5-aminolevulinic-acid guided resection

5-aminolevulinic-acid guided resection

In addition to stereotactic localization as well as intraoperative brain mapping, techniques to enhance visual identification of tumor intraoperatively may be used and include 5-aminolevulinic-acid (5-ALA). 5-ALA is metabolized into fluorescent porphyrins, which accumulate in malignant glioma cells. These property permits use of ultraviolet illumination during surgery as an adjunct to map out the tumor. This has been proven with RCT where the use of 5-ALA leads to more complete resection (65% vs. 36%, p < 0.0001), which translates into a higher 6-month progression-free survival (41% vs. 21.1%, p = 0.0003) but no effect on OS 1).


Fluorescein can be used as a viable alternative to 5-ALA for intraoperative fluorescent guidance in brain tumor surgery. Comparative, prospective, and randomized studies are much needed 2).


Indications

Meningeal sarcoma

First case published in the literature of meningeal sarcoma in a child in which intraoperative fluorescence with 5-ALA was used to achieve a complete resection 5).

Meningioma

Metabolic imaging tools such as 5-ALA fluorescence-guided resection and navigated FET-PET were helpful for the resection of complex-shaped, recurrent skull base meningioma. 5-ALA fluorescence was useful to dissect the adherent interface between tumor and brain. Furthermore, it helped to delineate tumor margins in the nasal cavity. FET-PET improved the assessment of bony and dural infiltration. We hypothesize that these imaging technologies may reduce recurrence rates through better visualization of tumor tissue that might be left unintentionally. This has to be verified in larger, prospective trials 6).

Tumor fluorescence can occur in benign meningiomas (WHO grade I) as well as in WHO grade II and WHO grade III meningiomas. Most of the reviewed studies report fluorescence of the main tumor mass with high sensitivity and specificity. However, different parts of the same tumor can present with a different fluorescent pattern (heterogenic fluorescence). Quantitative probe fluorescence can be superior, especially in meningiomas with difficult anatomical accessibility. However, only one study was able to consistently correlate resected tissue with histopathological results and nonspecific fluorescence of healthy brain tissue remains a confounder. The use of 5-ALA as a tool to guide resection of intracranial meningiomas remains experimental, especially in cases with tumor recurrence. The principle of intraoperative fluorescence as a real-time method to achieve complete resection is appealing, but the usefulness of 5-ALA is questionable. 5-ALA in intracranial meningioma surgery should only be used in a protocolled prospective and long-term study 7).

Doses

The highest visible and measurable fluorescence was yielded by 20 mg/kg. No fluorescence was elicited at 0.2 mg/kg. Increasing 5-ALA doses did not result in proportional increases in tissue fluorescence or PPIX accumulation in plasma, indicating that doses higher than 20 mg/kg will not elicit useful increases in fluorescence 8).


Application of 5mg/kg ALA was evaluated as equally reliable as the higher dose regarding the diagnostic performance when guidance was performed using a spectroscopic system. Moreover, no PpIX was detected in the skin of the patients 9).

Over time, several other tumour entities have been identified to metabolize 5-ALA and show a similar fluorescence pattern during surgical resection.

Further research is warranted to determine the role of 5-ALA accumulation in post-ischaemic and inflammatory brain tissue 10).

The positive predictive values (PPVs), of utilizing the most robust ALA fluorescence intensity (lava-like orange) as a predictor of tumor presence is high. However, the negative predictive values (NPVs), of utilizing the absence of fluorescence as an indicator of no tumor is poor. ALA intensity is a strong predictor for degree of tumor cellularity for the most fluorescent areas but less so for lower ALA intensities. Even in the absence of tumor cells, reactive changes may lead to ALA fluorescence 11).

Reviews

Senders et al., systematically review all clinically tested fluorescent agents for application in fluorescence guided surgery (FGS) for glioma and all preclinically tested agents with the potential for FGS for glioma.

They searched the PubMed and Embase databases for all potentially relevant studies through March 2016.

