Case Report Bilateral Surgical Reconstruction for Internal Jugular Veins Disease in Patients with Chronic Cerebrospinal Venous Insufficiency and Associated Multiple Sclerosis Salvatore Spagnolo,1,2,3 Filippo Scalise,2,3 Luciano Barbato,1,2,3 Maria Antonietta Grasso,1 and Ugo F. Tesler,1,2,3 Monza, Italy
Chronic cerebrospinal venous insufficiency (CCSVI) is a vascular condition characterized by morphologic alterations involving efferent cerebral vascular paths. CCSVI has been implicated as a contributing factor to multiple sclerosis (MS) but this theory is highly controversial. We report 3 cases of CCSVI patients with MS who had undergone internal jugular veins (IJVs) angioplasty to restore vessels patency. All patients reported significant symptomatic improvement after angioplasty until symptoms recurred after restenosis of the treated IJVs. Surgical IJVs reconstruction was performed. Patients’ symptoms gradually improved and the benefits were maintained at the 1-year follow-up.
Endovascular treatment of the narrowing of the jugular and/or the azygos veins for the treatment of multiple sclerosis (MS) is a procedure based on the hypothesis that an important role in the pathogenesis of this disease may be attributed to the obstructed outflow of the venous blood from the brain and the spinal chord, a condition that has been named chronic cerebrospinal venous insufficiency (CCSVI).1,2 Although both the pathogenetic hypothesis and mode of treatment are highly controversial issues3e5, a marked symptomatic improvement has been observed in several series of patients with MS who 1 Department of Cardiac and Vascular Surgery, Policlinico di Monza, Monza, Italy. 2 Cardiac and Vascular Catheterization Laboratory, Policlinico di Monza, Monza, Italy. 3
had undergone endovascular internal jugular veins (IJVs) angioplasty.6e10 Follow-up controls, however, have shown a substantial incidence of restenosis of the treated vessels, causing a recurrence of symptoms in patients who initially had experienced a marked improvement of their clinical condition after endovascular IJVs angioplasty for the treatment of CCSVI.10,11 Although in these cases repeat endovascular angioplasty is generally successful in relieving the recurrent vessel narrowing, in a certain number of patients a repeat endovascular procedure may not prove effective and a surgical reconstructive procedure may be indicated.12 This report presents the experience of open surgical IJVs reconstruction procedure for CCSVI performed in 3 patients who had experienced restenosis after successful IJVs endovascular angioplasty.
CCSVI Research Center, Policlinico di Monza, Monza, Italy.
Correspondence to: Filippo Scalise, MD, Cardiac and Vascular Catheterization Laboratory, Policlinico di Monza, Via Amati 111, 20900 Monza, Italy; E-mail: [email protected] Ann Vasc Surg 2014; -: 1–4 http://dx.doi.org/10.1016/j.avsg.2014.03.012 Ó 2014 Elsevier Inc. All rights reserved. Manuscript received: February 25, 2014; manuscript accepted: March 19, 2014; published online: ---.
CASE REPORT Three male patients aged 27, 27, and 30 years old, respectively with clinically proven relapsingeremitting MS, according to the revised McDonald criteria,13 were referred to our cardiovascular department for recurrent bilateral IJVs stenosis. After 1
2 Case Report
Annals of Vascular Surgery
Fig. 1. Venography of the right internal jugular vein (A) before and (B) after surgical reconstruction.
having been diagnosed with CCSVI by color-Doppler (CD) ultrasound14 and venography, they had undergone IJVs angioplasty. All patients had reported significant symptomatic improvement after the angioplasty until 8e12 weeks postintervention, when symptoms rapidly recurred and they were found to present restenosis of the treated IJVs. At the time of admission, the neurologic symptoms of these patients consisted of fatigue, muscle weakness and spasticity, problems with gait, mobility and balance, vision disturbances, reduced mental acuity, and neurogenic bowel and bladder dysfunction. All patients’ repeat CD ultrasound and venography confirmed the presence of restenosis of IJVs (Fig. 1). It was deemed that they were not candidates for repeat balloon angioplasty or stenting and were referred for open surgical jugular vein reconstruction. A segment of saphenous vein was harvested from the patients’ legs; it was incised longitudinally and it was shaped into an elongated patch. To obtain an optimal resolution of the IJV stenosis, the IJV incisions were carried down to their junction with the innominate vein. Full exposure of these anatomic structures required a collar incision and a short separate midline inverted-T superior ministernotomy, limited to the first intercostal space (Fig. 2). Under full heparinization, successive segments of the IJVs were clamped and a longitudinal incision was performed across the narrowed area of the anterior aspect of the stenotic IJVs. The venous valves and all potentially obstructing structures were excised (Fig. 3), and the incision was closed using the saphenous vein patch, thus relieving the stenosis by obtaining an enlargement of the vein caliber (Fig. 4). The heparin was reversed with protamine sulfate, the mini-sternotomy was approximated with steel wires, and the wound was
Fig. 2. Surgical view after upper mini-sternotomy. (A) Venous enlargement patch of the left internal jugular vein and (B) innominate vein.
