Harvey Cushing’s craniopharyngioma treatment: Part 2. Surgical strategies and results of his pioneering series

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OBJECTIVE

Harvey Cushing (1869–1939) developed pioneering surgical techniques for craniopharyngioma (CP) removal. This study exhaustively analyzes the pathological variables and surgical strategies that influenced Cushing’s results in his entire series of CP patients.

METHODS

The CP records from Cushing’s Brain Tumor Registry were carefully reviewed, as were his CP cases published in medical monographs and scientific reports.

RESULTS

One hundred twenty-four tumors with characteristics typical of CP comprise Cushing’s entire series (CP124). Cushing performed 198 surgical procedures in the patients in whom these tumors were treated, with a 23% mortality rate within the first 2 months after surgery. Three periods in Cushing’s CP surgical career can be differentiated: an early period (1901–1917, 39 patients) characterized by his use of the transsphenoidal approach and limited cyst drainage procedures, an intermediate period (1919–1925, 42 patients) in which the subfrontal approach was the standard procedure and maximal removal was attempted, and a late period (1926–1932, 43 patients) characterized by the use of air ventriculography for topographical diagnosis and limited resections via a transventricular approach. Among Cushing’s CP series were 92 cases that were pathologically verified (CP92). In this subcohort, the unilateral subfrontal approach was predominantly used (72% of cases), followed by the transsphenoidal (15%) and frontal transcortical-transventricular (8%) approaches. Drainage of the CP cystic component or partial excision of the solid component was achieved in 61% of the cases, subtotal removal in 23%, and macroscopic total removal in 10%. Satisfactory outcomes were obtained in 55% of the patients in CP92, whereas poor outcomes and/or death related to hypothalamic injury was observed in 28%. Postoperative symptoms related to hypothalamic dysfunction occurred 53% of the time. The subfrontal approach yielded the highest rates of radical removal (p < 0.001) and good outcomes (p = 0.01). Partial removals were associated with the highest rates of poor outcomes, including death (p = 0.009). Cushing’s removal of CPs with a primary infundibulo-tuberal topography or showing third ventricle invasion was associated with the highest rates of hypothalamic injury (p < 0.001) and the worst outcomes (p = 0.009).

CONCLUSIONS

Harvey Cushing’s techniques and surgical philosophy varied substantially throughout his career. The experience he gained with this large CP series made him aware of the importance of limiting the extent of tumor removal and leaving untouched the tumor portion strongly adhered to the hypothalamus.

ABBREVIATIONS BTR = Brain Tumor Registry; CP = craniopharyngioma; CP92 = Cushing’s subcohort of 92 pathologically verified CPs; CP124 = Cushing’s entire series of 124 CPs; DTC = decompressive temporal craniectomy; FTV = frontal transcortical-transventricular; IT = infundibulo-tuberal; SubF = subfrontal; TLT = trans–lamina terminalis; TSF = transsphenoidal; 3V = third ventricle; 3VF = 3V floor.

Article Information

Correspondence Ruth Prieto: Puerta de Hierro University Hospital, Madrid, Spain. rprieto29@hotmail.com.

INCLUDE WHEN CITING Published online October 5, 2018; DOI: 10.3171/2018.5.JNS18154.

R.P. and J.M.P. contributed equally to this work.

Disclosures The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

© AANS, except where prohibited by US copyright law.

Headings

Figures

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    Surgical approach, degree of tumor removal, and surgical outcome in CP124. A: Correlation between type of surgical approach used and degree of tumor removal. Note that the higher rates of subtotal and total CP removals were achieved with the SubF approach (38%), the SubF approach plus the TLT approach or optic chiasm splitting (SubF + TLT/Chi split; 27%), and the frontal transcortical-transventricular or transcallosal approach (FTV/TC; 50%; p < 0.001). B: Correlation between type of surgical approach and surgical outcome. The highest death rate occurred with the FTV/TC approach (37.5%), whereas more than 60% of cases treated via the SubF and transsphenoidal (TSF) approaches resulted in excellent or good outcomes (p = 0.010). C: Correlation between degree of tumor removal and surgical outcome. Note that the highest rate of excellent and good outcomes occurred following subtotal (69.5%) or gross-total (80%) removals. In contrast, no deaths were reported following cyst drainage or after biopsy of the lesion (p < 0.001). punct. = puncture. Figure is available in color online only.

