The 100 most-cited articles in spinal oncology

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OBJECTIVE

The authors' objective was to identify the 100 most-cited research articles in the field of spinal oncology.

METHODS

The Thomson Reuters Web of Science service was queried for the years 1864–2015 without language restrictions. Articles were sorted in descending order of the number of times they were cited by other studies, and all titles and abstracts were screened to identify the research areas of the top 100 articles. Levels of evidence were assigned on the basis of the North American Spine Society criteria.

RESULTS

The authors identified the 100 most-cited articles in spinal oncology, which collectively had been cited 20,771 times at the time of this writing. The oldest article on this top 100 list had been published in 1931, and the most recent in 2008; the most prolific decade was the 1990s, with 34 articles on this list having been published during that period. There were 4 studies with Level I evidence, 3 with Level II evidence, 9 with Level III evidence, 70 with Level IV evidence, and 2 with Level V evidence; levels of evidence were not assigned to 12 studies because they were not on therapeutic, prognostic, or diagnostic topics. Thirty-one unique journals contributed to the 100 articles, with the Journal of Neurosurgery contributing most of the articles (n = 25). The specialties covered included neurosurgery, orthopedic surgery, neurology, radiation oncology, and pathology. Sixty-seven articles reported clinical outcomes. The most common country of article origin was the United States (n = 62), followed by Canada (n = 8) and France (n = 7). The most common topics were spinal metastases (n = 35), intramedullary tumors (n = 18), chordoma (n = 17), intradural tumors (n = 7), vertebroplasty/kyphoplasty (n = 7), primary bone tumors (n = 6), and others (n = 10). One researcher had authored 6 studies on the top 100 list, and 7 authors had 3 studies each on this list.

CONCLUSIONS

This study identified the 100 most-cited research articles in the area of spinal oncology. The studies highlighted the multidisciplinary and multimodal nature of spinal tumor management. Recognition of historical articles may guide future spinal oncology research.

ABBREVIATIONSCY = citations per year.

OBJECTIVE

The authors' objective was to identify the 100 most-cited research articles in the field of spinal oncology.

METHODS

The Thomson Reuters Web of Science service was queried for the years 1864–2015 without language restrictions. Articles were sorted in descending order of the number of times they were cited by other studies, and all titles and abstracts were screened to identify the research areas of the top 100 articles. Levels of evidence were assigned on the basis of the North American Spine Society criteria.

RESULTS

The authors identified the 100 most-cited articles in spinal oncology, which collectively had been cited 20,771 times at the time of this writing. The oldest article on this top 100 list had been published in 1931, and the most recent in 2008; the most prolific decade was the 1990s, with 34 articles on this list having been published during that period. There were 4 studies with Level I evidence, 3 with Level II evidence, 9 with Level III evidence, 70 with Level IV evidence, and 2 with Level V evidence; levels of evidence were not assigned to 12 studies because they were not on therapeutic, prognostic, or diagnostic topics. Thirty-one unique journals contributed to the 100 articles, with the Journal of Neurosurgery contributing most of the articles (n = 25). The specialties covered included neurosurgery, orthopedic surgery, neurology, radiation oncology, and pathology. Sixty-seven articles reported clinical outcomes. The most common country of article origin was the United States (n = 62), followed by Canada (n = 8) and France (n = 7). The most common topics were spinal metastases (n = 35), intramedullary tumors (n = 18), chordoma (n = 17), intradural tumors (n = 7), vertebroplasty/kyphoplasty (n = 7), primary bone tumors (n = 6), and others (n = 10). One researcher had authored 6 studies on the top 100 list, and 7 authors had 3 studies each on this list.

CONCLUSIONS

This study identified the 100 most-cited research articles in the area of spinal oncology. The studies highlighted the multidisciplinary and multimodal nature of spinal tumor management. Recognition of historical articles may guide future spinal oncology research.

ABBREVIATIONSCY = citations per year.

In the last decades, spinal oncology has emerged as a separate subspecialty,114 reflecting years of research focused on innovative techniques for controlling spinal tumors and managing the pain and pathophysiology arising from these types of cancers.84 Although management of some diseases may involve few specialists, patients with spinal tumors are usually treated by a multidisciplinary team, including neurosurgeons, orthopedic surgeons, oncologists, radiation oncologists, and neurologists.84 Thus, the spinal oncology literature encompasses numerous researchers and countries, specialties, and scientific journals.

Citation analysis is a systematic approach for identifying scientific studies that have a high impact on medicine. This type of analysis has been applied to the literature on general neurosurgery,88 orthopedic surgery,67 otolaryngology,92 urology,64 and plastic surgery.76 Although bibliometric analyses have been performed on spinal surgery as a whole,84 as well as on spinal deformity surgery85 and lumbar spine surgery,103 little is known about the most frequently cited articles specifically related to spinal oncology.

Therefore, the purpose of this study was to identify the 100 most-cited articles on spinal tumors in an effort to identify important contributions to the literature in this field.