closed in a routine fashion. All patients were started on anticoagulation therapy with warfarin on postoperative day 3, which was continued for 6 months, when it was substituted with an antiaggregant regimen with an oral daily dose of 150 mg of acetylsalicylic acid. There were no postoperative complications. CD ultrasound performed before discharge from the hospital showed patency of all treated vessels. Based on the
Vol.
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No.
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2014
Fig. 3. Intraoperative image of the excision of the venous valves from the interior aspect of the right internal jugular vein.
evaluation performed by the hospital physiotherapy unit, patients already early postoperatively reported a decrease of fatigue, muscle weakness, spasticity, and vision disturbances; they experienced an improvement in gait, mobility, and balance; further, their mental acuity and neurogenic bowel and bladder dysfunction were improved (Table I). They were started on a physiotherapy rehabilitation program and they continued to present a gradual improvement of their symptomatology and disability. Follow-up at 1-year ascertained that the clinical benefits were maintained, while CD ultrasound and venography (Fig. 1) showed patency of the reconstructed veins.
DISCUSSION Evidence of the frequent association between CCSVI and MS has stimulated the performance of endovascular interventions designated to dilate the stenotic vessels, which have produced the regression of symptoms in several series of patients.6e11,15 Follow-up controls, however, have shown a substantial incidence of restenosis of the dilated vessels, causing a recurrence of symptoms in patients who,
Case Report 3
Fig. 4. Intraoperative image of the final result of internal jugular vein enlarged with a venous patch.
initially, had experienced a significant improvement in their condition after having been submitted to endovascular IJVs angioplasty for the treatment of CCSVI.10,15 The patients in our report had undergone angioplasty of the stenotic IJVs with favorable results that lasted for w3 months until they experienced the recurrence of symptomatology secondary to restenosis of the dilated vessels. All patients had already twice been submitted to repeat percutaneous transluminal angioplasty. It was therefore felt that repeating further balloon dilatation for restoring venous patency was not feasible because of the extensive intimal damage of the vessels. A stent implantation was excluded for the inherent high risk of thrombosis. After an extensive interdisciplinary discussion, it was therefore elected to perform a surgical reconstruction of the jugular veins using an autologous venous patch to increase the caliber of the vessel, thus ensuring an unimpeded blood flow. After the surgical procedure, the patients experienced a positive and durable improvement of MS symptoms. Because of the high thrombotic risk determined by the low velocity of the jugular venous flow, all patients were started on warfarin immediately after surgery. After consultation with hematology, this therapy was continued for 6 months and then
4 Case Report
Annals of Vascular Surgery
Table I. Postoperative symptoms’ improvement Muscle Patient Gender Age MS type Fatigue weakness Spasticity Gait
1 2 3
M M M
27 27 31
RR RR RR
++ +++ ++
+ ++ ++
++ +++ ++
Mobility and Mental Neurogenic Bladder Vision balance acuity bowel disfunction disturbances
+++ ++ +++ ++ +++ ++
+ ++ ++
++ + ++
++ ++ ++
++ +++ +++
+, small improvement; ++, moderate improvement; +++, big improvement; M, male; RR, relapsingeremitting.
