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M i c r o s u r g e r y 
f o r 
C e r e b r a l 
A r t e r i o v e n o u s 
M a l f o r m a t i o n s 
postoperative outcomes & 
predictors of complications 
in 264 cases 
Theofanis T, Chalouhi N, Dalyai R, Starke RM, 
Jabbour P, Rosenwasser RH, Tjoumakaris T 
Neurosurg Focus 37 (3):E10, 2014
AVM 
Vascular lesions composed of tortuous arteries and veins 
without intervening capillaries. 
• Found in approximately 0.1% of the US population 
• Responsible for approximately 2% of all hemorrhagic strokes, 
make up a particularly high percentage of hemorrhagic strokes 
in patients < 40 years 
• Annual risk of ICH: 1% - 25% 
• Due to the high risk of rupture in select AVM patients, 
intervention is an appropriate option 
AVM resection 
• was associated with significant morbidity and mortality. 
Microsurgical excision 
• Complete cure/ elimination of AVMs is more attainable over the 
past decades 
• Option in select patients due to the lack of a latency period for 
hemorrhage / low risk of future recurrence
Lancet 2014; 383: 614–21 
Microsurgical outcomes are arguably one of 
the biggest aspects lacking from the ARUBA trial 
5 patients in the treatment arm received open surgery 
[embolisation + surgery (12 px) | embolisation + radio + surgery (1 px) ] 
Stopped prematurely after a safety analysis
Objective 
• to assess the safety and efficacy of microsurgical 
resection of AVMs 
• determine predictors of complications
Methods 
Prospectively maintained database for patients with AVMs, underwent microsurgical resection, 
at Jefferson Hospital of Neuroscience, between 1994 - 2010 
264 patients [from 774 patients with cerebral AVMs] 
Surgical Techniques : permanently eliminating AVM, preserving full neurological function, 
reversing deficits 
Selecting the best therapy by 
doctors trained in 3 field 
Treatment decision: doctor + 
px 
Embolization 
Review 
Medical charts, imaging studies, and follow-up notes, SM grade, initial hemorrhage, clinical 
presentation, treatment modalities, clinical outcomes, obliteration rates
Outcome 
Statistical analysis 
unpaired t-tests, Chi-square, Fisher’s exact tests, ANOVA, univariate & multivariate analysis 
| p ≤ 0.05 | Stata 10.0 
Assessment of AVM 
obliteration: intraoperative 
angiography 
Neurological examination 
pre- & post-surgery 
modified Rankin Scale at 
arrival & discharge
Results 
Unruptured AVM SM grade 
I : 9% II : 45.8% III : 34.8% IV : 9% V : 1.4% 
Unruptured AVM size 
<3 cm : 78 3-6 cm : 62 > 6 cm : 4
Modalities 
Prior Embolization 
102 patients (38.6%) 
6 
session 
1 px 
3 
session 
10 px 
5 
session 
1 px 
2 
session 
19 px 
4 
session 
4 px 
1 
session 
67 px 
Prior Gamma 
Knife Procedure 
16 px (6%) 
1- 
stage 
12 px 
2- 
stage 
4 px 
Combination all modalities 
10 px 
Microsurgery 
alone 
Rupture 
7 patients 
Rupture 
2 patients
3.4% Post-op seizure (9) 
3% Post-op VP shunt (8) 
2.7% Death | At arrival: GCS ≤ 8, ruptur 
1.9% Permanent neurological deficits 
-Hemiparesis (2) 
-Hemiplegia (1) 
-Aphasia (1) 
-Vegetative state (1) 
1.9% Post-op infection (5) 
264 patients 
Microsurgery 
100% Complete AVM obliteration 
0% Post op hemorrhage 
86.4% Favorable outcome (mRS 0-2) 
92.4% Clinically unchanged 
6.9% Minor neurological deficits (10) 
3.5% Post-op seizure (5) 
1.4% Post-op VP shunt (2) 
0.69% Died (1) 
0.69% Permanent neurological deficit (1) 
0.69% Post-op infection (1) 
144 patients 
Unruptured 
AVMs 
AVMs of SM 
Grade III/higher 
accounted for 
the majority of 
the compli-cations
Embolization (-) Embolization (+) 
Complication 5.7% 9.4% 
Unruptured Hemorrhage 
mRS at discharge 0.074 1.22
Discussion 
Historically, surgery is reserved for hemorrhage, 
intractable epilepsy, progressive worsening 
Heros & Tu, 1985 | 
Rates of surgical Morbidity Mortality 
Unruptured (49) 14.2% 0% 
Rupture (54) 16.6% 1.6% 
Present study | 
data on a large single-center 
series of patients : 
2.7% death & 1.9% permanent 
neurological def. 