They assessed fluorescent agents by the following outcomes: rate of gross total resection (GTR), overall and progression free survival, sensitivity and specificity in discriminating tumor and healthy brain tissue, tumor-to-normal ratio of fluorescent signal, and incidence of adverse events.

The search strategy resulted in 2155 articles that were screened by titles and abstracts. After full-text screening, 105 articles fulfilled the inclusion criteria evaluating the following fluorescent agents: 5 aminolevulinic acid (5-ALA) (44 studies, including three randomized control trials), fluorescein (11), indocyanine green (five), hypericin (two), 5-aminofluorescein-human serum albumin (one), endogenous fluorophores (nine) and fluorescent agents in a pre-clinical testing phase (30). Three meta-analyses were also identified.

5-ALA is the only fluorescent agent that has been tested in a randomized controlled trial and results in an improvement of GTR and progression-free survival in high-grade gliomas. Observational cohort studies and case series suggest similar outcomes for FGS using fluorescein. Molecular targeting agents (e.g., fluorophore/nanoparticle labeled with anti-EGFR antibodies) are still in the pre-clinical phase, but offer promising results and may be valuable future alternatives. 12).

Complications

Despite its benefits, 5-ALA has not reached widespread popularity in the United States, primarily because of lack of Food and Drug Administration (FDA) approval. Even if it were approved, 5-ALA does have specific limitations including low depth of penetration, autofluorescence of background parenchyma


Findings suggest that the administration of 5-ALA or the combined effect of 5-ALA, anaesthesia and tumour resection can cause a mild and reversible elevation in liver enzymes. It therefore appears safe to change the regime of monitoring. Routine blood samples are thus abolished, though caution remains necessary in patients with known liver impairment 13).

For near infrared imaging, additional investigators have explored fluorescein as well as novel near-infrared (NIR) agents 14) 15) 16)

Stummer et al. showed that 5–ALA guided resections carry a higher risk of post-operative neurological deterioration than conventional resections (26% vs 15%, respectively), even though the difference vanished within weeks 17).

Just as tumour tissue is often indiscernible from normal brain tissue, functionally critical tissues are indistinguishable from tissues with less clinically relevant functions.

Thus, knowing when to stop a resection due to proximity to areas of crucial neurological functions is of obvious and utmost importance. Detailed knowledge of the normal brain anatomy and distribution of function is not sufficient during glioma resection. Interindividual variability and functional relocation (i.e., plasticity) induced by the presence of an infiltrating tumour 18) requires an exact functional brain map at the site of surgery in order to spare areas involved in crucial (so-called eloquent) functions. Preoperative localisation of function, either with functional MRI (fMRI) or navigated transcranial magnetic stimulation (nTMS), provides an approximate map 19) 20).

Furthermore, intra-operative direct cortical and subcortical electrical stimulation (DCS) for functional analysis of the tissue in the tumour’s infiltration zone is required for accurate identification of areas that need to be spared in order to retain the patient’s functional integrity 21) 22). Motor evoked potentials (MEP) provide real-time information on the integrity of the primary motor cortex and the corticospinal tract 23). Direct cortical mapping and phase reversal identify the primary motor and sensory cortices. Subcortical mapping can estimate the distance to the pyramidal tract, acting as guidance close to functionally critical areas 24). When integrated into the existing surgical tools, continuous and dynamic mapping enables more extensive resection while simultaneously protecting motor function 25). Using these techniques and a detailed electrophysiological “Bern-concept”, a group achieved complete motor function protection in 96% of patients with high-risk motor eloquent tumours 26). Furthermore, localisation of cortical and subcortical regions relevant to language function is essential for speech preservation during resection of gliomas in proximity to presumed speech areas 27) and requires the patient to be awake during the brain mapping part of surgery. Similarly, intra-operative mapping of visual functions may contribute to increased resections while avoiding tissue essential for vision within the temporal and occipital lobes 28).

