A Brief History of Occult Spinal Dysraphism

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1 THE SPINE SCHOLAR VOLUME 1, NUMBER 2, 2017 SEATTLE SCIENCE FOUNDATION A Brief History of Occult Spinal Dysraphism 1 Department of Anatomical Sciences, St. George s University, Grenada Chad J. Jensen 1 HISTORICAL Key Words: spine, tethered cord, spinal cord, congenital, dysraphic ABSTRACT The first documentation of spinal dysraphism appears in literature dating back to the 17 th century. Anatomist Nicolaes Tulp, famously portrayed in Rembrandt s painting, The Anatomy Lesson of Dr. Nicolaes Tulp, described congenital spinal abnormalities in his publication of the textbook Observationes Medicae. Here, in his 1641 edition, he described six cases of spinal dysraphism, where he first introduces the term spina bifida, literally meaning split spine. One of the cases, involving a lumbosacral lesion, was described as having the prolongations of the nerves scattered in different directions through the tumor. Later, in 1691, Dutch surgeon, Frederik Ruysch, published ten case reports of spina bifida. At the time, like Tulp, Ruysch recommended against surgical intervention due to high morbidity and mortality, considering the condition inoperable. While there has been a multiplicity of publications on dysraphic states throughout history, there was often disagreement on the pathogenesis, as well as regarding its clinical importance and surgical interventions. In a review of the history of occult spinal dysraphism, we find that it was not until the mid 20 th century when authoritative works were published, helping to guide the medical community into understanding the condition and offering therapeutic approaches and guidelines. Spine Scholar 1: , 2017 Early Accounts and Descriptions The dysraphic state as, published by Gardner (1973), refers to the abnormal closure of the neural tube, as opposed to araphia, meaning non-closure on the neural tube. As a matter of definition and classification of dysraphic states, it should be noted from the outset that the varying macroscopic pathological findings determine the more specific subtypes of dysraphia. The scope of this chapter is occult spinal dysraphism; occult, referring to that which is hidden, and as noted by Tubbs et al. (2016), the anomalies are almost entirely limited to bony elements with the underlying lesion completely covered by skin. This distinguishes it from its counterpart, spina bifida cystica. Spinal dysraphism includes a variety of conditions with varying clinical and pathological severities. According to Gardner (1973), the occult form of dysraphic states includes tethered cord syndrome, dilated spinal canal, posterior and anterior spina bifida, and split cord malformations. While the occult form remains covered with skin, there still may be a variety of external clues to an underlying pathology. Tubbs et al. (2016) describes the enigmatic human tail that dates back to antiquity where Pliny and Pausians, from the first and second centuries, respectively, noted the finding in India and peoples of remote islands in the Atlantic Ocean. Although rare, stories persisted through the centuries, and in a recent case report publication in 2013, Melo et al. (2013), described three cases of human tails. Magnetic resonance imaging in the three cases showed underlying spinal dysraphism. James and Lassman (1959) outline other cutaneous findings such as subcutaneous lipomas, hypertrichosis, angiomas, and dermal sinus tracts. Spinal dysraphism was introduced into the medical lexicon by Friedreich Bremer, a German neurologist in 1926 as noted by Pryse-Phillips (2009). Later, Lichtenstein (1940), reintroduced the term to refer to the defective fusion of the neural tube in the dorsal midline of embryological development, which may cause phenotypic abnormalities in the following germ layers: somatic ectoderm (cutaneous), mesoderm, and neurectoderm. These manifestations present with wide clinical variability manifesting abnormalities in the skin, muscles, vasculature, and nervous system. Lichtenstein drew attention to a number of cases that would appear more obscure, that is, without cutaneous or other external findings that were so often seen with overt spina bifida, which would soon earn the term occulta. By its definition, therefore, spinal dysraphism includes all forms of spina bifida: occulta, aperta, anterior and posterior. The designation of spina bifida occulta, is credited to Rudolf Virchow. Wherein the external lesions of meningoceles and myelomeningoceles are clearly visible, those in spina bifida occulta are not. As written in The Lancet by Sutton (1887), Virchow had addressed the Berliner Gesellschaft für Anthropologie in 1875 regarding a case that had been presented a few months prior by Dr. Bernhard Ornstein in Athens. Ornstein had earlier described a Greek soldier whose loins presented an abundant crop of long hairs. The hairy growth occupied the middle line of the back, and extended thence on each side. The hairs were so long, that the man found it necessary periodically to THE SPINE SCHOLAR 103 VOLUME 1, NUMBER 2, 2017

