Endovascular embolization and needle aspiration of a life-threatening cervical hematoma due to a neurofibromatosis type 1–associated arteriovenous fistula: illustrative case

Daigo KojimaDepartment of Neurosurgery, Iwate Prefectural Chubu Hospital, Kitakami, Iwate, Japan

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Yosuke AkamatsuDepartment of Neurosurgery, Iwate Prefectural Chubu Hospital, Kitakami, Iwate, Japan
Department of Neurosurgery, Iwate Medical University School of Medicine, Yahaba-cho, Iwate, Japan; and

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Kenta AsoDepartment of Neurosurgery, Iwate Prefectural Miyako Hospital, Miyako, Japan

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Kazuto KimuraDepartment of Neurosurgery, Iwate Prefectural Miyako Hospital, Miyako, Japan

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Yoshiyasu MatsumotoDepartment of Neurosurgery, Iwate Prefectural Chubu Hospital, Kitakami, Iwate, Japan
Department of Neurosurgery, Iwate Medical University School of Medicine, Yahaba-cho, Iwate, Japan; and

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Shinpei SatoDepartment of Neurosurgery, Iwate Prefectural Chubu Hospital, Kitakami, Iwate, Japan

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Hiroshi KashimuraDepartment of Neurosurgery, Iwate Prefectural Chubu Hospital, Kitakami, Iwate, Japan

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Yoshitaka KuboDepartment of Neurosurgery, Iwate Medical University School of Medicine, Yahaba-cho, Iwate, Japan; and

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Kuniaki OgasawaraDepartment of Neurosurgery, Iwate Medical University School of Medicine, Yahaba-cho, Iwate, Japan; and

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BACKGROUND

In cases of neurofibromatosis in which the bleeding source is considered strongly related to a neurofibroma, an open surgical approach could risk uncontrollable bleeding from the vascular wall infiltration by neurofibroma. The case of a neurofibromatosis type 1 (NF1)–associated arteriovenous fistula presenting with a life-threatening cervical hematoma that was successfully treated with alternative treatment is described.

OBSERVATIONS

A 68-year-old woman diagnosed with NF1 presented with sudden onset of a spontaneous right cervical mass. Neck imaging on admission showed a massive subcutaneous hematoma with tracheal deviation and abnormal vascular structure in the hematoma. Digital subtraction angiography showed that an arteriovenous fistula (AVF) fed from a vertebral artery located within the hematoma cavity was the primary source of bleeding and feeding arteries from the occipital artery to the neurofibroma. Embolization of the cervical neurofibroma, as well as the AVF, was performed to reduce the secondary risk of bleeding, and was accomplished. After endovascular treatment, needle aspiration of the cervical hematoma was performed to reduce the mass effect.

LESSONS

When performing open surgery via tissues with neurofibromatosis proliferation, uncontrollable bleeding can occur. Therefore, endovascular embolization and needle aspiration of the hematoma should be considered in this setting.

ABBREVIATIONS

ATF = arteriovenous fistula; CT = computed tomography; ICA = internal carotid artery; IJV = internal jugular vein; NBCA = N-butyl 2-cyanoacrylate; NF1 = neurofibromatosis type 1; OA = occipital artery; STA = superficial temporal artery; VA = vertebral artery

BACKGROUND

In cases of neurofibromatosis in which the bleeding source is considered strongly related to a neurofibroma, an open surgical approach could risk uncontrollable bleeding from the vascular wall infiltration by neurofibroma. The case of a neurofibromatosis type 1 (NF1)–associated arteriovenous fistula presenting with a life-threatening cervical hematoma that was successfully treated with alternative treatment is described.