Methods

The citation indexing service of Thomson Reuters Web of Science was queried.103 The search algorithm ([spine OR spinal OR vertebral] AND [tumor OR neoplasm OR cancer OR metastases]) was used in the “Topic” field to identify articles of interest. The following search parameters were used: 1) articles published in the years 1864–2015, and 2) all languages. The articles retrieved were then sorted in descending order of times cited.

All authors then reviewed the article titles and abstracts to identify the 100 most-cited articles in the area of spinal oncology. Data such as title, authors, author specialty, journal of publication, year of publication, number of citations, article category, and country of origin were recorded. The levels of evidence of the studies were assigned according to therapeutic, prognostic, and diagnostic criteria set by the North American Spine Society (https://www.spine.org/Portals/0/Documents/ResearchClinicalCare/LevelsOfEvidence.pdf). Under these criteria, Level I studies correspond to high-quality randomized controlled trials or systematic reviews of Level I randomized trials; Level II studies correspond to lesser-quality randomized controlled trials, prospective comparative studies, or systematic reviews of Level II studies; Level III studies correspond to case-control studies, retrospective comparative studies, or systematic reviews of Level III studies; Level IV studies correspond to case series; and Level V studies correspond to case reports or expert opinions.

To control for year of publication, a citations per year (CY) index was calculated as follows: CY index = total number of article citations/years the article has been published (up to 2015).

Results

Our search algorithm retrieved 157,468 articles, and the top 100 articles on topics related to spinal oncology were identified according to the number of times they were cited by other studies (Table 1). The articles on this top 100 list were cited between 120 (article Nos. 96–100) and 1164 times (top article), and all 100 articles had been collectively cited 20,771 times (with a mean number of citations of 207.7 for each paper). The oldest article on the top 100 list was from 1931, and the most recent from 2008. Ninety-nine articles were written in English, and 1 was written in French. The list comprised 4 Level I evidence studies, 3 Level II evidence studies, 9 Level III evidence studies, 70 Level IV evidence studies, and 2 Level V evidence studies; levels of evidence were not assigned to 12 studies because they were not on therapeutic, prognostic, or diagnostic topics. The top article according to the CY index had been cited 55.2 times per year and was No. 5 on the top 100 list, and the bottom article had been cited 1.61 times per year (No. 72 on the top 100 list). The most prolific decade was the 1990s, with 34 articles on the top 100 list (Table 2).

TABLE 1.

The top 100 most-cited articles in spinal oncology ranked by number of times cited

