Recurrence of arteriovenous malformation in an adult patient after complete resection: illustrative case

Delfina C Mazza Elizalde Neurosurgical Department, Hospital General de Agudos “Dr. Ignacio Pirovano,” Buenos Aires, Argentina; and

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Ricardo H Menendez Neurosurgical Department, Hospital General de Agudos “Dr. Ignacio Pirovano,” Buenos Aires, Argentina; and
Neurosurgical Department, Hospital Aleman, Buenos Aires, Argentina

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Maximiliano Di Fabio Neurosurgical Department, Hospital General de Agudos “Dr. Ignacio Pirovano,” Buenos Aires, Argentina; and

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Douglas Ruiz Neurosurgical Department, Hospital General de Agudos “Dr. Ignacio Pirovano,” Buenos Aires, Argentina; and

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Juan Manuel Eiroa Neurosurgical Department, Hospital General de Agudos “Dr. Ignacio Pirovano,” Buenos Aires, Argentina; and

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Catalina Vittar Neurosurgical Department, Hospital General de Agudos “Dr. Ignacio Pirovano,” Buenos Aires, Argentina; and

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German Arias Neurosurgical Department, Hospital General de Agudos “Dr. Ignacio Pirovano,” Buenos Aires, Argentina; and

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Horacio A Sole Neurosurgical Department, Hospital General de Agudos “Dr. Ignacio Pirovano,” Buenos Aires, Argentina; and

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BACKGROUND

Complete resection of an arteriovenous malformation (AVM) is considered a curative treatment. In this paper the authors discuss two possibilities in the event of hemorrhage after satisfactory resection of an AVM: recurrence or remnant.

OBSERVATIONS

A 33-year-old female patient was diagnosed with an incidental right frontal AVM that was microsurgically resected and whose postoperative angiography showed no remnant. Eight years later, she presented with an episode of headache and speech arrest. Magnetic resonance imaging showed bleeding in the previous surgical site, and a new angiography revealed the presence of a vascular blush not seen previously. The patient did not show the most frequently associated factors for recurrence described in the literature, which are hemorrhage on presentation and deep venous drainage. In addition, factors related to undetected vascular remnants, such as preoperative hemorrhage and early postoperative angiography, were absent.

LESSONS

Considering the characteristics of the case, we believe that the most likely explanation is the development of a de novo vascular formation secondary to factors not yet elucidated. Preexisting views on AVM formation, the curative value of resection, and long-term follow-up in certain patients should be reevaluated.

ABBREVIATIONS

AVM = arteriovenous malformation; GRE = gradient echo sequence; MRI = magnetic resonance imaging; SM = Spetlzer-Martin

BACKGROUND

Complete resection of an arteriovenous malformation (AVM) is considered a curative treatment. In this paper the authors discuss two possibilities in the event of hemorrhage after satisfactory resection of an AVM: recurrence or remnant.

OBSERVATIONS

A 33-year-old female patient was diagnosed with an incidental right frontal AVM that was microsurgically resected and whose postoperative angiography showed no remnant. Eight years later, she presented with an episode of headache and speech arrest. Magnetic resonance imaging showed bleeding in the previous surgical site, and a new angiography revealed the presence of a vascular blush not seen previously. The patient did not show the most frequently associated factors for recurrence described in the literature, which are hemorrhage on presentation and deep venous drainage. In addition, factors related to undetected vascular remnants, such as preoperative hemorrhage and early postoperative angiography, were absent.

LESSONS

Considering the characteristics of the case, we believe that the most likely explanation is the development of a de novo vascular formation secondary to factors not yet elucidated. Preexisting views on AVM formation, the curative value of resection, and long-term follow-up in certain patients should be reevaluated.

