Advances in complex endovascular aortic surgery
Dijkstra, Martijn Leander
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Spinal cord ischemia in endovascular thoracic and
thoraco-abdominal aortic repair: review of preventive
strategies
M.L. DIJKSTRA,
1T. VAINAS,
2C.J. ZEEBREGTS,
1I. L. HOOFT,
3M.J. VAN DER LAAN.
11 Department of Surgery, Division of Vascular Surgery, University Medical Center Groningen, University of
Groningen, Groningen, Th e Netherlands
2 Department of Vascular Surgery, Glenfi eld Hospital, University Hospitals of Leicester, Leicester, UK
3 Cochrane Netherlands, Julius Center for Health Sciences and Primary Care, University Medical Center
Utrecht, Utrecht, Th e Netherlands
absTracT
Introduction: The incidence of Spinal cord ischemia (SCI) and subsequent paraple-gia after thoracic (TEVAR) and thoraco-abdominal endovascular aneurysm repair is estimated between 2.5 % and 8 %. The aim of this review was to provide an overview of SCI preventive strategies in TEVAR and thoraco-abdominal repair and recommend an optimal strategy.
Methods: Pubmed, Embase and the Cochrane Library were searched for studies on TEVAR, thoraco-abdominal endovascular repair and the use of SCI preventive measures. The review was reported according to the PRISMA statement. Results: The final analysis included 43 studies (7168 patients). All studies are cohort studies (non-comparative cohorts n = 37, comparative cohorts n = 6) and largely performed retrospectively (n = 27). The included studies had an average MINORS score of 9 (range 6 - 13) for non-comparative studies and 15.5 (range 12 - 18) for comparative studies. Transient SCI occurred in 5.7 % (450/7168, 95 % CI 4.5- 6.9 %, range 0.3 - 30.6 %), permanent SCI in 2.2 % (232/7168, 95 % CI 1.6 - 2.8 %, range 0.3 - 20.8 %). There was a trend towards increased SCI incidence for more ‘high risk’ cohorts. Avoidance of hypotension resulted in a slightly lower permanent SCI rate 1.8 % (102/4216, 95 % CI 1.2- 2.3 %) compared to the overall cohort. A very low SCI estimate (transient and permanent) was found in the subgroup of studies (2 studies, n = 248) using (mild) peri-operative hypothermia (transient SCI 0.8 %, permanent SCI 0.4 %). In the subgroup using temporary permissive endoleak, there was a transient SCI estimate (15.4 %), with a permanent SCI estimate of 4.8 %. The remaining preventive measures did not significantly impact transient and permanent SCI estimates.
Conclusion: Low overall transient and permanent SCI rates are achieved during endovascular thoracic and thoraco-abdominal aortic repair. Permanent SCI rates up to 21 % are reported in high risk cohorts. The current SCI prevention proto-cols vary widely. Based on this review, selective spinal fluid drainage, avoidance of hypotension and mild hypothermia seems justified.
8
inTroducTion
Since its introduction endovascular aneurysm repair (EVAR) has evolved and is currently the predominant treatment modality for aortic aneurysms.1 Improved
operating techniques and devices allow for treatment of the majority of aortic lesions including thoracic aortic pathology by endovascular means and has become a preferred alternative to open repair with low overall mortality and morbidity.2–4 Spinal cord ischemia (SCI) and concomitant paraplegia are among
the most dreaded complications of thoracic endovascular aneurysm repair (TE-VAR) and endovascular thoraco-abdominal aortic repair.5 Although the incidence
of paraplegia is estimated between 2.5 % and 8 % and is lower compared to the paraplegia rate after open surgical repair, SCI remains a significant problem.6
Lower SCI incidences are achieved in high volume centers, and paraplegia rates seem to be declining in recent years.7 This decline has been attributed to the use
of rigorous multi-modality SCI prevention strategies.
The identification of risk factors for SCI, the categorization of specific high risk groups and the development of preventive measures for SCI have been subject of an extensive body of research. Suggested risk factors for SCI are aneurysm ex-tent, open surgical repair, prior distal aortic operations, and peri-operative hypo-tension. Furthermore, loss of intercostal arteries and collateral vasculature (e.g. subclavian, hypogastric) and duration of the procedure have been suggested as potential contributing factors.8 For most of the suggested risk factors however,
conflicting results have been reported. Similarly it remains unclear which specific patients are at risk for development of SCI and ultimately the development of a uniform multimodal preventive treatment protocol remains elusive.
With regard to the preventive measures for SCI after TEVAR and thoraco-abdominal repair, most of these strategies have proven their effectiveness in preventing SCI during open repair. Obviously, not all of the preventive measures used during open surgery are applicable, given the minimally invasive nature of these procedures. Currently used measures to prevent SCI after TEVAR and tho-raco-abdominal repair include spinal fluid drainage, avoidance of peri-operative hypotension (both aim to maintain adequate spinal cord perfusion), staging the repair and creating a permissive (temporary) endoleak to allow for temporary aneurysm (and spinal cord) perfusion. Additionally, peri-operative hypothermia and intra-thecal medication have been described as adjunct protective mea-sures.9 Although not necessarily a preventive measure in itself, intra-operative
neuro-monitoring has also been described as a strategy to reduce SCI rates by early identification of spinal cord mal-perfusion allowing for prompt initiation of measure to improve cord perfusion resulting in lower post-operative SCI rates.
Table 1. Guideline r ecommendations, including curr ent inter national recommendations on the pr evention of
SCI after thoracic
and thoraco-abdominal
endovascular
aortic r
epair
Guideline
Spinal fluid drain
A voidance of hypotension Hypothermia Staged procedur es LSA revascularization Permissive endoleak Peri-operative neur omonitoring
Management of Descending Thoracic Aorta Diseases - ESVS 2017
1 Selective a Ye s NR NR NR NR
Depending on institutional experience
Guidelines on the diagnosis and management of aortic diseases - ESC 2014
2 Selective a Ye s NR NR NR NR NR Endovascular r
epair of traumatic thoracic aortic injury - SVS
2011 3 Therapeutic NR NR NR Selective NR NR
Guidelines for the diagnosis and management of patients with thoracic aortic disease - AHA 2010
4
Selective
a
Ye
s
Open surgery only
NR
NR
NR
Depending on institutional experience
Management of the left subclavian artery with thoracic endovascular aortic r
epair - SVS 2009 5 NR NR NR NR Ye s NR NR
a Long segment coverage (> 200mm), pr
evious AAA r
epair
Abbreviations: ESVS, European society for V
ascular Surger
y; ESC, European society for Cardiologie; SVS; Society for V
ascular Suger
y; AHA, American Heart
Associa-tion; AAA, Abdominal Aortic Aneur
ysm; NR, Not reported; LSA, Left subclavian arter
y.
1 Riambau V et al. - Management of Descending Thoracic Aorta Diseases: Clinical Practice Guidelines of the European Society for V
ascular Surger
y (ESVS). Eur J V
asc
Endovasc Surg. 2017;53(1):4–52. 2 Erbel R et al. 2014 ESC guidelines on the diagnosis and treatment of aortic diseases. European Heart Journal. 2014;35(41):2873–
926.
