Publications by authors named "Shannon E Fogh"

24 Publications

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Lessons From Learners: Adapting Medical Student Education During and Post-COVID-19.

Acad Med 2021 May 4. Epub 2021 May 4.

M.R.H. Castro is a third-year medical student, University of California San Francisco School of Medicine, San Francisco, California; ORCID: https://orcid.org/0000-0002-2085-4893. L.M. Calthorpe is a third-year medical student, University of California San Francisco School of Medicine, San Francisco, California; ORCID: https://orcid.org/0000-0002-0496-9471. S.E. Fogh is associate professor, Department of Radiation Oncology, University of California San Francisco School of Medicine, San Francisco, California. S. McAllister is a third-year medical student, University of California San Francisco School of Medicine, San Francisco, California. C.L Johnson is a third-year medical student, University of California San Francisco School of Medicine, San Francisco, California. E.D. Isaacs is professor of emergency medicine, Department of Emergency Medicine, University of California San Francisco, San Francisco, California. A. Ishizaki is manager, Clinical Microsystems Clerkship, University of California San Francisco School of Medicine, San Francisco, California. A. Kozas is curriculum coordinator, Clinical Microsystems Clerkship, University of California San Francisco School of Medicine, San Francisco, California. D. Lo is assistant professor of medicine, Division of Geriatrics, Department of Medicine, University of California San Francisco School of Medicine; and Department of Geriatrics and Extended Care, San Francisco Veterans Affairs Health Care System, San Francisco, California. S. Rennke is professor of medicine, Division of Hospital Medicine, Department of Medicine, University of California San Francisco School of Medicine, San Francisco, California. J. Davis is professor of medicine and associate dean for curriculum, University of California San Francisco School of Medicine, San Francisco, California. A. Chang is professor of medicine, Division of Geriatrics, Department of Medicine, University of California San Francisco, San Francisco, California.

In response to the COVID-19 pandemic, many medical schools suspended clinical clerkships and implemented newly adapted curricula to facilitate continued educational progress. While the implementation of these new curricula has been described, an understanding of the impact on student learning outcomes is lacking. In 2020, the authors followed Kern's 6-step approach to curricular development to create and evaluate a novel COVID-19 curriculum for medical students at the University of California San Francisco School of Medicine and evaluate its learning outcomes. The primary goal of the curriculum was to provide third- and fourth-year medical students an opportunity for workplace learning in the absence of clinical clerkships, specifically for students to develop clerkship-level milestones in the competency domains of practice-based learning and improvement, professionalism, and systems-based practice. The curriculum was designed to match students with faculty-mentored projects occurring primarily in virtual formats. A total of 126 students enrolled in the curriculum and completed a survey about their learning outcomes (100% response rate). Of 35 possible clerkship-level milestones, there were 12 milestones for which over half of students reported development, in competency domains including practice-based learning and improvement, professionalism, and interpersonal and communication skills. Thematic analysis of students' qualitative survey responses demonstrated 2 central motivations for participating in the curriculum: identity as physicians-in-training, and patient engagement. Six central learning areas were developed during the curriculum: interprofessional teamwork, community resources, technology in medicine, skill-building, quality improvement, and specialty-specific learning. This analysis demonstrates that students can develop competencies and achieve rich workplace learning through project-based experiential learning, even in virtual clinical workplaces. Furthermore, knowledge of community resources, technology in medicine, and quality improvement were developed through the curriculum more readily than in traditional clerkships, and could be considered as integral learning objectives in future curricular design.
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http://dx.doi.org/10.1097/ACM.0000000000004148DOI Listing
May 2021

Neuro-Oncology Practice Clinical Debate: Early treatment or observation for patients with newly diagnosed oligodendroglioma and small-volume residual disease.

Neurooncol Pract 2021 Feb 27;8(1):11-17. Epub 2020 Jun 27.

Department of Hematology and Medical Oncology, New York University, New York, NY, USA.

Advances in treatment of oligodendroglioma represent arguably the most significant recent development in the treatment of brain tumors, with multiple clinical trials demonstrating that median survival is approximately doubled in patients with World Health Organization grade II and III 1p/19q codeleted gliomas (ie, oligodendrogliomas) treated with procarbazine, lomustine, vincristine chemotherapy and radiation vs radiation alone. However, chemoradiotherapy itself is not without morbidity, including both short-term toxicities primarily related to chemotherapy and longer-term cognitive issues likely due to radiation. Patients and physicians both desire maximally effective therapy with minimal toxicity, and it remains unclear whether some patients with macroscopic residual disease after surgery can safely delay therapy, to avoid or delay toxicity, while simultaneously preserving the full benefits of treatment. In this article, experts in the field discuss the rationale for the approaches of up-front treatment with chemoradiotherapy and initial observation, respectively.
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http://dx.doi.org/10.1093/nop/npaa037DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7906263PMC
February 2021

Germline MUTYH Mutation in a Pediatric Cancer Survivor Developing a Secondary Malignancy.

J Pediatr Hematol Oncol 2020 10;42(7):e647-e654

Department of Radiation Oncology.

Radiotherapy-induced second malignant neoplasms (SMNs) are a severe late complication in pediatric cancer survivors. Germline mutations in tumor suppressor genes contribute to SMNs; however, the most relevant germline variants mediating susceptibility are not fully defined. The authors performed matched whole-exome sequencing analyses of germline and tumor DNA from 4 pediatric solid tumor survivors who subsequently developed radiation-associated SMNs. Pathogenic and predicted deleterious germline variants were identified for each patient and validated with Sanger sequencing. These germline variants were compared with germline variants in a cohort of 59 pediatric patients diagnosed with primary sarcomas. Pathway analysis was performed to test for similarities in the germline variant profiles between individuals diagnosed with SMNs or primary sarcomas. One index patient was found to have a pathogenic germline monoallelic mutation in the MUTYH gene, which encodes the base excision repair enzyme adenine DNA glycosylase. This specific germline mutation is associated with a form of familial adenomatous polyposis, a new diagnosis in the patient. Germline-level genetic similarity exists between SMN-developing patients and patients developing primary sarcomas, with relevant genes involved in signal transduction and DNA repair mechanisms. The authors identify a germline MUTYH mutation in a pediatric cancer survivor developing an SMN. Germline mutations involving specific pathways such as base excision repair may identify individuals at risk for developing SMNs. The composition of germline variants in individual patients may enable estimates of patient-specific risk for developing SMNs. The authors anticipate that further analyses of germline genomes and epigenomes will reveal diverse genes and mechanisms influencing cancer risk.
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http://dx.doi.org/10.1097/MPH.0000000000001668DOI Listing
October 2020

High-risk Meningioma: Initial Outcomes From NRG Oncology/RTOG 0539.