Study: Dismal natural history of untreated AVM 
• The possibility of AVM rupture is one that 
should receive great weight in counseling 
patients on the decision of if, how, and 
when is best to treat the AVM 
• AVM detection prior to rupture remains a 
challenge 
• Possible direction of future research is to 
elucidate which patients may be identified 
as candidates to screen for a cerebral AVM. 
All deaths were in 
patients who 
presented with 
hemorrhage and 
underwent urgent 
surgery.
Unrupture AVM 
Lawton et al, 2005 
• 224 px AVM microsurgery 
• Outcome: mRS 
• Hemorrhagic presentation : 54% 
 improved after procedure 
• Unruptured AVMs: 
– Normal/nearly normal 
neurological function at 
presentation 
– Susceptible to worsening (slight) 
• 6.7% px died 
• Hemorrhagic brain injury and its 
secondary effects (pre-procedure) 
may mask the surgical morbidity. 
• Sensitive measures of clinical 
outcomes (mRS) are more likely 
to reveal slight changes in 
patients who initially were 
essentially without symptoms. 
• Counseling patients : important 
to note that even subtle 
postoperative deficits can be 
easily detected 
Operative intervention in patients with unruptured AVMs should be seriously 
considered at high-volume experienced centers . 
The patients who can benefit the most : 
- Good candidates for surgery 
- Lesions with characteristics & angioarchitecture high risk for rupture
Preoperative Embolization 
• Safely decrease the 
size of AVMs 
• Decrease the apparent 
risk of rupture in high-risk 
lesions 
• Eliminating deep 
feeding vessels 
• Operative blood loss 
can be greatly 
minimized 
Previous studies: 
highlight favorable 
clinical outcomes of 
multi-modality 
therapy for carefully 
selected patients
Nataraj et al 
265 px 
Rupture + Unrupture 
GOS 
(favorable/ 
score 4-5) 
Embolization  
microsurgical 
resection 
86% 
Microsurgical 
resection alone 
96.5% 
Presurgical embolization 
• Marker of patients with more 
complicated AVM 
angioarchitecture / high-risk 
for surgery 
• Potentially risky: 
– possibility of decreasing the 
flow too much in one area  
increased flow in other areas of 
the nidus / cerebral vasculature 
– diminishing venous outflow 
from embolization could cause 
AVM rupture
AVM size 
Stüer et al: 
• Small- and medium-sized AVMs : dynamic autoregulatory function seems 
to be intact in the surrounding cerebrovascular bed perioperatively. 
• Larger AVMs : more likely to have more draining veins & risk for 
postoperative breakthrough complications. 
• Emphasizes the importance of AVM size for 
stratification of surgical risk 
AVM size: strong independent 
predictor of surgical 
complications 
• More data on microsurgery treatment in a 
larger group of cases with high SM grade 
To elucidate specific 
components of the SM grading 
scale that can predict 
favorable operative outcomes 
in high-grade lesions
Microsurgery & ARUBA Trial 
The majority of patients in the ARUBA trial treatment arm received noninvasive and non-neurosurgical 
treatments 
Russin and Spetzler: it remains difficult to resolve why only 5 patients received resection 
alone when 76 patients in the treatment arm had Grade I or II AVMs. 