RankAuthors & YearArticle TitleJournalSpecialtyTotal No. of CitationsLevel of EvidenceCY (rank)
1Batson, 1940The function of the vertebral veins and their role in the spread of metastasesAnnals of SurgeryAnatomy1164NA15.52 (15)
2Galibert et al., 1987Preliminary note on the treatment of vertebral angioma by percutaneous acrylic vertebroplastyNeurochirurgieNeuroradiology1006IV35.93 (2)
3Cotten et al., 1996Percutaneous vertebroplasty for osteolytic metastases and myeloma: effects of the percentage of lesion filling and the leakage of methylmethacrylate at clinical follow-upRadiologyRadiology628IV33.05 (3)
4Gilbert et al., 1978Epidural spinal-cord compression from metastatic tumor: diagnosis and treatmentAnnals of NeurologyNeurology, radiology, & radiation therapy558III15.08 (19)
5Patchell et al., 2005Direct decompressive surgical resection in the treatment of spinal cord compression caused by metastatic cancer: a randomised trialThe LancetNeurosurgery552I55.20 (1)
6Weill et al., 1996Spinal metastases: indications for and results of percutaneous injection of acrylic surgical cementRadiologyNeuroradiology487IV25.63 (7)
7Tomita et al., 2001Surgical strategy for spinal metastasesSpineOrthopedic surgery383IV27.36 (6)
8Fourney et al., 2003Percutaneous vertebroplasty and kyphoplasty for painful vertebral body fractures in cancer patientsJournal of NeurosurgeryNeurosurgery344IV28.67 (5)
9McCormick et al., 1990Intramedullary ependymoma of the spinal cordJournal of NeurosurgeryNeurosurgery334IV13.36 (22)
10Young et al., 1980Treatment of spinal epidural metastases. Randomized prospective comparison of laminectomy and radiotherapyJournal of NeurosurgeryNeurosurgery & radiotherapy288I8.23 (43)
11Tomita et al., 1997Total en bloc spondylectomy. A new surgical technique for primary malignant vertebral tumorsSpineOrthopedic surgery287IV15.94 (13)
12Higinbotham et al., 1967Chordoma. Thirty-five-year study at Memorial HospitalCancerRadiology282IV5.88 (62)
13Dahlin & MacCarty, 1952ChordomaCancerNeurosurgery & pathology282IV4.48 (84)
14Barron et al., 1959Experiences with metastatic neoplasms involving the spinal cordNeurologyPathology279IV4.98 (77)
15Greenberg et al., 1980Epidural spinal cord compression from metastatic tumor: results with a new treatment protocolAnnals of NeurologyNeurology & radiation therapy261IV7.46 (50)
16Tokuhashi et al., 1990Scoring system for the preoperative evaluation of metastatic spine tumor prognosisSpineOrthopedic surgery260IV10.40 (33)
17Sen & Sekhar, 1990An extreme lateral approach to intradural lesions of the cervical spine and foramen magnumNeurosurgeryNeurosurgery255IV10.20 (34)
18Rich et al., 1985Clinical and pathologic review of 48 cases of chordomaCancerRadiation therapy, pathology, & orthopedic surgery251IV8.37 (42)
19Gerszten et al., 2007Radiosurgery for spinal metastases: clinical experience in 500 cases from a single institutionSpineNeurosurgery & radiation oncology246IV30.75 (4)
20McMaster et al., 2001Chordoma: incidence and survival patterns in the United States, 1973–1995Cancer Causes & ControlGenetic epidemiology245NA17.50 (11)
21Tokuhashi et al., 2005A revised scoring system for preoperative evaluation of metastatic spine tumor prognosisSpineOrthopedic surgery240III24.00 (8)
22Constans et al., 1983Spinal metastases with neurological manifestations. Review of 600 casesJournal of NeurosurgeryNeurosurgery240IV7.50 (48)
23Bergh et al., 2000Prognostic factors in chordoma of the sacrum and mobile spine: a study of 39 patientsCancerOrthopedic surgery & pathology229IV15.27 (17)
24Maranzano & Latini, 1995Effectiveness of radiation therapy without surgery in metastatic spinal cord compression: final results from a prospective trialInternational Journal of Radiation Oncology, Biology, PhysicsRadiation oncology229II11.45 (28)
25Boriani et al., 1997Primary bone tumors of the spine. Terminology and surgical stagingSpineOrthopedic surgery220NA12.22 (25)
26Chambers & Schwinn, 1979Chordoma. A clinicopathologic study of metastasisAmerican Journal of Clinical PathologyPathology201IV5.58 (67)
27Dudeney et al., 2002Kyphoplasty in the treatment of osteolytic vertebral compression fractures as a result of multiple myelomaJournal of Clinical OncologyOrthopedic surgery197IV15.15 (18)
28Ryu et al., 2001Image-guided hypo-fractionated stereotactic radiosurgery to spinal lesionsNeurosurgeryNeurosurgery & radiation oncology197IV14.0 (20)
29Black, 1979Spinal metastasis: current status and recommended guidelines for managementNeurosurgeryNeurosurgery197NA5.47 (69)
30Ryu et al., 2003Image-guided and intensity-modulated radiosurgery for patients with spinal metastasesCancerRadiation oncology & neurosurgery192IV16.00 (12)
31Robertson et al., 1998Survival and prognostic factors following radiation therapy and chemotherapy for ependymomas in children: a report of the Children's Cancer GroupJournal of NeurosurgeryMultidisciplinary191IV11.24 (30)
32Wong et al., 1990Spinal metastases: the obvious, the occult, and the impostorsSpineOrthopedic surgery & pathology191NA7.64 (45)
33Sonneland et al., 1985Myxopapillary ependymoma. A clinicopathologic and immunocytochemical study of 77 casesCancerNeurosurgery & pathology189IV6.30 (59)
34Cooper & Epstein, 1985Radical resection of intramedullary spinal cord tumors in adults. Recent experience in 29 patientsJournal of NeurosurgeryNeurosurgery187IV6.23 (60)