Int J Radiat Oncol Biol Phys 2020 03 29;106(4):790-799. Epub 2019 Nov 29.

Miami Cancer Institute, Baptist Health, Miami, Florida.

Background: Phase 2 cooperative group meningioma trial assessing the safety and efficacy of risk-adaptive management strategies. This is the initial analysis of the high-risk cohort.

Methods And Materials: High-risk patients were those with a new or recurrent World Health Organization (WHO) grade III meningioma of any resection extent, recurrent WHO grade II of any resection extent, or new WHO grade II after subtotal resection. Patients received intensity-modulated radiotherapy (IMRT) using a simultaneous integrated boost technique (60 Gy high dose and 54 Gy low dose in 30 fractions). Three-year progression-free survival (PFS) was the primary endpoint. Adverse events (AEs) were scored per NCI Common Terminology Criteria for Adverse Events version 3.

Results: Of 57 enrolled patients, 53 received protocol treatment. Median follow-up was 4.0 years (4.8 years for living patients). Two patients withdrew without progression before year 3; for the remaining 51 patients, 3-year PFS was 58.8%. Among all 53 protocol-treated patients, 3-year PFS was 59.2%. Three-year local control was 68.9%, and overall survival was 78.6%. Of 51 patients, 1 patient (1.9%) experienced a late grade-5 necrosis-related AE. All other acute (23 of 53 patients) and late (21 of 51 patients) AEs were grades 1 to 3.

Conclusions: Patients with high-risk meningioma treated with IMRT (60 Gy/30) experienced 3-year PFS of 58.8%. Combined acute and late AEs were limited to grades 1 to 3, except for a single necrosis-related grade 5 event. These results support postoperative IMRT for high-risk meningioma and invite ongoing investigations to improve outcomes further.
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http://dx.doi.org/10.1016/j.ijrobp.2019.11.028DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7117785PMC
March 2020

Reirradiation of recurrent high-grade glioma and development of prognostic scores for progression and survival.

Neurooncol Pract 2019 Sep 12;6(5):364-374. Epub 2019 Apr 12.

Department of Radiation Oncology, University of California San Francisco.

Background: Optimal techniques and patient selection for salvage reirradiation of high-grade glioma (HGG) are unclear. In this study, we identify prognostic factors for freedom from progression (FFP) and overall survival (OS) after reirradiation, risk factors for high-grade toxicity, and validate clinical prognostic scores.

Methods: A total of 116 patients evaluated between 2000 and 2018 received reirradiation for HGG (99 WHO grade IV, 17 WHO grade III). Median time to first progression after initial therapy was 10.6 months. Salvage therapies before reirradiation included surgery (31%) and systemic therapy (41%). Sixty-five patients (56%) received single-fraction stereotactic radiosurgery (SRS) as reirradiation. The median biologically effective dose (BED) was 47.25 Gy, and the median planning target volume (PTV) was 4.8 cc for SRS and 95.0 cc for non-SRS treatments. Systemic therapy was given concurrently to 52% and adjuvantly to 74% of patients.

Results: Median FFP was 4.9 months, and median OS was 11.0 months. Significant multivariable prognostic factors for FFP were performance status, time to initial progression, and BED; for OS they were age, time to initial progression, and PTV volume at recurrence. High-grade toxicity was correlated to PTV size at recurrence. Three-level prognostic scores were generated for FFP and OS, with cross-validated receiver operating characteristic area under the curve (AUC) of 0.640 and 0.687, respectively.

Conclusions: Clinical variables at the time of reirradiation for HGG can be used to prognosticate FFP and OS.
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http://dx.doi.org/10.1093/nop/npz017DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6753361PMC
September 2019

Palliative radiotherapy near the end of life.

BMC Palliat Care 2019 Mar 23;18(1):29. Epub 2019 Mar 23.

Department of Radiation Oncology, University of California, San Francisco, 505 Parnassus Ave, L-75, 1600 Divisadero St., H1031, San Francisco, CA, 94143, USA.

Background: A significant proportion of patients with advanced cancer undergo palliative radiotherapy (RT) within their last 30 days of life. This study characterizes palliative RT at our institution and aims to identify patients who may experience limited benefit from RT due to imminent mortality.

Methods: Five hundred and-eighteen patients treated with external beam RT to a site of metastatic disease between 2012 and 2016 were included. Mann-Whitney U and chi-squared tests were used to identify factors associated with RT within 30 days of death (DRT).

Results: Median age at RT was 63 years (IQR 54-71). Median time from RT to death was 74 days (IQR 33-174). One hundred and twenty-five patients (24%) died within 30 days of RT. DRT was associated with older age at RT (64 vs. 62 years, p = 0.04), shorter interval since diagnosis (14 vs. 31 months, p <  0.001), liver metastasis (p = 0.02), lower KPS (50 vs. 70, p <  0.001), lower BMI (22 vs. 24, p = 0.001), and inpatient status at consult (56% vs. 26%, p < 0.001). Patients who died within 30 days of RT were less likely to have hospice involved in their care (44% vs. 71%, p = 0.001). DRT was associated with higher Chow and TEACHH scores at consult (p < 0.001 for both).

Conclusions: Twenty-four percent of patients received palliative RT within 30 days of death. Additional tools are necessary to help physicians identify patients who would benefit from short treatment courses or alternative interventions to maximize quality at the end of life.
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http://dx.doi.org/10.1186/s12904-019-0415-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6431041PMC
March 2019

Radiation oncology resident training in patient safety and quality improvement: a national survey of residency program directors.

Radiat Oncol 2018 Sep 24;13(1):186. Epub 2018 Sep 24.

Department of Radiation Oncology, University of Washington, Seattle, WA, USA.

