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History of the pineal region tumor
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ARTICLE IN PRESS Neurochirurgie xxx (2014) xxx–xxx
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Report 2013: Tumors of the pineal region
History of the pineal region tumor Histoire de la tumeur de la région pinéale C. Mottolese ∗ , A. Szathmari Department of Paediatric Neurosurgery, Pierre-Wertheimer Hospital, CHU de Lyon, 59, boulevard Pinel, 69003 Lyon, France
a r t i c l e
i n f o
Article history: Received 25 March 2013 Received in revised form 27 March 2013 Accepted 30 March 2013 Available online xxx Keywords: History of pineal tumor History of pineal and pineal region surgery
a b s t r a c t The pineal gland has interested humans from millenniums. In this paper we review back in the history and the evolution of the pineal gland surgery. Originally, this surgery used to carry a high rate of morbidity and mortality. Nowadays the development of the anesthetic, radiological, surgical and intensive care techniques have been responsible of an improvement of the surgical results and better quality of life. It is always interesting to know from where we come. © 2014 Published by Elsevier Masson SAS.
r é s u m é Mots clés : Histoire de la glande pinéale Histoire de la chirurgie de la glande pinéale et de la région pinéale
La glande pinéale intéresse l’humanité depuis des millénaires. Dans cet article nous essayons de revoir l’histoire et l’évolution de la chirurgie de la glande pinéale. À l’origine, cette chirurgie était associée à un fort pourcentage de mortalité et morbidité. De nos jours, le développement des techniques d’anesthésie, de radiologie, de chirurgie et de soins intensifs a permis d’obtenir de bons résultats et une meilleure qualité de vie pour les patients. Il est toujours intéressant de savoir d’où l’on vient. © 2014 Publie´ par Elsevier Masson SAS.
It is difficult to report an exhaustive history of pineal gland and of the therapeutically strategies that have been developed but it seems important to us to remember some milestone about this subject as an introduction to a report concerning pineal tumours, also if other reviews on this particular topic can be found in literature. The pineal gland has interested humans from a long time because already, in China, during the reign of the Yellow Emperor (2697–2597 BC), have been found traces of this interest as reported by Veith [1]. In Hindu scriptures, the pineal gland was considered as one of the seven chakra: the crown chakra, representing the center of spiritual force [2,3]. Aelius Galenus (130–200 AC) reported that Herophilus (325–280) was the first to discover the pineal gland and to practice anatomical dissection in a scientific way and described the function of the gland as a valve or sphincter permitting to regulate the flow of “pneuma” from the third to the fourth ventricle.
∗ Corresponding author. E-mail address: [email protected] (C. Mottolese).
“Pneuma” was considered as the substance derived from air and responsible for thought (psycikon for Greeks) and also responsible of organic movements [4,5]. These anatomical and physiological considerations were unchanged until the Medieval Era and Andrea Vesalius (1514–1564); his new anatomical considerations were discussed and related in the “Humani Corporis Fabrica”, Libri Septem. In the same period, Niccolo’ Massa, an Italian anatomist, showed that in the ventricular system there was the liquor, the cerebro-spinal fluid [6]. René Descartes, French philosopher (1596–1650), affirmed that the pineal gland was the seat of the human soul, the seat of the “sensu communis” and consequently the pineal was the organ of the “res cogitans” the “anima”. The concept that information to the pineal gland was mediated by the eyes and optic nerves begin to develop. Francois Magendie (1783–1855), physiologist, advocated the function of tampon because the expansion or shrinkage of the body close off or open the aqueduct of Silvius. Gunz (1753) explained that the dementia was related to an impeded flow of the spirits caused by the pineal gland [7,8].
0028-3770/$ – see front matter © 2014 Published by Elsevier Masson SAS. http://dx.doi.org/10.1016/j.neuchi.2013.03.005
Please cite this article in press as: Mottolese C, Szathmari A. History of the pineal region tumor. Neurochirurgie (2014), http://dx.doi.org/10.1016/j.neuchi.2013.03.005
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New elements of comprehension of the human pineal physiology were reported with the development of anatomical and comparative studies of humans and animals including vertebrates and no vertebrates. Ahlborn and Rabl-Ruckhardt (1839–1906) showed the similarity between the non-mammalian pineal gland and the primary optic vesicles [9,10]. The role of pineal in reptiles and amphibian as photo sensory organ was elucidated and this function regressed and became vestigial in mammals [11,12]. Helena Blavatsky (1831–1891), advocating the third eye of Shiva, spoke of the third eye for human approaching the pineal gland to the organ of spiritual vision [13]. The demonstration of the two types of cells of the pineal gland was reported by Kolliker, preceding the hypothesis of Studnicka who announced that the pineal gland could have a glandular function and this function was also related to the precocious puberty of a patient with a pineal tumour [8]. Cajal thought that the nerve fiber of the pineal body was sympathetic and the body of the gland was a vascular structure [7]. Marburg reported that the activity of the pineal gland was that of regulating the hormonal cycles, and correlating the hypofunction of the gland with the apparition of a precocious puberty he explained the hypofunction with the destruction of the gland by the expansion of a pineal tumour [14,15]. During