ABBREVIATIONS

AVM = arteriovenous malformation; GRE = gradient echo sequence; MRI = magnetic resonance imaging; SM = Spetlzer-Martin

An arteriovenous malformation (AVM) is defined as an abnormal communication between arterial and venous channels with the absence of capillaries in between.1,2 This characteristic of their architecture causes a high blood flow shunt with arterialization of the venous system and an increased risk of hemorrhage. Traditionally, AVMs were considered to have a congenital nature, and the absence of capillary formation was thought to occur between the 7th and 12th week of intrauterine life.1,3 This concept has been challenged by some authors, and de novo AVMs have been described generally in the pediatric population and in patients with a previous cerebral event (trauma, radiotherapy, inflammatory conditions).4

Several therapeutic options are available for the treatment of AVM according to its characteristics. In this article, we present the case of a microsurgically treated AVM with a postoperative angiogram that revealed no remnants, although the AVM rebled 8 years after the first surgery. Here, we explore the different theories accounting for this event including the possibility of a recurrence after successful treatment. An AVM recurrence after complete excision is an event scarcely reported in the literature, and its mechanisms are not well understood.5–14

Illustrative Case

A 33-year-old female patient was being examined for sporadic headaches without any neurological deficit. Magnetic resonance imaging (MRI) revealed the presence of a vascular lesion located at the right frontal opercular region (Fig. 1A). This result prompted further study, and cerebral angiography was performed. The study showed a right frontal AVM formed by afferences from the middle cerebral artery and superficial venous drainage to the superior sagittal sinus and the superficial sylvian vein (Spetzler-Martin [SM] grade II AVM; Fig. 1B). Surgery was performed without preoperative embolization of the AVM, and complete microsurgical resection of the malformation was achieved through a right pterional approach. The patient was discharged neurologically intact. One month later, new angiography was performed, which showed the absence of vascular anomalies (Fig. 2). MRI studies were performed annually and showed no evidence of AVM. The postoperative follow-up was 5 years, when the last clinical and radiographic evaluations had been performed.

FIG. 1
FIG. 1

A: Preoperative axial FLAIR MRI showed large flow voids in the right frontal opercular region. B: Preoperative lateral angiography showed the AVM with feeding arteries from the middle cerebral artery and superficial venous drainage to the superior sagittal sinus and superficial sylvian vein. FLAIR = fluid-attenuated inversion-recovery.

FIG. 2
FIG. 2

One-month postoperative angiography on which no anomalous vessels can be observed.

Eight years after the surgical procedure, the patient experienced an episode of speech arrest and headache. New MRI with a gradient echo sequence (GRE) was ordered, and a small hemorrhagic focus was observed where the AVM had been previously seated (Fig. 3A). A new angiography was performed, which showed the presence of vessels, not previously observed, in the territory in which the original AVM had been located (Fig. 3B). This was interpreted as either a recurrence of the AVM or the presence of a remnant of the malformation, and treatment was subsequently planned. The patient was referred for radiosurgery.

FIG. 3
FIG. 3

A: GRE MRI sequence obtained after the neurological event showed a right frontal hemorrhagic focus. B: Lateral angiography on which the formation of new vessels was seen (red arrows).

Patient Informed Consent

The necessary patient informed consent was obtained in this study.

Discussion

Observations

Every vascular neurosurgeon is aware that after an AVM resection, careful inspection of the surroundings in search of an occult residual nidus must be done. At our center, this is performed in a standard fashion in all AVM surgeries. The presence of some portion of anomalous vasculature left behind can cause a subsequent episode of bleeding. In our case, a safe and complete resection of the AVM was performed. Our patient did not have factors that could have obscured correct visualization of the malformation such as a hematoma or edema8 because the AVM was an incidental finding during evaluation for migraines. Therefore, the surgeon considered that a correct and thorough inspection of the surgical site had been done without difficulties. Postoperative angiography is considered the standard study for documenting the excision of an AVM. However, there are no guidelines that clearly establish a postoperative time frame to perform this study. It could be argued that early postoperative angiography can fail to reveal remnants of the AVM if a hematoma, edema effects, or vasospasm are suspected to be present.4,8 In our case, the AVM did not preoperatively present with hematoma and the postoperative angiography was not done in early fashion since it was performed one month after the surgery. There were not, to our knowledge, factors of local compression that could have made the postoperative angiography unreliable. Taking these factors into account, the possibility of a recurrence could be considered. Reports of de novo formation are mostly described in the pediatric population. The accepted theory has been that a lack of maturity of the vascular system in the pediatric population makes these patients vulnerable to neoformation of the AVM after excision through angiogenic mechanisms not yet properly clarified.3,5,15