3 Lee W
A et al. Endovascular repair of traumatic thoracic aortic injur
y: clinical practice guidelines of the Society for V
ascular Surger y. J V asc Surg. 2011;53(1):187–92. 4 Hiratzka LF et al. 2010 ACCF/AHA/AA
TS/ACR/ASA/SCA/SCAI/SIR/STS/SVM guidelines for the
diagnosis and
management
of patients
with Thoracic Aortic Disease.
Circulation. 2010;121(13):e266–369. 5 Matsumura JS et al. The
Society for V
ascular Surger
y Practice Guidelines: management of the left subclavian arter
y with thoracic endovascular aortic repair
. J V
asc
8
Current international guidelines mention a number of preventive strategies but there is some variation in the recommendations (Table 1). For TEVAR, the major-ity do recommend the avoidance of hypotension and the use of selective cere-brospinal fluid drainage during endovascular thoracic aortic repair for patients at high risk (long segment coverage (> 200mm), previous AAA repair10–12
) of spinal cord ischemic injury. The level of evidence for these recommendations is low (class IIA, level C, European Society of Cardiology grading system). For thoraco-abdominal endovascular aortic repair, no clear recommendations are made. The aim of this review was to provide an overview of the current evidence on the effectiveness of peri-operative strategies to prevent spinal cord ischemia in TEVAR and thoraco-abdominal endovascular aortic repair and recommend an optimal preventive strategy based on the available data.
MeThods
The review was reported according to the Preferred Reporting Items for System-atic reviews and Meta-Analyses (PRISMA) statement.
search and selection
Pubmed, Embase and the Cochrane Library were searched for studies on both TEVAR and thoraco-abdominal endovascular aortic repair, and the use of spinal cord ischemia preventive measures (date of electronic search, July 13th
2016). The full search strategy is shown in appendix I. The reference lists of selected articles were screened for other relevant publications. Screening of title and abstract was conducted by two reviewers (MD and ML).
Given the paucity of randomized trials addressing our review question, a broader range of study designs were considered eligible for review, including compara-tive and non-comparacompara-tive cohort studies. Case reports, small sample (n ≤ 10) cohort studies, studies on open surgical repair, animal studies and non-English publications were excluded. Furthermore, studies were only included when the incidence of spinal cord ischemia and the use of one or more preventive measures during the procedures (elective or acute) were specified, specifically the use of spinal fluid drain, avoidance of hypotension, hypothermia, staged procedures, intra-thecal medication, left subclavian artery (LSA) revascularization or permissive (temporary) endoleak.
data collection and analysis
Study and patient characteristics were collected using standardized forms. The follow-ing data were extracted: authors, year of publication, number of patients included, inclusion period, disease type, type of SCI protocol, general patient characteristics and co-morbidities, incidence of SCI (permanent, transient), preventive measures, data necessary to calculate the Methodological Index for Non-Randomized Studies (MINORS) score and characteristics known to influence the incidence of SCI. The methodological quality of the included studies was assessed using the MINORS score.13 This instrument is specifically developed and validated to assess
surgical studies, either comparative or non-comparative, and consists of 12 items (the separate items are scored 0 (not reported), 1 (reported but inadequate) or 2 (reported and adequate). The ideal global scores for non-comparative studies and for comparative studies are 16 and 24, respectively.13
Indirect comparisons were attempted to compare the effectiveness of preventive measures. In order to correct for possible patient selection bias, all cohorts were evalu-ated for high risk demographics and each cohort was given the highest percentage reported (including: urgent procedures, previous aortic surgery, long segment cover-age > 200mm). Continuous variables are described as mean and standard deviation, or median and inter-quartile range (IQR) in case of skewed data. To test for normality a Kolmogorov-Smirnov test was performed. Differences between continuous variables were tested using a paired student T-test or Mann-Whitney U test in case of skewed data. Differences between categorical variables were tested using chi-squared test. Two-sided P values <.05 were considered significant. Data analysis was performed using SPSS statistics 20.0 (IBM corporation, Armonk, NY, USA). Meta-analysis was performed using OpenMeta (open source meta-analysis software, http://www.cebm. brown.edu/openmeta/). Calculation of 95 % confidence intervals was performed using logit transformed proportion metric and DerSimonian-Laird random-effects method.
resulTs
identification of studies
In total, 2404 potential relevant references were identified after removal of duplicates. After detailed assessment, 43 studies and 7168 patients describing 7 preventive measures were included in the final analysis. Insufficient data on the used preventive measures was the main reason for exclusion during full-text assessment (Figure 1). The full list of references for the included articles is shown in appendix 2.
8
Characteristics of included studies
There are no randomized controlled trials available to date, all included studies are cohort studies (non-comparative cohorts n = 37, comparative cohorts n = 6). The general study characteristics are shown in Table 2. The majority of studies were performed retrospectively (n = 27, 62.8 %). Nine (20.9 %) studies included patients with aneurysmal disease only, one (2.3 %) study with dissections only and the remaining included patients with mixed disease types (aneurysmal, dis-section, penetrating aortic ulcers, trauma). Overall mean age was 68.6 years and there was a male predominance (70.7 %).
A specific SCI prevention protocol was described in 33 (76.7 %) of the studies. With regard to the different preventive measures, a prophylactic spinal fluid drain was used in 10 studies (23.3 %) versus selective drains in 28 studies (65.1 %). Of these, selective drains were used in 11 (39.3 %) studies that included thoraco-Figure 1. PRISMA flow diagram.
Table 2.
Study and patient characteristics for the included studies.
Authors Cohort type Disease type SCI Nr of patients Age (mean) Male sex (%) Hypertension (%) Diabetes (%) Car diac disease (%) Pulmonary disease (%) Renal disease (%) Smoking (%) Acher , C. et al. 2016 Pr ospective Mixed Ye s 155 74.0 56.1 NR NR NR NR NR NR Amabile, P . et al. 2008 Retr ospective Mixed Ye s 67 66.0 80.6 53.7 3.0 20.9 19.4 17.9 49.3 Ar naoutakis, D. J. et al. 2014 Retr ospective Mixed Ye s 90 67.3 53.0 80.0 16.0 30.0 26.0 23.0 54.0 Banga, P . V . et al. 2016 Retr ospective Mixed Ye s 49 75.0 78.0 88.0 18.0 65.0 43.0 37.0 86.0 Bisdas, T . et al. 2015 Retr ospective Mixed Ye s 142 79.0 78.9 94.0 12.0 44.0 28.0 6.0 59.0 Bobadilla, J. L. et al. 2013 Pr ospective Mixed Ye s 94 54.0 60.0 80.0 2.0 32.0 21.0 NR NR Chiesa, R. et al. 2005 Pr ospective Mixed Ye s 103 70.1 83.5 70.0 9.7 45.6 48.5 13.6 64.1 Clough, R. E. et al. 2014 Pr ospective Mixed Ye s 309 72.0 67.6 NR NR NR NR NR NR Desart, K. et al. 2013 Retr ospective Mixed Ye s 607 64.5 68.0 32.8 4.8 9.4 8.2 9.1 16.3 Dias, N. V . et al. 2015 Retr ospective Aneurysmal Ye s 72 68.0 73.6 84.7 18.1 33.3 43.1 41.7 44.4 Drinkwater , S. L. et al. 2010 Retr ospective Mixed No 235 65.9 64.3 NR NR NR NR NR NR Guillou, M. et al. 2012 Pr ospective Aneurysmal Ye s 89 69.0 93.3 80.0 18.0 39.0 19.1 27.0 79.0 Hanna, J. M. et al. 2013 Retr ospective Aneurysmal Ye s 381 63.6 58.5 87.7 13.1 31.0 30.7 27.8 62.5 Harrison, S. C. et al. 2012 Pr ospective Mixed Ye s 10 73.8 60.0 80.0 NR 30.0 NR 100.0 70.0 Hnath, J. C. et al. 2008 Retr ospective Mixed Ye s 121 51.0 72.0 NR NR 42.0 33.0 18.0 NR Jayia, P . et al. 2015 Retr ospective Aneurysmal Ye s 47 72.1 68.0 48.0 6.0 21.0 NR 11.0 14.0 Jonker , F . H. W . et al. 2010 Retr ospective Mixed No 87 69.8 69.0 51.7 10.3 42.5 25.3 13.8 NR Kamada, T . et al. 2015 Retr ospective Mixed No 51 72.0 74.5 86.3 11.8 NR NR NR NR Kasprzak, P . M. et al. 2014 Pr ospective Aneurysmal Ye s 40 72.8 72.5 95.0 NR 52.5 27.5 37.5 60.0 Kato, M. et al. 2015 Retr ospective Mixed Ye s 54 74.0 78.0 96.0 13.0 41.0 43.0 9.0 82.0 Keith Jr , C. J. et al. 2012 Pr ospective Mixed Ye s 266 64.1 62.8 84.6 21.4 42.1 29.7 21.4 71.4 Khoynezhad, A. et al. 2007 Pr ospective Mixed No 153 71.0 61.4 73.2 11.1 32.0 20.9 14.4 52.3
8
Table 2.