the Second World War, in 1940, the electron microscope confirmed the secretory activity of the pineal gland, that was provided by the pinealocytes, neurosecretory cells, while the glial cells assure their support [16]. Aaron Lerner, in 1958, discovered the hormone of the pineal gland that he called “melatonin” that was implicated in the regulation of the circadian rythms of sleep/wake, mainly in the normal sleep/wake rhythm [17,18]. According to Choudry, the first case of a pineal tumour was reported by Charles Drelincourt in the seventeen century, and Blane was the first in English literature to report a pineal tumour [19]. Morgagni, an Italian anatomist, reported and discussed the case of a man who harboured a calcified pineal gland of the size of an egg [20]. Henry Parinaud in 1883 described a syndrome characterized by a paralysis of the vertical gaze that was explained by the compression of the mesencephalic tectum by a growing lesion of the pineal gland. In 1875, a German pathologist, Karl Weigert, reported the first well documented pineal tumour that was a pineal teratoma, describing a tumour with squamous and columnar epithelium including hair and skin elements and describing the microscopic histology [21]. After the report of cases by Gutzeit in 1909, the relation between precocious puberty and pineal teratomas was definitively established. Krabbe, in his thesis “Histological Studies of Pineal Body”, was the first to use the term of “Pinealoma” [22]. This is the origin of evolution of histological classification of pineal tumours because Percival Bayley, Cushing and Bayley, followed by Russel, Rubestein, Zulch, Globus and Dorothy Russel and Nathan Friedman gave the basis of the histological classification of pineal tumours [23–25]. The pathological idea have evolved and a new classification has been proposed by the WHO with the main contribution of Anne Jouvet, in Lyon [26]. The difficulties of surgical approach for pineal tumours can explain that for long time pineal region tumours have been considered as inoperable and consequently the recommended strategy for their treatment has been the cure of hydrocephaly followed
by irradiation and why Dandy stated “Pineal tumours are perhaps the most dangerous of all intracranial tumours to attack surgically” [27,28]. The history of surgery of pineal tumours started at beginning of the century to 1905 when Victor Horsley tried to remove a pineal tumour by a infratentorial approach unsuccessfully, while in 1904 Cushing reported a bitemporal craniectomy for a patient who some weeks later died while the autopsy revealed a quadrigeminal plate tumour [29,30]. Conrad MH Howell, discussing at the Royal Accademy on “Tumors of the Pineal Body”, reported the comments of Horsley on the failure of the infratentorial approach preconizing a new surgical avenue through a supratentorial approach splitting the tentorium and this discussion is always present in the neurosurgical world [29,31]. Pappenheim reported a surgical procedure realized by Anxenfeld in 1906 in Freiburg, and Marburg in 1908 describing a palliative approach by a supracerebellar route. The patient did not survive the surgical procedure [32]. In 1910, Pussep used a transverse transtentorial approach to remove a pineal tumour using the splitting of the transverse sinus and the tentorium. The patient survived to the surgical intervention for three days [33]. Bailey and Jelliffe reported an attempt of removal while Rydygier proposed a punction through the corpus callosum to decrease the intracranial hypertension [32]. In 1911, Krause suggested that the supracerebellar infratentorial approach could be the avenue to adopt for pineal tumour although he denied any practical experience of this surgery [34]. Brunner tried to remove a pineal tumour by a parietal route but the venous deep structures carried problems of hemostasis that pushed him to adopt an infratentorial supracerebellar approach [35]. One year later, he chose a completely different approach through the corpus callosum but with a limited view of the tumour and a severe venous hemorrhage obliged him to abandon the procedure [35]. Nassetti proposed on laboratory animals the approach of pineal region resecting the longitudinal sinus and the straight sinus but without clinical experience [36]. In 1913, Krause used an infratentorial supracerebellar approach with a sitting position and, as reported by Zulch in 1981, this was the first patient treated with success: the patient was 10-year-old and the lesion measured 4 cm in diameter [34,37]. The success of the surgical procedure was due to the preservation of the venous system, developed dorsally, and lateral to the lesion, avoiding the main cause of surgical morbidity [32,38]. In 1921, Dandy described the posterior trancallosal approach. Dandy, in 1912, tried the parieto-occipital approach on the midline with the transection of the posterior half of the corpus callosum. In spite that this approach was particularly difficult, he used this avenue in humans with survival that did not exceed a year [32,39,40]. In 1926, Krause proposed again the ITSC approach in three patients with success because of no mortality [41]. Foerster was the second surgeon who reported a successful removal of a pineal tumour an occipital craniotomy was realized, a puncture of the lateral ventricle permitted the decompression of the brain and retraction of the occipital lobe from the falx and the tentorium with a more easy exposition of the pineal tumour [32,42]. He used the occipital transtentorial approach preconized by Tandler and Ranzi in their “Surgical Anatomical Textbook” [43]. In 1929, Peet removed a pineal tumour with the approach proposed by Dandy: the patient was irradiated postoperatively and had a good clinical result with possibility of working as painter as reported by Camins [44].
