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Brain arteriovenous malformations in elderly patients: clinical features and treatment outcome

  • Clinical Article - Vascular
  • Published:
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Abstract

Background

In this aging society, attention has not been fully given to brain arteriovenous malformations (AVMs) in elderly patients. This study sought to describe a single institution’s experience treating arteriovenous malformations (AVMs) in elderly patients.

Methods

We conducted a retrospective review of brain AVMs in elderly patients treated at our institution between 1990 and 2012 with a focus on the clinical features, risk of hemorrhage and treatment outcomes.

Results

Of the 2790 patients in our AVM database, 98 patients were over the age of 60 at presentation. Forty-eight percent presented with hemorrhage. Risks of initial hemorrhage were history of hypertension, smaller AVM size (<3 cm) and exclusively deep venous drainage. Treatment modalities were microsurgical resection in 65 %, embolization alone in 10 %, stereotactic radiosurgery (SRS) in 11 % and observation in 14 %. Preoperative embolization was performed in 32 % in the surgical group. Complete obliteration was achieved in 95 % by microsurgery, 30 % by embolization alone and 45 % by SRS. Good functional outcome (modified Rankin Scale, mRS <2) was achieved in 69 % after a median follow-up of 5.8 years. Multivariate logistic analysis revealed that a pretreatment mRS score ≥2, eloquent location and higher S-M grade (IV or V) were associated with worsening functional status, whereas surgical resection was a negative factor. Posttreatment hemorrhage occurred in 8 %. AVM-related death occurred in three patients (2 by surgery and 1 by observation).

Conclusions

Brain AVMs in elderly patients still pose a high risk of hemorrhage. Initial hemorrhage may be associated with a history of hypertension, AVM size and exclusively deep venous drainage. Initial mRS score ≥2, eloquent location and higher S-M grade may be associated with worsening functional status. Microsurgical resection can be safe and effective for selected patients. Preoperative embolization is helpful in patients with S-M grade IV-V AVMs. For those with surgical contraindications, SRS and observation are treatment alternatives.

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Acknowledgments

This study was supported by Key Projects in the National Science & Technology Pillar Program during the Twelfth Five-year Plan Period (grant no. 2011BAI08B00). Author contributions to the study and manuscript preparation include the following. Conception and design: all authors. Acquisition of data: Tong, Wu, Lin. Analysis and interpretation of data: Tong, Wu. Drafting the article: Tong. Critically revising the article: all authors. Reviewing the submitted version of the manuscript: all authors. Approving the final version of the manuscript on behalf of all authors: Shuo Wang. Statistical analysis: Tong, Wu, Cao. Administrative/technical/material support: Shuo Wang. Study supervision: Yong Cao, Yuanli Zhao, Shuo Wang and Jizong Zhao.

Conflicts of interest

All authors certify that we have no affiliations with or involvement in any organization or entity with any financial interest (such as honoraria; educational grants; participation in speakers’ bureaus; membership, employment, consultancies, stock ownership, or other equity interest; and expert testimony or patent-licensing arrangements), or non-financial interest (such as personal or professional relationships, affiliations, knowledge or beliefs) in the subject matter or materials discussed in this manuscript.

Author information

Authors and Affiliations

  1. Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, 100050, People’s Republic of China

    Xianzeng Tong, Jun Wu, Fuxin Lin, Yong Cao, Yuanli Zhao, Bo Ning, Bing Zhao, Lijun Wang, Shuo Zhang, Shuo Wang & Jizong Zhao

  2. China National Clinical Research Center for Neurological Diseases, Beijing, People’s Republic of China

    Xianzeng Tong, Jun Wu, Fuxin Lin, Yong Cao, Yuanli Zhao, Bo Ning, Bing Zhao, Lijun Wang, Shuo Zhang, Shuo Wang & Jizong Zhao

  3. Center of Stroke, Beijing Institute for Brain Disorders, Beijing, People’s Republic of China

    Xianzeng Tong, Jun Wu, Fuxin Lin, Yong Cao, Yuanli Zhao, Bo Ning, Bing Zhao, Lijun Wang, Shuo Zhang, Shuo Wang & Jizong Zhao

  4. Beijing Key Laboratory of Translational Medicine for Cerebrovascular Diseases, Beijing, People’s Republic of China

    Xianzeng Tong, Jun Wu, Fuxin Lin, Yong Cao, Yuanli Zhao, Bo Ning, Bing Zhao, Lijun Wang, Shuo Zhang, Shuo Wang & Jizong Zhao

Authors
  1. Xianzeng Tong
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  2. Jun Wu
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  3. Fuxin Lin
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  4. Yong Cao
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  6. Bo Ning
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  7. Bing Zhao
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  8. Lijun Wang
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  9. Shuo Zhang
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  10. Shuo Wang
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  11. Jizong Zhao
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Corresponding author

Correspondence to Shuo Wang.

Additional information

Comment

The article by Xianzeng Tong and colleagues resulted from a search of, to my knowledge, the largest prospectively generated monocentric AVM database. Their experience with brain AVMs in the elderly population is valuable for mainly two aspects. First, it provides us with demographic information with regard to the age distribution of AVM manifestation; second, the authors confirm that with modern multidisciplinary management reasonable outcome results can be obtained even in elderly patients.