Study and patient characteristics for the included studies. (continued)
Authors Cohort type Disease type SCI Nr of patients Age (mean) Male sex (%) Hypertension (%) Diabetes (%) Car diac disease (%) Pulmonary disease (%) Renal disease (%) Smoking (%) Kitagawa, A. et al. 2013 Pr ospective Dissection Ye s 30 66.0 86.7 50.0 13.3 43.3 6.7 16.7 66.7 Knowles, M. et al. 2011 Retr ospective Mixed Ye s 96 66.4 57.3 69.8 14.6 36.5 20.8 16.7 66.7 Lee, M. et al. 2013 Retr ospective Mixed Ye s 145 62.0 63.0 83.0 15.0 27.0 37.0 22.0 NR Maldonado, T . S. et al. 2013 Retr ospective Mixed No 1189 67.8 59.1 84.9 17.3 42.7 30.9 13.6 53.8 Mastr or oberto, P . et al. 2013 Retr ospective Mixed Ye s 21 71.6 66.7 76.2 14.3 9.5 61.9 NR NR Matsuda, H. et al. 2010 Retr ospective Mixed Ye s 60 77.0 81.7 NR NR NR NR NR NR Maur el, B. et al. 2015 Retr ospective Aneurysmal Ye s 204 71.0 92.6 79.9 18.1 45.1 37.3 24.5 13.7 Patel, H. J. et al. 2006 Retr ospective Mixed Ye s 73 67.4 60.3 63.0 10.9 42.5 28.7 NR NR Pif far etti, G. et al. 2014 Retr ospective Mixed Ye s 77 72.0 91.0 92.0 16.0 35.0 49.0 7.0 NR Pr eventza, O. et al. 2009 Retr ospective Mixed Ye s 346 68.0 60.1 90.8 NR 7.8 23.7 19.1 NR Rossi, S. H. et al. 2015 Retr ospective Mixed Ye s 69 73.0 75.4 NR 19.8 50.0 30.0 NR NR Rylski, B. et al. 2013 Pr ospective Aneurysmal No 105 69.0 68.0 NR NR NR NR NR NR Schlösser , F . J. V . et al. 2009 Retr ospective Aneurysmal No 72 73.0 86.0 NR NR NR NR 14.0 NR Shah, T . R. et al. 2010 Pr ospective Mixed Ye s 59 69.2 51.0 67.8 23.7 25.4 27.1 15.3 62.7 Sobel, J. D. et al. 2015 Pr ospective Aneurysmal Ye s 116 72.0 74.0 94.0 13.0 56.0 49.0 21.0 93.0 Tanaka, K. et al. 2015 Retr ospective Mixed Ye s 148 72.8 67.6 81.1 16.9 18.9 10.1 4.1 NR Ullery , B. W . et al. 2011 Retr ospective Mixed Ye s 412 70.4 52.0 92.0 8.7 11.0 16.5 10.1 39.3 Y ingbin, J. et al. 2013 Retr ospective Mixed No 217 65.0 65.9 71.0 9.7 69.1 NR NR NR Zamor , K. C. et al. 2015 Pr ospective Mixed No 80 59.9 79.0 78.5 16.2 30.0 11.3 26.3 58.9 Zeng, Q. et al. 2016 Pr ospective Mixed Ye s 21 65.0 95.2 90.5 9.5 23.8 NR 14.3 42.9 Zipfel, B. et al. 2013 Pr ospective Mixed Ye s 406 63.0 74.0 NR NR NR NR NR NR Total 7168 68.6 70.7 77.4 13.3 35.1 29.2 21.1 56.8
Table 3.
Risk of bias analysis for the included studies.
Authors
MINORs scor
e
(max scor
e)
Risk factors reported High risk SCI cohort (%)
Pr
evious aortic
surgery (%)
Length of aortic coverage r
eported
Patent collateral vascular beds Intra-operative hypotension Operative time (min)
Acher , C. et al. 8 (16) Ye s 49.0 46.5 Ye s NR No NR Amabile, P . et al. 8 (16) Ye s 16.4 16.4 Ye s NR No NR Ar naoutakis, D. J. et al. 11 (16) Ye s 22.0 22.0 No NR No NR Banga, P . V . et al. 8 (16) Ye s 49.0 22.0 Ye s NR No 290 Bisdas, T . et al. 10 (16) Ye s 91.0 47.0 Ye s NR Ye s 272 Bobadilla, J. L. et al. 11 (16) Ye s 16.0 NR Ye s No Ye s NR Chiesa, R. et al. 12 (16) Ye s 12.6 12.6 Ye s Ye s Ye s NR Clough, R. E. et al. 11 (16) Ye s 32.0 NR No Ye s NR NR Desart, K. et al. 8 (16) Ye s 18.6 18.6 Ye s Ye s No NR Dias, N. V . et al. 10 (16) Ye s 76.0 56.9 No Ye s No 412 Drinkwater , S. L. et al. 9 (16) Ye s NR NR Ye s Ye s No 257 Guillou, M. et al. 13 (16) Ye s 75.0 30.0 No NR Ye s 221 Hanna, J. M. et al. 8 (16) Ye s 17.8 17.8 Ye s Ye s Ye s NR Harrison, S. C. et al. 8 (16) Ye s 100.0 20.0 Ye s No Ye s 557 Hnath, J. C. et al. 18 (24) Ye s 33.9 33.9 Ye s No Ye s NR Jayia, P . et al. 6 (16) Ye s 100.0 21.0 No No Ye s NR Jonker , F . H. W . et al. 7 (16) Ye s 100.0 12.6 Ye s No Ye s NR Kamada, T . et al. 6 (16) Ye s 7.8 7.8 No Ye s No NR Kasprzak, P . M. et al. 18 (24) Ye s 100.0 32.5 No No Ye s NR Kato, M. et al. 9 (16) Ye s 50.0 22.0 Ye s Ye s Ye s 200 Keith Jr , C. J. et al. 10 (16) Ye s 70.0 NR Ye s Ye s Ye s NR Khoynezhad, A. et al. 8 (16) Ye s 45.8 45.8 Ye s Ye s Ye s NR
8
Table 3.
