Acta Neurochir (2015) 157:1113–1116 DOI 10.1007/s00701-015-2428-2
CASE REPORT - VASCULAR
Acute subdural hematoma caused by a ruptured cavernous internal carotid artery giant aneurysm following abducens nerve palsy: case report and review of the literature Hideaki Shigematsu 1 & Takatoshi Sorimachi 1 & Rie Aoki 1 & Takahiro Osada 1 & Kittipong Srivatanakul 1 & Mitsunori Matsumae 1
Received: 3 March 2015 / Accepted: 14 April 2015 / Published online: 7 May 2015 # Springer-Verlag Wien 2015
Abstract The authors report a 61-year-old female patient with a giant cavernous aneurysm in the right internal carotid artery (ICA) leading to acute subdural hematoma (ASDH) 7 days after the occurrence of abducens nerve palsy. She underwent ICA occlusion associated with high-flow bypass. In all five reported patients with a cavernous ICA aneurysm causing ASDH, the size of the aneurysm was giant and cranial nerve signs preceded the rupture. When a patient with a symptomatic cavernous ICA giant aneurysm experiences suddenonset headache and/or consciousness disturbance, rupture of the aneurysm should be differentiated, even though a cavernous ICA aneurysm rarely causes ASDH. Keywords Acute subdural hematoma . Cavernous sinus syndrome . Magnetic resonance image . Oculomotor nerve palsy
Introduction Aneurysms of the cavernous portion of the internal carotid artery (ICA) are usually disclosed by the compressive symptoms, including cavernous sinus syndrome, and are rarely associated with hemorrhage because of the restraining support of the cavernous sinus dura [4, 6]. If rupture of the aneurysm does occur, it usually results in a carotid-cavernous fistula [12]. Previous studies reported that a life-threatening event seldom occurred in patients with cavernous ICA aneurysms * Takatoshi Sorimachi [email protected] 1
Department of Neurosurgery, Tokai University, 143, Simokasuya, Isehara, Kanagawa 259-1194, Japan
[4, 6]. Reports of rupture leading to intracranial hemorrhage, including subarachnoid hemorrhage, intracerebral hemorrhage, and subdural hematoma, are anecdotal [1–3, 5, 7]. Only four cases of acute subdural hematomas (ASDH) caused by ruptured cavernous ICA aneurysms have been reported [1–3, 7]. We report a case of a ruptured cavernous ICA aneurysm causing ASDH 7 days after occurrence of abducens nerve palsy and review the literature.
Case report This 61-year-old female presented to our hospital by ambulance with sudden-onset headache, nausea, vomiting, and transient consciousness disturbance that had occurred during calculation at home. She had a history of diplopia and mild headache 7 days before admission. She visited a local hospital 2 days later and showed right abducens nerve palsy. Computed tomography (CT) and magnetic resonance (MR) imaging performed in the local hospital revealed a giant partially thrombosed aneurysm in the cavernous portion of the right ICA without any apparent hemorrhage (Fig. 1a). In the local hospital, surgery for the cavernous ICA aneurysm could not be performed; therefore, she stayed at home to wait to visit another hospital as a referred outpatient. At admission to our hospital, she showed right complete oculomotor and right abducens nerve palsy. CT demonstrated a right cavernous ICA aneurysm with a maximum diameter of 35 mm and slight high density in the right cerebellar tentorium (Fig. 1b). MR imaging revealed a thin subdural hematoma in the posterior fossa and right cerebral convexity (Fig. 2). Cerebral angiography demonstrated a right cavernous ICA partially thrombosed aneurysm (Fig. 3). Cerebral angiography performed under right ICA manual compression revealed poor collateral flows from the left ICA through the anterior
1114
Acta Neurochir (2015) 157:1113–1116
