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A Case of Endofibrosis Presenting with Embolic Symptoms in a 43-Year-Old Cyclist
A Case of Endofibrosis Presenting with Embolic Symptoms in a 43-Year-Old Cyclist Charles S. DeCarlo,1 Emily L. Spangler,2 and Jennifer A. Stableford,2 Boston, Massachusetts and Lebanon, New Hampshire
Background: Endofibrosis is a rare clinical entity that usually manifests as claudication in cyclists and other endurance athletes. We report a case of a 43-year-old cyclist presenting with pain and cyanosis of his toes due to an embolism to his left anterior tibial artery. The source of the embolus was found to be an ulcerated, endofibrotic plaque in his left common femoral artery. Methods: We performed an extensive literature search using the PubMed database and identified 60 results on endofibrosis. Eight articles described thrombosis relating to endofibrosis. None of the articles described an embolic phenomenon relating to endofibrosis. The following search terms were used: endofibrosis, embolic, emboli, embolism, ‘‘distal occlusion,’’ cyanosis, thrombosis, and thrombus. Results: The patient is a 43-year-old male cyclist who presented with pain and cyanosis of his second and third toes on his left foot for 1 week. The affected toes had a dark-purple discoloration involving the tissue overlying the distal phalanges. Computed tomography angiography showed an abrupt occlusion of the left anterior tibial artery in the mid-calf with a non-calcified plaque in the left common femoral artery. There were no other signs of arterial disease. He underwent left common femoral endofibrosectomy with patch angioplasty that revealed an ulcerated endofibrotic plaque with mural thrombus. Conclusions: This case demonstrates an unusual presentation of a rare clinical entity. While there have been previous reports of thrombosis associated with endofibrosis, to our knowledge this is the first reported case of endofibrosis presenting with embolic symptoms.
Endofibrosis is a nonatherosclerotic arteriopathy that affects cyclists and other endurance athletes. Despite having minimal or no cardiovascular risk factors, young, highly trained athletes develop flow-limiting lesions in the external iliac, common iliac, or common femoral artery that manifest as unilateral claudication during maximal effort. These
1 Division of Vascular and Endovascular Surgery, Massachusetts General Hospital, Boston, MA. 2 Division of Vascular Surgery, Dartmouth-Hitchcock Medical Center, Lebanon, NH.
Correspondence to: Charles S. DeCarlo, MD, Division of Vascular and Endovascular Surgery, Massachusetts General Hospital, GRB425, Boston, MA 02214, USA; E-mail: [email protected] Ann Vasc Surg 2016; 36: 292.e5–292.e8 http://dx.doi.org/10.1016/j.avsg.2016.03.019 Ó 2016 Elsevier Inc. All rights reserved. Manuscript received: September 28, 2015; manuscript accepted: March 11, 2016; published online: 15 July 2016
lesions can occasionally be complicated by thrombosis or dissection.
CASE REPORT The patient is a 43-year-old man who presented with a 1-week history of pain and intermittent cyanosis of his left second and third toes. He reported having similar mild symptoms since 2007, but came for evaluation after the symptoms became severe over the past week. The pain and cyanosis were precipitated by cold weather and elevation of his foot. Nothing relieved the pain and there are no other associated symptoms; there was no inciting event that the patient could identify. He is an avid cyclist, partaking in amateur competition, cycling 4e8 hr/week since 2004. His total mileage most likely ranged from 50,000 to 100,000 total miles. He has a past medical history of hypertension and hyperlipidemia. He is a former smoker with a 16-pack-year history who quit 11 years ago. 292.e5
292.e6 Case reports
Annals of Vascular Surgery
Fig. 1. CT angiogram showing heterogeneous plaque in the left common femoral artery (red arrow).
Fig. 3. Arteriotomy revealing a thickened, endofibrotic intima with a large ulceration of the posterior wall.