Present data are encouraging. With modern-day techniques & approaches, microsurgery 
can be undertaken with extremely low complication rates and provide excellent outcomes 
for patients 
A trial comparing microsurgery and medical management is necessary to begin exploring the 
unanswered questions and clinical discrepancies raised by the ARUBA trial
Limitations 
• Retrospective data analysis 
• Single-center study 
• Recall bias
Conclusion 
• Microsurgical resection of AVMs is highly efficient 
and can be undertaken with low rates of 
morbidity at high-volume neurovascular centers. 
• Unruptured and larger AVMs were associated 
with higher complication rates
END. 
THANK YOU

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Microsurgery for Cerebral AVM Outcomes

  • 1. M i c r o s u r g e r y f o r C e r e b r a l A r t e r i o v e n o u s M a l f o r m a t i o n s postoperative outcomes & predictors of complications in 264 cases Theofanis T, Chalouhi N, Dalyai R, Starke RM, Jabbour P, Rosenwasser RH, Tjoumakaris T Neurosurg Focus 37 (3):E10, 2014
  • 2. AVM Vascular lesions composed of tortuous arteries and veins without intervening capillaries. • Found in approximately 0.1% of the US population • Responsible for approximately 2% of all hemorrhagic strokes, make up a particularly high percentage of hemorrhagic strokes in patients < 40 years • Annual risk of ICH: 1% - 25% • Due to the high risk of rupture in select AVM patients, intervention is an appropriate option AVM resection • was associated with significant morbidity and mortality. Microsurgical excision • Complete cure/ elimination of AVMs is more attainable over the past decades • Option in select patients due to the lack of a latency period for hemorrhage / low risk of future recurrence
  • 3. Lancet 2014; 383: 614–21 Microsurgical outcomes are arguably one of the biggest aspects lacking from the ARUBA trial 5 patients in the treatment arm received open surgery [embolisation + surgery (12 px) | embolisation + radio + surgery (1 px) ] Stopped prematurely after a safety analysis
  • 4. Objective • to assess the safety and efficacy of microsurgical resection of AVMs • determine predictors of complications
  • 5. Methods Prospectively maintained database for patients with AVMs, underwent microsurgical resection, at Jefferson Hospital of Neuroscience, between 1994 - 2010 264 patients [from 774 patients with cerebral AVMs] Surgical Techniques : permanently eliminating AVM, preserving full neurological function, reversing deficits Selecting the best therapy by doctors trained in 3 field Treatment decision: doctor + px Embolization Review Medical charts, imaging studies, and follow-up notes, SM grade, initial hemorrhage, clinical presentation, treatment modalities, clinical outcomes, obliteration rates
  • 6. Outcome Statistical analysis unpaired t-tests, Chi-square, Fisher’s exact tests, ANOVA, univariate & multivariate analysis | p ≤ 0.05 | Stata 10.0 Assessment of AVM obliteration: intraoperative angiography Neurological examination pre- & post-surgery modified Rankin Scale at arrival & discharge
  • 7. Results Unruptured AVM SM grade I : 9% II : 45.8% III : 34.8% IV : 9% V : 1.4% Unruptured AVM size <3 cm : 78 3-6 cm : 62 > 6 cm : 4
  • 8. Modalities Prior Embolization 102 patients (38.6%) 6 session 1 px 3 session 10 px 5 session 1 px 2 session 19 px 4 session 4 px 1 session 67 px Prior Gamma Knife Procedure 16 px (6%) 1- stage 12 px 2- stage 4 px Combination all modalities 10 px Microsurgery alone Rupture 7 patients Rupture 2 patients
  • 9. 3.4% Post-op seizure (9) 3% Post-op VP shunt (8) 2.7% Death | At arrival: GCS ≤ 8, ruptur 1.9% Permanent neurological deficits -Hemiparesis (2) -Hemiplegia (1) -Aphasia (1) -Vegetative state (1) 1.9% Post-op infection (5) 264 patients Microsurgery 100% Complete AVM obliteration 0% Post op hemorrhage 86.4% Favorable outcome (mRS 0-2) 92.4% Clinically unchanged 6.9% Minor neurological deficits (10) 3.5% Post-op seizure (5) 1.4% Post-op VP shunt (2) 0.69% Died (1) 0.69% Permanent neurological deficit (1) 0.69% Post-op infection (1) 144 patients Unruptured AVMs AVMs of SM Grade III/higher accounted for the majority of the compli-cations
  • 10. Embolization (-) Embolization (+) Complication 5.7% 9.4% Unruptured Hemorrhage mRS at discharge 0.074 1.22