Background: Physicians and physicists are expected to contribute to patient safety and quality improvement (QI) in Radiation Oncology (RO), but prior studies suggest that training for this may be inadequate. RO and medical physics (MP) program directors (PDs) were surveyed to better understand the current patient safety/QI training in their residency programs.

Methods: PDs were surveyed via email in January 2017. Survey questions inquired about current training, curriculum elements, and barriers to development and/or improvement of safety and QI training.

Results: Eighty-nine RO PDs and 84 MP PDs were surveyed, and 21 RO PDs (28%) and 31 MP PDs (37%) responded. Both RO and MP PDs had favorable opinions of current safety and QI training, and used a range of resources for program development, especially safety and QI publications. Various curriculum elements were reported. Curriculum elements used by RO and MP PDs were similar, except RO were more likely than MP PDs to implement morbidity and mortality (M&M) conference (72% vs. 45%, p < 0.05). RO and MP PDs similarly cited various barriers, but RO PDs were more likely to cite lack of experience than MP PDs (40% vs. 16%, p < 0.05). PDs responded similarly independent of whether they reported using a departmental incident learning system (ILS) or not.

Conclusions: PDs view patient safety/QI as an important part of resident education. Most PDs agreed that residents are adequately exposed to patient safety/QI and prepared to meet the patient safety/QI expectations of clinical practice. This conflicts with other independent studies that indicate a majority of residents feel their patient safety/QI training is inadequate and lacks formal exposure to QI tools.
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http://dx.doi.org/10.1186/s13014-018-1128-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6154943PMC
September 2018

A Randomized Phase 2 Trial of Prophylactic Manuka Honey for the Reduction of Chemoradiation Therapy-Induced Esophagitis During the Treatment of Lung Cancer: Results of NRG Oncology RTOG 1012.

Int J Radiat Oncol Biol Phys 2017 03 23;97(4):786-796. Epub 2016 Nov 23.

Emory University, Atlanta, Georgia.

Purpose: Randomized trials have shown that honey is effective for the prevention of radiation-induced mucositis in head and neck cancer patients. Because there is no efficacious preventative for radiation esophagitis in lung cancer patients, this trial compared liquid honey, honey lozenges, and standard supportive care for radiation esophagitis.

Methods: The patients were stratified by percentage of esophagus receiving specific radiation dose (V60 Gy esophagus <30% or ≥30%) and were then randomized between supportive care, 10 mL of liquid manuka honey 4 times a day, and 2 lozenges (10 mL of dehydrated manuka honey) 4 times a day during concurrent chemotherapy and radiation therapy. The primary endpoint was patient-reported pain on swallowing, with the use of an 11-point (0-10) scale at 4 weeks (Numerical Rating Pain Scale, NRPS). The study was designed to detect a 15% relative reduction of change in NRPS score. The secondary endpoints were trend of pain over time, opioid use, clinically graded and patient-reported adverse events, weight loss, dysphagia, nutritional status, and quality of life.

Results: 53 patients were randomized to supportive care, 54 were randomized to liquid honey, and 56 were randomized to lozenge honey. There was no significant difference in the primary endpoint of change in the NRPS at 4 weeks between arms. There were no differences in any of the secondary endpoints except for opioid use at 4 weeks during treatment between the supportive care and liquid honey arms, which was found to be significant (P=.03), with more patients on the supportive care arm taking opioids.

Conclusion: Honey as prescribed within this protocol was not superior to best supportive care in preventing radiation esophagitis. Further testing of other types of honey and research into the mechanisms of action are needed.
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http://dx.doi.org/10.1016/j.ijrobp.2016.11.022DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5673256PMC
March 2017

American College of Radiology (ACR) Radiation Oncology Practice Accreditation: A pattern of change.

Pract Radiat Oncol 2016 Sep-Oct;6(5):e171-e177. Epub 2016 Jan 26.

Radiation Oncology Practice Accreditation Program, American College of Radiology, Reston, VA.

Purpose: The American College of Radiology (ACR) Radiation Oncology Practice Accreditation (ROPA) program has accredited more than 600 sites since 2006, including practices within academic, hospital-based, and freestanding settings. The purpose of this report is to evaluate and compare patterns of change in common deficiencies over time.

Methods And Materials: The ACR database was queried to analyze the common deficiencies noted by the ACR ROPA program between 2012 and 2014. Deficiencies were ranked and compared to the top 10 items that were reported in 2006.

Results: Between 2012 and 2014, 272 new applications and 306 renewals were received. Timely verification of port films, documentation of physician peer review, inclusion of essential elements of a treatment prescription, evidence of a final physicist chart review, documentation of weekly treatment visits, and inclusion of key elements of brachytherapy documentation all improved when compared with 2000-2005. Deficiencies ranked higher on the current review compared with the previous analysis included documentation of a robust quality assurance program, missing elements from the history and physical documentation, and documentation of follow-up visits.

Conclusions: Our analysis of changes in patterns of deficiencies across radiation oncology practices reflects changes in our field such as the growing reliance on electronic records and imaging. Accreditation continues to play an integral role in establishing national standards and a nonpunitive, peer-reviewed method to evaluate a practice's compliance with national quality guidelines.
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http://dx.doi.org/10.1016/j.prro.2016.01.010DOI Listing
March 2017

Indications and Efficacy of Gamma Knife Stereotactic Radiosurgery for Recurrent Glioblastoma: 2 Decades of Institutional Experience.

Neurosurgery 2017 Jan;80(1):129-139

Department of Neurological Surgery and.

Background: The role of stereotactic radiosurgery (SRS) for recurrent glioblastoma and the radionecrosis risk in this setting remain unclear.

Objective: To perform a large retrospective study to help inform proper indications, efficacy, and anticipated complications of SRS for recurrent glioblastoma.

Methods: We retrospectively analyzed patients who underwent Gamma Knife SRS between 1991 and 2013. We used the partitioning deletion/substitution/addition algorithm to identify potential predictor covariate cut points and Kaplan-Meier and proportional hazards modeling to identify factors associated with post-SRS and postdiagnosis survival.