Risk of bias analysis for the included studies. (continued)
Authors
MINORs scor
e
(max scor
e)
Risk factors reported High risk SCI cohort (%)
Pr
evious aortic
surgery (%)
Length of aortic coverage r
eported
Patent collateral vascular beds Intra-operative hypotension Operative time (min)
Kitagawa, A. et al. 10 (16) Ye s 33.3 33.3 No No Ye s NR Knowles, M. et al. 7 (16) Ye s 32.3 32.3 Ye s No No NR Lee, M. et al. 9 (16) Ye s 31.0 31.0 Ye s Ye s No NR Maldonado, T . S. et al. 9 (16) Ye s 27.1 27.1 Ye s No No NR Mastr or oberto, P . et al. 10 (16) Ye s 30.0 9.5 No No Ye s 115 Matsuda, H. et al. 8 (16) Ye s 40.0 40.0 Ye s Ye s Ye s NR Maur el, B. et al. 16 (24) Ye s 50.0 29.4 Ye s Ye s Ye s 182 Patel, H. J. et al. 9 (16) Ye s 22.0 17.8 Ye s Ye s Ye s NR Pif far etti, G. et al. 10 (16) Ye s 66.0 66.0 Ye s No No NR Pr eventza, O. et al. 7 (16) Ye s 23.7 13.3 Ye s No NR NR Rossi, S. H. et al. 15 (24) Ye s 36.2 36.2 Ye s Ye s Ye s NR Rylski, B. et al. 12 (16) No 33.0 NR No No No NR Schlösser , F . J. V . et al. 9 (16) Ye s 100.0 100.0 Ye s Ye s Ye s NR Shah, T . R. et al. 14 (24) Ye s 5.1 5.1 Ye s Ye s No NR Sobel, J. D. et al. 10 (16) Ye s 44.0 44.0 Ye s No Ye s 499 Tanaka, K. et al. 11 (16) Ye s 38.4 12.2 Ye s NR Ye s NR Ullery , B. W . et al. 10 (16) Ye s 28.8 28.8 No Ye s Ye s NR Y ingbin, J. et al. 6 (16) No 9.2 NR No No Ye s NR Zamor , K. C. et al. 12 (24) No 25.0 NR No No No NR Zeng, Q. et al. 8 (16) Ye s 100.0 NR Ye s No Ye s 157 Zipfel, B. et al. 12 (16) Ye s 55.7 11.3 Ye s No Ye s NR
abdominal repairs. In three studies (7.0 %) no spinal fluid drainage was used and in the remaining two (4.7 %) a preventive protocol on the use of a drain was not specified. The use of an ‘emergent’ drain (e.g. in case of symptoms peri-operatively) was not included in this review, as this is a therapeutic and not a preventive measure. As for the other modalities, avoidance of hypotension was used in 32 (74.4 %), hypothermia in 2 (4.7 %), staged procedures in 7 (16.3 %), prophylactic LSA revascularization in 29 (67.4 %), permissive endoleaks in 6 (14.0 %) and peri-operative monitoring in 5 (11.6 %) of the preventive protocols. Intra-thecal medication was not described in any of the included papers. Four studies (9.3 %) used only one preventive measure. In 25 (58.1 %) studies more than two preventive measures were used, in 12 (27.9 %) more than three. Data was subsequently pooled and sub-analysis for each of the different preventive measures was performed. Analysis was performed for both transient and per-manent SCI.
Quality of included studies
Overall the included studies had an average MINORS score of 10.0 (range 6 – 18). For non-comparative studies this was 9.0 (range 6 – 13) and for compara-tive studies this was 15.5 (range 12 – 18). The majority of included studies did clearly state the aim of the study and there was no frequent loss to follow up. However, consecutive patients were not always included and data was collected retrospectively in the majority of the included studies, which mainly resulted in lower MINORS scores. Table 3 shows the MINORS score per study.
spinal cord ischemia
Overall, transient SCI occurred in 5.7 % (450/7168, 95 % CI 4.5– 6.9 %) and permanent SCI in 2.2 % (232/7168, 95 % CI 1.6 – 2.8 %, Figure 2 and Table 4). The highest transient SCI estimate was 30.6 % (Dias 2015), the lowest estimate was 0.3 % (Lee 2013). Estimates for permanent SCI ranged from 0.3 % (Archer 2016 and Lee 2013) to 20.8 % (Dias 2015). There was no time trend over the last decades for the incidence of SCI.
The studies were then grouped by preventive measure and the overall incidences of both transient and permanent SCI per preventive measure used are shown in Table 4. Avoidance of hypotension resulted in a slightly lower permanent SCI rate 1.8 % (102/4216, 95 % CI 1.2–2.3 %) compared to the overall cohort. A very low SCI estimate (both transient and permanent) was found in the small subgroup of studies (2 studies, n = 248) using (mild) peri-operative hypothermia (transient SCI 0.8 % and permanent SCI 0.4 %). Interestingly, in the subgroup
us-8
Figur
e 2.
For
est plot showing the transient SCI (left) and permanent SCI (right) estimates for the included studies. For each study the esti
mate and 95
% CI is given
(second column). The absolute number of events and total number of patients ar
e shown in the thir
d column and the for
ing temporary permissive endoleak, there was a transient SCI estimate of 15.4 % with a permanent SCI estimate of 4.8 %. The remaining preventive measures (selective spinal fluid drain, avoidance of hypotension, staged procedures, selec-tive revascularization, monitoring or the use of > 2 prevenselec-tive measures) did not have a significant impact on transient and permanent SCI estimates. Notably, there was a large overlap of the used preventive measures since the majority of the studies employed multiple preventive measures, and marked heterogene-ity of the cohorts, therefore no indirect comparisons were made and the data presented is solely descriptive.
When the individual cohorts were divided by a-priori SCI risk, there was a trend towards increased SCI incidence for more ‘high risk’ cohorts. Interestingly, this trend was more evident for prophylactic, compared to selective spinal fluid drainage (Figure 3).
Table 4. Pooled analyses per preventive measure used. The references correspond with the
included study reference list, appendix 2.