substituted with antiaggregant therapy with acetylsalicylic acid when it was estimated that the endothelialization of the damaged intima had been achieved. To our knowledge, only 1 case in which an analogous surgical procedure after restenosis of a percutaneously treated jugular vein has been reported.12 Unlike the experience of Fankhauser et al.,12 who used a spiral vein graft to bypass the occluded IJV, we elected to perform an enlargement venoplasty of the IJVs that, in our patients, were stenotic but not occluded. The hypothesis concerning the association of CCSVI with MS is highly controversial.3e5 If its role in determining the neurologic disease and the efficacy of the correction of the venous pathology should be confirmed, endovascular dilatation of the stenotic vessels should represent the treatment of choice for this disease. However, surgery should only be considered when venous anatomic abnormalities have been clearly identified in patients who had obtained a temporary clinical benefit related to the endovascular procedure until a restenosis of the dilated vessels had occurred. In our institution we do not offer primary open surgical treatment for CCSVI, and we believe these interventions would be best conducted within controlled clinical trials. In conclusion, open surgical IJVs reconstruction is technically feasible in most cases of CCSVI, but our limited experience does not support its widespread use as the elective treatment for MS. Moreover, our relatively short follow-up does not allow definite conclusions regarding the relative durability of venous surgical reconstruction compared with the endovascular dilatation. Randomized controlled trials are needed to validate the safety and efficacy of venous intervention in CCSVI. REFERENCES 1. Zamboni P, Galeotti R, Menegatti E, et al. Chronic cerebrospinal venous insufficiency in patients with multiple sclerosis. J Neurol Neurosurg Psychiatry 2009;80:392e9.
2. Zamboni P, Consorti G, Galeotti R, et al. Venous collateral circulation of the extra-cranial cerebrospinal outflow routes. Curr Neurovasc Res 2009;6:204e12. 3. Awad AM, Marder E, Milo R, et al. Multiple sclerosis and chronic cerebrospinal venous insufficiency: a critical review. Ther Adv Neurol Disord 2011;4:231e5. 4. Baracchini C, Perini P, Calabrese M, et al. No evidence of chronic cerebrospinal venous insufficiency at multiple sclerosis onset. Ann Neurol 2011;69:90e9. 5. Blinkenberg M, Akeson P, Sillesen H, et al. Chronic cerebrospinal venous insufficiency and venous stenoses in multiple sclerosis. Acta Neurol Scand 2012;126:421e7. 6. Zamboni P, Galeotti R, Weinstock-Guttman B, et al. Venous angioplasty in patients with multiple sclerosis: results of a pilot study. Eur J Vasc Endovasc Surg 2012;43:116e22. 7. Zamboni P, Galeotti R, Menegatti E, et al. A prospective open-label study of endovascular treatment of chronic cerebrospinal venous insufficiency. J Vasc Surg 2009;50: 1348e58. 8. Mandato KD, Hegener PF, Siskin GP, et al. Safety of endovascular treatment of chronic cerebrospinal venous insufficiency: a report of 240 patients with multiple sclerosis. J Vasc Interv Radiol 2012;23:55e9. 9. Salvi F, Bartolomei I, Buccelato E, et al. Venous angioplasty in multiple sclerosis: neurological outcome at two years in a cohort of relapsing-remitting patients. Funct Neurol 2012;27:55e9. 10. Radak D, Kolar J, Sagic D, et al. Percutaneous angioplasty of internal jugular and azygous veins in patients with chronic cerebrospinal venous insufficiency and multiple sclerosis: early and mid-term results. Phlebology 2013 Apr 5 [Epub ahead of print]. 11. Hubbard D, Ponec D, Gooding J, et al. Clinical improvement after extracranial venoplasty in multiple sclerosis. J Vasc Interv Radiol 2012;23:1302e8. 12. Fankhauser GT, Stone WM, Fu R, et al. Spiral vein graft for internal jugular bypass in a patient with multiple sclerosis and suspected chronic cerebrospinal venous insufficiency. Ann Vasc Surg 2013;27:673.e5e8. 13. Polman CH, Reingold SC, Edan G, et al. Diagnostic criteria for multiple sclerosis: 2005 revisions to the ‘McDonald Criteria’. Ann Neurol 2005;58:840e6. 14. Nicolaides AN, Morovic S, Menegatti E, et al. Screening for chronic cerebrospinal venous insufficiency (CCSVI) using ultrasound: recommendations for a protocol. Funct Neurol 2011;26:229e48. 15. Simka M, Janas P, Ludyga T, et al. Endovascular treatment for chronic cerebrospinal venous insufficiency in patients with multiple sclerosis. Vascular Diseases Management 2012;9:149e54.