Results: One hundred seventy-four glioblastoma patients (median age, 54.1 years) underwent SRS a median of 8.7 months after initial diagnosis. Seventy-five percent had 1 treatment target (range, 1-6), and median target volume and prescriptions were 7.0 cm 3 (range, 0.3-39.0 cm 3 ) and 16.0 Gy (range, 10-22 Gy), respectively. Median overall survival was 10.6 months after SRS and 19.1 months after diagnosis. Kaplan-Meier and multivariable modeling revealed that younger age at SRS, higher prescription dose, and longer interval between original surgery and SRS are significantly associated with improved post-SRS survival. Forty-six patients (26%) underwent salvage craniotomy after SRS, with 63% showing radionecrosis or mixed tumor/necrosis vs 35% showing purely recurrent tumor. The necrosis/mixed group had lower mean isodose prescription compared with the tumor group (16.2 vs 17.8 Gy; P = .003) and larger mean treatment volume (10.0 vs 5.4 cm 3 ; P = .009).

Conclusion: Gamma Knife may benefit a subset of focally recurrent patients, particularly those who are younger with smaller recurrences. Higher prescriptions are associated with improved post-SRS survival and do not seem to have greater risk of symptomatic treatment effect.
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http://dx.doi.org/10.1227/NEU.0000000000001344DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5235998PMC
January 2017

Resection and brain brachytherapy with permanent iodine-125 sources for brain metastasis.

J Neurosurg 2017 Jun 1;126(6):1749-1755. Epub 2016 Jul 1.

Neurological Surgery, University of California San Francisco.

OBJECTIVE Stereotactic radiosurgery (SRS) with or without whole-brain radiotherapy can be used to achieve local control (> 90%) for small brain metastases after resection. However, many brain metastases are unsuitable for SRS because of their size or previous treatment, and whole-brain radiotherapy is associated with significant neurocognitive morbidity. The purpose of this study was to investigate the efficacy and toxicity of surgery and iodine-125 (I) brachytherapy for brain metastases. METHODS A total of 95 consecutive patients treated for 105 brain metastases at a single institution between September 1997 and July 2013 were identified for this analysis retrospectively. Each patient underwent MRI followed by craniotomy with resection of metastasis and placement of I sources as permanent implants. The patients were followed with serial surveillance MRIs. The relationships among local control, overall survival, and necrosis were estimated by using the Kaplan-Meier method and compared with results of log-rank tests and multivariate regression models. RESULTS The median age at surgery was 59 years (range 29.9-81.6 years), 53% of the lesions had been treated previously, and the median preoperative metastasis volume was 13.5 cm (range 0.21-76.2 cm). Gross-total resection was achieved in 81% of the cases. The median number of I sources implanted per cavity was 28 (range 4-93), and the median activity was 0.73 mCi (range 0.34-1.3 mCi) per source. A total of 476 brain MRIs were analyzed (median MRIs per patient 3; range 0-22). Metastasis size was the strongest predictor of cavity volume and shrinkage (p < 0.0001). Multivariable regression modeling failed to predict the likelihood of local progression or necrosis according to metastasis volume, cavity volume, or the rate of cavity remodeling regardless of source activity or previous SRS. The median clinical follow-up time in living patients was 14.4 months (range 0.02-13.6 years), and crude local control was 90%. Median overall survival extended from 2.1 months in the shortest quartile to 62.3 months in the longest quartile (p < 0.0001). The overall risk of necrosis was 15% and increased significantly for lesions with a history of previous SRS (p < 0.05). CONCLUSIONS Therapeutic options for patients with large or recurrent brain metastases are limited. Data from this study suggest that resection with permanent I brachytherapy is an effective strategy for achieving local control of brain metastasis. Although metastasis volume significantly influences resection cavity size and remodeling, volumetric parameters do not seem to influence local control or necrosis. With careful patient selection, this treatment regimen is associated with minimal toxicity and can result in long-term survival for some patients. ▪ CLASSIFICATION OF EVIDENCE Type of question: therapeutic; study design: retrospective case series; evidence: Class IV.
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http://dx.doi.org/10.3171/2016.4.JNS152530DOI Listing
June 2017

Discovery of additional brain metastases on the day of stereotactic radiosurgery: risk factors and outcomes.

J Neurosurg 2017 Jun 1;126(6):1756-1763. Epub 2016 Jul 1.

Departments of 1 Radiation Oncology.

OBJECTIVE High-resolution double-dose gadolinium-enhanced Gamma Knife (GK) radiosurgery-planning MRI (GK MRI) on the day of GK treatment can detect additional brain metastases undiagnosed on the prior diagnostic MRI scan (dMRI), revealing increased intracranial disease burden on the day of radiosurgery, and potentially necessitating a reevaluation of appropriate management. The authors identified factors associated with detecting additional metastases on GK MRI and investigated the relationship between detection of additional metastases and postradiosurgery patient outcomes. METHODS The authors identified 326 patients who received GK radiosurgery at their institution from 2010 through 2013 and had a prior dMRI available for comparison of numbers of brain metastases. Factors predictive of additional brain metastases on GK MRI were investigated using logistic regression analysis. Overall survival was estimated by Kaplan-Meier method, and postradiosurgery distant intracranial failure was estimated by cumulative incidence measures. Multivariable Cox proportional hazards model and Fine-Gray regression modeling assessed potential risk factors of overall survival and distant intracranial failure, respectively. RESULTS The mean numbers of brain metastases (SD) on dMRI and GK MRI were 3.4 (4.2) and 5.8 (7.7), respectively, and additional brain metastases were found on GK MRI in 48.9% of patients. Frequencies of detecting additional metastases for patients with 1, 2, 3-4, and more than 4 brain metastases on dMRI were 29.5%, 47.9%, 55.9%, and 79.4%, respectively (p < 0.001). An index brain metastasis with a diameter greater than 1 cm on dMRI was inversely associated with detecting additional brain metastases, with an adjusted odds ratio of 0.57 (95% CI 0.4-0.9, p = 0.02). The median time between dMRI and GK MRI was 22 days (range 1-88 days), and time between scans was not associated with detecting additional metastases. Patients with additional brain metastases did not have larger total radiosurgery target volumes, and they rarely had an immediate change in management (abortion of radiosurgery or addition of whole-brain radiation therapy) due to detection of additional metastases. Patients with additional metastases had a higher incidence of distant intracranial failure than those without additional metastases (p = 0.004), with an adjusted subdistribution hazard ratio of 1.4 (95% CI 1.0-2.0, p = 0.04). Significantly worse overall survival was not detected for patients with additional brain metastases on GK MRI (log-rank p = 0.07), with the relative adjusted hazard ratio of 1.07, (95% CI 0.81-1.41, p = 0.65). CONCLUSIONS Detecting additional brain metastases on GK MRI is strongly associated with the number of brain metastases on dMRI and inversely associated with the size of the index brain metastasis. The discovery of additional brain metastases at time of GK radiosurgery is very unlikely to lead to aborting radiosurgery but is associated with a higher incidence of distant intracranial failure. However, there is not a significant difference in survival. ▪ CLASSIFICATION OF EVIDENCE Type of question: prognostic; study design: retrospective cohort trial; evidence: Class IV.
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http://dx.doi.org/10.3171/2016.4.JNS152319DOI Listing
June 2017