Preventive measure - Pooled analysis Transient SCI estimate Permanent SCI estimate
Profylactic spinal fluid drain2,3,8,12,14,17,25,32,35 11.1 %
(76/644, 0.060 – 0.162) 3.7 %
(34/644, 0.014 – 0.059) Selective spinal fluid
drain4–7, 9–11, 13, 15, 18–24, 26–31, 33, 34, 36, 37, 41, 42 5.3 %
(360/6088, 0.040 – 0.066) 2.3 %
(194/6088, 0.016 – 0.030)
No spinal fluid drain1, 16, 40 5.8 %
(9/139, 0.019 – 0.097) 1.8 % (3/139, -0.004 – 0.040) Avoidance of hypotension1, 3, 4, 8, 10–14, 17–21, 23, 25–31, 33–38, 40–43 5.5 % (248/4216, 0.042 – 0.068) 1.8 % (102/4216, 0.012–0.023) Hypothermia42, 43 0.8 % (2/249, -0.003 – 0.018) 0.4 % (0/249, -0.004 – 0.011) Staged procedures3, 6, 10, 17, 27, 29, 31 7.1 % (60/837, 0.045 – 0.096) 3.2 % (28/837, 0.020 – 0.043) Selective LSA revascularization1–3, 6–8, 10, 11, 18, 19, 21–24, 26–31, 34–37, 39–43 5.2 % (344/5764, 0.039 – 0.066) 2.3 % (193/5764, 0.015 – 0.030) Permissive temporary endoleak3, 12, 14, 17, 31, 35 15.4 % (56/331, 0.095 – 0.214) 4.8 % (19/331, 0.025 – 0.071) Neuromonitoring3, 8, 26, 31, 37 11.6 % (53/662, 0.038 – 0.194) 4.7 % (25/662, 0.007 – 0.087) > 2 preventive measures3, 6, 8, 10–12, 14, 17–19, 21, 23, 26–31, 34–37, 41–43 5.2 % (211/3711, 0.038–0.067) 1.8 % (91/3711, 0.012–0.024) ≤ 2 preventive measures1, 2, 4, 5, 7, 9, 13, 15, 16, 20, 22, 24, 25, 32, 33, 38–40 6.2 % (239/3457, 0.044–0.081) 2.6 % (141/3457, 0.014–0.037) Overall 5.7 % (450/7168, 0.045 – 0.069) 2.2 % (232/7168, 0.016 – 0.028) Abbreviations: LSA, Left subclavian artery; SCI, Spinal cord ischemia.
8
discussion
Based on the available data no definitive recommendations can be made with regard to the optimal preventive strategies for SCI in endovascular thoraco-abdominal aortic repair. Current knowledge is mainly based on non-comparative cohorts, there are no randomized controlled trials evaluating any of the preven-tive measures for SCI, let alone multiple intervention strategies. Therefore, one must conclude that the currently employed (multi-modality) protocols used are extrapolated from those used routinely in open surgical repair and based on the theoretical models of SCI pathophysiology.
As shown by Table 2, the data available are highly heterogeneous and largely retrospectively obtained. In addition, the majority of the included studies had a mixed population of aneurysmal disease, dissections, PAU and in some studies traumatic injury, further complicating the assessment. Patient characteristics in terms of co-morbidities were similar for the included studies (Table 2).
With the current treatment protocols, low overall rates of SCI are achieved (permanent SCI estimate 2.2 % (232/7168, 0.016 – 0.028), Figure 2), which is comparable to earlier reports of SCI rates being estimated at 2 – 6 %.6 There is
however a large variation for the individual cohorts, with the highest reported transient and permanent SCI rates being 30.6 % and 20.8 % respectively. These incidences were reported in the study by Dias et. al.14. In a sub-analysis
per-formed by the authors, the only factors independently associated with SCI were Crawford type II TAAA and a higher contrast volume. The authors do state that Figure 3. Scatter plot showing the permanent SCI estimate (y-axis) versus the percentage of
the implementation of a more standardized SCI protocol led to a reduction in SCI rate, but a residual SCI rate of 13.2 % at discharge is still considerably high. The relatively ‘high risk’ population may have attributed to this. Also, in this study SCI was the primary outcome measure and rigorous post-operative protocols for the detection of SCI were implemented, possibly adding to the high incidence of SCI.
In open thoracic and thoraco-abdominal aneurysm repair the use of spinal drains has been well established. The use of a spinal fluid drain reduces the intra-thecal pressure and is thus believed to improve spinal cord perfusion pressure.15 During
endovascular repair the potential gain is arguably lower due to less hemody-namic disturbances peri-operatively. Given the invasive nature of spinal drain insertion and the potential associated complications, consensus amongst experts is that the routine use of spinal fluid drains is not mandated but should be used selectively in high risk patients.6, 16, 17 High risk patients generally include
patients with previous aortic surgery and/or expected long segment coverage of the aorta (> 200mm). Other reported risk factors include advanced age, renal insufficiency and emergency procedures. More recently, compromised collateral vascular beds (e.g. occluded/stenosed subclavian and hypogastric arteries) have been associated with an increased risk of SCI.7 There is however no generally
accepted uniform algorithm to determine when a patient is ‘high risk’. Since the routine use of spinal drains does seem to have slightly less favorable outcomes, especially in ‘high risk’ cohorts (Figure 3) and given the invasive nature of this preventive measure, it could be argued a selective drainage protocol should be used in these categories of patients.
The use of vasopressive agents and intra-venous fluid administration to increase the mean arterial pressure as a treatment modality in case of spinal cord isch-emia or paraplegia have been described and proved to be successful in selected cohorts.18, 19 The risk of developing spinal cord ischemia during a hypotensive
pe-riod has also been described. A peri-operative pepe-riod of hypotension (MAP < 70 mmHg) was found to be a significant predictor or SCI and a MAP of at least 90 mmHg post-operatively is advised in order to prevent SCI.18
The current data shows an overall SCI estimate for permanent SCI of 1.8 % (n = 4216, 95 % CI 1.2 – 2.3 %) for studies using avoidance of hypotension, which is lower compared to the whole cohort (2.2 %, 95 % CI 1.6 – 2.8 %, Table 4). The routine implementa-tion of this relatively easy and non-invasive measure therefore seems reasonable. Hypothermia was only used in two studies, including a total of 249 patients.20, 21
Both studies used a multi-modality (> 3) preventive protocol. In the study by Acher et. al. patients were operated on moderate systemic hypothermia (34°C).
8
In addition, selective spinal fluid drainage, avoidance of hypotension and selec-tive LSA revascularization were included in the study protocol. The group led by Bobadilla also used a multi modality ‘proactive’ preventive protocol with moder-ate hypothermia (< 35°C), prophylactic spinal fluid drainage, avoidance of hy-potension and selective LSA revascularization. No permanent SCI was observed in either cohort (permanent SCI estimate 0.3 % and 0.5 %, respectively) and only two cases of transient SCI (one in each study) were witnessed. Interestingly, patients in the study by Acher et. al. had an average length of aortic coverage of 250mm and 46.5 % had undergone previous aortic surgery, making the very low SCI rate even more impressive. This would suggest that a multimodal approach including hypothermia had a significant effect in the prevention of the develop-ment of both transient and permanent SCI (Table 4). Therefore operating under moderate hypothermia may be considered beneficial. However, the sample size is small. Furthermore, several other preventive measures were used simultaneously, which makes is difficult to attribute the difference solely to the hypothermia. The concept of permissive or induced endoleak was first described in 2010 by Reilly and Chuter. The authors seemingly reversed symptoms of spinal cord isch-emia after endovascular repair of a type II TAAA by creating a temporary type Ib endoleak.22 Subsequently, the use of paraplegia preventing branches (PPBs), for
the creation of controlled type III endoleaks, has been described by Lioupis et al. in 2011.23 The current review showed that the use of permissive endoleak was
associated with a fairly high transient SCI estimate (Table 4), but no increased permanent SCI estimate. This seems counter-intuitive, as one would suggest that persistent perfusion of the aneurysm sac protect against SCI development. Six studies used this technique, including 331 patients.24–29 The majority of the
included patients were deemed at (very) high risk for the development of SCI, leading to possible bias. Patients treated in these studies were all deemed to be at high risk for developing SCI, although specific risk factors were not mentioned in either study.