Please cite this article in press as: Mottolese C, Szathmari A. History of the pineal region tumor. Neurochirurgie (2014), http://dx.doi.org/10.1016/j.neuchi.2013.03.005
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Walker perfecting the Dandy’s approach reported ten cases and emphasized the advantages of this approach that for long time was considered the most useful for surgery of pineal lesions and the neurological evaluation of patients showed the presence of cortical function disorder as alexia without agraphia [27]. The lateral transcortical transventricular approach was reported by Van Wanegen in 1931 and the ventricular dilatation seemed to facilitate the removal of pineal tumours [4]. This approach was particularly interesting in cases of huge ventricular dilatation because the opening of a thin medial ventricular wall permitted a lateral view of the tumour and of the pineal region. Pratt and Brooks, in 1934, reported with success the removal of a pineal tumour using a sub-occipital transtentorial approach that was later publicized by many other surgeons and that became the approach adopted for tumour of the pineal region in Lyon. Horrax, in 1937, proposed the approach of the pineal region with a parieto-occipital lobectomy with the consequence of visual field amputation and seizures. The occipital lobectomy permitted to gain a large space to expose the pineal region but at the same time he stressed the importance of a more conservative approach treating hydrocephalus with a ventriculo-atrial shunt followed by a cerebral irradiation [45]. Ward and Spurling reported a series of 14 patients treated with a subtemporal decompression and irradiation [46], while Torkildsen proposed the ventriculocisternal shunt followed by irradiation [47]. At that time, the mortality was high: for Dandy in 1945: 20%; for Lemmen in 1953: 70%; for Ringert in 1954: 58,8%; and the diversion of the CSF with ventriculo-peritoneal or ventriculo-atrial shunts followed by irradiation was commonly used for tumours of the pineal region. Zapletal, in 1956, revisited the infratentorial approach of Krause reporting four patients operated but this approach was popularized by Stein who used the sitting position, the surgical microscope and extending the sub-occipital craniectomy at the level of the transverse sinus reported a very low morbidity associated with no perioperative mortality [48,49]. J. Suzuki, in 1965, reported 19 patients treated with the Van Wanegen approach and only 2 patients were free of complications after the surgery [50]. The occipital transtentorial approach was popularized in 1959 by Heppener, and, in 1966, by Poppen [32]. In 1971, Jamieson reported the modification of the sub-occipital transtentorial approach modifying the axis of approach that became more medial and modifying the opening of the tentorium permitting a better exposition of the vermian and quadrigeminal arachnoidal space and of the pineal region [51]. Lapras modified the Jamieson’s approach proposing a diamondshaped bone flap with the lateral superior bone hole at the level of the parietal bossing and modifying the retraction of the occipital lobe that improved the exposure of the deep pineal region [52]. Our philosophy of the sub-occipital transtentorial approach is intact and our attempts to reduce the enlargement of the bone flap have been abandoned. Indeed in our opinion, it is crucial to gain enough space to control the venous bridging system in case of tearing during the retraction of the occipital lobe. In this way, we are faithful to the principle of a large bone flap for the exposition of the pineal region. It is obvious that the history of the surgical approach of the pineal region has completely evolved with the advent of the microsurgical era that started with Marino, Stein, Dierssen, Humphreys, Kurze, Lapras. The choice of the approach is related to the plane that delineates the pineal region that is represented by the tentorial plane. In the 1970 era, the introduction of stereotaxy facilitated the study of pineal region tumours favoring the diagnosis of different types of lesions and contemporary pioneers of the endoscopic
3
technology, as Fukushima, showed the possibility of visualizing the pineal region favoring the possibility to realize endoscopic biopsy and, sometimes, to treat hydrocephalus with a third ventriculostomy [53]. The endoscopic approach, favoring the treatment of hydrocephalus, the possibility of a histological diagnosis with a low morbidity is commonly proposed at the beginning of therapeutic strategies and Cohen was the first neurosurgeon to report this strategy [54]. In the modern period, the refinement of the endoscopic instrumentation has also permitted the endoscopic direct approach for removal of pineal tumours. The direct approaches to the pineal region in the large number of cases remain either infratentorial or supratentorial. The current application of microsurgical techniques for the infratentorial supracerebellar approach and for the sub-occipital transtentorial approach revisited by Lapras, Yasargil, Brotchi and others have allowed a dramatic reduction in mortality and in morbidity [55–59]. The surgical techniques have been associated with the development of the radiological techniques with a better definition of the relationships between the tumour and the surrounding anatomical structures and a better knowledge of the vascularization of lesions and the modern anesthesiological techniques including the improvement of the postoperative care have allowed to approach a nearly nil mortality [60]. As Herseniemi reported in the last years, surgeons have to remember the recommendations of Francis Bacon and Drake according to whom surgery has to be simple, fast with preservation of normal anatomy [61]. The pineal tumours are nowadays treated surgically in many center and even though the surgical approach of this region is challenging this surgery can be realized with good results and acceptable postoperative morbidity mainly in cases of benign lesions in children and adults patients. Postoperative adjunctive treatment should be indicated in cases of histological aggressive lesions [62]. In the future, the development of new technologies will permit safest surgery. The surgical approach has to be realized considering the citation of Charles IX, king of France that stated: “The most beautiful avenue in the world is the one that was argued in the best way”. References [1] Veith I. The Yellow Emperor’s classic of internal medicine. Berkeley and Los Angeles (CA): University of California Press; 2002. [2] Reiter R, Robinson J. Melatonin: your body’s natural wonder drug. New York (NY): Bantam Books; 1995. [3] Kappers J. Structure and functions of the epiphysis cerebri progress in Brain Research, 10. New York (NY): Elseiver; 1965. [4] Van Wanegen W. A surgical approach for the removal of certain pineal tumors. Surg Gynecol Obstet 1931;53:216–20. [5] Rand RW, Lemmen LJ. Tumors of the posterior portion of the third ventricle. J Neurosurg 1953;10(1):1–18. [6] Massa N, Weber G. Liber Introductorius Anatomiae. Firenze (Italy): Casa Editrice Leo S. Olschki; 2006. [7] Tilney F, Warren LF. The morphology and evolutional significance of the pineal body; being part of a contribution to the study of the epiphysis cerebri with an interpretation of the morphological, physiological and clinical evidence. Philadelphia: The Wistar Institute of Anatomy and Biology; 1919. [8] Heubner O. Tumor der glandulapinealis. Dtsch Med Wochenschr 1898;24:214. [9] Ahlborn F. Uber die bedeutung der zirbeldriise (glandulapinealis, commisur, Epiphysiscerebri). Z Zool 1884;40:331–7. [10] Rabl-Ruckhardt H. Ur deutung der zirbeldruse (epyphyse). Zool Anz 1886;9:536–47. [11] De Graaf HW. Bijdrage tot de kennis van den bouw en de ontwikkeling der epyphyse by Amphibian und Reptilian. Thesis. Leyden; 1886. [12] De Graaf HW. Zuranatomie und entwicklung der epiphysebei Amphibian und Reptilian. Zool Anz 1886;9:191–4. [13] Blavatski HP. The secret doctrine: the synthesis of science, religion and philosophy. London: Theosophycal Publishing Company; 1888.