35York et al., 1999Sacral chordoma: 40-year experience at a major cancer centerNeurosurgeryNeurosurgery, pathology, surgical oncology, & radiation oncology181IV11.31 (29)
36Catton et al., 1996Chordoma: long-term follow-up after radical photon irradiationRadiotherapy and OncologyRadiation oncology, surgical oncology, & oncological pathology180IV9.47 (38)
37Gokaslan et al., 1998Transthoracic vertebrectomy for metastatic spinal tumorsJournal of NeurosurgeryNeurosurgery, thoracic surgery, & cardiovascular surgery179IV10.53 (32)
38Tomita et al., 1994Total en bloc spondylectomy for solitary spinal metastasesInternational OrthopaedicsOrthopedic surgery179IV8.52 (39)
39Yuh et al., 1989Vertebral compression fractures: distinction between benign and malignant causes with MR imagingRadiologyRadiology177IV6.81 (53)
40Harrington, 1981The use of methylmethacrylate for vertebral-body replacement and anterior stabilization of pathological fracture-dislocations of the spine due to metastatic malignant diseaseJournal of Bone & Joint Surgery, American VolumeOrthopedic surgery175IV5.15 (74)
41Byrne, 1992Spinal cord compression from epidural metastasesThe New England Journal of MedicineNeurology174NA7.57 (47)
42Loblaw & Laperriere, 1998Emergency treatment of malignant extradural spinal cord compression: an evidence-based guidelineJournal of Clinical OncologyRadiation oncology171I10.06 (35)
43Harrington, 1986Metastatic disease of the spineJournal of Bone & Joint Surgery, American VolumeOrthopedic surgery169NA5.83 (65)
44Suit et al., 1982Definitive radiation therapy for chordoma and chondrosarcoma of base of skull and cervical spineJournal of NeurosurgeryRadiation medicine169IV5.12 (75)
45Bataille & Sany, 1981Solitary myeloma: clinical and prognostic features of a review of 114 casesCancerRheumatology169III4.97 (78)
46Barone & Elvidge, 1970Ependymomas. A clinical surveyJournal of NeurosurgeryNeurology & neurosurgery169IV3.76 (91)
47Epstein et al., 1993Adult intramedullary spinal cord ependymomas: the result of surgery in 38 patientsJournal of Neurosurgery Neurosurgery167IV7.59 (46)
48Algra et al., 1991Detection of vertebral metastases: comparison between MR imaging and bone scintigraphyRadiographicsRadiology, health sciences, & clinical oncology166III6.92 (52)
49Spetzler et al., 2002Modified classification of spinal cord vascular lesionsJournal of NeurosurgeryNeurosurgery164NA12.62 (24)
50Sundaresan et al., 1985Treatment of neoplastic epidural cord compression by vertebral body resection and stabilizationJournal of NeurosurgeryNeurosurgery164IV5.47 (70)
51Baker et al., 1990Benign versus pathologic compression fractures of vertebral bodies: assessment with conventional spin-echo, chemical-shift, and STIR MR imagingRadiologyRadiology & orthopedic surgery162III6.48 (58)
52Guidetti et al., 1981Long-term results of the surgical treatment of 129 intramedullary spinal gliomasJournal of NeurosurgeryNeurosurgery160IV4.71 (81)
53Cummings et al., 1983Chordoma: the results of megavoltage radiation therapyInternational Journal of Radiation Oncology, Biology, PhysicsRadiation oncology159IV4.97 (79)
54Ehni & Love, 1945Intraspinal lipomas: report of cases, review of the literature, and clinical and pathologic studyArchives of Neurology & PsychiatryNeurosurgery158IV2.26 (98)
55Chang et al., 2007Phase I/II study of stereotactic body radiotherapy for spinal metastasis and its pattern of failureJournal of Neurosurgery: SpineRadiation oncology, neurosurgery, radiation physics, biomathematics, & symptom research154II19.25 (10)
56Cooper, 1989Outcome after operative treatment of intramedullary spinal cord tumors in adults: intermediate and long-term results in 51 patientsNeurosurgeryNeurosurgery152IV5.85 (64)
57Sundaresan et al., 1979Spinal chordomasJournal of NeurosurgeryNeurosurgery, radiation therapy, & pathology152IV4.22 (87)
58Dupuy et al., 2000Radiofrequency ablation of spinal tumors: temperature distribution in the spinal canalAmerican Journal of RoentgenologyRadiology150NA10.00 (36)
59Bach et al., 1990Metastatic spinal cord compression. Occurrence, symptoms, clinical presentation and prognosis in 398 patients with spinal cord compressionActa NeurochirugicaOncology, neurology, & neurosurgery149IV5.96 (61)
60Yamada et al., 2008High-dose, single-fraction image-guided intensity-modulated radiotherapy for metastatic spinal lesionsInternational Journal of Radiation Oncology, Biology, PhysicsRadiation oncology, neurosurgery, medical physics, & biostatistics148IV21.14 (9)
61Constantini et al., 2000Radical excision of intramedullary spinal cord tumors: surgical morbidity and long-term follow-up evaluation in 164 children and young adultsJournal of NeurosurgeryNeurosurgery, neurology, & pathology146IV9.73 (37)
62Fox & Onofrio, 1993The natural history and management of symptomatic and asymptomatic vertebral hemangiomasJournal of NeurosurgeryNeurosurgery144IV6.55 (57)
63Cohen et al., 1989Malignant astrocytomas of the spinal cordJournal of NeurosurgeryNeurosurgery & neurooncology142IV5.46 (71)
64Boriani et al., 2006Chordoma of the mobile spine: fifty years of experienceSpineOrthopedic surgery141IV15.67 (14)
65Hamilton et al., 1995Preliminary clinical experience with linear accelerator-based spinal stereotactic radiosurgeryNeurosurgeryNeurosurgery & radiation oncology141IV7.05 (51)
66Findlay, 1984Adverse effects of the management of malignant spinal cord compressionJournal of Neurology, Neurosurgery & PsychiatryNeurosurgery141III4.55 (83)