Fig. 3 Cerebral angiograms. a A preoperative right internal carotid angiogram showing a partially thrombosed aneurysm in the cavernous portion of the right internal carotid artery (ICA). b A postoperative right common carotid angiogram demonstrating disappearance of the aneurysm associated with therapeutic ICA occlusion. The intracranial territory of the right ICA is supplied by a bypass graft from the external carotid artery to the M2 inferior trunk of the middle cerebral artery
of the middle cerebral artery using a radial artery graft to prevent ischemic complications (Fig. 3b). Postoperatively, the right abducens nerve palsy improved, although the occluomotor nerve palsy remained. The patient was discharged 4 weeks after the admission and returned to her previous life. Fig. 1 Computed tomography (CT) showing a right cavernous aneurysm. a A CT performed at the first local hospital shows no apparent hemorrhage. b A CT at admission to our hospital demonstrates a high-density lesion in the retrosellar portion (arrows), which indicates either a part of the aneurysm or a small subdural hematoma. Faint high density is noticed along the right cerebellar tentorium (arrows)
communicating artery and from the vertebro-basilar artery through the right posterior communicating artery. The results of the cerebral angiography suggested a high risk of cerebral infarction if simple ICA occlusion was selected for treatment of the aneurysm. Three days after admission, she underwent ICA occlusion at the cervical ICA orifice associated with high-flow bypass. Bypass surgery was performed between the right external carotid artery orifice and M2 inferior trunk
Fig. 2 A magnetic resonance (MR) image/fluid attenuated inversion recovery (FLAIR) at admission showing a right giant partially thrombosed aneurysm in the cavernous sinus. A thin subdural hematoma
Discussion The present patient with a ruptured cavernous ICA aneurysm causing ASDH had both a giant aneurysm and a preceding cavernous sinus syndrome. These two features were consistent with the previous reported four patients with a ruptured cavernous ICA aneurysm leading to ASDH [1–3, 7]. Table 1 shows characteristics of the five patients, including the present case, with a cavernous ICA aneurysm causing ASDH. The following mechanism was speculated to explain the occurrence of rupture after preceding cranial nerve signs in a giant aneurysm. As a cavernous ICA aneurysm enlarges, it extends
is demonstrated in the right retropetrous portion (a, arrows), the retrosellar portion (b, arrows), and the right cerebral convexity (c, arrows)
Acta Neurochir (2015) 157:1113–1116 Table 1
1115
Characteristics of five reported patients with a cavernous aneurysm causing acute subdural hematoma
Reference
Age/sex
*HT
Nationality
Preceding cranial nerve symptoms (duration)
Aneurysm size
Barr et al. [2], 1971
59/F
Yes
UK
35 mm (post-mortem)
Hodes et al. [3], 1988
62/F
No
USA
6th nerve (5 years) 5th nerve (a few days) 5th and 6th nerves (2 days)
Mclaughlin et al. [7], 1996
48/F
Yes
USA
3rd–6th nerves (5 days)
Andaluz et al. [1], 2006 Present case
33/F 61/F
n.a. No
USA Japan
Ophthalmoplegia (2 weeks) 6th nerve (7 days)
n.a. Giant n.a. Giant 26 mm 35 mm
*HT: hypertension
into the cavernous sinus and compresses the cranial nerves passing through the cavernous sinus, which can cause cavernous sinus syndrome [4, 6]. After the cavernous sinus is filled with the aneurysm, the aneurysm expands the cavernous sinus dura; then, the aneurysm can break a weak part of the cavernous sinus dura, which is presumably related to passages of cranial nerves. Thereafter, if the aneurysm ruptures, bleeding from the aneurysm results in ASDH. Hence, all the reported five patients, including the present patient, with a ruptured cavernous ICA aneurysm causing ASDH had both giant aneurysms and preceding cranial nerve signs. Symptoms of these reported patients at the rupture of the aneurysm were sudden-onset headache