Fig. 2. Three-dimensional reconstruction showing abrupt occlusion of the left anterior tibial artery. On physical examination, the patient is a fit, wellappearing man. His femoral, popliteal, dorsalis pedis, and posterior tibial pulses were intact, bilaterally. There was purple discoloration of the left second and third toes from the tip to distal interphalangeal joint. Noninvasive studies revealed an ankleebrachial index of 1.22 on the right and 1.20 on the left; however, his toee brachial index was 1.11 on the right and 0.38 on the left, suggesting a possible distal occlusion on the left. A computed tomography (CT) angiogram was obtained which showed an occlusion of the left anterior tibial artery in the mid-calf and an atheromatous-appearing plaque with intraluminal thrombus in the left common femoral artery (Figs. 1 and 2). The anterior tibial artery appeared normal, proximal to the occlusion and there were no other signs of arterial disease. The patient was diagnosed with an embolic occlusion of his left anterior tibial artery. The source was thought to either be endofibrosis of the left common femoral artery with mural thrombus or an aneurysmal left common femoral artery with endoluminal thrombus formation. The patient opted to undergo surgical intervention to remove the source to prevent further emboli. The left common femoral artery was dilated in the mid-portion with normal artery proximally and distally. Arteriotomy of the common femoral artery
Fig. 4. Resected ulcerated endofibrotic plaque.
revealed a thickened, endofibrotic intima with a large ulceration of the posterior wall containing endoluminal thrombus (Fig. 3). Endofibrosectomy was performed (Fig. 4) and the artery was closed using a bovine pericardial patch. The plaque was sent for pathology with sections. Histology of the specimen showed ‘‘thickening and fibroplasia of the intima. There is an overlying thrombus consisting of fibrin with scattered macrophages and lymphoplasmacytic inflammation but without typical atherosclerotic findings.’’ From pathology report: ‘‘Interpretation is that of arterial endofibrosis in the context of a 43-year-old man who is a competitive cyclist.’’ The patient returned to clinic 6 months postoperatively. He had returned to his full complement of physical activity, including cycling, running, and swimming, without thigh claudication. He has some residual cramping in the anterior compartment of his left leg with strenuous exercise. He continues to take aspirin and cilostazol, which he was prescribed postoperatively. He will followup again at 1 year, postoperatively, and then annually with a duplex of both femoral arteries.
Volume 36, October 2016
DISCUSSION Endofibrosis affects the external iliac artery in 90% of cases. Other possible locations include the common iliac artery, the common femoral artery, and the profunda femoris.1 Symptoms occur more commonly on the left side.2 First reported in 1985, it is most commonly described in cyclists; however, it has also been identified in speed skaters, endurance runners, triathletes, rugby players, soccer players, cross country skiers, and body-builders.3 Cyclists who undergo surgical intervention have cycled for a mean of 14 years and a total of 210,000 km.4 Over 90% of cases are seen in men, but this is most likely reflective of the prevalence of men participating in endurance sports as opposed to a real gender bias.3 While this patient’s total mileage is less than reported in the aforementioned series, his history still represents a significant amount of time and mileage. Endofibrosis occurs due to thickening of the vessel intima that manifests as a stenosis of the vessel lumen as the condition progresses. The disease process is distinct from atherosclerosis and the differences can be appreciated histologically. Loose collagen fibers, a moderate to large number of spindle and stellate cells, and a lack of inflammation, calcification, or atheroma characterize endofibrosis, histologically, while atherosclerosis is characterized by compact, acellular connective tissue, with inflammatory cells, calcification, and atheroma.5 Multiple factors, including psoas hypertrophy, arterial fixation, and excessive arterial length, have been implicated in the development of endofibrosis. Psoas hypertrophy, which increases the arterial displacement during hip flexion, can exacerbate kinking and increase mechanical stress on the artery. Arterial fixation prevents mobility of the artery during hip flexion, which exacerbates the traumatic effect of hyperflexion. Excessive arterial length is thought to facilitate kinking of the artery.3 While all the aforementioned proposed etiologies implicate reactive thickening as the pathogenesis of endofibrosis, the natural development of the disease is unknown. The most common presenting symptoms are lack of power, numbness, cramping, pain, or fatigue affecting the thigh at maximum effort and symptoms are relieved by rest.6,7 Less commonly, patients may develop subacute ischemia, due to thrombosis of the endofibrotic lesion, and present with intermittent claudication while walking.1,7e9 To our knowledge, however, embolism has not been reported as a complication of endofibrosis in the literature. Embolism has been observed in other trauma-related arteriopathies such a