The authors used a large AVM database of almost 3000 entries acquired after 1990, larger than the databases of the known western AVM projects. The proportion of patients over the age of 60 in this series was 3.5 %, which is in line with the proportion of the smaller multicentric series of Hofmeister et al., who found a rate of 5 % [2]. The slightly smaller rate of AVM patients in the Chinese cohort is well explained by the smaller proportion of people above the age of 60 in China of approximately 10 % in 2000 compared to 16–20 % in western Europe and USA [6, 8]. The rate of AVM patients becoming symptomatic at an age above 60 years is therefore definitely smaller than would be expected on the basis of the proportion of the population above 60 years. The same fact is reflected by the median age of AVM patients that varies from 35 to 40 years in most series. In Germany the median age of AVM patients in the year 2000 was around 40 years, whereas the median age in the population was around 45 years [4, 6, 8].

This demographic enigma, that the incidence of AVM decreases with age in contrast to other types of stroke, suggests that the prevalence of asymptomatic AVM becomes small in elderly people, or, in other words, most AVMs have become symptomatic before the age of 60. More concretely, based on the numbers given by Xianzeng Tong and colleagues, the number of AVMs in patients over 60 is only 35 % of the incidence expected on the grounds of the demographic distribution in China, or, the other way around, 65 % of the patients harboring an AVM had become symptomatic before the age of 60. This type of calculation theoretically allows for a different approach to the calculation of rupture rates of incidental AVMs. However, hospital-based data in this regard are too prone to selection bias to allow for a reliable calculation since there is a substantial section bias with regard to active treatment in elderly patients. The authors therefore state correctly: “Arteriovenous malformations are relatively uncommon in patients over the age of 60, as most become symptomatic (hemorrhage, seizure, chronic headache or focal deficit) by the fourth decade.” This is in line with other authors, e.g., ApSimon and coworkers summarized: “The great majority of AVM patients become symptomatic during the patient's lifetime, and the majority will bleed. The risk of first hemorrhage is lifelong and rises with age” [1].

The other conclusion to be drawn from the article is that AVM can be treated in elderly patients without an inappropriate risk. A good outcome (modified Rankin Scale, mRS <2) was achieved in 70 % after a median follow-up of 6 years, which appears comparable to other non-age-selected treatment series, although exact comparison is difficult because of the multiple treatment regimens. It appears that age is not a definite risk factor for an unfavorable outcome after treatment of AVMs, as for the microsurgical treatment of ruptured and unruptured aneurysms [3, 5, 7].

Hans-Jakob Steiger,

Düsseldorf, Germany

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Comment

In their article “Brain arteriovenous malformations in elderly patients: clinical features and treatment outcome,” Dr. Tong and colleagues performed a single-center, retrospective study of elderly patients who underwent treament for brain AVMs. Elderly was defined as above 60 years of age, in accordance with the WHO definition. From a database of 2790 patients with AVMs treated between 1990 and 2012, 98 patients (3.5 %) were elderly. This is in accordance with a previous studiy by Stapf and coworkers [2]. In their clinical practice, 48 % of the patients presented with hemorrhage, indicating that increasing age might be an independent predictor for AVM hemorrhage. The other risk factors for bleeding were a history of hypertension, smaller AVM size and exclusively deep venous drainage. The obliteration rates were 95, 45 and 30 % by microsurgery, SRS and embolization, respectively. The success rate of endovascular therapy is 2.3 times higher than that found in a metaanalysis by Beijnum et al. [4], but probably reflects, in part, a selection bias. The follow-up period, being somewhat short for a study period spanning more than 20 years, ranged from 3 to 13 years (mean 6 years). Risk factors for worsening functional status, defined as an increased mRS score, were a baseline mRS score ≥2, eloquent location and higher Spetzler-Martin grade. The authors conclude that microsurgical resection should be mainly used in AVMs of Spetzler-Martin grade I-II and some superficial grade III. This is in accordance with this author’s view [1]. For higher grade AVMs, microsurgical resection carries a higher risk of complications. In these patients, treatment alternatives such as SRS and observation should be considered [3].

Torsten Meling

Oslo, Norway

1. Meling TR (2015) Microsurgical resection of unruputured Spetzler-Ponce grade A arteriovenous malformations is worthwhile and still the “gold standard” therapy. Acta Neurochir (Wien) 157:1289–1290 doi:10.1007/s00701-015-2476-7

2. Stapf C, Khaw AV, Sciacca RR, Hofmeister C, Schumacher HC, Pile-Spellman J, Mast H, Mohr JP, Hartmann A (2003) Effect of age on clinical and morphological characteristics in patients with brain arteriovenous malformation. Stroke 34:2664–2669 doi:10.1161/01.STR.0000094824.03372.9B

3. Steiger HJ, Schaller K (2015) Treatment of unruptured brain AVM in the aftermath of ARUBA and the Scottish Audit of Intracranial Vascular Malformations. Acta Neurochir (Wien) 157:1291–1293 doi:10.1007/s00701-015-2477-6

4. van Beijnum J, van der Worp HB, Buis DR, Al-Shahi Salman R, Kappelle LJ, Rinkel GJ, van der Sprenkel JW, Vandertop WP, Algra A, Klijn CJ (2011) Treatment of brain arteriovenous malformations: a systematic review and meta-analysis. Jama 306:2011–2019 doi:10.1001/jama.2011.1632

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Tong, X., Wu, J., Lin, F. et al. Brain arteriovenous malformations in elderly patients: clinical features and treatment outcome. Acta Neurochir 157, 1645–1654 (2015). https://doi.org/10.1007/s00701-015-2521-6

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