Surgical Resection and Interstitial Iodine-125 Brachytherapy for High-Grade Meningiomas: A 25-Year Series.

Neurosurgery 2017 03;80(3):409-416

Department of Neurological Surgery, University of California, San Francisco, San Francisco, California.

Background: Atypical and malignant meningiomas can recur despite resection and radiation.

Objective: To determine outcomes of patients with recurrent atypical or malignant meningioma treated with repeat resection and permanent iodine-125 ( 125 I) brachy-therapy.

Methods: Charts of patients who underwent surgical resection and 125 I brachyther-apy implantation for atypical and malignant meningiomas between 1988 and 2013 were retrospectively reviewed. The Kaplan-Meier actuarial method was used to calculate progression-free and overall survival. The log-rank test was used to compare groups. Significance was set at P < .05.

Results: Forty-two patients underwent 50 resections with 125 I brachytherapy im-plantations. All patients had undergone previous resections and 85% had previously undergone radiation. Median follow-up was 7.5 years after diagnosis and 2.3 years after brachytherapy. Median time to progression after resection with 125 I brachytherapy was 20.9 months for atypical meningioma, 11.4 months for malignant meningioma, and 11.4 months for the combined groups. Median survival after re-resection and 125 I brachytherapy was 3.5 years for atypical meningioma, 2.3 years for malignant menin-gioma, and 3.3 years for all subjects. Median overall survival after diagnosis was 11.1 years for atypical meningioma, 9.1 years for malignant meningioma, and 9.4 years for all subjects. Complications occurred in 17 patients and included radiation necrosis (n = 8, 16%), wound breakdown (n = 6, 12%), hydrocephalus (n = 4, 8%), infection (n = 3, 6%), and a pseudomeningocele (n = 2, 5%).

Conclusion: This is the largest experience with adjuvant 125 I brachytherapy for recurrent high-grade meningiomas. The outcomes support the use of adjuvant brachytherapy as an option for these aggressive tumors.
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http://dx.doi.org/10.1227/NEU.0000000000001262DOI Listing
March 2017

: meningioma.

Neurooncol Pract 2016 Jun 13;3(2):120-134. Epub 2016 Jan 13.

Department of Radiation Oncology, University of California, San Francisco, San Francisco, CA, USA (S.E.F.); Department of Radiology, Mayo Clinic, Rochester, MN, USA (D.R.J., T.J.K.); Department of Neurosurgery, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA (F.G.B.); Division of Neuro-Oncology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA (P.K.B.); Department of Neurology and Department of Neurological Surgery, University of California, San Francisco, San Francisco, CA, USA (J.L.C.); Department of Neurology, Karl Landsteiner University Clinic, St Pölten, Austria (S.O.); Department of Internal Medicine, Medical University, Vienna, CCC, Austria (M.P.); Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, MN, USA (A.R.); Department of Pathology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA (S.S.); Department of Neurological Surgery, University of California, San Francisco, San Francisco, CA, USA (P.V.T.).

Meningioma is by far the most common primary intracranial tumor in adults. Treatment of meningioma is complex due to a tremendous amount of variability in tumor behavior. Many patients are incidentally found to have tumors that will remain asymptomatic throughout their lives. It is important to identify these patients so that they can be spared from potentially morbid interventions. On the other end of the spectrum, high-grade meningiomas can behave very aggressively. When treatment is necessary, surgical resection is the cornerstone of meningioma therapy. Studies spanning decades have demonstrated that extent of resection correlates with prognosis. Radiation therapy, either in the form of external beam radiation therapy or stereotactic radiosurgery, represents another important therapeutic tool that can be used in place of or as a supplement to surgery. There are no chemotherapeutic agents of proven efficacy against meningioma, and chemotherapy treatment is generally reserved for patients who have exhausted surgical and radiotherapy options. Ongoing and future studies will help to answer unresolved questions such as the optimum use of radiation in resected WHO grade II meningiomas and the efficacy of additional chemotherapy agents.
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http://dx.doi.org/10.1093/nop/npv063DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6668267PMC
June 2016

Assessment of image quality and dose calculation accuracy on kV CBCT, MV CBCT, and MV CT images for urgent palliative radiotherapy treatments.

J Appl Clin Med Phys 2016 03 8;17(2):279-290. Epub 2016 Mar 8.

University of California San Francisco.