Case reports 292.e7
hypothenar hammer syndrome, which most commonly presents with symptoms of digital artery occlusion due to emboli originating in the ulnar artery.10 Postexercise ankleebrachial index is an important diagnostic tool. A decrease in ankleebrachial indices after maximal effort on a stationary bike below 0.5 is 87% sensitive and 90% specific for detecting a moderate arterial lesion.1 Although controversial, angiography is generally considered the best means of diagnosis in terms of imaging. The diagnosis can be made with CT angiography, magnetic resonance angiography, or ultrasound, but there is a higher probability of a false negative result.11 Conservative therapy should be offered and attempted before surgical intervention. This ranges from changing the position of the cyclist’s handlebars and seat and avoiding maximal effort to avoiding cycling altogether.12 Competitive cyclists are generally not amenable to the latter option. Open surgical intervention is the preferred method of definite treatment. The two most commonly utilized methods of repair are endofibrosectomy with patch angioplasty or interposition grafting.1 Percutaneous balloon angioplasty may be utilized when shortterm relief is needed, but patients usually have a recurrence of symptoms within 8 weeks of treatment.13 We recommend initial therapy of conservative treatment for lesions causing claudication in the absence of embolization. In cases of embolization with residual ulcerated endofibrotic lesions present on imaging, surgical intervention is warranted to remove the embolic source.
CONCLUSION This case represents a previously unreported presentation of a rare clinical entity. When endoluminal thrombus develops in a patient with endofibrosis, there is a risk of embolism. The diagnosis of endofibrosis should be considered in any highly trained endurance athlete who presents with distal occlusive symptoms. REFERENCES 1. Feugier P, Chevalier JM. Endofibrosis of the iliac arteries: an underestimated problem. Acta Chir Belg 2003;104:635e40. 2. Rouviere O, Feugier P, Gutierrez JP, Chevalier JM. Arterial endofibrosis in endurance athletes: angiographic features and classification. Radiology 2014;273:294e303. 3. Peach G, Schep G, Palfreeman R, et al. Endofibrosis and kinking of the iliac arteries in athletes: a systematic review. Eur J Vasc Endovasc Surg 2012;43:208e17. 4. Bender MHM, Schep G, Bouts SW, et al. Endurance athletes with intermittent claudication caused by iliac artery stenosis treated by endarterectomy with vein patchdshort-
292.e8 Case reports
5.
6.
7.
8. 9.
and mid-term results. Eur J Vasc Endovasc Surg 2012;43: 472e7. Vink A, Bender MH, Schep G, et al. Histopathological comparison between endofibrosis of the high-performance cyclist and atherosclerosis in the external iliac artery. J Vasc Surg 2008;48:1458e63. Schep G, Bender MHM, Van de Tempel G, et al. Detection and treatment of claudication due to functional iliac obstruction in top endurance athletes: a prospective study. Lancet 2002;359:466e73. Bucci F, Ottaviani N, Plagnol P. Acute thrombosis of external iliac artery secondary to endofibrosis. Ann Vasc Surg 2011;25:698.e5. Venstermans C, Gielen JL, Salgado R, et al. Endofibrosis of the external iliac artery. J Belg Radiol 2009;92:184. van Rensburg DCJ, van Rensburg AJ, van Duuren EM, Grant CC. Iliac artery endofibrosis in a middle-aged female
Annals of Vascular Surgery
10.
11.
12.
13.
long-distance runner. Am J Phys Med Rehabil 2014;93: 1100e3. Larsen BT, Edwards WD, Jensen MH, et al. Surgical pathology of hypothenar hammer syndrome with new pathogenetic insights: a 25-year institutional experience with clinical and pathologic review of 67 cases. Am J Surg Pathol 2013;37:1700e8. Flors L, Leiva-Salinas C, Bozlar U, et al. Imaging evaluation of flow limitations in the iliac arteries in endurance athletes: diagnosis and treatment follow-up. Am J Roentgenol 2011;197:W948e55. Lindner D, Agar G, Domb BG, et al. An unusual case of leg pain in a competitive cyclist: a case report and review of the literature. Sports Health 2014;6:492e6. Wijesinghe LD, Coughlin PA, Robertson I, et al. Cyclist’s iliac syndrome: temporary relief by balloon angioplasty. Br J Sports Med 2001;35:70e1.