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[14] Marburg O. Die adipositas cerebralis. Wien Med Wochenschr 1908;17:2617–22. [15] Marburg O. Die physiologie der zibeldriise (glandula pinealis). Handbuch Der Normalen Und Pathologish en Physiologie 1930;13:493–590. [16] Oksche A, Hartwig HG. Pineal sense organs-components of photoendocrine system. Prog Brain Res 1979;52:113–30. [17] Collin JP. Contribution à l’étude de l’organe pinéale. De l’épiphyse sensorielle à la glande pinéale : modalité de transformation et implications fonctionelles. Ann Stat Biol 1969;(Suppl. 1):1–359. [18] Lerner AB, Case JD, Heinzelman RV. Structure of melatonin. J Am Chem Soc 1959;81:60–84. [19] Choudry O, Gupta G, Prestigiacomo CJ. On the surgery of the seat of soul: the pineal gland and the History of its surgical approaches. Neurosurg Clin N Am 2011;22(3):321–33. [20] De sedibus et causismorborum per anatomenindigatis (the seats and causes of diseases by anatomy) Bethesda (MD): Translation Published by Classic of Medicine Library Futura; Original in Italian – Translation by Alexander. [21] Weigert C. Zur lehre von den Tumoren der hirnanhange. 1. Teratom der zirbeldriise. Virchows Arch 1875;65:212–9. [22] Krabbe KH. The pineal gland, especially in relation to the problem on its supposed significance in sexual development. Endocrinology 1923;7(3):374–414. [23] Bailey P, Cushing H. A classification of the tumors of the glioma group on a histogenetic basis with a correlated study of prognosis. Philadelphia: Lippincott; 1926. [24] Russel DS, Rubinstein LJ. Pathology of tumors of the nervous system. London: Edward Arnold; 1959. [25] Friedman NB. Germinoma of the pineal. Its identity with germinoma (“seminoma”) of the testis. Cancer Res 1947;7:363–8. [26] Jouvet A, Saint-Pierre G, Fauchon F, Privat K, Bouffet E, Ruchoux MM, et al. Pineal parenchymal tumors: a correlation of histological features with prognosis in 66 cases. Brain Pathol 2000;10:49–60. [27] Dandy WE. Operative experiences in cases of pineal tumors. Arch Surg 1936;33:19–46. [28] Dandy WE. Surgery of the brain, a monography. Lewis’ Practice of surgery, XII. Hagerstown (MD): W.F. Prior Co, Inc; 1945. [29] Horsley V. Discussion of paper of CMH Howell on tumors of the pineal body. Proc R Soc Med 1910;3:77–8. [30] Cushing H. The establishment of cerebral hernia as a decompressive measure for inaccessible brain tumors. Surg Gynecol Obstet 1905;1:297–314. [31] Howell CM. Tumours of the pineal body. Proc R Soc Med 1910;3:65–77. [32] Pendl G. Pineal and midbrain lesions. Wien, New York: Springer-Verlag; 1985. [33] Pussep L. Die operative Entfernungeiner Zyste der Glandula pinealis. Neurol Zentralb 1914;33:560–3. [34] Oppenheim H, Krause F. Operative Erfolge bei Geschwiilsten der Sehhugel-und Vierhugelgegend. Bed Klin Wochenschr 1913;50:2316–22. [35] Brunner CR, Rorshach H. Ubereinen fall von tumor der glandula pinealis cerebri. Cor Blatt Schweiz Arzte 1911:642–3. [36] Nassetti F. Dell’operabiltà delle vie d’accesso ai tumori della ghiandola pineale. Il Policlinico Sez Chir 1913;20:497–501. [37] Zulch KJ. Reflections on the surgery of the pineal gland (a glimpse into the past). Gleanings from medical history. Neurosurg Rev 1981;4(3):159–63. [38] Schmidek H. Pineal tumors. Philadelphia (PA): Masson Publishing; 1977. [39] Dandy WE. An operation for the removal of pineal tumors. Surg Gynecol Obstet 1921;33:113–9.