67Vujovic et al., 2006Brachyury, a crucial regulator of notochordal development, is a novel biomarker for chordomasJournal of PathologyBiomedical research, oral pathology, neural development, & orthopedic surgery139NA15.44 (16)
68Levy et al., 1982Spinal cord meningiomaJournal of NeurosurgeryNeurosurgery136IV4.12 (88)
69Rades et al., 2005Evaluation of five radiation schedules and prognostic factors for metastatic spinal cord compressionJournal of Clinical OncologyRadiation oncology135III13.50 (21)
70Bauer & Wedin, 1995Survival after surgery for spinal and extremity metastases. Prognostication in 241 patientsActa Orthopedica ScandinavicaOrthopedic surgery135III6.75 (54)
71Edelson et al., 1972Intramedullary spinal cord metastases. Clinical and radiographic findings in nine casesNeurologyNeurology135IV3.14 (96)
72Kernohan et al., 1931Intramedullary tumors of the spinal cord: A review of fifty-one cases with an attempt at histologic classificationArchives of Neurology & PsychiatryPathology135IV1.61 (100)
73Wise et al., 1999Complication, survival rates, and risk factors of surgery for metastatic disease of the spineSpineOrthopedic surgery134IV8.38 (41)
74Harrington, 1984Anterior cord compression and spinal stabilization for patients with metastatic lesions of the spineJournal of NeurosurgeryOrthopedic surgery134IV4.32 (85)
75Weiss, 1955A metastasizing ependymoma of the cauda equinaCancerNA134V6.70 (56)
76Solero et al., 1989Spinal meningiomas: review of 174 operated casesNeurosurgeryNeurosurgery132IV5.08 (76)
77Epstein et al., 1992Adult intramedullary astrocytomas of the spinal cordJournal of NeurosurgeryNeurosurgery131IV5.70 (66)
78Volpe & Mazabraud, 1983A clinicopathologic review of 25 cases of chordoma (a pleomorphic and metastasizing neoplasm)American Journal of Surgical PathologyPathology131IV4.09 (89)
79Boriani et al., 1996En bloc resections of bone tumors of the thoracolumbar spine. A preliminary report on 29 patientsSpineOrthopedic surgery128IV6.74 (55)
80Sundaresan et al., 1991Treatment of neoplastic spinal cord compression: results of a prospective studyNeurosurgeryNeurosurgery128II5.33 (73)
81Fuchs et al., 2005Operative management of sacral chordomaJournal of Bone & Joint Surgery, American VolumeOrthopedic surgery & surgical pathology127IV12.70 (23)
82Murphy & Deramond, 2000Percutaneous vertebroplasty in benign and malignant diseaseNeuroimaging Clinics of North AmericaRadiology127NA8.47 (40)
83Bruce & Schut, 1979Spinal lipomas in infancy and childhoodChilds BrainNeurosurgery126IV3.50 (93)
84Eimoto et al., 1978Plasma cell granuloma (inflammatory pseudotumor) of the spinal cord meninges: report of a caseCancerNeurosurgery126V3.41 (94)
85Livingston & Perrin, 1978The neurosurgical management of spinal metastases causing cord and cauda equina compressionJournal of NeurosurgeryNeurosurgery125IV3.38 (95)
86Sørensen et al., 1990Metastatic epidural spinal cord compression. Results of treatment and survivalCancerOncology, neurology, & neurosurgery124IV4.96 (80)
87Cosgrove et al., 1988Cavernous angiomas of the spinal cordJournal of NeurosurgeryNeurosurgery124IV4.59 (82)
88Laredo et al., 1986Vertebral hemangiomas: radiologic evaluationRadiologyRadiology124IV4.28 (86)
89Stark et al., 1982Spinal metastases. A retrospective survey from a general hospitalBrainNeurology & clinical epidemiology124IV3.76 (90)
90Weigel et al., 1999Surgical management of symptomatic spinal metastases. Postoperative outcome and quality of lifeSpineOrthopedic surgery123IV7.69 (44)
91Cristante & Herrmann, 1994Surgical management of intramedullary spinal cord tumors: functional outcome and sources of morbidityNeurosurgeryNeurosurgery123IV5.86 (63)
92Gerszten et al., 2004CyberKnife frameless stereotactic radiosurgery for spinal lesions: clinical experience in 125 casesNeurosurgeryNeurosurgery & radiation oncology122IV11.09 (31)
93Mullan et al., 1966The use of an anterior approach to ventrally placed tumors in the foramen magnum and vertebral columnJournal of NeurosurgeryNeurosurgery & otolaryngology122IV2.49 (97)
94Coman & deLong, 1951The role of the vertebral venous system in the metastasis of cancer to the spinal column; experiments with tumor-cell suspensions in rats and rabbitsCancerPathology122NA1.91 (99)
95Herman et al., 1993Analysis of 153 patients with myelomeningocele or spinal lipoma reoperated upon for a tethered cord. Presentation, management and outcomePediatric NeurosurgeryNeurosurgery121IV5.50 (68)
96Loblaw et al., 2005Systematic review of the diagnosis and management of malignant extradural spinal cord compression: Cancer Care Ontario Practice Guidelines Initiative's Neuro-Oncology Disease Site GroupJournal of Clinical OncologyRadiation oncology & medicine120I12.00 (26)
97Klimo et al., 2005A meta-analysis of surgery versus conventional radiotherapy for the treatment of metastatic spinal epidural diseaseNeuro-OncologyNeurosurgery, family & preventive medicine, & spinal oncology120III12.00 (27)
98Cheng et al., 1999Lumbosacral chordoma. Prognostic factors and treatmentSpineOrthopedic surgery120IV7.50 (49)
99Bjornsson et al., 1993Chordoma of the mobile spine. A clinicopathologic analysis of 40 patientsCancerSurgical pathology & neurosurgery120IV5.45 (72)
100Epstein & Epstein, 1982Surgical treatment of spinal cord astrocytomas of childhood. A series of 19 patientsJournal of NeurosurgeryNeurosurgery120IV3.64 (92)
NA = not assigned.
TABLE 2.