Background: Endofibrosis is a rare clinical entity that usually manifests as claudication in cyclists and other endurance athletes. We report a case of a 43-year-old cyclist presenting with pain and cyanosis of his toes due to an embolism to his left anterior tibial artery. The source of the embolus was found to be an ulcerated, endofibrotic plaque in his left common femoral artery. Methods: We performed an extensive literature search using the PubMed database and identified 60 results on endofibrosis. Eight articles described thrombosis relating to endofibrosis. None of the articles described an embolic phenomenon relating to endofibrosis. The following search terms were used: endofibrosis, embolic, emboli, embolism, ‘‘distal occlusion,’’ cyanosis, thrombosis, and thrombus. Results: The patient is a 43-year-old male cyclist who presented with pain and cyanosis of his second and third toes on his left foot for 1 week. The affected toes had a dark-purple discoloration involving the tissue overlying the distal phalanges. Computed tomography angiography showed an abrupt occlusion of the left anterior tibial artery in the mid-calf with a non-calcified plaque in the left common femoral artery. There were no other signs of arterial disease. He underwent left common femoral endofibrosectomy with patch angioplasty that revealed an ulcerated endofibrotic plaque with mural thrombus. Conclusions: This case demonstrates an unusual presentation of a rare clinical entity. While there have been previous reports of thrombosis associated with endofibrosis, to our knowledge this is the first reported case of endofibrosis presenting with embolic symptoms.
Endofibrosis is a nonatherosclerotic arteriopathy that affects cyclists and other endurance athletes. Despite having minimal or no cardiovascular risk factors, young, highly trained athletes develop flow-limiting lesions in the external iliac, common iliac, or common femoral artery that manifest as unilateral claudication during maximal effort. These
1 Division of Vascular and Endovascular Surgery, Massachusetts General Hospital, Boston, MA. 2 Division of Vascular Surgery, Dartmouth-Hitchcock Medical Center, Lebanon, NH.
Correspondence to: Charles S. DeCarlo, MD, Division of Vascular and Endovascular Surgery, Massachusetts General Hospital, GRB425, Boston, MA 02214, USA; E-mail: [email protected] Ann Vasc Surg 2016; 36: 292.e5–292.e8 http://dx.doi.org/10.1016/j.avsg.2016.03.019 Ó 2016 Elsevier Inc. All rights reserved. Manuscript received: September 28, 2015; manuscript accepted: March 11, 2016; published online: 15 July 2016
lesions can occasionally be complicated by thrombosis or dissection.
CASE REPORT The patient is a 43-year-old man who presented with a 1-week history of pain and intermittent cyanosis of his left second and third toes. He reported having similar mild symptoms since 2007, but came for evaluation after the symptoms became severe over the past week. The pain and cyanosis were precipitated by cold weather and elevation of his foot. Nothing relieved the pain and there are no other associated symptoms; there was no inciting event that the patient could identify. He is an avid cyclist, partaking in amateur competition, cycling 4e8 hr/week since 2004. His total mileage most likely ranged from 50,000 to 100,000 total miles. He has a past medical history of hypertension and hyperlipidemia. He is a former smoker with a 16-pack-year history who quit 11 years ago. 292.e5
292.e6 Case reports
Annals of Vascular Surgery
Fig. 1. CT angiogram showing heterogeneous plaque in the left common femoral artery (red arrow).
Fig. 3. Arteriotomy revealing a thickened, endofibrotic intima with a large ulceration of the posterior wall.