References

1) , 3)

Stummer W, Pichlmeier U, Meinel T, Wiestler OD, Zanella F, Reulen HJ; ALA-Glioma Study Group. Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial. Lancet Oncol. 2006 May;7(5):392-401. PubMed PMID: 16648043.
2)

Hansen RW, Pedersen CB, Halle B, Korshoej AR, Schulz MK, Kristensen BW, Poulsen FR. Comparison of 5-aminolevulinic acid and sodium fluorescein for intraoperative tumor visualization in patients with high-grade gliomas: a single-center retrospective study. J Neurosurg. 2019 Oct 4:1-8. doi: 10.3171/2019.6.JNS191531. [Epub ahead of print] PubMed PMID: 31585425.
4)

Lakomkin N, Hadjipanayis CG. Fluorescence-guided surgery for high-grade gliomas. J Surg Oncol. 2018 Aug 19. doi: 10.1002/jso.25154. [Epub ahead of print] Review. PubMed PMID: 30125355.
5)

Bernal García LM, Cabezudo Artero JM, Royano Sánchez M, Marcelo Zamorano MB, López Macías M. Fluorescence-guided resection with 5-aminolevulinic acid of meningeal sarcoma in a child. Childs Nerv Syst. 2015 Apr 12. [Epub ahead of print] PubMed PMID: 25863951.
6)

Cornelius JF, Slotty PJ, Stoffels G, Galldiks N, Langen KJ, Steiger HJ. 5-Aminolevulinic Acid and (18)F-FET-PET as Metabolic Imaging Tools for Surgery of a Recurrent Skull Base Meningioma. J Neurol Surg B Skull Base. 2013 Aug;74(4):211-6. doi: 10.1055/s-0033-1342918. Epub 2013 Apr 1. PubMed PMID: 24436914.
7)

Motekallemi A, Jeltema HR, Metzemaekers JD, van Dam GM, Crane LM, Groen RJ. The current status of 5-ALA fluorescence-guided resection of intracranial meningiomas-a critical review. Neurosurg Rev. 2015 Mar 5. [Epub ahead of print] PubMed PMID: 25736455.
8)

Stummer W, Stepp H, Wiestler OD, Pichlmeier U. Randomized, Prospective Double-Blinded Study Comparing 3 Different Doses of 5-Aminolevulinic Acid for Fluorescence-Guided Resections of Malignant Gliomas. Neurosurgery. 2017 Apr 1. doi: 10.1093/neuros/nyx074. [Epub ahead of print] PubMed PMID: 28379547.
9)

Haj-Hosseini N, Richter J, Hallbeck M, Wårdell K. Low dose 5-aminolevulinic acid: Implications in spectroscopic measurements during brain tumor surgery. Photodiagnosis Photodyn Ther. 2015 Mar 25. pii: S1572-1000(15)00031-9. doi: 10.1016/j.pdpdt.2015.03.004. [Epub ahead of print] PubMed PMID: 25818546.
10)

Behling F, Hennersdorf F, Bornemann A, Tatagiba M, Skardelly M. 5-Aminolevulinic acid accumulation in a cerebral infarction mimicking high-grade glioma, a case report. World Neurosurg. 2016 May 10. pii: S1878-8750(16)30271-6. doi: 10.1016/j.wneu.2016.05.009. [Epub ahead of print] PubMed PMID: 27178236.
11)

Lau D, Hervey-Jumper SL, Chang S, Molinaro AM, McDermott MW, Phillips JJ, Berger MS. A prospective Phase II clinical trial of 5-aminolevulinic acid to assess the correlation of intraoperative fluorescence intensity and degree of histologic cellularity during resection of high-grade gliomas. J Neurosurg. 2015 Nov 6:1-10. [Epub ahead of print] PubMed PMID: 26544781.
12)

Senders JT, Muskens IS, Schnoor R, Karhade AV, Cote DJ, Smith TR, Broekman ML. Agents for fluorescence-guided glioma surgery: a systematic review of preclinical and clinical results. Acta Neurochir (Wien). 2017 Jan;159(1):151-167. doi: 10.1007/s00701-016-3028-5. Review. PubMed PMID: 27878374; PubMed Central PMCID: PMC5177668.
13)

Offersen CM, Skjoeth-Rasmussen J. Evaluation of the risk of liver damage from the use of 5-aminolevulinic acid for intra-operative identification and resection in patients with malignant gliomas. Acta Neurochir (Wien). 2016 Nov 10. [Epub ahead of print] PubMed PMID: 27832337.
14)