The possibility of AVM regrowth in the adult population stems from the ever-increasing evidence that AVMs may not be congenital and static lesions, but rather dynamic ones that can form because of inciting events such as trauma, inflammation, and hemorrhage in addition to the possible increase in the expression of vascular endothelial growth factor in the AVM and neighboring tissue.10,11

An AVM recurrence in an adult patient after complete resection with a confirmatory postoperative angiogram is a rare event. Some studies have tried to elucidate factors that could be associated with AVM regrowth such as deep venous drainage, preoperative hematoma, and a finding of overexpression of vascular endothelial growth factor in a histological examination of the AVM or the evidence of some form of excessive angiogenic signaling.

In Table 1,8,10–12,14 we assembled information on AVM recurrence. The literature sought after consisted of cases of rebleeding after complete excision of an AVM in adult patients. Most of the studies were case reports. The largest case series was that of Sorenson et al., with rebleeding reported in 73 patients, although the study included both adult and pediatric populations and 11 patients had undergone preoperative embolization. The role of preoperative embolization in relation to an increased risk of recurrence needs further study.11 As shown in the table, almost all patients had rupture as the initial mode of presentation, the AVM had deep venous drainage, and postoperative angiography was performed within 10 days of the surgical procedure. SM grade was included as reported in the literature, and most cases consisted of grade II and III AVMs. Authors made no clear correlation between SM grade and the risk of recurrence.12

TABLE 1

Cases of recurrence of AVM and possible factors associated

Authors & YearNo. of Pts w/ Recurrence ReportedPt AgeRupture as Presentation (no. of cases)Deep Venous DrainageSM GradeTreatmentTime to Postoperative AngiographyTissular Factor Overexpression (VEGF)
Morgan et al., 2012128<20 yrs, 20–39 yrs, >40 yrs, oldest pt 42 yrs66II (2), III (3), IV (3)Opw/in 7 daysNot reported
Sorenson et al., 2018117346 pediatric (<18 yrs), 14 adults (age reported in 60 pts)54 (mode of initial presentation reported in 60 pts)26 (pattern reported in 38 pts)Mean 2.5 (grade reported in 52 pts)Op, 11 pts had previous endovascular embolizationIntraop (9 pts), w/in 10 days after op (60 pts), btwn 17 days & 6 mos after op (4 pts)Not reported
Gabriel et al., 19968119 yrs1Not reportedNot reportedOp7 days after opNot reported
Codd et al., 200814133 yrs1NoIIIOpw/in 10 days after opNot reported
Marutani et al., 202010151 yrs11Not reportedOpNot reportedYes

Pt = patient; VEGF = vascular endothelial growth factor.

Our case did not exhibit any of the possible recurrence risk factors mentioned above because the venous drainage was superficial, and the presentation was incidental. Angiogenic tissular factors were not measured in the histological sample.

Lessons

After microsurgical excision of the AVM, our patient was considered cured. The discovery of a vascular blush on the angiogram 8 years after surgery opened the possibility that a de novo vascular malformation could have formed. The finding of new vessels responsible for the hemorrhage at the previous surgical site could challenge commonly accepted concepts of AVM formation, the curative value of microsurgical excision, and the necessity of follow-up after a negative postoperative angiogram in an adult patient. Dogmatic views about the congenital nature of these lesions and the impossibility of recurrence after complete removal of the malformation in adult patients may need further study. Nonetheless, this report entails the description of only one patient, and the predisposing factors for AVM recurrence need further investigation.