Fig. 2. Three-dimensional reconstruction showing abrupt occlusion of the left anterior tibial artery. On physical examination, the patient is a fit, wellappearing man. His femoral, popliteal, dorsalis pedis, and posterior tibial pulses were intact, bilaterally. There was purple discoloration of the left second and third toes from the tip to distal interphalangeal joint. Noninvasive studies revealed an ankleebrachial index of 1.22 on the right and 1.20 on the left; however, his toee brachial index was 1.11 on the right and 0.38 on the left, suggesting a possible distal occlusion on the left. A computed tomography (CT) angiogram was obtained which showed an occlusion of the left anterior tibial artery in the mid-calf and an atheromatous-appearing plaque with intraluminal thrombus in the left common femoral artery (Figs. 1 and 2). The anterior tibial artery appeared normal, proximal to the occlusion and there were no other signs of arterial disease. The patient was diagnosed with an embolic occlusion of his left anterior tibial artery. The source was thought to either be endofibrosis of the left common femoral artery with mural thrombus or an aneurysmal left common femoral artery with endoluminal thrombus formation. The patient opted to undergo surgical intervention to remove the source to prevent further emboli. The left common femoral artery was dilated in the mid-portion with normal artery proximally and distally. Arteriotomy of the common femoral artery
Fig. 4. Resected ulcerated endofibrotic plaque.
revealed a thickened, endofibrotic intima with a large ulceration of the posterior wall containing endoluminal thrombus (Fig. 3). Endofibrosectomy was performed (Fig. 4) and the artery was closed using a bovine pericardial patch. The plaque was sent for pathology with sections. Histology of the specimen showed ‘‘thickening and fibroplasia of the intima. There is an overlying thrombus consisting of fibrin with scattered macrophages and lymphoplasmacytic inflammation but without typical atherosclerotic findings.’’ From pathology report: ‘‘Interpretation is that of arterial endofibrosis in the context of a 43-year-old man who is a competitive cyclist.’’ The patient returned to clinic 6 months postoperatively. He had returned to his full complement of physical activity, including cycling, running, and swimming, without thigh claudication. He has some residual cramping in the anterior compartment of his left leg with strenuous exercise. He continues to take aspirin and cilostazol, which he was prescribed postoperatively. He will followup again at 1 year, postoperatively, and then annually with a duplex of both femoral arteries.
Volume 36, October 2016
DISCUSSION Endofibrosis affects the external iliac artery in 90% of cases. Other possible locations include the common iliac artery, the common femoral artery, and the profunda femoris.1 Symptoms occur more commonly on the left side.2 First reported in 1985, it is most commonly described in cyclists; however, it has also been identified in speed skaters, endurance runners, triathletes, rugby players, soccer players, cross country skiers, and body-builders.3 Cyclists who undergo surgical intervention have cycled for a mean of 14 years and a total of 210,000 km.4 Over 90% of cases are seen in men, but this is most likely reflective of the prevalence of men participating in endurance sports as opposed to a real gender bias.3 While this patient’s total mileage is less than reported in the aforementioned series, his history still represents a significant amount of time and mileage. Endofibrosis occurs due to thickening of the vessel intima that manifests as a stenosis of the vessel lumen as the condition progresses. The disease process is distinct from atherosclerosis and the differences can be appreciated histologically. Loose collagen fibers, a moderate to large number of spindle and stellate cells, and a lack of inflammation, calcification, or atheroma characterize endofibrosis, histologically, while atherosclerosis is characterized by compact, acellular connective tissue, with inflammatory cells, calcification, and atheroma.5 Multiple factors, including psoas hypertrophy, arterial fixation, and excessive arterial length, have been implicated in the development of endofibrosis. Psoas hypertrophy, which increases the arterial displacement during hip flexion, can exacerbate kinking and increase mechanical stress on the artery. Arterial fixation prevents mobility of the artery during hip flexion, which exacerbates the traumatic effect of hyperflexion. Excessive arterial length is thought to facilitate kinking of the artery.3 While all the aforementioned proposed etiologies implicate reactive thickening as the pathogenesis of endofibrosis, the natural development of the disease is unknown. The most common presenting symptoms are lack of power, numbness, cramping, pain, or fatigue affecting the thigh at maximum effort and symptoms are relieved by rest.6,7 Less commonly, patients may develop subacute ischemia, due to thrombosis of the endofibrotic lesion, and present with intermittent claudication while walking.1,7e9 To our knowledge, however, embolism has not been reported as a complication of endofibrosis in the literature. Embolism has been observed in other trauma-related arteriopathies such a
Case reports 292.e7
hypothenar hammer syndrome, which most commonly presents with symptoms of digital artery occlusion due to emboli originating in the ulnar artery.10 Postexercise ankleebrachial index is an important diagnostic tool. A decrease in ankleebrachial indices after maximal effort on a stationary bike below 0.5 is 87% sensitive and 90% specific for detecting a moderate arterial lesion.1 Although controversial, angiography is generally considered the best means of diagnosis in terms of imaging. The diagnosis can be made with CT angiography, magnetic resonance angiography, or ultrasound, but there is a higher probability of a false negative result.11 Conservative therapy should be offered and attempted before surgical intervention. This ranges from changing the position of the cyclist’s handlebars and seat and avoiding maximal effort to avoiding cycling altogether.12 Competitive cyclists are generally not amenable to the latter option. Open surgical intervention is the preferred method of definite treatment. The two most commonly utilized methods of repair are endofibrosectomy with patch angioplasty or interposition grafting.1 Percutaneous balloon angioplasty may be utilized when shortterm relief is needed, but patients usually have a recurrence of symptoms within 8 weeks of treatment.13 We recommend initial therapy of conservative treatment for lesions causing claudication in the absence of embolization. In cases of embolization with residual ulcerated endofibrotic lesions present on imaging, surgical intervention is warranted to remove the embolic source.