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    Influence of CP topography on surgical outcome and pattern of tumor adherence in CP92. A: Correlation between CP topography and surgical outcome. The highest rate of excellent and good outcomes occurred among sellar/suprasellar (Sellar-SS; 81%) and pseudointraventricular (SS-Pseudo 3V; 75%) CPs, the two topographies sparing the hypothalamus. In contrast, in almost half of the CP cases with an infundibulo-tuberal (IT) topography (primarily developing within the hypothalamus), the patient had a poor outcome or died following surgery (p = 0.009). B: Correlation between CP topography and hypothalamic damage. Note that signs indicating hypothalamic damage were observed postoperatively in 90% of IT CPs and in 62% of lesions with a secondary intraventricular (Secondary 3V) topography (hypothalamic encroachment from an original sellar/suprasellar position; p < 0.001). C: Relationship between CP topography and pattern of tumor adherence. Half of the CPs with a strict intraventricular topography (3V-Strict) had a pedicle attachment to the inner lining of the 3V, whereas more than two-thirds of IT CPs either presented with a strong attachment to the 3V walls or had replaced the 3VF during their growth (p < 0.001). Figure is available in color online only.

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    Evolution of surgical strategies and results throughout Cushing’s career (CP124). A: Relationship between surgical periods and surgical approach. Note that the use of DTC and the TSF approach progressively declined from the initial to the final period. In contrast, the FTV/TC and SubF+TLT/Chi split were used increasingly in the late period (p < 0.001). B: Relationship between Cushing’s surgical periods and degree of tumor removal. Note that the highest rate of total removal occurred in the intermediate period (1919–1925, 16.7%), whereas the late period of Cushing’s career was characterized by the use of less radical partial or subtotal CP removals (p < 0.001). C: Correlation between Cushing’s surgical period and postoperative hypothalamic damage. Note that the lowest rate of postoperative hypothalamic damage occurred in the initial period (13%), whereas the highest one occurred in the second period (63%; p < 0.001), characterized by Cushing’s attempts at radical dissection of the CP-hypothalamus cleavage plane. D: Relationship between surgical periods and surgical outcome. Note that 87.5% of cases in the second period resulted in a poor outcome or postoperative death, whereas 68% of cases in the last period had an excellent or good outcome (p = 0.015), a result related to Cushing’s awareness of the vital importance of hypothalamus preservation and the use of less aggressive procedures. Figure is available in color online only.

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    Cushing’s surgical approaches to CPs. A1: Sublabial-TSF approach employed by Cushing from 1908 to 1929 for the removal of pituitary tumors and CPs. From Cushing: JAMA 63:1515–1525, 1914. Public domain. A2: Cushing’s sketches of the intraoperative view obtained with the TSF approach in a CP case (H.B., case 23). Note how the normal pituitary gland, pushed against the sellar floor by most CPs, is exposed at the opening of the sella floor, hindering access to the tumor. This major shortcoming made Cushing favor the SubF over the TSF approach in the 1920s. B1: Cushing’s SubF approach to CPs. Notice the wide exposure of this suprasellar prechiasmatic cyst between the stretched optic nerves obtained with this approach (W.C.C., case 44). B2 and B3: Cushing’s drawings of the CP cystic extensions in a pediatric patient (E.J., case 96). The cysts of this giant, multilobulated CP could be outlined and emptied via the SubF approach. C1: Subfrontal approach to a retrochiasmatic CP. Note the prefixed, swollen chiasm and the route employed to gain access to the intraventricular tumor, which protruded through the lamina terminalis and remained tightly attached to the optic chiasm and 3V walls. This patient died without regaining consciousness from cardiac complications due to hypothalamic injury (E.M.L., case 113). C2: Cushing’s drawings of a tumor found at autopsy. Note the primary IT topography of this lesion, whose solid growth was expanding within the hypothalamus and 3V, above an intact pituitary stalk. From Cushing: Papers Relating to the Pituitary Body, Hypothalamus and Parasympathetic Nervous System, Charles C. Thomas, 1932. D: Subfrontal TLT approach. This retrochiasmatic, cystic CP expanding within the 3V was emptied and partially removed through the opening of the lamina terminalis, in August 1926 (F.W., case 91). E: Subfrontal approach and chiasm splitting for CP removal. This method allowed access to the retrochiasmatic 3V portion of CPs hidden behind the optic chiasm (A.Z., case 93). Panels A2–C1 and D–E reproduced from Cushing’s BTR. Public domain. Courtesy of the Manuscript and Archives department of the Sterling Memorial Library, Yale University.