and/or consciousness disturbance [1–3, 7]. Although life-threatening events were seldom reported in the previous studies [4, 6], when a patient with a cavernous ICA giant aneurysm showing a preceding cavernous sinus syndrome experiences sudden-onset headache and/or consciousness disturbance, rupture of the aneurysm resulting in ASDH should be differentiated. Considering that two of the five reported patients died of ASDH, early surgery to prevent rerupture from an aneurysm must be performed in patients with an ASDH [2, 3]. The preceding symptoms were observed in all five patients [1–3, 7], suggesting that surgery should not be performed in patients with an asymptomatic cavernous ICA aneurysm to prevent ASDH [4, 6]. In the three patients undergoing surgery, ICA occlusion was selected to treat the aneurysms [1, 7]. In two patients without bypass surgery, transient hemiparesis caused by cerebral infarction occurred after the ICA occlusion [1, 7]. High-flow bypass associated with ICA occlusion is necessary to prevent ischemic complication when a poor collateral flow has been observed on preoperative angiograms. In terms of endovascular therapy for a symptomatic cavernous ICA aneurysm, intraaneurysmal coil embolization, with or without stent assist, can seldom obtain complete improvement of the cavernous sinus syndrome [8]. Recently, a flow diverter stent has been reported to treat an unruptured giant symptomatic cavernous ICA aneurysm effectively [10]; however, early aneurysm rupture after treatment has been described [11]. In case of a ruptured aneurysm, because of both
continuous blood flow into the aneurysm without intraaneurysmal pressure reduction immediately after device deployment [9] and the necessity of antiplatelet use during the perioperative period, prompt prevention of the aneurysmal rerupture could not be obtained. Therefore, ICA occlusion with high-flow bypass seems to be the first choice treatment for ruptured giant cavernous ICA aneurysms. Patient consent-case reports The patient consented to submission of this case report to the journal. Conflict of interest All authors certify that they have no affiliations with or involvement in any organization or entity with any financial interest (such as honoraria; educational grants; participation in speakers’ bureaus; membership, employment, consultancies, stock ownership, or other equity interest; and expert testimony or patent-licensing arrangements), or non-financial interest (such as personal or professional relationships, affiliations, knowledge or beliefs) in the subject matter or materials discussed in this manuscript.
References 1.
2.
3.
4.
5.
6.
7.
Andaluz N, Tomsick TA, Keller JT, Zuccarello M (2006) Subdural hemorrhage in the posterior fossa caused by a ruptured cavernous carotid artery aneurysm after a balloon occlusion test. Case report. J Neurosurg 105:315–319 Barr HWK, Blackwood W, Meadows SP (1971) Intracavernous carotid aneurysms. A clinical-pathological report. Brain 94:607– 622 Hodes JE, Fletcher WA, Goodman DF, Hoyt WF (1988) Rupture of cavcavernous carotid artery aneurysm causing subdural hematoma and death. Case report. J Neurosurg 69:617–619 Kupersmith MJ, Hurst R, Berenstein A, Choi IS, Jafar J, Ransohoff J (1992) The benign course of cavernous carotid artery aneurysms. J Neurosurg 77:690–693 Lee AG, Mawad ME, Baskin DS (1996) Fatal subarachnoid hemorrhage from the rupture of a totally intracavernous carotid artery aneurysm: case report. Neurosurgery 38:596–599 Linskey ME, Sekhar LN, Hirsch WL Jr, Yonas H, Horton JA (1990) Aneurysms of the intracavernous carotid artery: natural history and indications for treatment. Neurosurgery 26:933–938 McLaughlin MR, Jho HD, Kwon Y (1996) Acute subdural hematoma caused by a ruptured giant intracavernous aneurysm: case report. Neurosurgery 38:388–392
1116 8.
9.
10.
