NI FEATURE: JOURNEY THROUGH THE EONS – COMMENTARY Year : 2017 | Volume : 65 | Issue : 2 | Page : 245-249 DEEP TENDON REFLEX: THE BACKGROUND STORY OF A SIMPLE TECHNIQUE Kalyan B Bhattacharyya (1) Amrapali Point, Flat 1C, 59F, Bosepukur Road, Kolkata - 700 042, West Bengal India Abstract Wilhelm Erb and Carl Otto Westphal from Prussia first described the knee jerk in the same issue of the journal Archiv für Psychiatrie und Nervenkrankheiten in January 1875. This article retraces the history of development of 'deep tendon reflex' as an integral clinical sign during every neurological examination. The history of the evolving shapes of the reflex hammer, the iconic trademark and the ultimate signature of a neuroscientist, is also presented. Keywords: Clinical signs in neurology deep tendon reflex, history, reflex hammer Citation : Bhattacharyya KB. Deep tendon reflex: The background story of a simple technique. Neurol India [serial online] 2017 [cited 2019 Sep 28];65:245-9. Available from: http://www.neurologyindia.com/text.asp?2017/65/2/245/201824 Elicitation of a tendon jerk is essentially a form of reaction to percussion. This method was first used in clinical medicine by Leopold Auenbrugger of Vienna (1722–1809) in the year 1761 by tapping lightly on the chest and listening to the sound that was produced. He got this idea from his father's hotel where the wine casks in the cellar were tested in this manner to know the level to which they were full. In this manner, he could finally determine, with reasonable success, the outline of the heart in pericardial effusion and wrote an article, “New invention to detect diseases hidden deep within the chest.”[1],[2],[3] In 1826, Pierre Adolphe Piorry (1794–1879) of France placed a small disc on the chest and struck it with the fingers, which was known as a pleximeter.[2] In 1841, Max Wintrich (1812–1882) of Germany popularized a kind of percussion hammer which underwent various changes in form and size,[2] until John Madison Taylor (1855– 1931) of the United States of America popularized it in 1884 with a triangular piece of rubber at one end.[4],[5] In the early 19th century, reflex action was conceived as the manifestation of the active spirit inside an organism.[2] Jan Swammerdam (1637–1680), a Dutch biologist, demonstrated that nerves attached to a muscle were irritable, and Albrecht von Haller (1708–1777), a Swiss anatomist lent credence to the idea that muscles could also be stimulated. Robert Whytt (1714–1766), the esteemed physiologist from Edinburgh, clearly documented the reflex arc and the stretch reflex in 1763. He wrote, ”Whatever stretches the fibres of any muscle so far as to extend them beyond their usual length, excites them into contraction in about the same manner, as if they had been irritated by a sharp instrument, or acrid liquor. The motion of stretching the fibres of any muscle will be greater or less, as the muscle is more or less stretched; unless it be so extended as NI FEATURE: JOURNEY THROUGH THE EONS – COMMENTARY Year : 2017 | Volume : 65 | Issue : 2 | Page : 245-249 quite to lose its paralytic.”[2] tone and become In 1833, Marshall Hall (1790–1857) from England described the reflex as an “excito-motor system” of the spinal cord and nerves after the extirpation of the brain and introduced the term “diastaltic,” referring to the reflex action through the spinal cord.[2] Wilhelm Heinrich Erb (1840–1921) was born in Bavaria and graduated from Munich University in 1864, and trained with Nikolous Friedreich (1825–1882) at the Heidelberg University.[6],[7] In 1875, he sent an article on the knee jerk to the famed journal Archiv für Psychiatrie und Nervenkrankheiten for publication in the January issue. Bernhardt von Gudden (1824–1886), Theodor Meynert (1833– 1892), and Carl Friedrich Otto Westphal (1833–1890), noted neurologists and psychiatrists of Prussia, were the editors of the journal. Westphal reviewed the paper and decided that Erb's paper should be published and he would write an editorial in the same issue. Erb called it the “patellar tendon reflex,” while Westphal used the term “the lower limb phenomenon.”[8] He wrote, ”During the preparation of this essay for publication, I received the preceding manuscript of Professor Erb. To my surprise, I saw that my honored friend was reporting facts that, in part, were virtually identical to those to be published by myself.”