Shinoda J, Yano H, Yoshimura SI, et al. Fluorescence-guided resection of glioblastoma multiforme by using high-dose fluorescein sodium. Technical note. J Neurosurg. 2003;99(3):597–603.
15)

Rey-Dios R, Cohen-Gadol AA. Technical principles and neurosurgical applications of fluorescein fluorescence using a microscope-integrated fluorescence module. Acta Neurochir (Wien). 2013;155(4):701–706.
16)

Swanson KI, Clark PA, Zhang RR, et al. Fluorescent cancer-selective alkylphosphocholine analogs for intraoperative glioma detection. Neurosurgery. 2015;76(2):115–123.
17)

Stummer W1, Tonn JC, Mehdorn HM, Nestler U, Franz K, Goetz C, et al. ALA-Glioma Study Group. Counterbalancing risks and gains from extended resections in malignant glioma surgery: a supplemental analysis from the randomized 5–aminolevulinic acid glioma resection study. J Neurosurg. 2011;114(3):613–23. doi: 10.3171/2010.3
18)

Ojemann G, Ojemann J, Lettich E, Berger M. Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. J Neurosurg. 1989;71(3):316–26.
19)

Seghier ML, Lazeyras F, Pegna AJ, Annoni JM, Zimine I, Mayer E, et al. Variability of fMRI activation during a phonological and semantic language task in healthy subjects. Hum Brain Mapp. 2004;23(3):140–55.
20)

Krieg SM, Shiban E, Buchmann N, Gempt J, Foerschler A, Meyer B, et al. Utility of presurgical navigated transcranial magnetic brain stimulation for the resection of tumors in eloquent motor areas. J Neurosurg. 2012;116(5):994–1001. doi: 10.3171/2011.12.JNS111524
21) , 27)

Duffau H, Capelle L, Sichez N, Denvil D, Lopes M, Sichez JP, et al. Intraoperative mapping of the subcortical language pathways using direct stimulations. An anatomo-functional study. Brain. 2002;125(1):199–214.
22)

Duffau H, Capelle L, Denvil D, Sichez N, Gatignol P, Taillandier L, et al. Usefulness of intraoperative electrical subcortical mapping during surgery for low-grade gliomas located within eloquent brain regions: functional results in a consecutive series of 103 patients. J Neurosurg. 2003;98(4):764–78.
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Seidel K, Beck J, Stieglitz L, Schucht P, Raabe A. The warning-sign hierarchy between quantitative subcortical motor mapping and continuous motor evoked potential monitoring during resection of supratentorial brain tumors. J Neurosurg. 2013;118(2):287–96.
24)

Seidel K, Beck J, Stieglitz L, Schucht P, Raabe A. Low Threshold Monopolar Motor Mapping for Resection of Primary Motor Cortex Tumors. Neurosurgery. 2012;71(1):104–14.
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Raabe A, Beck J, Schucht P, Seidel K. Continuous dynamic mapping of the corticospinal tract during surgery of motor eloquent brain tumors: evaluation of a new method. J Neurosurg. 2014;120(5)1015–24. doi: 10.3171/2014.1.JNS13909.
26)

Schucht P, Seidel K. Beck J, Murek M, Jilch A, Wiest R, et al. Intraoperative monopolar mapping during 5-ALA-guided resections of glioblastomas adjacent to motor eloquent areas: evaluation of resection rates and neurological outcome. Neurosurg Focus. 2014;27(6):E16.
28)

Gras-Combe G, Moritz-Gasser S, Herbet G, Duffau H. Intraoperative subcortical electrical mapping of optic radiations in awake surgery for glioma involving visual pathways. J Neurosurg. 2012;117(3):466–73.

Microvascular decompression for hemifacial spasm outcome

Microvascular decompression for hemifacial spasm outcome

Microvascular decompression is an effective treatment for hemifacial spasm. Given that postoperative delayed cure was unavoidable, even with accurate identification of the offending vessel and sufficient decompression of the root exit zone, the delayed cure should be considered in patients undergoing reoperation due to lack of remission or relapse after the operation. Additionally, the timing of efficacy assessments should be delayed 1).