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    Cushing’s transventricular methods of approach to CPs expanding within the 3V. A: Cushing’s sketches of his first transcallosal procedure for the removal of an IT CP, performed on January 20, 1925 (A.M., case 75). B1: Midsagittal brain autopsy specimen showing a strictly intraventricular CP (L.G.B., case 78). This patient underwent two surgical procedures employing the SubF approach, which failed to provide a proper view of the intraventricular mass, which was only emptied and partially removed twice. B2: Cushing’s drawing showing the IT topography of a CP operated on using a SubF TLT approach in March 1927 (M.E.D., case 94). C: Cushing’s sketches showing an FTV technique, which he employed in April 1932, to successfully remove a papillary CP from the 3V (M.S.B., case 122). All panels reproduced from Cushing’s BTR. Public domain. Courtesy of the Manuscript and Archives department of the Sterling Memorial Library, Yale University.

References

  • 1

    Cohen-Gadol AAGeryk BBinder DKTubbs RS: Conquering the third ventricular chamber. J Neurosurg 111:5905992009

  • 2

    Cohen-Gadol AALaws ERSpencer DDDe Salles AAF: The evolution of Harvey Cushing’s surgical approach to pituitary tumors from transsphenoidal to transfrontal. J Neurosurg 103:3723772005

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Cohen-Gadol AASpencer DD: The Legacy of Harvey Cushing. Profiles of Patient Care. New York: Thieme2007 pp 193

  • 4

    Cushing H: The chiasmal syndrome of primary optic atrophy and bitemporal field defects in adults with normal sella turcica. Arch Ophtalmol (Paris) 3:5055511930

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5

    Cushing H: The establishment of cerebral hernia as a decompressive measure for inaccessible brain tumors; with the description of intermuscular methods of making the bone defect in temporal and occipital regions. Surg Gynecol Obstet 1:2973141905

    • Search Google Scholar
    • Export Citation
  • 6

    Cushing H: The hypophysis cerebri: clinical aspects of hyperpituitarism and of hypopituitarism. JAMA 53:2492551909

  • 7

    Cushing H: Intracranial Tumors. Notes Upon a Series of Two Thousand Verified Cases With Surgical Mortality Percentages Pertaining Thereto. Springfield, IL: Charles C. Thomas1932 pp 9398

    • Search Google Scholar
    • Export Citation
  • 8

    Cushing H: Papers Relating to the Pituitary Body Hypothalamus and Parasympathetic Nervous System. Springfield, IL: Charles C. Thomas 1932 pp 4356

    • Search Google Scholar
    • Export Citation
  • 9

    Cushing H: The Pituitary Body and Its Disorders. Philadelphia: JB Lippincott1912

  • 10

    Cushing H: Sexual infantilism with optic atrophy in cases of tumor affecting the hypophysis cerebri. J Nerv Ment Dis 33:7047161906

  • 11

    Cushing H: The Weir Mitchell Lecture. Surgical experiences with pituitary disorders. JAMA 63:151515251914

  • 12

    Dandurand CSepehry AAAsadi Lari MHAkagami RGooderham P: Adult craniopharyngioma: case series, systematic review and meta-analysis. Neurosurgery [epub ahead of print] 2017

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Fulton JF: Harvey Cushing. A Biography. Springfield, IL: Charles C. Thomas1946

  • 14

    Fulton JFBailey P: Tumors in the region of the third ventricle: their diagnosis and relation to pathological sleep. J Nerv Mental Dis 69:125145–164 261–277 1929

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15

    Henderson WR: The pituitary adenomata. A follow-up study of the surgical results in 338 cases (Dr. Harvey Cushing’s series). Br J Surg 26:8119211939

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16

    Kassam ABGardner PASnyderman CHCarrau RLMintz AHPrevedello DM: Expanded endonasal approach, a fully endoscopic transnasal approach for the resection of midline suprasellar craniopharyngiomas: a new classification based on the infundibulum. J Neurosurg 108:7157282008