Decades of publication

DecadeNo. of Articles (n = 100)
1930s1
1940s2
1950s3
1960s2
1970s9
1980s26
1990s34
2000s23

The top 100 articles were published in 31 different journals, with the Journal of Neurosurgery contributing most studies (i.e., 25 articles), followed by Cancer and Spine, (each having published 12 articles on this list) (Table 3). When we analyzed the articles by study scope and type, 67 were identified as clinical outcome studies (i.e., case series, retrospective cohort studies, prospective studies, and randomized controlled trials), 9 were review articles (including systematic reviews and meta-analyses), 6 were anatomical or pathological studies, 5 were technical notes, 4 were staging or prognostic studies, 4 were radiology studies, 2 were basic science or animal studies, 2 were case reports, and 1 was an epidemiological study. The most common article topics were spinal metastases (n = 35), followed by intramedullary tumors (n = 18), chordoma (n = 17), intradural tumors (n = 7), vertebroplasty or kyphoplasty (n = 7), primary bone tumors (n = 6), and others (n = 10).

TABLE 3.

Journals of publication

JournalNo. of Articles (n = 100)
Journal of Neurosurgery*25
Cancer12
Spine12
Neurosurgery10
Radiology5
Journal of Clinical Oncology4
International Journal of Radiation Oncology, Biology, Physics3
Journal of Bone and Joint Surgery, American Volume3
Annals of Neurology2
Archives of Neurology and Psychiatry2
Neurology2
Others20

Also includes Journal of Neurosurgery: Spine, a separate journal that started publication in 1999 (1 article on the top 100 list was from JNS: Spine).

These include journals that each contributed 1 article to the top 100 article list.

The country with the highest number of articles on the top 100 list was the United States (n = 62), followed by Canada and France, with 8 and 7 articles each, respectively (Table 4). The author with the largest number of articles on the top 100 list was Fred J. Epstein (sometimes cited as Epstein, F.) with 6 articles, followed by K. D. Harrington (United States), Z. L. Gokaslan (United States), K. Tomita (Japan), N. Kawahara (Japan), S. Boriani (Italy), R. Biagini (Italy), and N. Sundaresan (United States), who each had authored or coauthored 3 articles on this list.

TABLE 4.

Countries of article origin

Country of OriginNo. of Articles (n = 100)
United States62
Canada8
France7
Italy6
Japan6
Germany3
United Kingdom3
Denmark2
Sweden2
Netherlands1

Discussion

Spinal oncology has exponentially grown during the last decades, currently involves numerous specialties, and is considered by many a distinct subspecialty.114 In this study, we sought to identify the most-cited 100 articles in spinal oncology, in an effort to gain insight into the history and future directions of spinal tumor research. Not surprisingly, we found that the top 100 most-cited articles were written by authors in a variety of specialties, including neurosurgery, orthopedic surgery, neurology, pathology, radiology, and radiation oncology. In contrast to other research fields in which most high-impact articles are published in only a few journals,88 the most-cited articles pertaining to spinal oncology were published in 31 different journals, also reflecting the multidisciplinary nature of spinal tumor research.

The article that had received the most citations on our top 100 list was an anatomical pathology study by Oscar Vivian Batson, in which the author described a valveless venous system (now known as Batson's plexus) that connects the deep pelvic and thoracic veins to the vertebral venous plexus, a circulation system that most likely is involved in the spread of metastatic disease to the spine.8 This article was No. 1 on the list when ranked by the total number of received citations, but it was ranked No. 15 according to the CY index, with 15.52 citations per year since its publication in 1940. The second and third most-cited articles were by French authors, and both studies described vertebroplasty and kyphoplasty, techniques used to treat intractable pain and provide stability to osteoporotic or pathological compression fractures;32,51 the description of vertebroplasty for spinal angiomas by Galibert and colleagues was the only article on the list in a language other than English (French in this case). These 2 articles were No. 2 and No. 3 also on the CY index list, and their high ranks on both lists support the assertion that both of these studies made a significant impact on the management of pathological compression fractures. Notably, vertebroplasty and kyphoplasty were also the focus of articles that were ranked No. 6 and 8 according to the CY index; in both studies, the authors examined the role of these techniques in the treatment of pathological fractures due to metastatic disease.