[8],[9] Westphal further wrote that he had been aware of the reflex since 1871, while Erb noticed it in 1870 and that the account provided by Erb was in greater detail.[8],[9] It is worthwhile considering how Erb and Westphal were able to speculate that this sign would be relevant to clinical neurology. Erb himself declared with rare candor, ”I believe that I am not saying anything to my colleagues that is startlingly new; most of them are familiar with this phenomenon.'… Already for quite some time, I have noticed in the healthy and especially in the spinal cord-diseased, reflexes in the quadriceps muscle that are striking, and which can be readily and promptly elicited. To me they merit some notice and they seem capable of practical use… They can be elicited by light tapping of the tendon of the quadriceps above or below the patella and best produced from the ligamentum patellae; they certainly indicate an especially intimate and close relation between this tendon and the muscles that are part of it… The literature is completely silent on this… Therefore, I feel justified in a brief note regarding these tendon reflexes… The quadriceps reflex… can be produced as follows: if one firmly holds and supports the leg to be examined, slightly bent at the hip and knee joint… and then lightly and elastically taps the region of the ligamentum patellae with the finger or with the percussion hammer, each tap is immediately followed by a slight but significant and evidently reflex contraction of the quadriceps;… This causes the lower leg to display a marked and often very strong movement… The reflex is particularly striking when one examines a leg which is crossed over the other with the lower leg swinging loosely'[9] Westphal wrote, ”However, one may also bring about this phenomenon in healthy subjects and, as I noted later, laymen are also aware of it as a curiosity… 1871, a patient who consulted me because of motor weakness in a leg and certain cerebral symptoms, informed me that when he sat on a chair and lightly tapped the area below the knee cap of the affected leg, it moved forwards with a sudden jerk. Because the complaints of the patient were sometimes difficult to interpret, one might have been inclined to regard this peculiar symptom as the NI FEATURE: JOURNEY THROUGH THE EONS – COMMENTARY Year : 2017 | Volume : 65 | Issue : 2 | Page : 245-249 outcome of hypochondriacal imagination. However, I easily convinced myself that I was dealing here with a phenomenon that had nothing to do with imagination and which could not be duplicated in the other leg… One taps the ligamentum patellae lightly, but with rapid, brief taps- best done by placing the index finger and the middle finger and letting it fly back with a jerk, or still more effectively with a percussion hammer… one may also produce the same sign in certain cases with the subject in a horizontal bed, that is, with the knee-joint almost completely flexed.”[9] It is noteworthy that Silas Weir Mitchell (1829–1914), of the United States of America demonstrated “a peculiar contraction” produced by a percussion hammer in 1859, 16 years before Erb and Westphal brought the deep tendon jerk to light,[10] and William Gowers named it the knee jerk.[11] Later, the absence of this reflex in tabes dorsalis was named the Erb– Westphal phenomenon,[8] though they differed radically in the interpretation of its pathophysiology. Westphal speculated that the reflex was the result of a direct stimulation of the quadriceps muscle, while Erb felt that it was mediated by a reflex arc.[12] Erb used the term, Patellarsehnenreflex, meaning patellar tendon reflex, in his paper, and his subsequent publications indicate his insight into the fundamental physiological processes, including spinal inhibition, the reflex arc, the sensory and motor neurons, and the excitomotor spinal system in the gray matter; whereas, Westphal's nomenclature, Unterschenkelphänomen, or the lower limb phenomenon, almost reflects an isolated clinical observation in the legs, following irritation of the patellar tendon, having little to do with spinal control mechanisms. However, Westphal did allude to a central influence in his paper but was not clear whether the influence was excitatory or inhibitory in nature, and wrote, “… in a manner that is unknown, certain circumstances arise that facilitate the appearance of the phenomenon.”[9] In 1876, Erb wrote a treatise, Handbuch der Krankheiten des Nervensystems, literally meaning, “Handbook of the Diseases of the Nervous System,” where he elucidated the scientific basis of the physiology of the reflex arc.