2 cut them, in order to prevent interference with defaecation (Sutton, 1887). Virchow, who at the time was working at the Institute for Pathology at Charité, a teaching hospital in Berlin, noted in his address to the society that he had a similar case of a 24-year-old female who had died from peritonitis secondary to typhoid fever. Virchow described a patch of hair measuring ten centimeters in width, with the hairs six to seven centimeters in length, with normal appearing skin at the site. This patch, which he likened to the tuft of feathers on a Polish fowl, and thus yielding the description tuft of hair, was associated with a palpable depression in the spine (Sutton 1887; Braithwaite, 1888). On dissection, Virchow found that the upper sacral vertebrae were replaced by membrane (Sutton 1887). He opined at the time that the patch of hair was the result of local irritation, due to disturbance during the development of the spinal column (Sutton, 1887). While Virchow is credited with coining the term, cases have been documented much earlier, as aforementioned in the 17 th century. Noted by Tubbs et al. (2013), Govert Bidloo, an anatomist, playwright and student of Ruysch, published a case in 1708 in his surgical book, Exercitationum Anatomico-chirurgicarum, that is mostly likely the first documented lipomyelomeningocele. On autopsy, the conus medullaris was found to be within the sacrum. According to Bosmia et al. (2014), Johnson had been credited as the first to describe what later was later named lipomyelomeningocele by Rogers in 1971, however, it was in fact Bidloo, 172 years before Johnson, who discovered this dysraphia. Soon after Virchow s description in the 19 th century, physicians began publishing case reports of spina bifida occulta and its associated clinical findings. Virchow s own pupil, German pathologist, Friedrich Daniel von Recklinghausen, reported on a case of a nine-year-old girl who had a tuft of hair in the lumbosacral region with spinal depression, and on autopsy, confirmed absence of the fifth lumbar spinous process. He described how the cord was tethered at S2 vertebra by a fatty tumor and that the fluid in spina bifida was indeed from the subarachnoid space (Goodrich, 2008). He noted that she also suffered from chronic otitis of the metatarsals of the left foot with an area of anesthesia. von Recklinghausen had another case of a man with spina bifida occulta and club-foot, a neurotic ulcer, and decreased sensation on the left foot. His thesis on spina bifida illustrated a split cord malformation (Fig. 1). Anatomist and physician, Johann Conrad Brunner, famously known for his research on the pancreas and duodenum, yielding the eponymous Brunner s glands, presented a similar case years prior which also confirms that spina bifida occulta was often associated with other physical findings such as hypertrichosis and club foot (Sutton, 1887). Figure 1: Axial drawing of the two hemicords as seen by von Recklinghausenin a split cord malmormation. In a historical review by Tubbs et al. (2010), the authors discussed another account of associated findings with dysraphic states in Brunner s 1688 publication of a newborn with hydrocephalus and a cavity within in it. Brunner furthermore noted a lumbosacral dysraphism and intramedullary cyst, which was punctured by a different physician leading to the infant s death. Autopsy showed dysraphia as seen by failure of fusion in the vertebral arches with myelomeningocele, hydrocephalus, and syringomyelia, which would have been described here 150 years before the term was coined. In his conclusion, he believed that the syrinx was either a stand-alone malformation or part of the lumbosacral dysraphia (Tubbs et al., 2010). This latter case, although not an example of occult spinal dysraphia due to the presence of myelomeningocele and hydrocephalus not being a component of occult states, the case nonetheless helped draw attention to an important group of clinically challenging cases. To the like, Giuseppe Muscatello ( ), who had been a pupil of von Recklinghausen at the Institute of Pathology and is credited for his pioneering work to establish cancer research as its own field and the first cancer center in Italy, had also completed work studying spina bifida aperta and occulta. In various documentations, he made on occult spinal dysraphism, he found an associated dermoid cyst at the spinal lesion, other patients with the commonly seen focal tuft of hair, and some with split cords. He had even stated at the time that he believed some of these cases to be hereditary (Tardieu et al., 2017). These contributions additionally helped establish spina bifida occulta as a clinical entity, sparking wide interest into its pathogenesis and, ultimately, its therapeutic options. THE SPINE SCHOLAR 104 VOLUME 1, NUMBER 2, 2017

3 Forms of Occult Dysraphism Tethered Cord Syndrome and Filum Terminale Syndrome Before Virchow used the term spina bifida occulta, a case in 1857, presented by Dr. Johnson, was likely the first documented tethered cord syndrome as it became known in the latter half of the 20 th century. The patient was a ten-month-old boy who experienced twitches and convulsive-like movement in the right leg. There was a swelling over the sacrum, which Johnson operated on, discovering a lipoma emerging from the spinal canal and adhered to the membranes enveloping the spinal cord. It was successfully dissected from the cord and the patient s twitches completely resolved after the operation (Johnson, 1857). In 1891, Jones performed what is now called the surgical untethering of the spinal cord in a 20-year-old male who developed incontinence, club