Acta Neurochir (2015) 157:1113–1116 Morita K, Sorimachi T, Ito Y, Nishino K, Jimbo Y, Kumagai T et al (2011) Intra-aneurysmal coil embolization for large or giant carotid artery aneurysms in the cavernous sinus. Neurol Med Chir (Tokyo) 51:762–766 Schneiders JJ, VanBavel E, Majoie CB, Ferns SP, van den Berg R (2013) A flow-diverting stent is not a pressure-diverting stent. AJNR Am J Neuroradiol 34:E1–E4 Szikora I, Berentei Z, Kulcsar Z, Marosfoi M, Vajda ZS et al (2010) Treatment of intracranial aneurysms by functional reconstruction of the parent artery: the Budapest
experience with the pipeline embolization device. AJNR Am J Neuroradiol 31:1139–1147 11. Turowski B, Macht S, Kulcsár Z, Hänggi D, Stummer W (2011) Early fatal hemorrhage after endovascular cerebral aneurysm treatment with a flow diverter (SILK-Stent): do we need to rethink our concepts? Neuroradiology 53:37–41 12. van Rooij WJ, Sluzewski M, Beute GN (2006) Ruptured cavernous sinus aneurysms causing carotid cavernous fistula: incidence, clinical presentation, treatment, and outcome. AJNR Am J Neuroradiol 27:185–189
Copyright of Acta Neurochirurgica is the property of Springer Science & Business Media B.V. and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.
CASE REPORT - VASCULAR
Acute subdural hematoma caused by a ruptured cavernous internal carotid artery giant aneurysm following abducens nerve palsy: case report and review of the literature Hideaki Shigematsu 1 & Takatoshi Sorimachi 1 & Rie Aoki 1 & Takahiro Osada 1 & Kittipong Srivatanakul 1 & Mitsunori Matsumae 1
Received: 3 March 2015 / Accepted: 14 April 2015 / Published online: 7 May 2015 # Springer-Verlag Wien 2015
Abstract The authors report a 61-year-old female patient with a giant cavernous aneurysm in the right internal carotid artery (ICA) leading to acute subdural hematoma (ASDH) 7 days after the occurrence of abducens nerve palsy. She underwent ICA occlusion associated with high-flow bypass. In all five reported patients with a cavernous ICA aneurysm causing ASDH, the size of the aneurysm was giant and cranial nerve signs preceded the rupture. When a patient with a symptomatic cavernous ICA giant aneurysm experiences suddenonset headache and/or consciousness disturbance, rupture of the aneurysm should be differentiated, even though a cavernous ICA aneurysm rarely causes ASDH. Keywords Acute subdural hematoma . Cavernous sinus syndrome . Magnetic resonance image . Oculomotor nerve palsy
Introduction Aneurysms of the cavernous portion of the internal carotid artery (ICA) are usually disclosed by the compressive symptoms, including cavernous sinus syndrome, and are rarely associated with hemorrhage because of the restraining support of the cavernous sinus dura [4, 6]. If rupture of the aneurysm does occur, it usually results in a carotid-cavernous fistula [12]. Previous studies reported that a life-threatening event seldom occurred in patients with cavernous ICA aneurysms * Takatoshi Sorimachi [email protected] 1
Department of Neurosurgery, Tokai University, 143, Simokasuya, Isehara, Kanagawa 259-1194, Japan
[4, 6]. Reports of rupture leading to intracranial hemorrhage, including subarachnoid hemorrhage, intracerebral hemorrhage, and subdural hematoma, are anecdotal [1–3, 5, 7]. Only four cases of acute subdural hematomas (ASDH) caused by ruptured cavernous ICA aneurysms have been reported [1–3, 7]. We report a case of a ruptured cavernous ICA aneurysm causing ASDH 7 days after occurrence of abducens nerve palsy and review the literature.