A clinical workflow was developed for urgent palliative radiotherapy treatments that integrates patient simulation, planning, quality assurance, and treatment in one 30-minute session. This has been successfully tested and implemented clinically on a linac with MV CBCT capabilities. To make this approach available to all clin-ics equipped with common imaging systems, dose calculation accuracy based on treatment sites was assessed for other imaging units. We evaluated the feasibility of palliative treatment planning using on-board imaging with respect to image quality and technical challenges. The purpose was to test multiple systems using their commercial setup, disregarding any additional in-house development. kV CT, kV CBCT, MV CBCT, and MV CT images of water and anthropomorphic phantoms were acquired on five different imaging units (Philips MX8000 CT Scanner, and Varian TrueBeam, Elekta VersaHD, Siemens Artiste, and Accuray Tomotherapy linacs). Image quality (noise, contrast, uniformity, spatial resolution) was evaluated and compared across all machines. Using individual image value to density calibrations, dose calculation accuracies for simple treatment plans were assessed for the same phantom images. Finally, image artifacts on clinical patient images were evaluated and compared among the machines. Image contrast to visualize bony anatomy was sufficient on all machines. Despite a high noise level and low contrast, MV CT images provided the most accurate treatment plans relative to kV CT-based planning. Spatial resolution was poorest for MV CBCT, but did not limit the visualization of small anatomical structures. A comparison of treatment plans showed that monitor units calculated based on a prescription point were within 5% difference relative to kV CT-based plans for all machines and all studied treatment sites (brain, neck, and pelvis). Local dose differences > 5% were found near the phantom edges. The gamma index for 3%/3 mm criteria was ≥ 95% in most cases. Best dose calculation results were obtained when the treatment isocenter was near the image isocenter for all machines. A large field of view and immediate image export to the treatment planning system were essential for a smooth workflow and were not provided on all devices. Based on this phantom study, image quality of the studied kV CBCT, MV CBCT, and MV CT on-board imaging devices was sufficient for treatment planning in all tested cases. Treatment plans provided dose calculation accuracies within an acceptable range for simple, urgently planned palliative treatments. However, dose calculation accuracy was compromised towards the edges of an image. Feasibility for clinical implementation should be assessed separately and may be complicated by machine specific features. Image artifacts in patient images and the effect on dose calculation accuracy should be assessed in a separate, machine-specific study.
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http://dx.doi.org/10.1120/jacmp.v17i2.6040DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5874969PMC
March 2016

Feasibility of MV CBCT-based treatment planning for urgent radiation therapy: dosimetric accuracy of MV CBCT-based dose calculations.

J Appl Clin Med Phys 2015 11 8;16(6):458-471. Epub 2015 Nov 8.

University of California San Francisco.

Unlike scheduled radiotherapy treatments, treatment planning time and resources are limited for emergency treatments. Consequently, plans are often simple 2D image-based treatments that lag behind technical capabilities available for nonurgent radiotherapy. We have developed a novel integrated urgent workflow that uses onboard MV CBCT imaging for patient simulation to improve planning accuracy and reduce the total time for urgent treatments. This study evaluates both MV CBCT dose planning accuracy and novel urgent workflow feasibility for a variety of anatomic sites. We sought to limit local mean dose differences to less than 5% compared to conventional CT simulation. To improve dose calculation accuracy, we created separate Hounsfield unit-to-density calibration curves for regular and extended field-of-view (FOV) MV CBCTs. We evaluated dose calculation accuracy on phantoms and four clinical anatomical sites (brain, thorax/spine, pelvis, and extremities). Plans were created for each case and dose was calculated on both the CT and MV CBCT. All steps (simulation, planning, setup verification, QA, and dose delivery) were performed in one 30 min session using phantoms. The monitor units (MU) for each plan were compared and dose distribution agreement was evaluated using mean dose difference over the entire volume and gamma index on the central 2D axial plane. All whole-brain dose distributions gave gamma passing rates higher than 95% for 2%/2 mm criteria, and pelvic sites ranged between 90% and 98% for 3%/3 mm criteria. However, thoracic spine treatments produced gamma passing rates as low as 47% for 3%/3 mm criteria. Our novel MV CBCT-based dose planning and delivery approach was feasible and time-efficient for the majority of cases. Limited MV CBCT FOV precluded workflow use for pelvic sites of larger patients and resulted in image clearance issues when tumor position was far off midline. The agreement of calculated MU on CT and MV CBCT was acceptable for all treatment sites.
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http://dx.doi.org/10.1120/jacmp.v16i6.5625DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5690985PMC
November 2015

Looking Ahead: Practicing Radiation Oncology in the Era of ICD-10.

Int J Radiat Oncol Biol Phys 2015 Dec 11;93(5):949-52. Epub 2015 Nov 11.

Department of Radiation Oncology, University of California, San Francisco, San Francisco, California.

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http://dx.doi.org/10.1016/j.ijrobp.2015.08.039DOI Listing
December 2015

: newly diagnosed glioblastoma.

Neurooncol Pract 2015 Sep 21;2(3):106-121. Epub 2015 Jul 21.

Department of Neurology and Division of Medical Oncology, Mayo Clinic, Rochester, Minnesota (D.R.J.); Department of Radiation Oncology, University of California, San Francisco, California (S.E.F.); Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, Minnesota (C.G., A.R.); Department of Radiology, Mayo Clinic, Rochester, Minnesota (T.J.K.); Department of Neurological Surgery, University of California, San Francisco, California (P.V.T.); Department of Neurology and Department of Neurological Surgery, University of California, San Francisco, California (J.L.C.).

Glioblastoma (WHO grade IV astrocytoma) is the most common and most aggressive primary brain tumor in adults. Optimal treatment of a patient with glioblastoma requires collaborative care across numerous specialties. The diagnosis of glioblastoma may be suggested by the symptomatic presentation and imaging, but it must be pathologically confirmed via surgery, which can have dual diagnostic and therapeutic roles. Standard of care postsurgical treatment for newly diagnosed patients involves radiation therapy and oral temozolomide chemotherapy. Despite numerous recent trials of novel therapeutic approaches, this standard of care has not changed in over a decade. Treatment options under active investigation include molecularly targeted therapies, immunotherapeutic approaches, and the use of alternating electrical field to disrupt tumor cell division. These trials may be aided by new insights into glioblastoma heterogeneity, allowing for focused evaluation of new treatments in the patient subpopulations most likely to benefit from them. Because glioblastoma is incurable by current therapies, frequent clinical and radiographic assessment is needed after initial treatment to allow for early intervention upon progressive tumor when it occurs.
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http://dx.doi.org/10.1093/nop/npv020DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6668273PMC
September 2015

Interval From Imaging to Treatment Delivery in the Radiation Surgery Age: How Long Is Too Long?

Int J Radiat Oncol Biol Phys 2015 Sep 7;93(1):126-32. Epub 2015 May 7.

Department of Radiation Oncology, University of California at San Francisco, San Francisco, California.

Purpose: The purpose of this study was to evaluate workflow and patient outcomes related to frameless stereotactic radiation surgery (SRS) for brain metastases.

Methods And Materials: We reviewed all treatment demographics, clinical outcomes, and workflow timing, including time from magnetic resonance imaging (MRI), computed tomography (CT) simulation, insurance authorization, and consultation to the start of SRS for brain metastases.