[40] Horrax G, Bailey P. Tumors of the pineal body. Arch Neurol Psych 1925;13(4):423–70. [41] Krause F. Operative Freilegung der Vierhuegel, nebst Beobchtungen uber Hirndruck und Dekompression. Zbl Chirurgie 1926;53:2812–9. [42] Foerster O. Ein fall vierhfigeltumordurch operation entfernt. Nervenkr Arch Psychiatr 1928;84:515–6. [43] Tandler J, Ranzi E. Chirurgische Anatomie und Operationtechnik des Zentralnervensystem. In: Kirschner M, Norman O, editors. Die Chirurgie. Berlin: Springer; 1920. [44] Camins MB, Schlesinger EB. Treatment of tumors of the posterior part of the third ventricle and the pineal region: a long-term follow-up. ActaNeurochir 1978;40:131–43. [45] Horrax G. Extirpation of a large pinealoma from a patient with pubertas precox: a new operative approach. Arch Neurol Psychiatr 1937;37:385–97. [46] Ward A, Spurling RG. The conservative treatment of third ventricle tumors. J Neurosurgery 1948;5(2):124–30. [47] Torkildsen A. Should extirpation be attempted in cases of neoplasm in or near the third ventricle of the brain? Experience with a palliative method. J Neurosurg 1948;5:249–75. [48] Zapletal B. Surgical approach to the region of incisura tentoria. Zentralbl Neurochir 1956;16(2):64–9. [49] Stein BM. The infratentorial supracerebellar approach to pineal lesions. J Neurosurg 1971;35(2):197–202. [50] Suzuki J, Iwabuchi. Surgical removal of pineal tumors (pinealoblastomas and teratomas). J Neurosurg 1965;23:565–71. [51] Jamieson KG. Excision of pineal tumors. J Neurosurg 1971;35:550–3. [52] Lapras C, Patet JD. Controversies, techniques, and strategies for pineal tumor surgery. In: Apuzzo MLJ, editor. Surgery of the third ventricle. Baltimore: Williams and Wilkins; 1987. p. 649–62. [53] Fukushima T, Ishijima B, Hirakawa K, et al. Ventriculofiberscope: a new technique of endoscopic diagnosis and operation: technical note. J Neurosurg 1973;38(2):251–6. [54] Robinson S, Cohen AR. The role of neuroendoscopy in the treatment of pineal region tumors. Surg Neurol 1997;48(4):360–7. [55] Brotchi J, Raftopulos C, Levier M, Dewitte O, Pirottes B, Vandesteen A, et al. Lesion of the pineal and tentorial region: occipito-parietal approach in the three-quarter prone position with infrasagittal craniotomy. Neurochirurgie 1991;37(6):410–5. [56] Brotchi J, Levier M, Raftopulos C, Dewitte O, Pirotte B, Noterman J. Threequarter prone approach to the pineal tentorial region; report of seven cases. Acta Neurochirurg Suppl (Wien) 1991;53:144–7. [57] Bruce JN, Ogden AT. Surgical strategies for treating patients with pineal region tumors. J Neuroncol 2004;69:221–36. [58] Pendl G. The surgery of pineal lesions. Historical perspective. In: Neuwelt EA, editor. Diagnosis and treatment of pineal region tumors. Baltimore (MD): Williams and Wilkins; 1984. p. 139–54. [59] Yasargil MG. Paramedian sub-occipital approach. In: Yasargil MG, editor. Microneurosurgery, 4B. New York: Thieme; 1995. p. 58–64. [60] Pearce JM. Parinaud’s syndrome. J Neurol Neurosurg Psychiatr 2005;76(1):99. [61] Hernesniemi J, Romani R, Albayrak BS, Lehto H, Dashti R, Ramsey C, et al. Microsurgical management of pineal region lesions: personal experience with 119 patients. Surg Neurol 2008;70:576–83. [62] Bruce JN. Pineal tumor. In: Winn RH, editor. Youman’s neurological surgery, 56, 5th ed. Philadelphia: Saunders, Elsevier; 2004. p. 1011–29.
Please cite this article in press as: Mottolese C, Szathmari A. History of the pineal region tumor. Neurochirurgie (2014), http://dx.doi.org/10.1016/j.neuchi.2013.03.005
ARTICLE IN PRESS Neurochirurgie xxx (2014) xxx–xxx
Disponible en ligne sur
www.sciencedirect.com
Report 2013: Tumors of the pineal region
History of the pineal region tumor Histoire de la tumeur de la région pinéale C. Mottolese ∗ , A. Szathmari Department of Paediatric Neurosurgery, Pierre-Wertheimer Hospital, CHU de Lyon, 59, boulevard Pinel, 69003 Lyon, France
a r t i c l e
i n f o
Article history: Received 25 March 2013 Received in revised form 27 March 2013 Accepted 30 March 2013 Available online xxx Keywords: History of pineal tumor History of pineal and pineal region surgery
a b s t r a c t The pineal gland has interested humans from millenniums. In this paper we review back in the history and the evolution of the pineal gland surgery. Originally, this surgery used to carry a high rate of morbidity and mortality. Nowadays the development of the anesthetic, radiological, surgical and intensive care techniques have been responsible of an improvement of the surgical results and better quality of life. It is always interesting to know from where we come. © 2014 Published by Elsevier Masson SAS.
r é s u m é Mots clés : Histoire de la glande pinéale Histoire de la chirurgie de la glande pinéale et de la région pinéale
La glande pinéale intéresse l’humanité depuis des millénaires. Dans cet article nous essayons de revoir l’histoire et l’évolution de la chirurgie de la glande pinéale. À l’origine, cette chirurgie était associée à un fort pourcentage de mortalité et morbidité. De nos jours, le développement des techniques d’anesthésie, de radiologie, de chirurgie et de soins intensifs a permis d’obtenir de bons résultats et une meilleure qualité de vie pour les patients. Il est toujours intéressant de savoir d’où l’on vient. © 2014 Publie´ par Elsevier Masson SAS.
