fogarty Scholar in Residence atthe National Institutes of Health for one year and thenentered a phase of semi-retirement. Denny-Brown was pro-foundly influenced by Sir Charles Sherrington and GordonHolmes8. He died at the age of 79 from complications of mul-tiple myeloma at his home in Cambridge, Massachusetts25.
Robert Wartenberg (1887-1956) was born in the RussianEmpire and graduated in Germany. In 1933, he was head ofthe neurological clinic at Freiburg. Persecuted by the Nazis,he left Germany and settled in USA in 1953. Wartenberg wasappointed clinical professor of neurology at the University ofCalifornia, San Francisco21. He was considered an outstand-ing teacher, book reviewer/critic, and editor who despisedmediocrity. In 1945 published “The Examination of Reflex:A Simplification” (reprinted in 1946) (Figure 7)28. With anintroduction by Foster Kennedy and the preface byWartenberg himself, the book highlights the reflexes as beingthe most important part of the NE. The exquisite book has222 pages, only seven figures, and 465 excellent references.After nearly 70 years from publication, no other book rivalsits depth and clarity on this issue. In 1953 he released“Diagnostic Tests in Neurology: A Selection for Office Use”,reprinted in April 195429 (Figure 7). The “ diagnostic tests” listmaneuvers that easily applied at bedside. The audience wassaid to be general practitioners, although Holmes clarified in
Figure 6. Derek Denny-Brown and the cover of his book, 1942edition, reprint in 1952.
Figure 7. Robert Wartenberg. The front page of his ReflexExamination book 1945, reprinted 1946 (left), and the cover ofhis Diagnostic Test book, English 1953 edition, reprinted in U.S.A., 1954 (right).
Péricles Maranhão-Filho et al. Pioneering authors and their books 143
the foreword that the book would be useful for neurologists aswell. In 228 pages, Wartenberg exalts the importance and sub-tlety of the various signals present in patients with neuro-logical ailments, like the precocity and longevity of absentlid vibration in cases of peripheral facial palsy, the arm stretch-ing in lesions of the spinal nerve, and the trick to palpate thetendons hypotonia in cases of peripheral nerve injury. He bril-liantly explores the diagnostic possibilities in relation to thedeep and superficial abdominal reflexes alterations. The book,containing two indexes – a general one and other specialbased on the morbid condition and its pertinent bedside tests– was translated into several languages, and went throughthree editions in German (one in English). Another exampleof his didactic and writing abilities may be found in the firstissue of the Neurology journal ( January 1951), whereWartenberg publishes the article "Pendulousness of the Legsas a Diagnostic Test"30, showing elegantly how to draw severalconclusions concerning the pendulum movements from thesimple act of lifting and dropping the leg in a sitting extrapyr-amidal rigidity patient.
Gordon Morgan Holmes (1876-1965), was born in afamily line of protestant farmers at Castlebellingham,Louth County, Ireland9,23. He studied medicine in Dublinand graduated from the Trinity College in medicine at age23. He then spent two years doing research with Edingerand Weigert in Frankfurt21. Holmes went to London in1903 and completed his neurological training as AssistantHouse Physician at National Hospital, Queen Square,where he worked for Hughlings Jackson24. He eventuallybecame Physician and Director of research at the NationalHospital, consultant to the British Expeditionary Force inWorld War I, and editor of the journal Brain between 1922and 1937. Holmes was remembered as a big man with blackcurly hair, dark black eyes and a thick moustache, and wasknown for his remarkable bedside teaching ability.Macdonald Critchley noted “He could coax physical signsout of a patient like Paganini on the violin”24.
With Grainger Stewart he described the rebound phenom-enon in cerebellar diseases (Stewart-Holmes Symptom). WithW. J. Adie he established the myotonic, or Holmes Adie,pupil. Holmes’ Syndrome is a hereditary degenerative cerebel-lar ataxia involving the olivary nucleus23.
Gordon Holmes, more than any other individual, wasresponsible for the form of the NE as it is now performed;and his insights are fundamental to the way that, nowadays,we think about vision, somato-sensory function, the spinalcord and the cerebellum24,31,32.
Holmes distilled the essence of his teaching at theNational Hospital in his classic 1946 book “Introduction toClinical Neurology”, laying down the foundations of themodern NE. The last of three editions, with 187 pages and21 chapters32, and revised by Bryan Matthews, was publishedin 1968 and reprinted in 1971 (Figure 8). The writing style is
elegant and sober and the figures are simple diagrams. Hisaccount of the mental state exam is clear and succinctand provides a useful framework even by modern’s stan-dards. In a section on suggestibility (page 179), he says “evennormal persons are suggestible; any one can walk along aplank lying on firm ground, but may be unable to do sowhen it spans an abyss”. Two curiosities are queer in thisbook: First, there are no references; second, although thereare five pages on the vestibular system in the Appendix,when he describes “a scheme for the clinical investigationof the function of the nervous system,” there is no mentionof the vestibulocochlear nerve examination.