[13] Erb and Westphal's description was not readily accepted, and in as many as three articles in the celebrated journal Brain in 1878, in the very second year of its publication, there was no mention of this reflex in three clear cases of upper or lower motor neuron lesions, though various other clinical tests were described in detail.[14],[15],[16] However, in 1888, Allan McLane Hamilton (1848–1919), from Queen Square, London, alluded to this sign in an article entitled, “The value of absent tendon reflex as a diagnostic sign in locomotor ataxia, with an analysis of eight cases” and referred liberally to the study of Erb and Westphal; and, Charles Mill, from the University of Pennsylvania wrote an article in 1885, entitled, “Some forms of myelitis, their diagnosis from each other and from hysterical paraplegia,” where he referred to the use of eliciting the knee jerk. He wrote, “Investigations of the reflexes showed the plantar and patellar absent in both legs,….”[17],[18] An interesting work was carried out by Kuban et al., on ten classical deep tendon reflexes in 62 premature infants. They observed that the pectoralis major reflex was the easiest to elicit and found in all the children, whereas the finger flexion reflex, jaw reflex, and triceps reflex were somewhat difficult to elicit and prior theophylline therapy seemed to augment the ankle jerk.[19] Sometimes, reflexes may be difficult to elicit in normal individuals because of the global hypoexcitability of ventral motor neurons, and in such situations they can be brought about by a reinforcement mechanism such as the Jendrassik maneuvre. Initially NI FEATURE: JOURNEY THROUGH THE EONS – COMMENTARY Year : 2017 | Volume : 65 | Issue : 2 | Page : 245-249 thought to increase the fusimotor drive, the maneuver is now believed to operate through a direct excitatory influence upon the alpha motor neurons.[20],[21] It is generally assumed that the ankle jerk may be absent in old age. However, in one study, among 200 consecutive patients above the age of 65, it has been shown that it is not elicited in only 6% of the individuals; one recent work has suggested that the ideal method of eliciting the reflex in old age is not to strike the tendo achillis but to tap the sole of the foot, and some asymmetry in the degree of excursion of the sole is also within allowable limits. The yield on striking the tendo achillis was also higher in the hands of the more experienced clinicians.[22],[23],[24],[25] The pathophysiology of the exaggerated deep tendon reflexes was addressed by Charles Scott Sherrington (1857–1952), the Nobel Laureate, in 1932; he suggested that it was due to loss of supraspinal inhibitory influences on the spinal cord.[8] Tapping a tendon to elicit a tendon jerk often results in contraction of the surrounding muscles in the hyperexcitable state, which is due to the irradiation of the reflex to the neighboring motor neuron pool supplying the synergistic muscles. In states of severe hyperreflexia, irradiation may be so pronounced that some authors feel that, if on tapping the radial bone at the lower end, the biceps jerk could be elicited, it is no longer necessary to elicit the latter jerk any more in the classical manner.[26],[27] The stretch reflex and tendon reflex: A fascinating ongoing debate For ages, the stretch reflex has been considered as a variety of pure spinal reflex of short latency, which was identical to the tendon reflex subserving the same reflex arc. Sherrington et al., adduced enough evidence in favor of this hypothesis in decerebrate cats and called it “tonic reflex” in 1924. Sherrington wrote, “there could be little doubt that the knee jerk, a reaction, long familiar to the physician, is a fractional manifestation of it… The physician in testing the knee jerk is in fact, testing the stretch reflex of an anti-gravity muscle.”[28],[29] However, disparities in the status of the two reflexes in certain clinical conditions led C David Marsden (1938–1998), and his colleagues such as Patrick Merton (1920–2000) and HB Morton from Queen Square, London to carry out a series of experiments that helped to establish that the two reflexes had different anatomical pathways, and therefore, they were not identical.