Acknowledgments

The authors are indebted to Dr. Elisa Estenssoro and Prof. Noemi Schneck for English editing of the manuscript and thank Dr. Horacio Barea Segovia for his critical revision of the manuscript and valuable insight.

Author Contributions

Conception and design: Mazza Elizalde, Eiroa, Arias, Sole. Acquisition of data: Mazza Elizalde, Di Fabio, Ruiz, Arias. Analysis and interpretation of data: Mazza Elizalde, Menendez, Ruiz, Arias. Drafting the article: Mazza Elizalde. Critically revising the article: Mazza Elizalde, Menendez, Arias. Reviewed submitted version of manuscript: Mazza Elizalde, Menendez, Vittar, Sole. Approved the final version of the manuscript on behalf of all authors: Mazza Elizalde. Administrative/technical/material support: Mazza Elizalde, Ruiz. Study supervision: Mazza Elizalde, Menendez, Ruiz, Vittar, Arias, Sole.

References

  • 1

    Morales-Valero SF, Bortolotti C, Sturiale C, Lanzino G. Are parenchymal AVMs congenital lesions? Neurosurg Focus. 2014;37(3):E2.

  • 2

    Steiger HJ. Recent progress understanding pathophysiology and genesis of brain AVM--a narrative review. Neurosurg Rev. 2021; 44(6):31653175.

  • 3

    Tasiou A, Tzerefos C, Alleyne CH Jr, et al. Arteriovenous malformations: congenital or acquired lesions? World Neurosurg. 2020;134:e799e807.

  • 4

    Mahajan A, Manchandia TC, Gould G, Bulsara KR. De novo arteriovenous malformations: case report and review of the literature. Neurosurg Rev. 2010;33(1):115119.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Copelan A, Drocton G, Caton MT, et al. Brain arteriovenous malformation recurrence after apparent microsurgical cure: increased risk in children who present with arteriovenous malformation rupture. Stroke. 2020;51(10):29902996.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Aboukaïs R, Vinchon M, Quidet M, Bourgeois P, Leclerc X, Lejeune JP. Reappearance of arteriovenous malformations after complete resection of ruptured arteriovenous malformations: true recurrence or false-negative early postoperative imaging result? J Neurosurg. 2017;126(4):10881093.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Dalton A, Dobson G, Prasad M, Mukerji N. De novo intracerebral arteriovenous malformations and a review of the theories of their formation. Br J Neurosurg. 2018;32(3):305311.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Gabriel EM, Sampson JH, Wilkins RH. Recurrence of a cerebral arteriovenous malformation after surgical excision. Case report. J Neurosurg. 1996;84(5):879882.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Rapaport S, Feghali J, Yang W, et al. Hemorrhage following complete arteriovenous malformation resection with no detectable recurrence: insights from a 27-year registry. Neurosurgery. 2021;89(2):212219.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Marutani A, Nakano R, Yamada T. Recurrence of arteriovenous malformation in adulthood five years after complete surgical resection: A case report. Neurochirurgie. 2020;66(5):405407.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Sorenson TJ, Brinjikji W, Bortolotti C, Kaufmann G, Lanzino G. Recurrent Brain Arteriovenous Malformations (AVMs): A Systematic Review. World Neurosurg. 2018;116:e856e866.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Morgan MK, Patel NJ, Simons M, Ritson EA, Heller GZ. Influence of the combination of patient age and deep venous drainage on brain arteriovenous malformation recurrence after surgery. J Neurosurg. 2012;117(5):934941.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Pellettieri L, Svendsen P, Wikholm G, Carlsson CA. Hidden compartments in AVMs--a new concept. Acta Radiol. 1997; 38(1):27.