The definitive treatment for hemifacial spasm is microvascular decompression (MVD), which cures the disease in 85% to 95% of patients according to reported series. In expert hands, the MVD procedure can be done with relatively low morbidity.

Post-operatively, there may be episodes of mild HFS, however they usually begin to diminish 2–3 days following MVD. Severe spasm that does not abate suggests failure to achieve adequate decompression, and reoperation should be considered.

Surgical results of MVD depends on the duration of symptoms (shorter duration has better prognosis) as well as on the age of the patient (elderly patients do less well). Complete resolution of HFS occurred in 44 (81%) of 54 patients undergoing MVD, however, 6 of these patients had relapse 2). 5 patients (9%) had partial improvement, and 5 (9%) had no relief.


Complete resolution of spasm occurs in ≈ 85–93% 3) 4) 5) 6) 7). Spasm is diminished in 9%, and unchanged in 6% 8). Of 29 patients with complete relief, 25 (86%) had immediate post-op resolution, and the remaining 4 patients took from 3 mos to 3 yrs to attain quiescence.

Recurrence

References

1)

Li MW, Jiang XF, Wu M, He F, Niu C. Clinical Research on Delayed Cure after Microvascular Decompression for Hemifacial Spasm. J Neurol Surg A Cent Eur Neurosurg. 2019 Oct 10. doi: 10.1055/s-0039-1698461. [Epub ahead of print] PubMed PMID: 31600810.
2)

Auger RG, Peipgras DG, Laws ER. Hemifacial Spasm: Results of Microvascular Decompression of the Facial Nerve in 54 Patients. Mayo Clin Proc. 1986; 61:640–644
3)

Rhoton AL. Comment on Payner T D and Tew J M: Recurren ce of Hemifacial Spasm After Microvascular Decompression. Neurosurgery. 1996; 38
4)

Jannetta PJ. Neurovascular Compression in Cranial Nerve and Systemic Disease. Ann Surg. 1980; 192:518–525
5)

Loeser JD, Chen J. Hemifacial Spasm: Treatment by Microsurgical Facial Nerve Decompression. Neurosurgery. 1983; 13:141–146
6)

Huang CI, Chen IH, Lee LS. Microvascular Decompression for Hemifacial Spasm: Analyses of Operative Findings and Results in 310 Patients. Neurosurgery. 1992; 30:53–57
7) , 8)

Payner TD, Tew JM. Recurrence of Hemifacial Spasm After Microvascular Decompression. Neurosurgery. 1996; 38:686–691

Unplanned hospital readmission after cranial neurosurgery

Unplanned hospital readmission after cranial neurosurgery

Many readmissions may be preventable and occur at predictable time intervals. The causes and timing of readmission vary significantly across neurosurgical subgroups. Future studies should focus on detecting specific complications in select cohorts at predefined time points, which may allow for interventions to lower costs and reduce patient morbidity 1).


Hospital readmission to a hospital (non-index) other than the one from which patients received their original care (index) has been associated with increases in both morbidity and mortality for cancer patients.

Of patient readmissions following brain tumor resection, 15.6% occur at a non-index facility. Low procedure volume is a confounder for non-index analysis and is associated with an increased likelihood of major complications and mortality, as compared to readmission to high-procedure-volume hospitals. Further studies should evaluate interventions targeting factors associated with unplanned readmission 2).


In a single-center Canadian experience. Almost one-fifth of neurosurgical patients were readmitted within 30 days of discharge. However, only about half of these patients were admitted for an unplanned reason, and only 10% of all readmissions were potentially avoidable. This study demonstrates unique challenges encountered in a publicly funded healthcare setting and supports the growing literature suggesting 30-day readmission rates may serve as an inappropriate quality of care metric in neurosurgical patients. Potentially avoidable readmissions can be predicted, and further research assessing predictors of avoidable readmissions is warranted 3).