OBSERVATIONS

A 68-year-old woman diagnosed with NF1 presented with sudden onset of a spontaneous right cervical mass. Neck imaging on admission showed a massive subcutaneous hematoma with tracheal deviation and abnormal vascular structure in the hematoma. Digital subtraction angiography showed that an arteriovenous fistula (AVF) fed from a vertebral artery located within the hematoma cavity was the primary source of bleeding and feeding arteries from the occipital artery to the neurofibroma. Embolization of the cervical neurofibroma, as well as the AVF, was performed to reduce the secondary risk of bleeding, and was accomplished. After endovascular treatment, needle aspiration of the cervical hematoma was performed to reduce the mass effect.

LESSONS

When performing open surgery via tissues with neurofibromatosis proliferation, uncontrollable bleeding can occur. Therefore, endovascular embolization and needle aspiration of the hematoma should be considered in this setting.

ABBREVIATIONS

ATF = arteriovenous fistula; CT = computed tomography; ICA = internal carotid artery; IJV = internal jugular vein; NBCA = N-butyl 2-cyanoacrylate; NF1 = neurofibromatosis type 1; OA = occipital artery; STA = superficial temporal artery; VA = vertebral artery

Neurofibromatosis type 1 (NF1)–associated vasculopathy, such as stenosis, dissection, aneurysm, arteriovenous fistula (AVF), or rupture of affected vasculature, has been reported.1,2 Smooth muscle dysplasia and direct infiltration of neurofibroma tissue into vasculature are known as mechanisms of the vascular tissue fragility in patients with NF1.1–7 As previously reported, an open surgical approach could risk uncontrollable bleeding from the vascular wall infiltration by a neurofibroma.3,4,6,7 Therefore, in cases in which the bleeding source is considered strongly related to a neurofibroma, treatment strategies avoiding unnecessary damage of vascular structures should be considered.

A case of a NF1-associated arteriovenous fistula presenting with life-threatening cervical hematoma that was successfully treated with endovascular embolization and needle aspiration is described.

Illustrative Case

A 68-year-old woman diagnosed with NF1 presented with a 3-day history of the sudden onset of a spontaneous right cervical mass and was transferred to our institute for emergent treatment (Fig. 1A). On review of her past medical history, she had a 30-year history of multiple neurofibromas. She had undergone internal carotid artery (ICA) trapping combined with superficial temporal artery (STA)–middle cerebral artery bypass for an unruptured right ICA petrous aneurysm 15 years earlier in our institute. Based on the operative record, intraoperative hemostasis was difficult due to fibromatosis tissues that had required wound packing and blood transfusion at that time. Digital subtraction angiography 1 year after the aneurysm trapping demonstrated that the right vertebral artery (VA) terminated at the V3 segment, as well as the common and external carotid arteries with no AVF (Fig. 1B and C). However, contrast-enhanced cervical computed tomography (CT) obtained on admission demonstrated a massive subcutaneous hematoma with tracheal deviation and a thrombosed right internal jugular vein (IJV) (Fig. 1D). Abnormal vascular structures were also detected beside the hematoma (Fig. 1E). Angiography was performed for further investigation of the vascular pathology. After the introduction of a 4-Fr sheath via the right radial artery, right VA injection showed that the right VA comprised reconstituted muscular branches, and it fed into an AVF and drained into both subcutaneous veins and the sigmoid sinus via an emissary vein through a large shunt pouch (Fig. 2A and B). The right IJV distal to the junction of the subclavian vein was not opacified in its venous phase (Fig. 2C). Cone-beam CT of the right VA showed a dilated venous pouch lateral to the hematoma cavity, indicating the source of the hemorrhage (Fig. 2D). Right common carotid artery injection demonstrated feeding arteries to the neurofibroma from the occipital artery (OA) and STA (Fig. 2E). Left common carotid and left vertebral injection showed no feeder involved in the AVF or neurofibroma. Based on the findings, the AVF was considered the primary source of bleeding. Moreover, it was considered that the damaged neurofibroma tissues by massive cervical hemorrhage could also be a secondary bleeding source. Therefore, it was decided to embolize the cervical neurofibroma, as well as the AVF, under general anesthesia with endotracheal intubation. A 4-Fr FUBUKI guiding sheath (Asahi Intech Co., Ltd.) was navigated into the right common carotid artery via the right radial artery, and systemic heparinization was started. The feeding arteries from the OA were embolized using 25% 300–500-µm trisacryl gelatin microspheres (Embosphere) and coil through an Excelsior SL-10 microcatheter (Boston Scientific). Transarterial embolization of the AVF was then performed. The 4-Fr guiding sheath was navigated into the right VA, and the Excelsior SL-10 was placed in the shunt pouch. After placement of multiple coils to reduce shunt flow, a DeFrictor Nano Catheter (Medico’s Hirata) was navigated coaxially into the shunt pouch, and 16.7% N-butyl 2-cyanoacrylate (NBCA) was injected (total: 1.48 mL), resulting in complete obliteration of the AVF (Fig. 3A). After endovascular treatment, the antithrombotic effect of heparin was reversed by protamine. Then, the right cervical hematoma was punctured by palpation and aspirated using a 16-gauge vein custody needle (V-1, TOP Corporation) to reduce the mass effect, and 38 mL of liquid hematoma was finally drained (Fig. 3B). The patient remained intubated until hemostasis was confirmed 1 day after the intervention. The patient’s postoperative course was uneventful, and significant reduction in the cervical mass effect was achieved up to 14 days after the intervention, which was also confirmed by cervical CT (Fig. 3C and D). The patient has been free from new symptoms for 6 months after the intervention.