Two randomized controlled trials were among the top 10 articles on the top 100 list. A trial by Young et al. published in 1980 investigated the outcomes among patients with metastatic epidural spinal cord compression treated with laminectomy plus radiotherapy versus patients treated with radiotherapy alone; the authors reported that the 2 treatment modalities do not significantly differ in providing pain relief or in improving ambulation or sphincter function.123 This trial led to the general belief that outcomes after radiotherapy alone can be equivalent to those after laminectomy without instrumentation. Several years later, Patchell and colleagues reported outcomes of “direct decompressive surgery,” in which the pathological compression (most often located anteriorly to the spinal canal) was addressed anteriorly rather than posteriorly via a laminectomy.87 The findings of this trial indicated a significant treatment difference: patients who underwent direct decompression plus radiotherapy were more likely to walk after treatment and retain the ability to walk longer distances than patients who underwent only radiation.87 The study by Patchell et al. had received 552 citations, and was one of the few articles on our top 10 list published in a high–impact factor medical journal (The Lancet). More importantly, however, this article was ranked No. 1 according to the CY index, with 55.2 citations per year since its publication in 2005; this highlights the impact this study had on the management of metastatic epidural spinal cord compression.

Another noteworthy article on our top 10 list was the study by Tomita et al. (from Japan), which was ranked No. 7 on the regular list and No. 6 on the CY index list (with 27.36 citations per year since 2001), and in which the authors described a surgical strategy to approach spinal metastases.112 This strategy was based on those reported in several other studies on the top 100 list, mainly the initial report of en bloc spondylectomy for spinal tumors also by Tomita et al. (articles No. 11 and 38) and of the Tokuhashi scoring system (article No. 16). When examining studies by research topic, we found that more than one-third of the articles had a focus on spinal metastases, a disease condition that is the most common type of spinal tumor and observed in 36% of patients who die of cancer.120

The second most common topic among the 100 most-cited articles was intramedullary tumors. Although these tumors account for only 2%–4% of all CNS tumors,95 18 articles on the topic of intramedullary tumors were on the top 100 list; these articles focused on outcomes after surgery for ependymoma, cavernous angioma, gliomas, and other tumors. Research focused on chordoma was the third most common area on the top 100 list, with 17 articles (articles No. 12, 13, 18, 20, 23, 26, 35, 36, 44, 53, 57, 64, 67, 78, 81, 98, and 99) investigating the genes involved in chordoma, outcomes after surgery or radiation for chordoma, epidemiology of this disease, and other chordoma-related topics. Chordoma has an estimated incidence of 0.08 per 100,000 cases, and is considered the most common primary malignant bone tumor of the sacrum and mobile spine.79 Although relatively rare, significant efforts have been directed toward identifying a cure for this disease. Current research has focused on stereotactic body radiotherapy, proton-beam therapy, and novel agents such as nilotinib, dasatinib, and imatinib (all tyrosine kinase inhibitors) to treat chordoma patients.17,18

The most prolific decade was the 1990s with 34 articles. Eighty-three of the 100 articles were published after 1980; this observation is similar to findings by Steinberger et al. who examined the top 100 articles published on lumbar spine surgery.103 The oldest article on our top 100 list was from 1931 by the Irish-American pathologist James Watson Kernohan and colleagues (article No. 72), in which the authors described pathological findings of intramedullary tumors.68 The most recent was from 2008 by radiation oncologist Yamada and colleagues (article No. 60), in which the authors examined the effect of high-dose, single-fraction, image-guided, intensity-modulated radiotherapy for local tumor control in patients with metastatic spinal lesions.121 This article was No. 60 on the top 100 list and No. 9 according to the CY index (21.14 CY since 2008).

Although authors from the United States contributed most of the studies to the top 100 list (i.e., 62), it is of note that authors from 9 other countries also contributed. When we examined the articles for individual authors, we found that Fred J. Epstein was an author on 6 articles on the list, all focused on intramedullary tumors (articles No. 34, 47, 61, 63, 77, and 100); 7 other authors appeared 3 times each on this list.

According to the level-of-evidence grading, 70% of the articles were Level IV evidence studies, and only 4% were high-quality Level I evidence studies. Even though this observation implied scarce high-quality evidence for management of spinal tumors, the challenges of conducting randomized controlled surgical trials must be acknowledged. Such studies require multicenter collaborations, a lot of personnel, large funding, and patients' consent to receiving either an experimental intervention or no intervention. Additionally, we also observed very few Level III evidence studies (case-control studies or retrospective comparative studies), which may be the next step in spinal oncology research. Level III studies are less challenging to conduct than randomized trials, but they allow for multivariable analyses or direct comparison of interventions. We also note that the lower representation of higher-level-evidence studies on the top 100 list does not necessarily mean that these studies have not been frequently conducted—it may simply imply that these types of studies may have not been cited as many times as studies with lower levels of evidence.

To identify temporal trends in spinal tumor treatments, studies reporting on particular techniques were stratified by time published (Table 5). Resection (either subtotal or gross total) was the main topic in articles published in the 1930s and 1940s, and the combination of surgery plus radiation therapy began to be reported in 1950. This treatment modality then became the mainstay of treatment for spinal tumors up to the 1990s when en bloc resection was shown to achieve superior outcomes compared with intralesional or subtotal resection. Likewise, the introduction of vertebroplasty and kyphoplasty did not happen until the 1980s. Last, frequently cited studies reporting on radiosurgery and photon therapy for spinal tumors were published in the 1990s and 2000s.