  • 14

    Shi S, Gupta R, Moore JM, et al. De novo AVM formation following venous sinus thrombosis and prior AVM resection in adults: report of 2 cases. J Neurosurg. 2018;128(2):506510.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Codd PJ, Mitha AP, Ogilvy CS. A recurrent cerebral arteriovenous malformation in an adult. J Neurosurg. 2008;109(3):486491.

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  • FIG. 1

    A: Preoperative axial FLAIR MRI showed large flow voids in the right frontal opercular region. B: Preoperative lateral angiography showed the AVM with feeding arteries from the middle cerebral artery and superficial venous drainage to the superior sagittal sinus and superficial sylvian vein. FLAIR = fluid-attenuated inversion-recovery.

  • FIG. 2

    One-month postoperative angiography on which no anomalous vessels can be observed.

  • FIG. 3

    A: GRE MRI sequence obtained after the neurological event showed a right frontal hemorrhagic focus. B: Lateral angiography on which the formation of new vessels was seen (red arrows).

  • 1

    Morales-Valero SF, Bortolotti C, Sturiale C, Lanzino G. Are parenchymal AVMs congenital lesions? Neurosurg Focus. 2014;37(3):E2.

  • 2

    Steiger HJ. Recent progress understanding pathophysiology and genesis of brain AVM--a narrative review. Neurosurg Rev. 2021; 44(6):31653175.

  • 3

    Tasiou A, Tzerefos C, Alleyne CH Jr, et al. Arteriovenous malformations: congenital or acquired lesions? World Neurosurg. 2020;134:e799e807.

  • 4

    Mahajan A, Manchandia TC, Gould G, Bulsara KR. De novo arteriovenous malformations: case report and review of the literature. Neurosurg Rev. 2010;33(1):115119.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Copelan A, Drocton G, Caton MT, et al. Brain arteriovenous malformation recurrence after apparent microsurgical cure: increased risk in children who present with arteriovenous malformation rupture. Stroke. 2020;51(10):29902996.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Aboukaïs R, Vinchon M, Quidet M, Bourgeois P, Leclerc X, Lejeune JP. Reappearance of arteriovenous malformations after complete resection of ruptured arteriovenous malformations: true recurrence or false-negative early postoperative imaging result? J Neurosurg. 2017;126(4):10881093.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Dalton A, Dobson G, Prasad M, Mukerji N. De novo intracerebral arteriovenous malformations and a review of the theories of their formation. Br J Neurosurg. 2018;32(3):305311.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Gabriel EM, Sampson JH, Wilkins RH. Recurrence of a cerebral arteriovenous malformation after surgical excision. Case report. J Neurosurg. 1996;84(5):879882.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Rapaport S, Feghali J, Yang W, et al. Hemorrhage following complete arteriovenous malformation resection with no detectable recurrence: insights from a 27-year registry. Neurosurgery. 2021;89(2):212219.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Marutani A, Nakano R, Yamada T. Recurrence of arteriovenous malformation in adulthood five years after complete surgical resection: A case report. Neurochirurgie. 2020;66(5):405407.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Sorenson TJ, Brinjikji W, Bortolotti C, Kaufmann G, Lanzino G. Recurrent Brain Arteriovenous Malformations (AVMs): A Systematic Review. World Neurosurg. 2018;116:e856e866.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Morgan MK, Patel NJ, Simons M, Ritson EA, Heller GZ. Influence of the combination of patient age and deep venous drainage on brain arteriovenous malformation recurrence after surgery. J Neurosurg. 2012;117(5):934941.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Pellettieri L, Svendsen P, Wikholm G, Carlsson CA. Hidden compartments in AVMs--a new concept. Acta Radiol. 1997; 38(1):27.

  • 14

    Shi S, Gupta R, Moore JM, et al. De novo AVM formation following venous sinus thrombosis and prior AVM resection in adults: report of 2 cases. J Neurosurg. 2018;128(2):506510.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Codd PJ, Mitha AP, Ogilvy CS. A recurrent cerebral arteriovenous malformation in an adult. J Neurosurg. 2008;109(3):486491.

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