FIG. 1.
FIG. 1.

Preoperative photograph (A) of the neck showing subcutaneous hematoma and cervical swelling from the right neck to the precordia. Anteroposterior view of right common carotid artery angiography (B) and right vertebral artery angiography (C) obtained 1 year after aneurysm trapping, showing no vascular lesion. (D) Contrast-enhanced cervical CT showing a dilated IJV (arrowheads) and a filling defect in the IJV (arrow). (E) Dilated vascular structure is indicated beside the hematoma at the level of C2 (arrowheads).

FIG. 2.
FIG. 2.

Anteroposterior (A) and lateral (B) views of right vertebral injection showing a vertebral arteriovenous fistula draining into the emissary vein into the ipsilateral sigmoid sinus SS-IJV, the subcutaneous vein, and the subcutaneous vein via the proximal (arrowhead) and the distal (arrow) shunt pouch. (C) Anteroposterior view of the right vertebral artery injection demonstrating contrast pooling in the IJV (arrowheads) in the venous phase. (D) Cone-beam CT of the right vertebral artery injection showing an abnormal vascular structure (arrowheads) beside the hematoma cavity. Lateral view of the right common carotid injection showing tumor staining fed from the subcutaneous branches of horizontal segments of the OA (arrows) and a parietal branch of the STA (arrowheads).

FIG. 3.
FIG. 3.

(A) Lateral view of the postoperative right vertebral artery injection showing complete obliteration of the fistula. The coil mass and NBCA cast are pasted in the right upper corner. (B) A photograph showing needle aspiration of the hematoma. (C) CT on postoperative day 12 showing low density and a smaller hematoma. (D) A photograph obtained on postoperative day 14 showing significant reduction in the cervical mass effect and subcutaneous hematoma.

Discussion

Observations

A case of life-threatening cervical hematoma due to an NF1-associated AVF was described. Vascular disease associated with NF1 is thought to be the result of congenital mesodermal dysplasia, and an acquired mechanism, dysplastic smooth muscle or neurofibromatosis proliferation in arterial walls, could lead to aneurysm formation, leakage, and ultimately rupture into adjacent veins.8,9

Two possible mechanisms of AVF formation can be considered in the present case. First, repetitive minor trauma such as neck motion of the pathological vasculature may be associated with aneurysm or fistula formation and eventual rupture. In fact, in the present patient, the vertebral AVF was not congenital but acquired, since it was not observed 15 years before the onset of the cervical hematoma. Second, occlusion of the IJV due to the mass effect of neurofibromatosis and/or thrombotic change may have contributed to AVF formation in the present case, since venous hypertension and hypoxic stimulation could promote local angiogenesis within the tumor, eventually leading to fistula formation in the adjacent artery.10