[30] To prove their hypothesis, Marsden lent his right flexor pollicis longus muscle for investigation and observed that the contracting flexed thumb, when extended, showed multiple components, and that the latency of the reflex was nearly double for a pure spinal reflex elicited by tapping the tendon;[31] a similar result was also obtained by other workers.[32],[33] These works led Marsden and his colleagues to question whether a transcortical pathway operates in the genesis of the stretch reflex, in which on stretching a muscle passively, the afferent impulse travels up the spinal cord to the cortex and thereafter returns to the spinal efferent neurons. The latter then fire impulses for the effector muscles to contract in contradistinction to the tendon reflex, which was purely spinal and therefore of short latency.[31] CG Philips, from his extensive works on the hands of baboons, remarked that the spinal stretch reflex “had been overlaid in the course of evolution by some transcortical circuit.”[33] Finally, the evidence of stimulus-sensitive myoclonus, which shows cortical discharges before the electromyographic discharges on lightly flicking a peripheral small joint, lends credence to the long-loop circuit for stretch reflexes.[30],[34],[35] The vindication for a transcortical loop for stretch reflexes came from the works of Kugelberg and Widen, as well as Adrian and Moruzzi who NI FEATURE: JOURNEY THROUGH THE EONS – COMMENTARY Year : 2017 | Volume : 65 | Issue : 2 | Page : 245-249 showed that a patient with myoclonus in the lower limb had contralateral abnormal spikes in the electroencephalogram during operation and focal cortical excision led to the amelioration of the symptoms.[36],[37] Finally, a few words about the origin and the subsequent evolution in reflex hammer will not be out of place [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7]. As has already been mentioned, both Erb and Westphal used their fingers to tap the ligamentum patellae to elicit the knee jerk, and though Max Wintrich designed the first percussion hammer in 1841, the palm goes to John Madison Taylor for devising the first reflex hammer in 1888, 13 years after the description by Erb and Westphal.[3],[4],[5],[9] This consisted of a triangular rubber head, and when this invention was exhibited in the 1988 meeting of the Philadelphia Neurological Society, the minutes read, “… a cone flattened on the opposite side, with apex and base carefully bevelled or rounded, of about the thickness throughout of the human index finger.… The special feature of this hammer is that the shape of the striking surface is like the outer surface of the extended hand, palm downward, which is more often used in obtaining tendon jerk.”[4],[5] William Christopher Krauss (1863–1909) devised a model which had two rounded pieces, a large piece for the knee jerk and one small for the biceps jerk, which were attached to a metal and a rubber handle. This was presented before the annual meeting of the American Academy of Neurology in 1894.[4],[5],[38],[39] Ernst LO Tromner (1868–1930) from Germany designed one variety where the handle was made of metal, tapering into a thin end, which could be utilised for testing cutaneous reflexes.[5],[5],[38],[39] Other hammers of different designs include the Queen Square Hammer, designed at the National Hospital for Nervous Diseases, where the handle was made of plastic and a round black head was mounted on it; the Babinski hammer, devised by Joseph Babinski (1857–1932) in 1912, which looks like the Queen Square hammer, the handle being made of steel; the Buck hammer, looking like the Babinski hammer with the addition of a built-in brush for testing cutaneous sensation; Berliner hammer, where the rubber was attached to the handle at a right angle looking like a throwing axe; and the Stookey hammer, which was collapsible and accompanied by two sharp pins for testing pain and two point discrimination, a camel hair brush for testing touch sensation, and a sufficiently rough structure to test the plantar response.[39] CONCLUSION It is to be noted that Erb and Westphal did not provide the first account of reflex activity in man; that credit goes to René Descartes (1596–1650), of France, who described the menace reflex, also known as Descartes reflex.[40] The independent observation regarding the knee jerk by Erb and Westphal, and their publication in the same issue of a reputed journal by the magnanimous gesture of the latter, one of the editors, is rather serendipitous in nature. 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