foot, and weakness and atrophy of the lower extremities. In his operation, Jones successfully dissected a densely fibrous band stating the spine [was] trephined to relieve pressure on the cauda equina (Bui et al., 2007). The patient was able to walk without pain six months after the operation. According to Hoffman et al. (1976), it was not until 1940, when Lichtenstein first proposed that tethering of the cord may cause paraplegia, though, his hypothesis was not accepted at the time. A few years later in 1953, Garceau, an orthopedic surgeon, whose interest in congenital club foot and scoliosis, led him to make the discovery which he termed Filum Terminale syndrome or Cord-Traction syndrome. Garceau had seen three cases, one with congenital scoliosis, a second with idiopathic scoliosis and a third with tuberculosis of the spine who were experiencing lower extremity spastic paralysis. All three underwent laminectomy and resection of a thickened and tightened filum. He had noted that in the patient with congenital scoliosis, the conus medullaris had remained in its fetal position and in another patient, the filum separated one centimeter after sectioning (Garceau, 1953). Consequently, Garceau, based on surgical findings and symptom improvement postoperatively, posited that tension on the filum, exacerbated by spine flexion or extension, pulls on the hindbrain, displacing it downward through the foramen magnum and essentially exhibiting a Chiari malformation (Bui et al., 2007; Garceau, 1953; Lew and Kauthbauer, 2007). Then in 1976, Hoffman et al. introduced the term tethered spinal cord syndrome in a publication on 31 patients who had motor and sensory deficits in the lower extremities. They confirmed that symptoms improved after dividing a thickened filum terminale, which the authors defined as greater than 2 mm (Bui et al. 2007; Hoffman et al. 1976). According to Yamada (2010), the establishment of tethered cord syndrome was fraught with disagreement among physicians and scientists due in part to the fact that evidence for it was based solely on visual findings upon dissection. Split Cord Malformation In addition to tethered spinal cord as a type of occult spinal dysgraphia, the discovery of spinal cord malformation (SCM), formerly known as diastematomyelia, further expanded the clinical entity. Historically, the earliest known case of SCM dates to circa AD 100 from Israel s Negev Desert. The bones of a 20-year-old man were discovered in a tomb and upon examination, he was found to have a butterfly vertebra with a bony process dividing the spinal canal into two halves at the thoracolumbar junction (Saker et al., 2017). A number of cases had since been recorded, describing the same findings as disjunction of the cord per Mathern, Peacock, and Perret in 1624 (Saker et al., 2017). However, it was not until 1837 that we see Ollivier d Angers, a pathologist, coin the term diastematomyelia; diastema, cleft and myelos, spinal cord in Greek (Saker et al., 2017). von Recklinghausen, in addition to his aforementioned documentation on spina bifida occulta and associated clinical findings, also remarked on SCM in a 31-year-old female with a split cord malformation from the thoracolumbar spine to the cauda equina. In the ensuing years, Hertwig described the condition as two hemicords within their own dural sacs separated by a bony process differentiating the finding from what he called diplomyelia, wherein the cord itself has been duplicated and without any such sectioning by a bony process (Saker et al., 2017). Herren and Edwards (1940) disputed this difference, stating that based on their findings in 42 autopsies, the cord is in fact duplicated. The confusion between terms has persisted drawing need for a more concise and accepted classification system. Humphry (1886) published findings on the dissections of six specimens with spina bifida, which account for early descriptions of split cord malformation. One specimen was described as having deficiencies in the vertebral arches above the spina bifida with a notable projection of bony processes from the vertebral bodies, bisecting the spinal cord. In another specimen, Humphry found a similar presentation in lumbosacral spina bifida with a median process perforating the spinal cord directly above the spina bifida, noting severe anatomical abnormality in the vertebral bodies of the lower spine. Later, in 1973, Gardner, whose work on the dysraphic states as previously mentioned, described split cord malformations as an asymmetrical and longitudinal division in the spinal cord. At the level of the spine involved, he noted that there is often shortening, scoliosis, or fusion between the vertebral bodies, widening of the spinal canal, and that the two hemicords more commonly within their own dural sac and less commonly within the same (Gardner, 1973). To avoid confusion of the terminology and definitions, Pang et al. (1992) set to succinctly classify the condition, and published a typing criteria that uses the following three points: the presence of two cords, the nature of the dural sacs, and the characteristics of the median septum. He defined the differences into type I and type II. Type I SCM, having two hemicords each within their own dural sac, being separated by a midline bony septum; and type II SCM, two hemicords within a single dural sac, separated by a non-rigid, fibrous median septum. THE SPINE SCHOLAR 105 VOLUME 1, NUMBER 2, 2017