A study of Elsamadicy et al. suggested that infection, altered mental status, and new sensory/motor deficits were the primary complications leading to unplanned 30-day readmission after cranial neurosurgery 4).


The preponderance of postdischarge mortality and complications requiring readmission highlights the importance of posthospitalization management 5).


Obstructive sleep apnea (OSA) is known to be associated with negative outcomes and is underdiagnosed. The STOP-Bang questionnaire is a screening tool for OSA that has been validated in both medical and surgical populations. Given that readmission, after surgical intervention is an undesirable event, Caplan et al. sought to investigate, among patients not previously diagnosed with OSA, the capacity of the STOP-Bang questionnaire to predict 30-day readmissions following craniotomy for a supratentorial tumor.

For patients undergoing craniotomy for treatment of a supratentorial neoplasm within a multiple-hospital academic medical center, data were captured in a prospective manner via the Neurosurgery Quality Improvement Initiative (NQII) EpiLog tool. Data were collected over a 1-year period for all supratentorial craniotomy cases. An additional criterion for study inclusion was that the patient was alive at 30 postoperative days. Statistical analysis consisted of simple logistic regression, which assessed the ability of the STOP-Bang questionnaire and additional variables to effectively predict outcomes such as 30-day readmission, 30-day emergency department (ED) visit, and 30-day reoperation. The C-statistic was used to represent the receiver operating characteristic (ROC) curve, which analyzes the discrimination of a variable or model.

Included in the sample were all admissions for supratentorial neoplasms treated with craniotomy (352 patients), 49.72% (n = 175) of which were female. The average STOP-Bang score was 1.91 ± 1.22 (range 0-7). A 1-unit higher STOP-Bang score accurately predicted 30-day readmissions (OR 1.31, p = 0.017) and 30-day ED visits (OR 1.36, p = 0.016) with fair accuracy as confirmed by the ROC curve (C-statistic 0.60-0.61). The STOP-Bang questionnaire did not correlate with 30-day reoperation (p = 0.805) or home discharge (p = 0.315).

The results of this study suggest that undiagnosed OSA, as assessed via the STOP-Bang questionnaire, is a significant predictor of patient health status and readmission risk in the brain tumor craniotomy population. Further investigations should be undertaken to apply this prediction tool in order to enhance postoperative patient care to reduce the need for unplanned readmissions 6).


Lopez Ramos et al., from the Department of Neurological Surgery, University of California San Diego, La Jolla, CA, USA, examined clinical risk factors and postoperative complications associated with 30-day unplanned hospital readmissions after cranial neurosurgery.

They queried the American College of Surgeons National Surgical Quality Improvement Program database from 2011-2016 for adult patients that underwent a cranial neurosurgical procedure. Multivariable logistic regression with backwards model selection was used to determine predictors associated with 30-day unplanned hospital readmission.

Of 40,802 cranial neurosurgical cases, 4,147 (10.2%) had an unplanned readmission. Postoperative complications were higher in the readmission cohort (18.5% vs 9.9%, p <0.001). On adjusted analysis, clinical factors predictive of unplanned readmission included hypertension, COPD, diabetes, coagulopathy, chronic steroid use, and preoperative anemia, hyponatremia, and hypoalbuminemia (all p ≤ 0.01). Higher ASA class (III-V), operative time >216 minutes, and unplanned reoperation were also associated with an increased likelihood of readmission (all p ≤0.001). Postoperative complications predictive of unplanned readmissions were wound infection (OR 4.90, p <0.001), pulmonary embolus (OR 3.94, p <0.001), myocardial infarction/cardiac arrest (OR 2.37, p <0.001), sepsis (OR 1.73, p <0.001), deep venous thrombosis (1.50, p=0.002), and urinary tract infection (OR 1.45, p=0.002). Female sex, transfer status, and postoperative pulmonary complications were protective of readmission (all p <0.05)

Unplanned hospital readmission after cranial neurosurgery is a common event. Identification of high-risk patients who undergo cranial procedures may allow hospitals to reduce unplanned readmissions and associated healthcare costs 7).