With regard to staged procedures, evidence shows that in open thoracic pro-cedures a previous abdominal repair generates an increased risk for spinal cord ischemia if a supplementary thoracic repair is carried out.17 The
pathophyiologi-cal mechanism is most likely multifactorial. Recent clinipathophyiologi-cal studies show that the perfusion of the spinal cord is regulated by an extensive collateral network. The collateral network consist of paraspinous arterial collaterals, segmental spinal arteries, and intercostal and lumbar arteries.30 Taking the previous considerations
into account staged interventions may show a lower rate of SCI, potentially through provoked expansion of the collateral network or the formation of new vessel leading to sufficient perfusion of the spinal cord.31, 32
current review failed to show a beneficial effect for staged endovascular repair of extensive (thoraco)abdominal aneurysms (Table 4). Recently, sequential coil embolization of intercostal arteries has been suggested as a method to protect the spinal cord after TEVAR through stimulation of collateral flow of the spinal cord. No results of this technique in men have been published.33
There are numerous publications on collateral re-vascularization and SCI preven-tion, largely focused on LSA revascularization (since endovascular repair does not allow for re-implantation of intercostal arteries). A systematic review and meta-analysis by Rizvi et al. showed that coverage of the LSA without revascularization was associated with a trend towards an increased risk of paraplegia (odds ratio [OR] = 2.69, [CI] 0.75–9.68) when compared with patients who underwent LSA revascularization.34
A review by Weigang et al. in 2011 concluded that patients should undergo prophylactic LSA transposition or carotid-LSA bypass if coverage of the LSA origin is anticipated, to prevent neurological complications including paraplegia.35 The current data does not corroborate these statements, since
there is no difference in either transient or permanent SCI with or without selec-tive LSA revascularization. A possible association between LSA occlusion and SCI was not part of this review.
Finally, if the pathophysiological mechanism occurring in SCI is multi-factorial, using multiple preventive measures in unison could result in lower SCI rates. The presented meta-analysis however did not show a significant difference in SCI rates if a SCI preventive protocol including multiple preventive strategies was used.
The current meta-analysis has several caveats and possible sources of bias. First, the data is very heterogeneous. Given the heterogeneity of the data, no direct or indirect comparisons between the different preventive measures could be made. Nonetheless, it was opted to pool these data for a number of reasons; first to give insight in overall SCI estimates, second to emphasize that current treat-ment protocols are not always clear and vary widely, and third because given the available data this was the only viable option. The majority of the included data was collected retrospectively. Not all studies were conducted with SCI as the primary outcome measure and there is a large variety in follow up protocols and post-operative examinations. A number of studies had strict post-operative protocols, including serial examinations by independent neurologists, which will undoubtedly lead to a higher incidence of (at least transient) SCI. Also, the length of aortic coverage was not included in the analysis. This proved to be impossible based on the available data, where the length of coverage was frequently not reported or reported in such a way that a comparison could not be made.
8
In summary, low transient and especially permanent SCI rates are achieved dur-ing endovascular thoracic and thoraco-abdominal aortic repair. These SCI rates are achieved using multiple preventive measures, often used in unison. It seems reasonable to employ several preventive measures, including selective spinal fluid drainage, avoidance of hypotension and mild hypothermia, However, no definitive recommendation on spinal cord ischemia preventive measures can be made based upon the current literature. To acquire sufficient and high quality data a large international multi-center registry should be instated.
conclusion
Low overall transient and permanent SCI rates are achieved during endovascular thoracic and thoraco-abdominal aortic repair. However, permanent SCI rates up to 21 % are reported in high risk cohorts. The current SCI prevention protocols vary widely. Based on the presented data the employment of selective spinal fluid drainage in high risk patients, avoidance of hypotension and mild hypother-mia seems justified. Further high quality data is needed to establish a definitive preventive strategy.
references
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5. DeSart K, Scali ST, Feezor RJ, Hong M, Hess PJ, Jr., Beaver TM, et al. Fate of patients with spinal cord ischemia complicating thoracic endovascular aortic repair. J Vasc Surg. 2013; 58(3): 635-42 e2.
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7. Eagleton MJ, Shah S, Petkosevek D, Mastracci TM, Greenberg RK. Hypogastric and subclavian artery patency affects onset and recovery of spinal cord ischemia associ-ated with aortic endografting. J Vasc Surg. 2014; 59(1): 89-94.
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9. Etz CD, Weigang E, Hartert M, Lonn L, Mestres CA, Di Bartolomeo R, et al. Con-temporary spinal cord protection during thoracic and thoracoabdominal aortic surgery and endovascular aortic repair: a position paper of the vascular domain of the European Association for Cardio-Thoracic Surgerydagger. Eur J Cardiothorac Surg. 2015; 47(6): 943-57.
10. Khoynezhad A, Donayre CE, Bui H, Kopchok GE, Walot I, White RA. Risk factors of neurologic deficit after thoracic aortic endografting. Ann Thorac Surg. 2007; 83(2): S882-9; discussion S90-2.
11. Amabile P, Grisoli D, Giorgi R, Bartoli JM, Piquet P. Incidence and determinants of spinal cord ischaemia in stent-graft repair of the thoracic aorta. Eur J Vasc Endovasc Surg. 2008; 35(4): 455-61.
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12. Schlosser FJ, Verhagen HJ, Lin PH, Verhoeven EL, van Herwaarden JA, Moll FL, et al. TEVAR following prior abdominal aortic aneurysm surgery: increased risk of neurological deficit. J Vasc Surg. 2009; 49(2): 308-14; discussion 14.
13. Slim K, Nini E, Forestier D, Kwiatkowski F, Panis Y, Chipponi J. Methodological index for non-randomized studies (minors): development and validation of a new instrument. ANZ J Surg. 2003; 73(9): 712-6.
14. Dias NV, Sonesson B, Kristmundsson T, Holm H, Resch T. Short-term outcome of spi-nal cord ischemia after endovascular repair of thoracoabdomispi-nal aortic aneurysms. Eur J Vasc Endovasc Surg. 2015; 49(4): 403-9.
15. Acher CW, Wynn MM, Hoch JR, Popic P, Archibald J, Turnipseed WD. Combined use of cerebral spinal fluid drainage and naloxone reduces the risk of paraplegia in thoracoabdominal aneurysm repair. J Vasc Surg. 1994; 19(2): 236-46; discussion 47-8.
16. Erbel R, Aboyans V, Boileau C, Bossone E, Di Bartolomeo R, Eggebrecht H, et al. 2014 ESC guidelines on the diagnosis and treatment of aortic diseases. European Heart Journal. 2014; 35(41): 2873-926.
17. Hiratzka LF, Bakris GL, Beckman JA, Bersin RM, Carr VF, Casey DE, Jr., et al. 2010 ACCF/AHA/AATS/ACR/ASA/SCA/SCAI/SIR/STS/SVM guidelines for the diagnosis and management of patients with Thoracic Aortic Disease: a report of the Ameri-can College of Cardiology Foundation/AmeriAmeri-can Heart Association Task Force on Practice Guidelines, American Association for Thoracic Surgery, American College of Radiology, American Stroke Association, Society of Cardiovascular Anesthesi-ologists, Society for Cardiovascular Angiography and Interventions, Society of Interventional Radiology, Society of Thoracic Surgeons, and Society for Vascular Medicine. Circulation. 2010; 121(13): e266-369.