CONCLUSION This case represents a previously unreported presentation of a rare clinical entity. When endoluminal thrombus develops in a patient with endofibrosis, there is a risk of embolism. The diagnosis of endofibrosis should be considered in any highly trained endurance athlete who presents with distal occlusive symptoms. REFERENCES 1. Feugier P, Chevalier JM. Endofibrosis of the iliac arteries: an underestimated problem. Acta Chir Belg 2003;104:635e40. 2. Rouviere O, Feugier P, Gutierrez JP, Chevalier JM. Arterial endofibrosis in endurance athletes: angiographic features and classification. Radiology 2014;273:294e303. 3. Peach G, Schep G, Palfreeman R, et al. Endofibrosis and kinking of the iliac arteries in athletes: a systematic review. Eur J Vasc Endovasc Surg 2012;43:208e17. 4. Bender MHM, Schep G, Bouts SW, et al. Endurance athletes with intermittent claudication caused by iliac artery stenosis treated by endarterectomy with vein patchdshort-
292.e8 Case reports
5.
6.
7.
8. 9.
and mid-term results. Eur J Vasc Endovasc Surg 2012;43: 472e7. Vink A, Bender MH, Schep G, et al. Histopathological comparison between endofibrosis of the high-performance cyclist and atherosclerosis in the external iliac artery. J Vasc Surg 2008;48:1458e63. Schep G, Bender MHM, Van de Tempel G, et al. Detection and treatment of claudication due to functional iliac obstruction in top endurance athletes: a prospective study. Lancet 2002;359:466e73. Bucci F, Ottaviani N, Plagnol P. Acute thrombosis of external iliac artery secondary to endofibrosis. Ann Vasc Surg 2011;25:698.e5. Venstermans C, Gielen JL, Salgado R, et al. Endofibrosis of the external iliac artery. J Belg Radiol 2009;92:184. van Rensburg DCJ, van Rensburg AJ, van Duuren EM, Grant CC. Iliac artery endofibrosis in a middle-aged female
Annals of Vascular Surgery
10.
11.
12.
13.
long-distance runner. Am J Phys Med Rehabil 2014;93: 1100e3. Larsen BT, Edwards WD, Jensen MH, et al. Surgical pathology of hypothenar hammer syndrome with new pathogenetic insights: a 25-year institutional experience with clinical and pathologic review of 67 cases. Am J Surg Pathol 2013;37:1700e8. Flors L, Leiva-Salinas C, Bozlar U, et al. Imaging evaluation of flow limitations in the iliac arteries in endurance athletes: diagnosis and treatment follow-up. Am J Roentgenol 2011;197:W948e55. Lindner D, Agar G, Domb BG, et al. An unusual case of leg pain in a competitive cyclist: a case report and review of the literature. Sports Health 2014;6:492e6. Wijesinghe LD, Coughlin PA, Robertson I, et al. Cyclist’s iliac syndrome: temporary relief by balloon angioplasty. Br J Sports Med 2001;35:70e1.