It is difficult to report an exhaustive history of pineal gland and of the therapeutically strategies that have been developed but it seems important to us to remember some milestone about this subject as an introduction to a report concerning pineal tumours, also if other reviews on this particular topic can be found in literature. The pineal gland has interested humans from a long time because already, in China, during the reign of the Yellow Emperor (2697–2597 BC), have been found traces of this interest as reported by Veith [1]. In Hindu scriptures, the pineal gland was considered as one of the seven chakra: the crown chakra, representing the center of spiritual force [2,3]. Aelius Galenus (130–200 AC) reported that Herophilus (325–280) was the first to discover the pineal gland and to practice anatomical dissection in a scientific way and described the function of the gland as a valve or sphincter permitting to regulate the flow of “pneuma” from the third to the fourth ventricle.
∗ Corresponding author. E-mail address: [email protected] (C. Mottolese).
“Pneuma” was considered as the substance derived from air and responsible for thought (psycikon for Greeks) and also responsible of organic movements [4,5]. These anatomical and physiological considerations were unchanged until the Medieval Era and Andrea Vesalius (1514–1564); his new anatomical considerations were discussed and related in the “Humani Corporis Fabrica”, Libri Septem. In the same period, Niccolo’ Massa, an Italian anatomist, showed that in the ventricular system there was the liquor, the cerebro-spinal fluid [6]. René Descartes, French philosopher (1596–1650), affirmed that the pineal gland was the seat of the human soul, the seat of the “sensu communis” and consequently the pineal was the organ of the “res cogitans” the “anima”. The concept that information to the pineal gland was mediated by the eyes and optic nerves begin to develop. Francois Magendie (1783–1855), physiologist, advocated the function of tampon because the expansion or shrinkage of the body close off or open the aqueduct of Silvius. Gunz (1753) explained that the dementia was related to an impeded flow of the spirits caused by the pineal gland [7,8].
0028-3770/$ – see front matter © 2014 Published by Elsevier Masson SAS. http://dx.doi.org/10.1016/j.neuchi.2013.03.005
Please cite this article in press as: Mottolese C, Szathmari A. History of the pineal region tumor. Neurochirurgie (2014), http://dx.doi.org/10.1016/j.neuchi.2013.03.005
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New elements of comprehension of the human pineal physiology were reported with the development of anatomical and comparative studies of humans and animals including vertebrates and no vertebrates. Ahlborn and Rabl-Ruckhardt (1839–1906) showed the similarity between the non-mammalian pineal gland and the primary optic vesicles [9,10]. The role of pineal in reptiles and amphibian as photo sensory organ was elucidated and this function regressed and became vestigial in mammals [11,12]. Helena Blavatsky (1831–1891), advocating the third eye of Shiva, spoke of the third eye for human approaching the pineal gland to the organ of spiritual vision [13]. The demonstration of the two types of cells of the pineal gland was reported by Kolliker, preceding the hypothesis of Studnicka who announced that the pineal gland could have a glandular function and this function was also related to the precocious puberty of a patient with a pineal tumour [8]. Cajal thought that the nerve fiber of the pineal body was sympathetic and the body of the gland was a vascular structure [7]. Marburg reported that the activity of the pineal gland was that of regulating the hormonal cycles, and correlating the hypofunction of the gland with the apparition of a precocious puberty he explained the hypofunction with the destruction of the gland by the expansion of a pineal tumour [14,15]. During the Second World War, in 1940, the electron microscope confirmed the secretory activity of the pineal gland, that was provided by the pinealocytes, neurosecretory cells, while the glial cells assure their support [16]. Aaron Lerner, in 1958, discovered the hormone of the pineal gland that he called “melatonin” that was implicated in the regulation of the circadian rythms of sleep/wake, mainly in the normal sleep/wake rhythm [17,18]. According to Choudry, the first case of a pineal tumour was reported by Charles Drelincourt in the seventeen century, and Blane was the first in English literature to report a pineal tumour [19]. Morgagni, an Italian anatomist, reported and discussed the case of a man who harboured a calcified pineal gland of the size of an egg [20]. Henry Parinaud in 1883 described a syndrome characterized by a paralysis of the vertical gaze that was explained by the compression of the mesencephalic tectum by a growing lesion of the pineal gland. In 1875, a German pathologist, Karl Weigert, reported the first well documented pineal tumour that was a pineal teratoma, describing a tumour with squamous and columnar epithelium including hair and skin elements and describing the microscopic histology [21]. After the report of cases by Gutzeit in 1909, the relation between precocious puberty and pineal teratomas was definitively established. Krabbe, in his thesis “Histological Studies of Pineal Body”, was the first to use the term of “Pinealoma” [22]. This is the origin of evolution of histological classification of pineal tumours because Percival Bayley, Cushing and Bayley, followed by Russel, Rubestein, Zulch, Globus and Dorothy Russel and Nathan Friedman gave the basis of the histological classification of pineal tumours [23–25]. The pathological idea have evolved and a new classification has been proposed by the WHO with the main contribution of Anne Jouvet, in Lyon [26]. The difficulties of surgical approach for pineal tumours can explain that for long time pineal region tumours have been considered as inoperable and consequently the recommended strategy for their treatment has been the cure of hydrocephaly followed