18. Chiesa R, Melissano G, Marrocco-Trischitta MM, Civilini E, Setacci F. Spinal cord ischemia after elective stent-graft repair of the thoracic aorta. J Vasc Surg. 2005; 42(1): 11-7.
19. Ullery BW, Cheung AT, Fairman RM, Jackson BM, Woo EY, Bavaria J, et al. Risk factors, outcomes, and clinical manifestations of spinal cord ischemia following thoracic endovascular aortic repair. J Vasc Surg. 2011; 54(3): 677-84.
20. Bobadilla JL, Wynn M, Tefera G, Acher CW. Low incidence of paraplegia after tho-racic endovascular aneurysm repair with proactive spinal cord protective protocols. J Vasc Surg. 2013; 57(6): 1537-42.
21. Acher C, Acher CW, Marks E, Wynn M. Intraoperative neuroprotective interven-tions prevent spinal cord ischemia and injury in thoracic endovascular aortic repair. J Vasc Surg. 2016; 63(6): 1458-65.
22. Reilly LM, Chuter TA. Reversal of fortune: induced endoleak to resolve neurological deficit after endovascular repair of thoracoabdominal aortic aneurysm. J Endovasc Ther. 2010; 17(1): 21-9.
23. Lioupis C, Corriveau MM, Mackenzie KS, Obrand DI, Steinmetz OK, Ivancev K, et al. Paraplegia prevention branches: a new adjunct for preventing or treating spinal cord injury after endovascular repair of thoracoabdominal aneurysms. J Vasc Surg. 2011; 54(1): 252-7.
24. Banga PV, Oderich GS, Reis de Souza L, Hofer J, Cazares Gonzalez ML, Pulido JN, et al. Neuromonitoring, Cerebrospinal Fluid Drainage, and Selective Use of Iliofemoral Conduits to Minimize Risk of Spinal Cord Injury During Complex Endovascular Aortic Repair. J Endovasc Ther. 2016; 23(1): 139-49.
25. Harrison SC, Agu O, Harris PL, Ivancev K. Elective sac perfusion to reduce the risk of neurologic events following endovascular repair of thoracoabdominal aneurysms. J Vasc Surg. 2012; 55(4): 1202-5.
26. Jayia P, Constantinou J, Hamilton H, Ivancev K. Temporary Perfusion Branches to Decrease Spinal Cord Ischemia in the Endovascular Treatment of Thoraco-Abdom-inal Aortic Aneurysms: Based on a Presentation at the 2013 VEITH Symposium, November 19-23, 2013 (New York, NY, USA). Aorta (Stamford, Conn). 2015; 3(2): 56-60.
27. Kasprzak PM, Gallis K, Cucuruz B, Pfister K, Janotta M, Kopp R. Editor’s Choice - Temporary Aneurysm Sac Perfusion as an Adjunct for Prevention of Spinal Cord Ischemia After Branched Endovascular Repair of Thoracoabdominal Aneurysms. Eur J Vasc Endovasc Surg. 2014; 48(3): 258-65.
28. Rossi SH, Patel A, Saha P, Gwozdz A, Salter R, Gkoutzios P, et al. Neuroprotec-tive Strategies Can Prevent Permanent Paraplegia in the Majority of Patients Who Develop Spinal Cord Ischaemia After Endovascular Repair of Thoracoabdominal Aortic Aneurysms. Eur J Vasc Endovasc Surg. 2015; 50(5): 599-607.
29. Sobel JD, Vartanian SM, Gasper WJ, Hiramoto JS, Chuter TA, Reilly LM. Lower extremity weakness after endovascular aneurysm repair with multibranched thora-coabdominal stent grafts. J Vasc Surg. 2015; 61(3): 623-8.
30. Etz CD, Kari FA, Mueller CS, Silovitz D, Brenner RM, Lin HM, et al. The collateral network concept: a reassessment of the anatomy of spinal cord perfusion. J Thorac Cardiovasc Surg. 2011; 141(4): 1020-8.
31. Etz CD, Zoli S, Mueller CS, Bodian CA, Di Luozzo G, Lazala R, et al. Staged repair significantly reduces paraplegia rate after extensive thoracoabdominal aortic aneu-rysm repair. J Thorac Cardiovasc Surg. 2010; 139(6): 1464-72.
32. Bischoff MS, Brenner RM, Scheumann J, Zoli S, Di Luozzo G, Etz CD, et al. Staged approach for spinal cord protection in hybrid thoracoabdominal aortic aneurysm repair. Ann Cardiothorac Surg. 2012; 1(3): 325-8.
33. Geisbusch S, Stefanovic A, Koruth JS, Lin HM, Morgello S, Weisz DJ, et al. Endovas-cular coil embolization of segmental arteries prevents paraplegia after subsequent thoracoabdominal aneurysm repair: an experimental model. J Thorac Cardiovasc Surg. 2014; 147(1): 220-6.
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34. Rizvi AZ, Sullivan TM. Incidence, prevention, and management in spinal cord pro-tection during TEVAR. J Vasc Surg. 2010; 52(4 Suppl): 86S-90S.
35. Weigang E, Parker JA, Czerny M, Lonn L, Bonser RS, Carrel TP, et al. Should inten-tional endovascular stent-graft coverage of the left subclavian artery be preceded by prophylactic revascularisation? Eur J Cardiothorac Surg. 2011; 40(4): 858-68.
aPPendix
appendix 1
SearchThe following searches were used: 1. Pubmed: “(Aortic OR Aorta OR Aorta [Mesh]) AND (Endovascular OR TEVAR OR EVAR OR “endovascular procedures”[MeSH]) AND (“spinal cord ischemia” OR “Spinal cord”[Mesh] OR “spinal cord ischemia”[Mesh] OR paraplegia OR paraplegia[MeSH] OR paralysis OR paralysis [MeSH])”, 2. Embase: “(Aortic OR Aorta OR ‘Aorta’/exp OR ‘Aorta sinus’/exp) AND (Endovascular OR TEVAR OR EVAR OR ‘Endovascular surgery’/exp OR ‘Angioplasty’/exp OR ‘Atherectomy’/exp OR ‘Angioscopy’/exp OR ‘Catheter-ization’/exp OR ‘Percutaneous cardiovascular procedure’/exp) AND (‘spinal cord ischemia’ OR ‘Spinal cord’/exp OR ‘spinal cord ischemia’/exp OR ‘extrapyramidal system’/exp OR ‘gray matter’/exp OR ‘pyramidal tract’/exp OR ‘spinothalamic tract’/exp OR ‘white matter’/exp OR ‘posterior horn cell’/exp OR ‘anterior horn cell’/exp OR paraplegia OR ‘paralysis’/exp)” and 3. Cochrane Library: “Spinal cord ischemia” AND “Aortic Aneurysm”.
8
appendix 2
Reference list of included articles.
1. Acher C, Acher CW, Marks E, Wynn M. Intraoperative neuroprotective interven-tions prevent spinal cord ischemia and injury in thoracic endovascular aortic repair. J Vasc Surg. 2016; 63(6): 1458-65.
2. Amabile P, Grisoli D, Giorgi R, Bartoli JM, Piquet P. Incidence and determinants of spinal cord ischaemia in stent-graft repair of the thoracic aorta. Eur J Vasc Endovasc Surg. 2008; 35(4): 455-61.