4 Dysraphia since the Mid 20 th Century These dysraphic states were extensively researched in the 1940 s by Ingraham documenting associated congenital anomalies and providing criteria for surgical intervention. Then, through the 1950 s to 1970 s, James and Lassman, who were inspired by the works of Ingraham, furthered the field s understanding of occult dysraphic states in their authoritative book, Spinal Dysraphism: Spina Bifida Occulta (James and Lassman 1972). Their focus was spina bifida occulta, distinct from overt spina bifida or aperta. In a 1959 publication, the authors noted that spina bifida occulta had been regarded as a curiosity rather than as an entity with possible clinical implications as it was often discovered on routine x-rays, but not remarked on clinically (James and Lassman, 1959). In their work, they relied on a differentiation they attribute to Koch, wherein macroscopically on surgical exploration of the spine, there is no herniation of neural contents (James and Lassman, 1972). During the preceding years, spinal surgical management posed high morbidity and mortality, particularly in predating the introduction of antibiotics in the 1940 s. The authors noted that there was an urgency to survey the literature and begin their own research with the purpose of improving management and outcomes. James and Lassman suggest that this urgency is due to the following: The clinical importance lies in the extrinsic anomalies which bind down the spinal cord or its nerve roots and prevent them from changing their position within the vertebral canal as they normally should to accommodate the growth of the vertebral column and of the spinal cord. If the spinal cord is tethered it will suffer a traction force during vertebral growth which it can accommodate to some degree in some cases by increasing its rate of growth, but when this compensatory reaction can do no more, the traction force will cause failure of neuronal conduction and ischaemia owing to failure of blood supply or to venous congestion with possible thrombosis It is all these factors which produce the changes in the lower limbs, bladder and bowel (James and Lassman, 1972). Their research has since helped to establish recommendations on when surgical intervention is appropriate. It has also set forth a thorough analysis of associated clinical findings in patients with spina bifida occulta so as to aid the physician in early diagnosis and consequently better clinical outcomes. Moreover, James and Lassman are particularly known for their work on tethered spinal cord syndrome, and also in 1972, published their findings and coining the term meningocele manqué (MM). Manqué, a French term, refers to that which is lacking; and the authors posited that the bands are remnants of meningoceles that had failed to arrange in embryonic development (Schmidt et al., 2017). Various cases since James and Lassman s publication, challenged the definition that tethering bands terminate at the inner aspect of the dura. Although their definition did not provide a strict guideline on termination locations as a qualification for MM, they modified the definition in 1977 stating that bands may terminate outside the dura in defective lamina of the vertebra or in the skin (Schmidt et al., 2017). Rajpal et al. (2007) also challenged the classification, setting out to establish a system that placed tethering tracts into short tethering tracts and long tethering tracts, further identifying the two based on histological features as having either epithelial components or non-epithelial components. This eventually led to what would once have been classified as MM into their own categories, i.e.: dermal sinus tracts and limited dorsal myeloschisis. As noted by Schmidt et al. (2017), further subdivision may take place, but the authors note that MM is an entity in itself, adequately defined as tethering of the spinal cord, nerve roots, and/or filum terminale by single and/or multiple aberrant nerve roots, fibrous bands, and/or adhesions, which terminate onto the dorsal dura mater, epidural space, or overlying lamina. CONCLUSION The history of occult spinal dysraphism is expanse with a plethora of cases documented in the medical literature since the 17 th century, though we have even seen cases from antiquity that, retrospectively, are in fact those of spinal dysraphism. Renowned pathologists such as Virchow and von Recklinghausen began an inquiry into cases of neurological deficits and apparent orthopedic cases such as the club foot, to embark on a journey of better understanding this clinical entity that Virchow would term spina bifida occulta. Spinal dysraphism, as had been coined by Bremer in 1926 and reintroduced by Lichtenstein in the 1940s, refers to the defective fusion of the neural tube in the dorsal midline of embryological development. The manifestations therein are wide, from an overt spina bifida as seen externally along the spine such as spina bifida cystica, to the hidden what is covered by a layer of skin and therefore called occulta. As time went on, cases emerged further enhancing the medical community s discoveries into the embryology and pathology of dysraphic states, and most importantly into the management of such cases as pioneered by Ingraham and later, James and Lassman. 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