Results: A total of 82 patients with 151 brain metastases treated with SRS were evaluated. The median times from consultation, insurance authorization, CT simulation, and MRI for treatment planning were 15, 7, 6, and 11 days to SRS. Local freedom from progression (LFFP) was lower in metastases with MRI ≥ 14 days before treatment (P = .0003, log rank). The 6- and 12-month LFFP rate were 95% and 75% for metastasis with interval of <14 days from MRI to treatment compared to 56% and 34% for metastases with MRI ≥ 14 days before treatment. On multivariate analysis, LFFP remained significantly lower for lesions with MRI ≥ 14 days at SRS (P = .002, Cox proportional hazards; hazard ratio: 3.4, 95% confidence interval: 1.6-7.3).

Conclusions: Delay from MRI to SRS treatment delivery for brain metastases appears to reduce local control. Future studies should monitor the timing from imaging acquisition to treatment delivery. Our experience suggests that the time from MRI to treatment should be <14 days.
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http://dx.doi.org/10.1016/j.ijrobp.2015.05.001DOI Listing
September 2015

Adverse radiation effect after stereotactic radiosurgery for brain metastases: incidence, time course, and risk factors.

J Neurosurg 2015 Aug 15;123(2):373-86. Epub 2015 May 15.

Departments of 1 Radiation Oncology and.

Object: The authors sought to determine the incidence, time course, and risk factors for overall adverse radiation effect (ARE) and symptomatic ARE after stereotactic radiosurgery (SRS) for brain metastases.

Methods: All cases of brain metastases treated from 1998 through 2009 with Gamma Knife SRS at UCSF were considered. Cases with less than 3 months of follow-up imaging, a gap of more than 8 months in imaging during the 1st year, or inadequate imaging availability were excluded. Brain scans and pathology reports were reviewed to ensure consistent scoring of dates of ARE, treatment failure, or both; in case of uncertainty, the cause of lesion worsening was scored as indeterminate. Cumulative incidence of ARE and failure were estimated with the Kaplan-Meier method with censoring at last imaging. Univariate and multivariate Cox proportional hazards analyses were performed.

Results: Among 435 patients and 2200 brain metastases evaluable, the median patient survival time was 17.4 months and the median lesion imaging follow-up was 9.9 months. Calculated on the basis of 2200 evaluable lesions, the rates of treatment failure, ARE, concurrent failure and ARE, and lesion worsening with indeterminate cause were 9.2%, 5.4%, 1.4%, and 4.1%, respectively. Among 118 cases of ARE, approximately 60% were symptomatic and 85% occurred 3-18 months after SRS (median 7.2 months). For 99 ARE cases managed without surgery or bevacizumab, the probabilities of improvement observed on imaging were 40%, 57%, and 76% at 6, 12, and 18 months after onset of ARE. The most important risk factors for ARE included prior SRS to the same lesion (with 20% 1-year risk of symptomatic ARE vs 3%, 4%, and 8% for no prior treatment, prior whole brain radiotherapy [WBRT], or concurrent WBRT) and any of these volume parameters: target, prescription isodose, 12-Gy, or 10-Gy volume. Excluding lesions treated with repeat SRS, the 1-year probabilities of ARE were < 1%, 1%, 3%, 10%, and 14% for maximum diameter 0.3-0.6 cm, 0.7-1.0 cm, 1.1-1.5 cm, 1.6-2.0 cm, and 2.1-5.1 cm, respectively. The 1-year probabilities of symptomatic ARE leveled off at 13%-14% for brain metastases maximum diameter > 2.1 cm, target volume > 1.2 cm(3), prescription isodose volume > 1.8 cm(3), 12-Gy volume > 3.3 cm(3), and 10-Gy volume > 4.3 cm(3), excluding lesions treated with repeat SRS. On both univariate and multivariate analysis, capecitabine, but not other systemic therapy within 1 month of SRS, appeared to increase ARE risk. For the multivariate analysis considering only metastases with target volume > 1.0 cm(3), risk factors for ARE included prior SRS, kidney primary tumor, connective tissue disorder, and capecitabine.

Conclusions: Although incidence of ARE after SRS was low overall, risk increased rapidly with size and volume, leveling off at a 1-year cumulative incidence of 13%-14%. This study describes the time course of ARE and provides risk estimates by various lesion characteristics and treatment parameters to aid in decision-making and patient counseling.
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http://dx.doi.org/10.3171/2014.10.JNS141610DOI Listing
August 2015

Quality improvement of International Classification of Diseases, 9th revision, diagnosis coding in radiation oncology: single-institution prospective study at University of California, San Francisco.

Pract Radiat Oncol 2015 Jan-Feb;5(1):e45-51. Epub 2014 May 22.

Department of Radiation Oncology, University of California, San Francisco (UCSF), School of Medicine, San Francisco, California. Electronic address:

Purpose: Accurate International Classification of Diseases (ICD) diagnosis coding is critical for patient care, billing purposes, and research endeavors. In this single-institution study, we evaluated our baseline ICD-9 (9th revision) diagnosis coding accuracy, identified the most common errors contributing to inaccurate coding, and implemented a multimodality strategy to improve radiation oncology coding.

Methods And Materials: We prospectively studied ICD-9 coding accuracy in our radiation therapy--specific electronic medical record system. Baseline ICD-9 coding accuracy was obtained from chart review targeting ICD-9 coding accuracy of all patients treated at our institution between March and June of 2010. To improve performance an educational session highlighted common coding errors, and a user-friendly software tool, RadOnc ICD Search, version 1.0, for coding radiation oncology specific diagnoses was implemented. We then prospectively analyzed ICD-9 coding accuracy for all patients treated from July 2010 to June 2011, with the goal of maintaining 80% or higher coding accuracy. Data on coding accuracy were analyzed and fed back monthly to individual providers.

Results: Baseline coding accuracy for physicians was 463 of 661 (70%) cases. Only 46% of physicians had coding accuracy above 80%. The most common errors involved metastatic cases, whereby primary or secondary site ICD-9 codes were either incorrect or missing, and special procedures such as stereotactic radiosurgery cases. After implementing our project, overall coding accuracy rose to 92% (range, 86%-96%). The median accuracy for all physicians was 93% (range, 77%-100%) with only 1 attending having accuracy below 80%. Incorrect primary and secondary ICD-9 codes in metastatic cases showed the most significant improvement (10% vs 2% after intervention).