  • 11. Discussion Historically, surgery is reserved for hemorrhage, intractable epilepsy, progressive worsening Heros & Tu, 1985 | Rates of surgical Morbidity Mortality Unruptured (49) 14.2% 0% Rupture (54) 16.6% 1.6% Present study | data on a large single-center series of patients : 2.7% death & 1.9% permanent neurological def. Study: Dismal natural history of untreated AVM • The possibility of AVM rupture is one that should receive great weight in counseling patients on the decision of if, how, and when is best to treat the AVM • AVM detection prior to rupture remains a challenge • Possible direction of future research is to elucidate which patients may be identified as candidates to screen for a cerebral AVM. All deaths were in patients who presented with hemorrhage and underwent urgent surgery.
  • 12. Unrupture AVM Lawton et al, 2005 • 224 px AVM microsurgery • Outcome: mRS • Hemorrhagic presentation : 54%  improved after procedure • Unruptured AVMs: – Normal/nearly normal neurological function at presentation – Susceptible to worsening (slight) • 6.7% px died • Hemorrhagic brain injury and its secondary effects (pre-procedure) may mask the surgical morbidity. • Sensitive measures of clinical outcomes (mRS) are more likely to reveal slight changes in patients who initially were essentially without symptoms. • Counseling patients : important to note that even subtle postoperative deficits can be easily detected Operative intervention in patients with unruptured AVMs should be seriously considered at high-volume experienced centers . The patients who can benefit the most : - Good candidates for surgery - Lesions with characteristics & angioarchitecture high risk for rupture
  • 13. Preoperative Embolization • Safely decrease the size of AVMs • Decrease the apparent risk of rupture in high-risk lesions • Eliminating deep feeding vessels • Operative blood loss can be greatly minimized Previous studies: highlight favorable clinical outcomes of multi-modality therapy for carefully selected patients
  • 14. Nataraj et al 265 px Rupture + Unrupture GOS (favorable/ score 4-5) Embolization  microsurgical resection 86% Microsurgical resection alone 96.5% Presurgical embolization • Marker of patients with more complicated AVM angioarchitecture / high-risk for surgery • Potentially risky: – possibility of decreasing the flow too much in one area  increased flow in other areas of the nidus / cerebral vasculature – diminishing venous outflow from embolization could cause AVM rupture
  • 15. AVM size Stüer et al: • Small- and medium-sized AVMs : dynamic autoregulatory function seems to be intact in the surrounding cerebrovascular bed perioperatively. • Larger AVMs : more likely to have more draining veins & risk for postoperative breakthrough complications. • Emphasizes the importance of AVM size for stratification of surgical risk AVM size: strong independent predictor of surgical complications • More data on microsurgery treatment in a larger group of cases with high SM grade To elucidate specific components of the SM grading scale that can predict favorable operative outcomes in high-grade lesions
  • 16. Microsurgery & ARUBA Trial The majority of patients in the ARUBA trial treatment arm received noninvasive and non-neurosurgical treatments Russin and Spetzler: it remains difficult to resolve why only 5 patients received resection alone when 76 patients in the treatment arm had Grade I or II AVMs. Present data are encouraging. With modern-day techniques & approaches, microsurgery can be undertaken with extremely low complication rates and provide excellent outcomes for patients A trial comparing microsurgery and medical management is necessary to begin exploring the unanswered questions and clinical discrepancies raised by the ARUBA trial
  • 17. Limitations • Retrospective data analysis • Single-center study • Recall bias
  • 18. Conclusion • Microsurgical resection of AVMs is highly efficient and can be undertaken with low rates of morbidity at high-volume neurovascular centers. • Unruptured and larger AVMs were associated with higher complication rates

Editor's Notes

  1. Embolization : Transfemoral approach, under monitored anesthetic care, biological agents used were N-butyl- 2-cyanoacrylate (Codman Neurovascular) or Onyx (eV3).  reducing blood flow to the AVM incrementally over time
  2. In our series, all patients except for 1 were age 55 years or younger, and the majority were free of any major comorbidities. More than half of the patients had an AVM with a size of 3 cm or greater. ???? The majority of our patients who received operative intervention in the context of an unruptured AVM had SM Grade I–III lesions and were deemed good candidates for microsurgery, wherein the benefits outweighed the risks.