There have been 4 cases of cervical subcutaneous hemorrhage due to an NF1-associated vertebral AVF, including the present case2,7,11 (Table 1). Of them, Narayanamurthy et al.7 reported a fatal case of cervical spontaneous hemorrhage that underwent endovascular obliteration followed by surgical hematoma removal to prevent airway obstruction. However, uncontrollable bleeding from the vasculature and damaged tissue required wound packing and transfusion of red blood cells, fresh frozen plasma, and platelets, resulting in a fatal outcome. Higa et al.2 also described a case of a ruptured vertebral AVF that underwent endovascular treatment alone. Although marked reduction in the fistulous flow and hemostasis were achieved, the patient could not be extubated, requiring open tracheostomy, and she then developed weakness of her upper extremity due to compression of the brachial nerve plexus by a massive cervical hematoma. These 2 cases suggested the difficulty in hemostasis during the open surgical therapy even after obliteration of the fistula and the necessity of timely decompression of the hematoma. Furthermore, the Japan Medical Safety Research Organization also issued a warning regarding vessel rupture in patients with NF1 undergoing open surgery along large vessels due to loss and thinning of the vascular mesothelium, rupture of the internal elastic lamina, and deposition of mucus-like material in the vasculature by infiltration of NF1.12 Therefore, we believe that endovascular embolization of the AVF followed by needle aspiration of the hematoma was a practical strategy with less-invasive hematoma decompression compared with surgical hematoma removal, which might have led to uncontrollable bleeding from neurofibromatosis tissue or vasculature replaced by neurofibroma.

TABLE 1.

Arteriovenous fistula with cervical hemorrhage in patients with neurofibromatosis type 1

Case No.Authors & YearAge (yr)/ SexFeeder/DrainerLevel of AVFTracheal DistortionIntubationTreatmentOutcome
1Roth et al., 20001136/FVA/epidural & paraspinal venous plexusV2 proximalYesYesEVT + OSGR
2Higa et al., 2010260/FVA, ECA, OA/unknownV2YesYesEVTSD
3Narayanamurthy

et al., 20167
40/MVA/unknownV2YesYesEVT + OSD
4Present case68/FVA/SS, PVVV2YesYesEVT + aspirationGR

D = death; ECA = external carotid artery; EVT = endovascular treatment; GR = good recovery; OS = open surgery; PVV = paravertebral venous plexus; SD = severe disabled; SS = sigmoid sinus.

Lessons

We report on a patient presenting with a life-threatening cervical hematoma due to an NF1-associated AVF. Since airway obstruction due to hematoma compression and uncontrollable bleeding from tumor-proliferating vessels and tissues can occur during surgical hematoma removal in NF1-associated hemorrhage, treatment involving endovascular embolization and needle aspiration of the hematoma should be considered.

Acknowledgments

We thank FORTE Science Communications for assistance with English-language editing.

Disclosures

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: Akamatsu, Kojima. Acquisition of data: Akamatsu, Kojima, Aso, Kimura, Sato, Kashimura. Analysis and interpretation of data: Akamatsu, Kojima, Sato. Drafting of the article: Akamatsu, Kojima. Critically revising the article: Akamatsu, Kashimura, Kubo. Reviewed submitted version of the manuscript: Akamatsu, Matsumoto, Kashimura, Kubo, Ogasawara. Approved the final version of the manuscript on behalf of all authors: Akamatsu. Administrative/technical/material support: Kubo. Study supervision: Kashimura, Kubo, Ogasawara.