Conclusions: Identifying common coding errors and implementing both education and systems changes led to significantly improved coding accuracy. This quality assurance project highlights the potential problem of ICD-9 coding accuracy by physicians and offers an approach to effectively address this shortcoming.
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http://dx.doi.org/10.1016/j.prro.2014.03.007DOI Listing
October 2015

Value of fluoro-2-deoxy-D-glucose-positron emission tomography for detecting metastatic lesions in head and neck cancer.

Am J Clin Oncol 2012 Aug;35(4):311-5

Department of Radiation Oncology, Jefferson Medical College of Thomas Jefferson University, Philadelphia, PA, USA.

Objectives: The role of positron emission tomography (PET) scans in the staging of head and neck cancer (HNC) is unclear. The National Comprehensive Cancer Network guidelines do not recommend routine metastatic workup beyond physical examination, chest x-ray, and laboratory tests. The purpose of this report is to examine the accuracy of staging PET scans for detecting distant metastatic disease in patients with HNC.

Methods: Retrospective review of 182 consecutive newly diagnosed HNC patients who had a staging PET scan at Thomas Jefferson University Hospital between 2003 and 2007.

Results: The overall incidence of confirmed distant metastatic disease in this population was 5.0%. About 26 of the staging PET scans had areas suspicious for a metastatic lesion(s). Of total, 23 patients were further evaluated with imaging and/or biopsy, revealing 9 (39%) true positives, and 14 (60%) false positives. Of the 156 negative PET scans, there was 1 false negative and 155 true negatives. Thus, the sensitivity of PET was 90% and specificity was 92%. Positive predictive value was 39% and negative predictive value was 99.4%. No patients with pre-PET clinical stage I or II cancer had confirmed distant metastases. The only statistically significant predictor for metastatic disease was clinical stage IV versus all other stages (P=0.03).

Conclusions: Given the marked differences in the treatment of locally advanced/nonmetastatic HNC versus metastatic HNC, we recommend PET for clinical stage IV disease. Although the sensitivity, specificity, and negative predictive value rates were acceptable, the positive predictive value was suboptimal. Patients found to have a PET scan "positive" for metastatic disease require confirmatory imaging or ideally biopsy.
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http://dx.doi.org/10.1097/COC.0b013e3181ec5f2eDOI Listing
August 2012

Do elderly patients experience increased perioperative or postoperative morbidity or mortality when given neoadjuvant chemoradiation before esophagectomy?

Int J Radiat Oncol Biol Phys 2011 Aug 23;80(5):1372-6. Epub 2010 Nov 23.

Department of Radiation Oncology, University of California, San Francisco, CA 94143, USA.

Background: The use of induction chemoradiotherapy followed by surgery has been widely used for the treatment of esophageal cancer. The presumed risk of increased postoperative morbidity and mortality with this regimen has led to reluctance to offer this therapy to elderly patients. We compared the perioperative morbidity and mortality of patients 70 years old and older with those of patients younger than 70 who received CRT followed by esophagectomy and sought to identify preoperative risk factors that may predict higher risk of postoperative death or complications.

Methods And Materials: We identified 260 patients who underwent preoperative chemoradiotherapy followed by esophagectomy. The association of age with postoperative death and complications was evaluated. The Charlson index, prior cardiac history, and diabetes were identified as preoperative risk factors and were evaluated as potential confounders or effect modifiers.

Results: Cardiac disease and the Charlson index were potential modifiers of the effect of age on length of hospital stay (p = 0.08 and p = 0.07, respectively) and postoperative complications (p = 0.1 and p = 0.2) but were not statistically significant. There was a slight nonsignificant decrease in the risk of death in elderly patients after adjustment for the Charlson index (p = 0.2).

Conclusion: No significant differences were detected with respect to morbidity and mortality in elderly patients. The presence of cardiac disease, higher scores on the Charlson index, or diabetes did not significantly influence length of stay, postoperative complications, or postoperative death. Given the potential to improve outcomes, this regimen should not be discounted in elderly patients.
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http://dx.doi.org/10.1016/j.ijrobp.2010.04.055DOI Listing
August 2011

Hypofractionated stereotactic radiation therapy: an effective therapy for recurrent high-grade gliomas.

J Clin Oncol 2010 Jun 17;28(18):3048-53. Epub 2010 May 17.

Department of Radiation Oncology, Neurological Surgery, Kimmel Cancer Center, Thomas Jefferson University, Philadelphia, PA, USA. [corrected]

Purpose: Salvage options for recurrent high-grade gliomas (HGGs) are limited by cumulative toxicity and limited efficacy despite advances in chemotherapeutic and radiotherapeutic techniques. Previous studies have reported encouraging survival results and favorable toxicity with fractionated stereotactic radiotherapy, and small studies have shown similar benefit using a shortened course of hypofractionated stereotactic radiation therapy (H-SRT). We sought to determine the efficacy and toxicity profile of H-SRT alone or in addition to repeat craniotomy or concomitant chemotherapy.

Patients And Methods: Between 1994 and 2008, 147 patients with recurrent HGG were treated with H-SRT (median dose, 35 Gy in 3.5-Gy fractions). Cox regression models were used to analyze survival outcomes. Variables included age, surgery before H-SRT, time to first recurrence, reirradiation dose, inclusion of chemotherapy with H-SRT, and gross tumor volume (GTV).

Results: Younger age (P = .001), smaller GTV (P = .025), and shorter time between diagnosis and recurrence (P = .034) were associated with improvement in survival from H-SRT. Doses of radiation > or = 35 Gy approached significance (P = .07). There was no significant benefit of surgical resection or chemotherapy in this population when analysis was controlled for other prognostic factors.

Conclusion: H-SRT was well tolerated and resulted in a median survival time of 11 months after H-SRT, independent of re-operation or concomitant chemotherapy. Patients who experienced recurrence within 6 months after initial treatment had an excellent response and should not be disqualified from H-SRT. This is the largest series to examine the efficacy and tolerability of H-SRT in recurrent HGG.
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http://dx.doi.org/10.1200/JCO.2009.25.6941DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2982785PMC
June 2010