Cusimano et al., conducted a systematic review of several databases; a manual search of the Journal of NeurosurgeryNeurosurgeryActa NeurochirurgicaCanadian Journal of Neurological Sciences; and the cited references of the selected articles. Quality review was performed using the STROBE (Strengthening the Reporting of Observational Studies in Epidemiology) criteria. Findings are reported according to the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) guidelines.

A total of 1344 articles published between 1947 and 2015 were identified; 25 were considered potentially eligible, of which 12 met inclusion criteria. The 30-day readmission rates varied from 6.9% to 23.89%. Complications arising during or after neurosurgical procedures were a prime reason for readmission. Race, comorbidities, and longer hospital stay put patients at risk for readmission.

Although readmission may be an important indicator for good care for the subset of acutely declining patients, neurosurgery should aim to reduce 30-day readmission rates with improved quality of care through systemic changes in the care of neurosurgical patients that promote preventive measures 8).

References

1)

Taylor BE, Youngerman BE, Goldstein H, Kabat DH, Appelboom G, Gold WE, Connolly ES Jr. Causes and Timing of Unplanned Early Readmission After Neurosurgery. Neurosurgery. 2016 Sep;79(3):356-69. doi: 10.1227/NEU.0000000000001110. PubMed PMID: 26562821.
2)

Jarvis CA, Bakhsheshian J, Ding L, Wen T, Tang AM, Yuan E, Giannotta SL, Mack WJ, Attenello FJ. Increased complication and mortality among non-index hospital readmissions after brain tumor resection is associated with low-volume readmitting hospitals. J Neurosurg. 2019 Oct 4:1-13. doi: 10.3171/2019.6.JNS183469. [Epub ahead of print] PubMed PMID: 31585421.
3)

Wilson MP, Jack AS, Nataraj A, Chow M. Thirty-day readmission rate as a surrogate marker for quality of care in neurosurgical patients: a single-center Canadian experience. J Neurosurg. 2018 Jul 1:1-7. doi: 10.3171/2018.2.JNS172962. [Epub ahead of print] PubMed PMID: 29979117.
4)

Elsamadicy AA, Sergesketter A, Adogwa O, Ongele M, Gottfried ON. Complications and 30-Day readmission rates after craniotomy/craniectomy: A single Institutional study of 243 consecutive patients. J Clin Neurosci. 2018 Jan;47:178-182. doi: 10.1016/j.jocn.2017.09.021. Epub 2017 Oct 12. PubMed PMID: 29031542.
5)

Dasenbrock HH, Yan SC, Smith TR, Valdes PA, Gormley WB, Claus EB, Dunn IF. Readmission After Craniotomy for Tumor: A National Surgical Quality Improvement Program Analysis. Neurosurgery. 2017 Apr 1;80(4):551-562. doi: 10.1093/neuros/nyw062. PubMed PMID: 28362921.
6)

Caplan IF, Glauser G, Goodrich S, Chen HI, Lucas TH, Lee JYK, McClintock SD, Malhotra NR. Undiagnosed obstructive sleep apnea as a predictor of 30-day readmission for brain tumor patients. J Neurosurg. 2019 Jul 19:1-6. doi: 10.3171/2019.4.JNS1968. [Epub ahead of print] PubMed PMID: 31323636.
7)

Lopez Ramos C, Brandel MG, Rennert RC, Wali AR, Steinberg JA, Santiago-Dieppa DR, Burton BN, Pannell JS, Olson SE, Khalessi AA. Clinical Risk Factors and Postoperative Complications Associated with Unplanned Hospital Readmissions After Cranial Neurosurgery. World Neurosurg. 2018 Jul 24. pii: S1878-8750(18)31614-0. doi: 10.1016/j.wneu.2018.07.136. [Epub ahead of print] PubMed PMID: 30053566.
8)

Cusimano MD, Pshonyak I, Lee MY, Ilie G. A systematic review of 30-day readmission after cranial neurosurgery. J Neurosurg. 2017 Aug;127(2):342-352. doi: 10.3171/2016.7.JNS152226. Epub 2016 Oct 21. PubMed PMID: 27767396.
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