  3. A multimodality, minimally invasive approach of embolization and radiosurgery may perhaps be a safer means of curing a large AVM if it is detected in a timely manner.
  4. However, as these deaths illustrate, there is risk in using embolization to reduce AVM flow instead of volume, with a resulting possibility of short-term postembolization hemorrhage. Du and colleagues: The effects of diffuseness and deep perforating artery supply on outcomes after microsurgical resection of brain arteriovenous malformations. 10.1227/01.NEU.0000255401.46151.8A http://www.ncbi.nlm.nih.gov/pubmed/17415200 We believe that the major benefit of embolization is the elimination of deep feeding arteries, which have been suggested to be the limiting factor in the morbidity and surgical resectability for Spetzler-Martin have shown that diffuseness and deep perforating artery supply are subtle features of an AVM that predict worse outcomes after microsurgical resection, since deep perforators are friable, poorly visualized, and located in eloquent white matter tracts. 9 Therefore, for microsurgery candidates, embolization is especially beneficial for elimination of deep feeding vessels.
  5. Concept of normal perfusion pressure breakthrough (NPPB) Normalized perfusion pressure in parts of vessels whose autoregulatory capacity has been lost following surgical resection of a large, high flow arteriovenous malformation (AVM) is thought to be a transitory cause of NPPB. Resumption of normal perfusion pressure in the brain around the AVM is believed to result in local capillary breakthrough, leading to uncontrollable cerebral swelling and hemorrhage.[1] Al-Rodhan et al[2] presented an alternative concept of occlusive hyperemia. They argued that postoperative intracranial bleeding or edema may result in (1) occlusion of the draining venous system in the brain surrounding the AVM, followed by passive hyperemia and stagnation; and (2) stagnation in the feeding artery for the AVM and in the blood flow in the parenchymatous branching of the artery, followed by exacerbation of pre-existing hypoperfusion, ischemia, or edema. Wilson et al[3] argue that this condition is observed frequently following embolization. Rapid neurological deterioration follows thrombus formation in a main draining vein. This is called "venous overload". They state that venous overload can be "malignant" if venous occlusion occurs in the presence of nidus remnant. (Kumar et al 2004) Among the disadvantages to a direct surgical approach are: ischemic stroke, the potential for significant intraoperative bleeding, and damage to adjacent neural tissue. In most AVM cases, the arteries that supply the AVM also supply intact neural tissue. These must not be destroyed while attempting to selectively interrupt the arterial supply to the AVM. There is theadditional risk for "perfusion-breakthrough bleeding". This is a dreadful complication resulting in post-operative hemorrhage into the healthy part of the Brain caused by sudden hemodynamic shifts. These "shifts" result from the removal of a large AV malformation which had previously been "shunting" blood rapidly. Once that "shunt" is removed thesubsequent increased flow to the previously underperfused Brain can result in this type of haemorrhage. (http://www.neurosurgerydallas.com/2_1_5_2.php) specific components of the SM grading scale that can predict favorable operative outcomes in high-grade lesions: located superficially or not involving critical components, resection can be expected to yield a good outcome.