Chronic cerebrospinal venous insufficiency (CCSVI) is a vascular condition characterized by morphologic alterations involving efferent cerebral vascular paths. CCSVI has been implicated as a contributing factor to multiple sclerosis (MS) but this theory is highly controversial. We report 3 cases of CCSVI patients with MS who had undergone internal jugular veins (IJVs) angioplasty to restore vessels patency. All patients reported significant symptomatic improvement after angioplasty until symptoms recurred after restenosis of the treated IJVs. Surgical IJVs reconstruction was performed. Patients’ symptoms gradually improved and the benefits were maintained at the 1-year follow-up.
Endovascular treatment of the narrowing of the jugular and/or the azygos veins for the treatment of multiple sclerosis (MS) is a procedure based on the hypothesis that an important role in the pathogenesis of this disease may be attributed to the obstructed outflow of the venous blood from the brain and the spinal chord, a condition that has been named chronic cerebrospinal venous insufficiency (CCSVI).1,2 Although both the pathogenetic hypothesis and mode of treatment are highly controversial issues3e5, a marked symptomatic improvement has been observed in several series of patients with MS who 1 Department of Cardiac and Vascular Surgery, Policlinico di Monza, Monza, Italy. 2 Cardiac and Vascular Catheterization Laboratory, Policlinico di Monza, Monza, Italy. 3
had undergone endovascular internal jugular veins (IJVs) angioplasty.6e10 Follow-up controls, however, have shown a substantial incidence of restenosis of the treated vessels, causing a recurrence of symptoms in patients who initially had experienced a marked improvement of their clinical condition after endovascular IJVs angioplasty for the treatment of CCSVI.10,11 Although in these cases repeat endovascular angioplasty is generally successful in relieving the recurrent vessel narrowing, in a certain number of patients a repeat endovascular procedure may not prove effective and a surgical reconstructive procedure may be indicated.12 This report presents the experience of open surgical IJVs reconstruction procedure for CCSVI performed in 3 patients who had experienced restenosis after successful IJVs endovascular angioplasty.
CCSVI Research Center, Policlinico di Monza, Monza, Italy.
Correspondence to: Filippo Scalise, MD, Cardiac and Vascular Catheterization Laboratory, Policlinico di Monza, Via Amati 111, 20900 Monza, Italy; E-mail: [email protected] Ann Vasc Surg 2014; -: 1–4 http://dx.doi.org/10.1016/j.avsg.2014.03.012 Ó 2014 Elsevier Inc. All rights reserved. Manuscript received: February 25, 2014; manuscript accepted: March 19, 2014; published online: ---.
CASE REPORT Three male patients aged 27, 27, and 30 years old, respectively with clinically proven relapsingeremitting MS, according to the revised McDonald criteria,13 were referred to our cardiovascular department for recurrent bilateral IJVs stenosis. After 1
2 Case Report
Annals of Vascular Surgery
Fig. 1. Venography of the right internal jugular vein (A) before and (B) after surgical reconstruction.
having been diagnosed with CCSVI by color-Doppler (CD) ultrasound14 and venography, they had undergone IJVs angioplasty. All patients had reported significant symptomatic improvement after the angioplasty until 8e12 weeks postintervention, when symptoms rapidly recurred and they were found to present restenosis of the treated IJVs. At the time of admission, the neurologic symptoms of these patients consisted of fatigue, muscle weakness and spasticity, problems with gait, mobility and balance, vision disturbances, reduced mental acuity, and neurogenic bowel and bladder dysfunction. All patients’ repeat CD ultrasound and venography confirmed the presence of restenosis of IJVs (Fig. 1). It was deemed that they were not candidates for repeat balloon angioplasty or stenting and were referred for open surgical jugular vein reconstruction. A segment of saphenous vein was harvested from the patients’ legs; it was incised longitudinally and it was shaped into an elongated patch. To obtain an optimal resolution of the IJV stenosis, the IJV incisions were carried down to their junction with the innominate vein. Full exposure of these anatomic structures required a collar incision and a short separate midline inverted-T superior ministernotomy, limited to the first intercostal space (Fig. 2). Under full heparinization, successive segments of the IJVs were clamped and a longitudinal incision was performed across the narrowed area of the anterior aspect of the stenotic IJVs. The venous valves and all potentially obstructing structures were excised (Fig. 3), and the incision was closed using the saphenous vein patch, thus relieving the stenosis by obtaining an enlargement of the vein caliber (Fig. 4). The heparin was reversed with protamine sulfate, the mini-sternotomy was approximated with steel wires, and the wound was
Fig. 2. Surgical view after upper mini-sternotomy. (A) Venous enlargement patch of the left internal jugular vein and (B) innominate vein.