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Müller HLMerchant TEPuget SMartinez-Barbera JP: New outlook on the diagnosis, treatment and follow-up of childhood-onset craniopharyngioma. Nat Rev Endocrinol 13:2993122017

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Pascual JMCarrasco RPrieto RGonzalez-Llanos FAlvarez FRoda JM: Craniopharyngioma classification. J Neurosurg 109:118011832008

  • 19

    Pascual JMPrieto R: Harvey Cushing and pituitary Case Number 3 (Mary D.): the origin of this most baffling problem in neurosurgery. Neurosurg Focus 41(1):E62016

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20

    Pascual JMPrieto RCarrasco R: Infundibulo-tuberal or not strictly intraventricular craniopharyngioma: evidence for a major topographical category. Acta Neurochir (Wien) 153:240324262011

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21

    Pascual JMPrieto RCarrasco RBarrios L: Displacement of mammillary bodies by craniopharyngiomas involving the third ventricle: surgical-MRI correlation and use in topographical diagnosis. J Neurosurg 119:3814052013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Pascual JMPrieto RCastro-Dufourny ICarrasco RStrauss SBarrios L: Development of intracranial approaches for craniopharyngiomas: an analysis of the first 160 historical procedures. Neurosurg Focus 36(4):E132014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Pascual JMPrieto RNavas MCarrasco R: Conquest of third ventricle craniopharyngiomas. J Neurosurg 112:115611612010

  • 24

    Pascual JMMongardi LPrieto RCastro-Dufourny IRosdolsky MStrauss S: Giovanni Verga (1879–1923), author of a pioneering treatise on pituitary surgery: the foundations of this new field in Europe in the early 1900s. Neurosurg Rev 40:5595752017

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Pendleton CAdams HMathioudakis NQuiñones-Hinojosa A: Sellar door: Harvey Cushing’s entry into the pituitary gland, the unabridged Johns Hopkins experience 1896–1912. World Neurosurg 79:3944032013

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26

    Prieto RPascual JM: Norman M. Dott, master of hypothalamic craniopharyngioma surgery: the decisive mentoring of Harvey Cushing and Percival Bailey at Peter Bent Brigham Hospital. J Neurosurg 127:9279402017

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27

    Prieto RPascual JMRosdolsky MBarrios L: Preoperative assessment of craniopharyngioma adherence: magnetic resonance imaging findings correlated with the severity of tumor attachment to the hypothalamus. World Neurosurg 110:e404e4262018

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28

    Prieto RPascual JMRosdolsky MCastro-Dufourny ICarrasco RStrauss S: Craniopharyngioma adherence: a comprehensive topographical categorization and outcome-related risk stratification model based on the methodical examination of 500 tumors. Neurosurg Focus 41(6):E132016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Puget SGarnett MWray AGrill JHabrand JLBodaert N: Pediatric craniopharyngiomas: classification and treatment according to the degree of hypothalamic involvement. J Neurosurg 106 (1 Suppl):3122007

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Qi SPan JLu Y (eds): Frontiers of Neurosurgery. Craniopharyngiomas—Classification and Surgical Treatment. Sharjah UAE: Bentham Science Publishers2017

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31

    Sainte-Rose CPuget SWray AZerah MGrill JBrauner R: Craniopharyngioma: the pendulum of surgical management. Childs Nerv Syst 21:6916952005

  • 32

    Shi XZhou ZWu BZhang YQian HSun Y: Outcome of radical surgical resection for craniopharyngioma with hypothalamic preservation: a single-center retrospective study of 1054 patients. World Neurosurg 102:1671802017

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Steňo JBízik ISteňo AMatejčík V: Craniopharyngiomas in children: how radical should the surgeon be? Childs Nerv Syst 27:41542011

  • 34

    Steňo JMalácek MBízik I: Tumor-third ventricular relationships in supradiaphragmatic craniopharyngiomas: correlation of morphological, magnetic resonance imaging, and operative findings. Neurosurgery 54:105110602004

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Yaşargil MG: Craniopharyngioma, in: Microneurosurgery. Microneurosurgery of CNS Tumors. New York: Thieme1996Vol IVB pp 205223

    • Export Citation

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