TABLE 5.

Spinal tumor treatment strategies stratified by decade of publication*

TopicDecade of Publication
1930s1940s1950s1960s1970s1980s1990s2000s
VP/KP00000223
Surgery11103561
Surgery + RT0012412124
En bloc resection00000032
RT00000320
Radiosurgery00000016
Photon therapy00000010
RT = radiotherapy; VP/KP = vertebroplasty/kyphoplasty.

The data represent number of articles.

As mentioned above, spinal oncology is a dynamic field, and the articles identified in this study reflected that dynamism. Ranging from anatomical pathology studies to randomized controlled trials to systematic reviews, the top 100 most-cited articles focused on topics such as metastatic spinal tumors, primary vertebral column tumors, radiation oncology, surgical techniques, intramedullary tumors, staging and scoring systems, and many other areas. The fact that many distinct specialties and journals were represented among the studies on this list is very interesting and supports the notion that spinal tumors are best treated in a multidisciplinary and multimodal fashion.114

Advances in genetics-based treatments,37 radiosurgery,17 proton-beam therapy,2,86 immunotherapy,18 and minimally invasive surgery,36,38,70,81 among others, will be an important part of the future of spinal oncology. Treatments involving wild-type neurofibromatosis 2 gene insertion, oncolytic viruses, and transfer of gene-silencing ribonucleic acid have all shown promising results in vitro for meningiomas.37 Stereotactic body radiotherapy (radiosurgery) has been used as a first-line treatment for metastatic lesions, after failure of conventional radiotherapy, after separation surgery, and as first-line treatment for primary tumors and has shown promising results in each approach.17 Recently, proton-beam therapy has gained attention because it can deliver high doses of energy to a small tissue volume; clinical studies have shown high local tumor control and overall patient survival rates, particularly for chordoma.80,86

The aforementioned tyrosine kinase inhibitors are currently being investigated for the treatment of chordoma;18 other immunotherapeutic agents have also been investigated for metastatic melanoma to the spine.20 Last, minimally invasive surgery has been shown to provide outcomes in terms of neurological recovery similar to outcomes of traditional open surgery for vertebral thoracic metastases causing acute myelopathy;81 other studies have also examined the role of minimally invasive surgery on intradural tumors.52 Although each of these techniques has shown favorable results, patients will most likely have best outcomes when treated by a multidisciplinary team that uses a combination of multimodal strategies.

Limitations

This study has several limitations. First, some studies have suggested that citation analyses may favor older studies, since these studies had more time to accumulate citations.56,96 For example, it could be argued that clinical studies such as that by Patchell et al.87 on direct decompressive surgery plus radiotherapy have much more clinical “impact” than the anatomical study by Batson,8 and yet the latter had more than double the number of citations. For this reason, in an attempt to control for this potential bias, we utilized the CY index. When we ranked the studies according to the CY index, the study by Patchell et al. jumped to No. 1, and the top 10 articles on the CY list included those on topics such as vertebroplasty/kyphoplasty, radiotherapy, and radiosurgery. Second, although Web of Science has been used for citation analysis, we note that this index does not always include citations from textbooks or journals written in languages other than English.88 Third, although we ranked articles by number of citations, we excluded some studies in a subjective manner, and it may be possible that other relevant articles were missed. Last, the number of times an article has been cited does not directly reflect its quality. As shown in this study, most articles were Level IV evidence studies, and only 4 were Level I evidence studies.

Conclusions

In this study, the 100 most-cited articles in spinal oncology were examined, and important contributions from various authors, specialties, and countries were identified. More than one-third of the research in these articles was focused on spinal metastases, followed by intramedullary tumors and chordoma. The top 100 articles were published in 31 different journals, reflecting the multidisciplinary nature of spinal tumor care. Recognition of important historical contributions to this field may guide future investigations into spinal oncology.

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Disclosures

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

Author Contributions

Conception and design: Caro-Osorio, De la Garza-Ramos. Acquisition of data: De la Garza-Ramos, Benvenutti-Regato. Analysis and interpretation of data: all authors. Drafting the article: all authors. Critically revising the article: all authors. Reviewed submitted version of manuscript: Caro-Osorio. Approved the final version of the manuscript on behalf of all authors: Caro-Osorio. Statistical analysis: De la Garza-Ramos. Study supervision: Caro-Osorio.

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Article Information

Contributor Notes

INCLUDE WHEN CITING Published online January 15, 2016; DOI: 10.3171/2015.8.SPINE15674.Correspondence Enrique Caro-Osorio, Neurology and Neurosurgery Institute, Centro Médico Zambrano Hellion, TecSalud, Batallón de San Patricio 112, 8th Fl., Monterrey 66278, Mexico. email: ecaro@itesm.mx.

© AANS, except where prohibited by US copyright law.

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