closed in a routine fashion. All patients were started on anticoagulation therapy with warfarin on postoperative day 3, which was continued for 6 months, when it was substituted with an antiaggregant regimen with an oral daily dose of 150 mg of acetylsalicylic acid. There were no postoperative complications. CD ultrasound performed before discharge from the hospital showed patency of all treated vessels. Based on the
Vol.
-,
No.
-, -
2014
Fig. 3. Intraoperative image of the excision of the venous valves from the interior aspect of the right internal jugular vein.
evaluation performed by the hospital physiotherapy unit, patients already early postoperatively reported a decrease of fatigue, muscle weakness, spasticity, and vision disturbances; they experienced an improvement in gait, mobility, and balance; further, their mental acuity and neurogenic bowel and bladder dysfunction were improved (Table I). They were started on a physiotherapy rehabilitation program and they continued to present a gradual improvement of their symptomatology and disability. Follow-up at 1-year ascertained that the clinical benefits were maintained, while CD ultrasound and venography (Fig. 1) showed patency of the reconstructed veins.
DISCUSSION Evidence of the frequent association between CCSVI and MS has stimulated the performance of endovascular interventions designated to dilate the stenotic vessels, which have produced the regression of symptoms in several series of patients.6e11,15 Follow-up controls, however, have shown a substantial incidence of restenosis of the dilated vessels, causing a recurrence of symptoms in patients who,
Case Report 3
Fig. 4. Intraoperative image of the final result of internal jugular vein enlarged with a venous patch.
initially, had experienced a significant improvement in their condition after having been submitted to endovascular IJVs angioplasty for the treatment of CCSVI.10,15 The patients in our report had undergone angioplasty of the stenotic IJVs with favorable results that lasted for w3 months until they experienced the recurrence of symptomatology secondary to restenosis of the dilated vessels. All patients had already twice been submitted to repeat percutaneous transluminal angioplasty. It was therefore felt that repeating further balloon dilatation for restoring venous patency was not feasible because of the extensive intimal damage of the vessels. A stent implantation was excluded for the inherent high risk of thrombosis. After an extensive interdisciplinary discussion, it was therefore elected to perform a surgical reconstruction of the jugular veins using an autologous venous patch to increase the caliber of the vessel, thus ensuring an unimpeded blood flow. After the surgical procedure, the patients experienced a positive and durable improvement of MS symptoms. Because of the high thrombotic risk determined by the low velocity of the jugular venous flow, all patients were started on warfarin immediately after surgery. After consultation with hematology, this therapy was continued for 6 months and then
4 Case Report
Annals of Vascular Surgery
Table I. Postoperative symptoms’ improvement Muscle Patient Gender Age MS type Fatigue weakness Spasticity Gait
1 2 3
M M M
27 27 31
RR RR RR
++ +++ ++
+ ++ ++
++ +++ ++
Mobility and Mental Neurogenic Bladder Vision balance acuity bowel disfunction disturbances
+++ ++ +++ ++ +++ ++
+ ++ ++
++ + ++
++ ++ ++
++ +++ +++
+, small improvement; ++, moderate improvement; +++, big improvement; M, male; RR, relapsingeremitting.