3. Arnaoutakis DJ, Arnaoutakis GJ, Beaulieu RJ, Abularrage CJ, Lum YW, Black JH, 3rd. Results of adjunctive spinal drainage and/or left subclavian artery bypass in thoracic endovascular aortic repair. Ann Vasc Surg. 2014; 28(1): 65-73.
4. Banga PV, Oderich GS, Reis de Souza L, Hofer J, Cazares Gonzalez ML, Pulido JN, et al. Neuromonitoring, Cerebrospinal Fluid Drainage, and Selective Use of Iliofemoral Conduits to Minimize Risk of Spinal Cord Injury During Complex Endovascular Aortic Repair. J Endovasc Ther. 2016; 23(1): 139-49.
5. Bisdas T, Panuccio G, Sugimoto M, Torsello G, Austermann M. Risk factors for spinal cord ischemia after endovascular repair of thoracoabdominal aortic aneurysms. J Vasc Surg. 2015; 61(6): 1408-16.
6. Bobadilla JL, Wynn M, Tefera G, Acher CW. Low incidence of paraplegia after tho-racic endovascular aneurysm repair with proactive spinal cord protective protocols. J Vasc Surg. 2013; 57(6): 1537-42.
7. Chiesa R, Melissano G, Marrocco-Trischitta MM, Civilini E, Setacci F. Spinal cord ischemia after elective stent-graft repair of the thoracic aorta. J Vasc Surg. 2005; 42(1): 11-7.
8. Clough RE, Patel AS, Lyons OT, Bell RE, Zayed HA, Carrell TW, et al. Pathology specific early outcome after thoracic endovascular aortic repair. Eur J Vasc Endovasc Surg. 2014; 48(3): 268-75.
9. DeSart K, Scali ST, Feezor RJ, Hong M, Hess PJ, Jr., Beaver TM, et al. Fate of patients with spinal cord ischemia complicating thoracic endovascular aortic repair. J Vasc Surg. 2013; 58(3): 635-42 e2.
10. Dias NV, Sonesson B, Kristmundsson T, Holm H, Resch T. Short-term outcome of spi-nal cord ischemia after endovascular repair of thoracoabdomispi-nal aortic aneurysms. Eur J Vasc Endovasc Surg. 2015; 49(4): 403-9.
11. Drinkwater SL, Goebells A, Haydar A, Bourke P, Brown L, Hamady M, et al. The incidence of spinal cord ischaemia following thoracic and thoracoabdominal aortic endovascular intervention. Eur J Vasc Endovasc Surg. 2010; 40(6): 729-35.
12. Guillou M, Bianchini A, Sobocinski J, Maurel B, D’Elia P, Tyrrell M, et al. Endovascu-lar treatment of thoracoabdominal aortic aneurysms. Journal of VascuEndovascu-lar Surgery. 2012; 56(1): 65-73.
13. Hanna JM, Andersen ND, Aziz H, Shah AA, McCann RL, Hughes GC. Results with selective preoperative lumbar drain placement for thoracic endovascular aortic repair. Ann Thorac Surg. 2013; 95(6): 1968-74; discussion 74-5.
14. Harrison SC, Agu O, Harris PL, Ivancev K. Elective sac perfusion to reduce the risk of neurologic events following endovascular repair of thoracoabdominal aneurysms. J Vasc Surg. 2012; 55(4): 1202-5.
15. Hnath JC, Mehta M, Taggert JB, Sternbach Y, Roddy SP, Kreienberg PB, et al. Strategies to improve spinal cord ischemia in endovascular thoracic aortic repair: Outcomes of a prospective cerebrospinal fluid drainage protocol. J Vasc Surg. 2008; 48(4): 836-40.
16. Jayia P, Constantinou J, Hamilton H, Ivancev K. Temporary Perfusion Branches to Decrease Spinal Cord Ischemia in the Endovascular Treatment of Thoraco-Abdom-inal Aortic Aneurysms: Based on a Presentation at the 2013 VEITH Symposium, November 19-23, 2013 (New York, NY, USA). Aorta (Stamford, Conn). 2015; 3(2): 56-60.
17. Jonker FH, Verhagen HJ, Lin PH, Heijmen RH, Trimarchi S, Lee WA, et al. Outcomes of endovascular repair of ruptured descending thoracic aortic aneurysms. Circula-tion. 2010; 121(25): 2718-23.
18. Kamada T, Yoshioka K, Tanaka R, Makita S, Abiko A, Mukaida M, et al. Strategy for thoracic endovascular aortic repair based on collateral circulation to the artery of Adamkiewicz. Surg Today. 2015.
19. Kasprzak PM, Gallis K, Cucuruz B, Pfister K, Janotta M, Kopp R. Editor’s choice— Temporary aneurysm sac perfusion as an adjunct for prevention of spinal cord ischemia after branched endovascular repair of thoracoabdominal aneurysms. Eur J Vasc Endovasc Surg. 2014; 48(3): 258-65.
20. Kato M, Motoki M, Isaji T, Suzuki T, Kawai Y, Ohkubo N. Spinal cord injury after endovascular treatment for thoracoabdominal aneurysm or dissection. Eur J Car-diothorac Surg. 2015; 48(4): 571-7.
21. Keith Jr CJ, Passman MA, Carignan MJ, Parmar GM, Nagre SB, Patterson MA, et al. Protocol implementation of selective postoperative lumbar spinal drainage after thoracic aortic endograft. Journal of Vascular Surgery. 2012; 55(1): 1-8.
22. Khoynezhad A, Donayre CE, Bui H, Kopchok GE, Walot I, White RA. Risk factors of neurologic deficit after thoracic aortic endografting. Ann Thorac Surg. 2007; 83(2): S882-9; discussion S90-2.
23. Kitagawa A, Greenberg RK, Eagleton MJ, Mastracci TM, Roselli EE. Fenestrated and branched endovascular aortic repair for chronic type B aortic dissection with thoracoabdominal aneurysms. J Vasc Surg. 2013; 58(3): 625-34.
8
24. Knowles M, Murphy EH, Dimaio JM, Modrall JG, Timaran CH, Jessen ME, et al. The effects of operative indication and urgency of intervention on patient outcomes after thoracic aortic endografting. J Vasc Surg. 2011; 53(4): 926-34.
25. Lee M, Lee do Y, Kim MD, Won JY, Yune YN, Lee TY, et al. Selective coverage of the left subclavian artery without revascularization in patients with bilateral patent vertebrobasilar junctions during thoracic endovascular aortic repair. J Vasc Surg. 2013; 57(5): 1311-6.
26. Maldonado TS, Dexter D, Rockman CB, Veith FJ, Garg K, Arko F, et al. Left subcla-vian artery coverage during thoracic endovascular aortic aneurysm repair does not mandate revascularization. J Vasc Surg. 2013; 57(1): 116-24.
27. Mastroroberto P, Ciranni S, Indolfi C. Extensive endovascular repair of thoracic aorta: observational analysis of the results and effects on spinal cord perfusion. J Cardiovasc Surg (Torino). 2013; 54(4): 523-30.
28. Matsuda H, Ogino H, Fukuda T, Iritani O, Sato S, Iba Y, et al. Multidisciplinary approach to prevent spinal cord ischemia after thoracic endovascular aneurysm repair for distal descending aorta. Ann Thorac Surg. 2010; 90(2): 561-5.
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