References

  • 1

    Sheerin UM, Holmes P, Childs L, Roy A, Ferner RE. Neurovascular complications in adults with neurofibromatosis type 1: a national referral center experience. Am J Med Genet A. 2022;188(10):30093015.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Higa G, Pacanowski JP Jr, Jeck DT, Goshima KR, León LR Jr. Vertebral artery aneurysms and cervical arteriovenous fistulae in patients with neurofibromatosis 1. Vascular. 2010;18(3):166177.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Hiraki T, Higashi M, Goto Y, et al. A rare case of internal jugular vein aneurysm with massive hemorrhage in neurofibromatosis type 1. Cardiovasc Pathol. 2014;23(4):244247.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Morita R, Abo D, Soyama T, et al. Spontaneous rupture of the pancreatic arcade artery caused by neurofibromatosis type 1 successfully treated using emergency transcatheter arterial embolization, partial intra-aortic balloon occlusion, and stent graft placement: a case report and review of the literature. CVIR Endovasc. 2020;3(1):37.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Liang Y, Tong F, Zhang L, Li W, Zhou Y. Sudden death due to rupture of the right internal carotid artery in neurofibromatosis type 1: a case report. Leg Med (Tokyo). 2016;21:3337.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Dova S, Ktenidis K, Karkos P, et al. A rare case of a spontaneous neck hematoma in a patient with type 1 neurofibromatosis. Auris Nasus Larynx. 2016;43(5):591594.

    • Search Google Scholar
    • Export Citation
  • 7

    Narayanamurthy H, El-Badawy S, Mukonoweshuro W, Whitfield P. A case of spontaneous haematoma from vertebral artery arterio-venous fistula in a patient with neurofibromatosis type 1. Br J Neurosurg. 2017;31(6):736737.

    • Search Google Scholar
    • Export Citation
  • 8

    Ushikoshi S, Goto K, Uda K, Ogata N, Takeno Y. Vertebral arteriovenous fistula that developed in the same place as a previous ruptured aneurysm: a case report. Surg Neurol. 1999;51(2):168173.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Daly MP, Rubinstein MN. A case of neurofibromatosis associated with a coronary artery aneurysm and myocardial infarction. Clin Cardiol. 1992;15(8):616618.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Lukies MW, Osuga K, Nakazawa T, et al. Endovascular management of an acquired subclavian arteriovenous fistula secondary to chronic venous occlusion after pacemaker insertion. Interventional Radiology. 2017;2:3337.

    • Search Google Scholar
    • Export Citation
  • 11

    Roth TC, Manness WK, Hershey BL, Yazdi J. Complex vertebral arteriovenous fistula and ruptured aneurysm in neurofibromatosis: a therapeutically challenging case. Skull Base Surg. 2000;10(1):3541.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Japan Medical Safety Research Organization. The risk of the vascular breakdown in von Recklinghausen’s disease. Medical Safety Information. 2014; 4. Accessed January 10, 2023. http://www.medsafe.jp/activ_alarm/activ_alarm_004.pdf (in Japanese).

    • Search Google Scholar
    • Export Citation
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  • View in gallery
    FIG. 1.

    Preoperative photograph (A) of the neck showing subcutaneous hematoma and cervical swelling from the right neck to the precordia. Anteroposterior view of right common carotid artery angiography (B) and right vertebral artery angiography (C) obtained 1 year after aneurysm trapping, showing no vascular lesion. (D) Contrast-enhanced cervical CT showing a dilated IJV (arrowheads) and a filling defect in the IJV (arrow). (E) Dilated vascular structure is indicated beside the hematoma at the level of C2 (arrowheads).

  • View in gallery
    FIG. 2.