substituted with antiaggregant therapy with acetylsalicylic acid when it was estimated that the endothelialization of the damaged intima had been achieved. To our knowledge, only 1 case in which an analogous surgical procedure after restenosis of a percutaneously treated jugular vein has been reported.12 Unlike the experience of Fankhauser et al.,12 who used a spiral vein graft to bypass the occluded IJV, we elected to perform an enlargement venoplasty of the IJVs that, in our patients, were stenotic but not occluded. The hypothesis concerning the association of CCSVI with MS is highly controversial.3e5 If its role in determining the neurologic disease and the efficacy of the correction of the venous pathology should be confirmed, endovascular dilatation of the stenotic vessels should represent the treatment of choice for this disease. However, surgery should only be considered when venous anatomic abnormalities have been clearly identified in patients who had obtained a temporary clinical benefit related to the endovascular procedure until a restenosis of the dilated vessels had occurred. In our institution we do not offer primary open surgical treatment for CCSVI, and we believe these interventions would be best conducted within controlled clinical trials. In conclusion, open surgical IJVs reconstruction is technically feasible in most cases of CCSVI, but our limited experience does not support its widespread use as the elective treatment for MS. Moreover, our relatively short follow-up does not allow definite conclusions regarding the relative durability of venous surgical reconstruction compared with the endovascular dilatation. Randomized controlled trials are needed to validate the safety and efficacy of venous intervention in CCSVI. REFERENCES 1. Zamboni P, Galeotti R, Menegatti E, et al. Chronic cerebrospinal venous insufficiency in patients with multiple sclerosis. J Neurol Neurosurg Psychiatry 2009;80:392e9.
2. Zamboni P, Consorti G, Galeotti R, et al. Venous collateral circulation of the extra-cranial cerebrospinal outflow routes. Curr Neurovasc Res 2009;6:204e12. 3. Awad AM, Marder E, Milo R, et al. Multiple sclerosis and chronic cerebrospinal venous insufficiency: a critical review. Ther Adv Neurol Disord 2011;4:231e5. 4. Baracchini C, Perini P, Calabrese M, et al. No evidence of chronic cerebrospinal venous insufficiency at multiple sclerosis onset. Ann Neurol 2011;69:90e9. 5. Blinkenberg M, Akeson P, Sillesen H, et al. Chronic cerebrospinal venous insufficiency and venous stenoses in multiple sclerosis. Acta Neurol Scand 2012;126:421e7. 6. Zamboni P, Galeotti R, Weinstock-Guttman B, et al. Venous angioplasty in patients with multiple sclerosis: results of a pilot study. Eur J Vasc Endovasc Surg 2012;43:116e22. 7. Zamboni P, Galeotti R, Menegatti E, et al. A prospective open-label study of endovascular treatment of chronic cerebrospinal venous insufficiency. J Vasc Surg 2009;50: 1348e58. 8. Mandato KD, Hegener PF, Siskin GP, et al. Safety of endovascular treatment of chronic cerebrospinal venous insufficiency: a report of 240 patients with multiple sclerosis. J Vasc Interv Radiol 2012;23:55e9. 9. Salvi F, Bartolomei I, Buccelato E, et al. Venous angioplasty in multiple sclerosis: neurological outcome at two years in a cohort of relapsing-remitting patients. Funct Neurol 2012;27:55e9. 10. Radak D, Kolar J, Sagic D, et al. Percutaneous angioplasty of internal jugular and azygous veins in patients with chronic cerebrospinal venous insufficiency and multiple sclerosis: early and mid-term results. Phlebology 2013 Apr 5 [Epub ahead of print]. 11. Hubbard D, Ponec D, Gooding J, et al. Clinical improvement after extracranial venoplasty in multiple sclerosis. J Vasc Interv Radiol 2012;23:1302e8. 12. Fankhauser GT, Stone WM, Fu R, et al. Spiral vein graft for internal jugular bypass in a patient with multiple sclerosis and suspected chronic cerebrospinal venous insufficiency. Ann Vasc Surg 2013;27:673.e5e8. 13. Polman CH, Reingold SC, Edan G, et al. Diagnostic criteria for multiple sclerosis: 2005 revisions to the ‘McDonald Criteria’. Ann Neurol 2005;58:840e6. 14. Nicolaides AN, Morovic S, Menegatti E, et al. Screening for chronic cerebrospinal venous insufficiency (CCSVI) using ultrasound: recommendations for a protocol. Funct Neurol 2011;26:229e48. 15. Simka M, Janas P, Ludyga T, et al. Endovascular treatment for chronic cerebrospinal venous insufficiency in patients with multiple sclerosis. Vascular Diseases Management 2012;9:149e54.