Russell Nelson DeJong (1907-1990) has been associatedwith the University of Michigan since he enrolled as anundergraduate in 1925. He then also attended medicalschool, postgraduate training, and worked at the universityuntil he became Chairman of the Department ofNeurology in 195034. He was president of the AmericanBoard of Psychiatry and Neurology, and the AmericanNeurological Association33. He was also editor of the YearBook of Neurology since 1969 and has served with numerousgovernmental, professional, and voluntary health agencies.Since the beginning, and for 26 years thereafter, DeJongwas editor of the Neurology, where he heavily influencedneurology in the U.S.A.34,36.
In 1950 he published his massive 1,079 pages “TheNeurologic Examination”35 (Figure 9). The book divided in10 parts, is based on lectures on the NE given to studentsin the University of Michigan Medical School. Already onthe first page the reader comes across a famous quote from
Figure 8. Sir Gordon Holmes and the first page of his book,third edition (1968), reprinted in 1971.
Figure 9. Russel N. DeJong and his first edition book (1950).
144 Arq Neuropsiquiatr 2015;73(2):140-146
William Osler; “To study the phenomena of disease withoutbooks is to sail an uncharted sea, while to study books with-out patients is not to go to sea at all.” In the preface, DeJonghimself emphasizes the importance of neuroanatomy andneurophysiology for an adequate understanding of diseasesof the nervous system.
Part one concerns the place and importance of neurologicevaluations in the general field of medicine, and contains adiscussion of anamnesis and testing of the mental status.Part Five talks about a few reflexes indicative of damage inthe basal ganglia, which are not currently surveyed. PartTen is on examination of the spinal fluid. The book has anextensive reference list, and unlike prior NE books, containsa detailed chapter with 27 pages on the exam of patients witheither hysteria or malingering. In 1992 this textbook wasrenamed “DeJong’s The Neurologic Examination”33. This iscertainly the most read neurological examination book inthe Western world. The most recent edition, the seventh,was revised by William W. Campbell and published in 201337.
In conclusion, it is worth questioning what these unforget-table authors possessed in common, besides, of course, a pas-sion for neurology and a delicate, precise, and detailed fineNE. First, all have sought the opportunity of a great education,
lived and followed masterful examples of good and outstand-ing medical scientists. As their professors, they were excellentand careful observers. Second, they persist on the path ofbelief in the purest science, always seeking the truth despitenumerous vicissitudes such as political persecution and wars.The authors mentioned herein have made history and provideus with some of the most relevant contributions to the neuro-logic examination.
Many other authors such as Bordas, Austregesilo,Mumenthaler, Gardner and Lassek wrote magnificent booksdealing with neurophysiology38, clinical neurology38,39,40,41,and specific neurological aspects40,42, but since their mainfocuses were not the systematization of the neurologicalexamination they were not included in the present review.For the same reason, later authors that contributed to thisfield but did not pioneer the establishment of a neurologicalexamination were also excluded.
Acknowledgement
The authors are in debt with Péricles Maranhão Neto forhis technical assistance.
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Table. Pioneering textbooks on neurological examination and their authors.
Title Author 1th Edition
A treatise on the nervous diseases* John Cooke (1756–1838) 1820The nervous system of the human body* Charles Bell (1774 –1842) 1830Lectures on the nervous system and its diseases* Marshal Hall (1790-1857) 1836Teaching book of nervous diseases of man* Moritz Romberg (1795-1873) 1840Treatise on diseases of the nervous system William Hammond (1826-1900) 1872A manual of diseases of the nervous system William Gowers (1845-1915) 1888The nervous system and its diseases, a practical treatise onneurology for the use of physician and students
Charles Mills (1845-1931) 1898
Tractado de semiotica nervosa Aloysio de Castro (1881-1959) 1914Clinical examination of the nervous system Monrad-Krohn (1884-1964) 1921Handbook of neurological examination and case recording Derek Denny-Brown (1901-1980) 1942The examination of reflex a simplification Robert Wartenberg (1887-1956) 1945Introduction to clinical neurology Gordon Holmes (1876-1965) 1946The neurologic examination Russel N. DeJong (1907-1990) 1950Diagnostic tests in neurology: a selection for office use Robert Wartenberg (1887-1956) 1953
* Only mentioned in text.
Péricles Maranhão-Filho et al. Pioneering authors and their books 145
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12. Gowers WR. A manual of diseases of the nervous system.Philadelphia: P. Blakiston; 1888.
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25. Gilman SD. Denny-Brown 1901-1981. Neurology. 1982;32(1):1-6.
26. Denny-Brown D. Handbook of neurological examination and caserecording. Cambridge: Massachusetts Harvard University Press;1952.
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28. Wartenberg R. The examination of reflexes a simplification. Chicago:Year Book; 1946.
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38. Bordas LB. Neurologia fundamental. Barcelona: Kalimax; 1973.
39. Austregesilo A. Clínica neurológica. Rio de Janeiro: Francisco Alves;1917.
40. Mumenthaler M, Schliack H. Patologia de los nervios periféricos:diagnóstico y tratamiento. Barcelona: Toray; 1976.
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