by irradiation and why Dandy stated “Pineal tumours are perhaps the most dangerous of all intracranial tumours to attack surgically” [27,28]. The history of surgery of pineal tumours started at beginning of the century to 1905 when Victor Horsley tried to remove a pineal tumour by a infratentorial approach unsuccessfully, while in 1904 Cushing reported a bitemporal craniectomy for a patient who some weeks later died while the autopsy revealed a quadrigeminal plate tumour [29,30]. Conrad MH Howell, discussing at the Royal Accademy on “Tumors of the Pineal Body”, reported the comments of Horsley on the failure of the infratentorial approach preconizing a new surgical avenue through a supratentorial approach splitting the tentorium and this discussion is always present in the neurosurgical world [29,31]. Pappenheim reported a surgical procedure realized by Anxenfeld in 1906 in Freiburg, and Marburg in 1908 describing a palliative approach by a supracerebellar route. The patient did not survive the surgical procedure [32]. In 1910, Pussep used a transverse transtentorial approach to remove a pineal tumour using the splitting of the transverse sinus and the tentorium. The patient survived to the surgical intervention for three days [33]. Bailey and Jelliffe reported an attempt of removal while Rydygier proposed a punction through the corpus callosum to decrease the intracranial hypertension [32]. In 1911, Krause suggested that the supracerebellar infratentorial approach could be the avenue to adopt for pineal tumour although he denied any practical experience of this surgery [34]. Brunner tried to remove a pineal tumour by a parietal route but the venous deep structures carried problems of hemostasis that pushed him to adopt an infratentorial supracerebellar approach [35]. One year later, he chose a completely different approach through the corpus callosum but with a limited view of the tumour and a severe venous hemorrhage obliged him to abandon the procedure [35]. Nassetti proposed on laboratory animals the approach of pineal region resecting the longitudinal sinus and the straight sinus but without clinical experience [36]. In 1913, Krause used an infratentorial supracerebellar approach with a sitting position and, as reported by Zulch in 1981, this was the first patient treated with success: the patient was 10-year-old and the lesion measured 4 cm in diameter [34,37]. The success of the surgical procedure was due to the preservation of the venous system, developed dorsally, and lateral to the lesion, avoiding the main cause of surgical morbidity [32,38]. In 1921, Dandy described the posterior trancallosal approach. Dandy, in 1912, tried the parieto-occipital approach on the midline with the transection of the posterior half of the corpus callosum. In spite that this approach was particularly difficult, he used this avenue in humans with survival that did not exceed a year [32,39,40]. In 1926, Krause proposed again the ITSC approach in three patients with success because of no mortality [41]. Foerster was the second surgeon who reported a successful removal of a pineal tumour an occipital craniotomy was realized, a puncture of the lateral ventricle permitted the decompression of the brain and retraction of the occipital lobe from the falx and the tentorium with a more easy exposition of the pineal tumour [32,42]. He used the occipital transtentorial approach preconized by Tandler and Ranzi in their “Surgical Anatomical Textbook” [43]. In 1929, Peet removed a pineal tumour with the approach proposed by Dandy: the patient was irradiated postoperatively and had a good clinical result with possibility of working as painter as reported by Camins [44].
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Walker perfecting the Dandy’s approach reported ten cases and emphasized the advantages of this approach that for long time was considered the most useful for surgery of pineal lesions and the neurological evaluation of patients showed the presence of cortical function disorder as alexia without agraphia [27]. The lateral transcortical transventricular approach was reported by Van Wanegen in 1931 and the ventricular dilatation seemed to facilitate the removal of pineal tumours [4]. This approach was particularly interesting in cases of huge ventricular dilatation because the opening of a thin medial ventricular wall permitted a lateral view of the tumour and of the pineal region. Pratt and Brooks, in 1934, reported with success the removal of a pineal tumour using a sub-occipital transtentorial approach that was later publicized by many other surgeons and that became the approach adopted for tumour of the pineal region in Lyon. Horrax, in 1937, proposed the approach of the pineal region with a parieto-occipital lobectomy with the consequence of visual field amputation and seizures. The occipital lobectomy permitted to gain a large space to expose the pineal region but at the same time he stressed the importance of a more conservative approach treating hydrocephalus with a ventriculo-atrial shunt followed by a cerebral irradiation [45]. Ward and Spurling reported a series of 14 patients treated with a subtemporal decompression and irradiation [46], while Torkildsen proposed the ventriculocisternal shunt followed by irradiation [47]. At that time, the mortality was high: for Dandy in 1945: 20%; for Lemmen in 1953: 70%; for Ringert in 1954: 58,8%; and the diversion of the CSF with ventriculo-peritoneal or ventriculo-atrial shunts followed by irradiation was commonly used for tumours of the pineal region. Zapletal, in 1956, revisited the infratentorial approach of Krause reporting four patients operated but this approach was popularized by Stein who used the sitting position, the surgical microscope and extending the sub-occipital craniectomy at the level of the transverse sinus reported a very low morbidity associated with no perioperative mortality [48,49]. J. Suzuki, in 1965, reported 19 patients treated with the Van Wanegen approach and only 2 patients were free of complications after the surgery [50]. The occipital transtentorial approach was popularized in 1959 by Heppener, and, in 1966, by Poppen [32]. In 1971, Jamieson reported the modification of the sub-occipital transtentorial approach modifying the axis of approach that became more medial and modifying the opening of the tentorium permitting a better exposition of the vermian and quadrigeminal arachnoidal space and of the pineal region [51]. Lapras modified the Jamieson’s approach proposing a diamondshaped bone flap with the lateral superior bone hole at the level of the parietal bossing and modifying the retraction of the occipital lobe that improved the exposure of the deep pineal region [52]. Our philosophy of the sub-occipital transtentorial approach is intact and our attempts to reduce the enlargement of the bone flap have been abandoned. Indeed in our opinion, it is crucial to gain enough space to control the venous bridging system in case of tearing during the retraction of the occipital lobe. In this way, we are faithful to the principle of a large bone flap for the exposition of the pineal region. It is obvious that the history of the surgical approach of the pineal region has completely evolved with the advent of the microsurgical era that started with Marino, Stein, Dierssen, Humphreys, Kurze, Lapras. The choice of the approach is related to the plane that delineates the pineal region that is represented by the tentorial plane. In the 1970 era, the introduction of stereotaxy facilitated the study of pineal region tumours favoring the diagnosis of different types of lesions and contemporary pioneers of the endoscopic
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technology, as Fukushima, showed the possibility of visualizing the pineal region favoring the possibility to realize endoscopic biopsy and, sometimes, to treat hydrocephalus with a third ventriculostomy [53]. The endoscopic approach, favoring the treatment of hydrocephalus, the possibility of a histological diagnosis with a low morbidity is commonly proposed at the beginning of therapeutic strategies and Cohen was the first neurosurgeon to report this strategy [54]. In the modern period, the refinement of the endoscopic instrumentation has also permitted the endoscopic direct approach for removal of pineal tumours. The direct approaches to the pineal region in the large number of cases remain either infratentorial or supratentorial. The current application of microsurgical techniques for the infratentorial supracerebellar approach and for the sub-occipital transtentorial approach revisited by Lapras, Yasargil, Brotchi and others have allowed a dramatic reduction in mortality and in morbidity [55–59]. The surgical techniques have been associated with the development of the radiological techniques with a better definition of the relationships between the tumour and the surrounding anatomical structures and a better knowledge of the vascularization of lesions and the modern anesthesiological techniques including the improvement of the postoperative care have allowed to approach a nearly nil mortality [60]. As Herseniemi reported in the last years, surgeons have to remember the recommendations of Francis Bacon and Drake according to whom surgery has to be simple, fast with preservation of normal anatomy [61]. The pineal tumours are nowadays treated surgically in many center and even though the surgical approach of this region is challenging this surgery can be realized with good results and acceptable postoperative morbidity mainly in cases of benign lesions in children and adults patients. Postoperative adjunctive treatment should be indicated in cases of histological aggressive lesions [62]. In the future, the development of new technologies will permit safest surgery. The surgical approach has to be realized considering the citation of Charles IX, king of France that stated: “The most beautiful avenue in the world is the one that was argued in the best way”. References [1] Veith I. The Yellow Emperor’s classic of internal medicine. Berkeley and Los Angeles (CA): University of California Press; 2002. [2] Reiter R, Robinson J. Melatonin: your body’s natural wonder drug. New York (NY): Bantam Books; 1995. [3] Kappers J. Structure and functions of the epiphysis cerebri progress in Brain Research, 10. New York (NY): Elseiver; 1965. [4] Van Wanegen W. A surgical approach for the removal of certain pineal tumors. Surg Gynecol Obstet 1931;53:216–20. [5] Rand RW, Lemmen LJ. Tumors of the posterior portion of the third ventricle. J Neurosurg 1953;10(1):1–18. [6] Massa N, Weber G. Liber Introductorius Anatomiae. Firenze (Italy): Casa Editrice Leo S. Olschki; 2006. [7] Tilney F, Warren LF. The morphology and evolutional significance of the pineal body; being part of a contribution to the study of the epiphysis cerebri with an interpretation of the morphological, physiological and clinical evidence. Philadelphia: The Wistar Institute of Anatomy and Biology; 1919. [8] Heubner O. Tumor der glandulapinealis. Dtsch Med Wochenschr 1898;24:214. [9] Ahlborn F. Uber die bedeutung der zirbeldriise (glandulapinealis, commisur, Epiphysiscerebri). Z Zool 1884;40:331–7. [10] Rabl-Ruckhardt H. Ur deutung der zirbeldruse (epyphyse). Zool Anz 1886;9:536–47. [11] De Graaf HW. Bijdrage tot de kennis van den bouw en de ontwikkeling der epyphyse by Amphibian und Reptilian. Thesis. Leyden; 1886. [12] De Graaf HW. Zuranatomie und entwicklung der epiphysebei Amphibian und Reptilian. Zool Anz 1886;9:191–4. [13] Blavatski HP. The secret doctrine: the synthesis of science, religion and philosophy. London: Theosophycal Publishing Company; 1888.
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Please cite this article in press as: Mottolese C, Szathmari A. History of the pineal region tumor. Neurochirurgie (2014), http://dx.doi.org/10.1016/j.neuchi.2013.03.005