    Anteroposterior (A) and lateral (B) views of right vertebral injection showing a vertebral arteriovenous fistula draining into the emissary vein into the ipsilateral sigmoid sinus SS-IJV, the subcutaneous vein, and the subcutaneous vein via the proximal (arrowhead) and the distal (arrow) shunt pouch. (C) Anteroposterior view of the right vertebral artery injection demonstrating contrast pooling in the IJV (arrowheads) in the venous phase. (D) Cone-beam CT of the right vertebral artery injection showing an abnormal vascular structure (arrowheads) beside the hematoma cavity. Lateral view of the right common carotid injection showing tumor staining fed from the subcutaneous branches of horizontal segments of the OA (arrows) and a parietal branch of the STA (arrowheads).

  • View in gallery
    FIG. 3.

    (A) Lateral view of the postoperative right vertebral artery injection showing complete obliteration of the fistula. The coil mass and NBCA cast are pasted in the right upper corner. (B) A photograph showing needle aspiration of the hematoma. (C) CT on postoperative day 12 showing low density and a smaller hematoma. (D) A photograph obtained on postoperative day 14 showing significant reduction in the cervical mass effect and subcutaneous hematoma.

  • 1

    Sheerin UM, Holmes P, Childs L, Roy A, Ferner RE. Neurovascular complications in adults with neurofibromatosis type 1: a national referral center experience. Am J Med Genet A. 2022;188(10):30093015.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Higa G, Pacanowski JP Jr, Jeck DT, Goshima KR, León LR Jr. Vertebral artery aneurysms and cervical arteriovenous fistulae in patients with neurofibromatosis 1. Vascular. 2010;18(3):166177.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Hiraki T, Higashi M, Goto Y, et al. A rare case of internal jugular vein aneurysm with massive hemorrhage in neurofibromatosis type 1. Cardiovasc Pathol. 2014;23(4):244247.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Morita R, Abo D, Soyama T, et al. Spontaneous rupture of the pancreatic arcade artery caused by neurofibromatosis type 1 successfully treated using emergency transcatheter arterial embolization, partial intra-aortic balloon occlusion, and stent graft placement: a case report and review of the literature. CVIR Endovasc. 2020;3(1):37.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Liang Y, Tong F, Zhang L, Li W, Zhou Y. Sudden death due to rupture of the right internal carotid artery in neurofibromatosis type 1: a case report. Leg Med (Tokyo). 2016;21:3337.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Dova S, Ktenidis K, Karkos P, et al. A rare case of a spontaneous neck hematoma in a patient with type 1 neurofibromatosis. Auris Nasus Larynx. 2016;43(5):591594.

    • Search Google Scholar
    • Export Citation
  • 7

    Narayanamurthy H, El-Badawy S, Mukonoweshuro W, Whitfield P. A case of spontaneous haematoma from vertebral artery arterio-venous fistula in a patient with neurofibromatosis type 1. Br J Neurosurg. 2017;31(6):736737.

    • Search Google Scholar
    • Export Citation
  • 8

    Ushikoshi S, Goto K, Uda K, Ogata N, Takeno Y. Vertebral arteriovenous fistula that developed in the same place as a previous ruptured aneurysm: a case report. Surg Neurol. 1999;51(2):168173.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Daly MP, Rubinstein MN. A case of neurofibromatosis associated with a coronary artery aneurysm and myocardial infarction. Clin Cardiol. 1992;15(8):616618.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Lukies MW, Osuga K, Nakazawa T, et al. Endovascular management of an acquired subclavian arteriovenous fistula secondary to chronic venous occlusion after pacemaker insertion. Interventional Radiology. 2017;2:3337.

    • Search Google Scholar
    • Export Citation
  • 11

    Roth TC, Manness WK, Hershey BL, Yazdi J. Complex vertebral arteriovenous fistula and ruptured aneurysm in neurofibromatosis: a therapeutically challenging case. Skull Base Surg. 2000;10(1):3541.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Japan Medical Safety Research Organization. The risk of the vascular breakdown in von Recklinghausen’s disease. Medical Safety Information. 2014; 4. Accessed January 10, 2023. http://www.medsafe.jp/activ_alarm/activ_alarm_004.pdf (in Japanese).

    • Search Google Scholar
    • Export Citation

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