Case report This 61-year-old female presented to our hospital by ambulance with sudden-onset headache, nausea, vomiting, and transient consciousness disturbance that had occurred during calculation at home. She had a history of diplopia and mild headache 7 days before admission. She visited a local hospital 2 days later and showed right abducens nerve palsy. Computed tomography (CT) and magnetic resonance (MR) imaging performed in the local hospital revealed a giant partially thrombosed aneurysm in the cavernous portion of the right ICA without any apparent hemorrhage (Fig. 1a). In the local hospital, surgery for the cavernous ICA aneurysm could not be performed; therefore, she stayed at home to wait to visit another hospital as a referred outpatient. At admission to our hospital, she showed right complete oculomotor and right abducens nerve palsy. CT demonstrated a right cavernous ICA aneurysm with a maximum diameter of 35 mm and slight high density in the right cerebellar tentorium (Fig. 1b). MR imaging revealed a thin subdural hematoma in the posterior fossa and right cerebral convexity (Fig. 2). Cerebral angiography demonstrated a right cavernous ICA partially thrombosed aneurysm (Fig. 3). Cerebral angiography performed under right ICA manual compression revealed poor collateral flows from the left ICA through the anterior
1114
Acta Neurochir (2015) 157:1113–1116
Fig. 3 Cerebral angiograms. a A preoperative right internal carotid angiogram showing a partially thrombosed aneurysm in the cavernous portion of the right internal carotid artery (ICA). b A postoperative right common carotid angiogram demonstrating disappearance of the aneurysm associated with therapeutic ICA occlusion. The intracranial territory of the right ICA is supplied by a bypass graft from the external carotid artery to the M2 inferior trunk of the middle cerebral artery
of the middle cerebral artery using a radial artery graft to prevent ischemic complications (Fig. 3b). Postoperatively, the right abducens nerve palsy improved, although the occluomotor nerve palsy remained. The patient was discharged 4 weeks after the admission and returned to her previous life. Fig. 1 Computed tomography (CT) showing a right cavernous aneurysm. a A CT performed at the first local hospital shows no apparent hemorrhage. b A CT at admission to our hospital demonstrates a high-density lesion in the retrosellar portion (arrows), which indicates either a part of the aneurysm or a small subdural hematoma. Faint high density is noticed along the right cerebellar tentorium (arrows)
communicating artery and from the vertebro-basilar artery through the right posterior communicating artery. The results of the cerebral angiography suggested a high risk of cerebral infarction if simple ICA occlusion was selected for treatment of the aneurysm. Three days after admission, she underwent ICA occlusion at the cervical ICA orifice associated with high-flow bypass. Bypass surgery was performed between the right external carotid artery orifice and M2 inferior trunk
Fig. 2 A magnetic resonance (MR) image/fluid attenuated inversion recovery (FLAIR) at admission showing a right giant partially thrombosed aneurysm in the cavernous sinus. A thin subdural hematoma
Discussion The present patient with a ruptured cavernous ICA aneurysm causing ASDH had both a giant aneurysm and a preceding cavernous sinus syndrome. These two features were consistent with the previous reported four patients with a ruptured cavernous ICA aneurysm leading to ASDH [1–3, 7]. Table 1 shows characteristics of the five patients, including the present case, with a cavernous ICA aneurysm causing ASDH. The following mechanism was speculated to explain the occurrence of rupture after preceding cranial nerve signs in a giant aneurysm. As a cavernous ICA aneurysm enlarges, it extends
is demonstrated in the right retropetrous portion (a, arrows), the retrosellar portion (b, arrows), and the right cerebral convexity (c, arrows)
Acta Neurochir (2015) 157:1113–1116 Table 1
1115
Characteristics of five reported patients with a cavernous aneurysm causing acute subdural hematoma
Reference
Age/sex
*HT
Nationality
Preceding cranial nerve symptoms (duration)
Aneurysm size
Barr et al. [2], 1971
59/F
Yes
UK
35 mm (post-mortem)
Hodes et al. [3], 1988
62/F
No
USA
6th nerve (5 years) 5th nerve (a few days) 5th and 6th nerves (2 days)
Mclaughlin et al. [7], 1996
48/F
Yes
USA
3rd–6th nerves (5 days)
Andaluz et al. [1], 2006 Present case
33/F 61/F
n.a. No
USA Japan
Ophthalmoplegia (2 weeks) 6th nerve (7 days)
n.a. Giant n.a. Giant 26 mm 35 mm
*HT: hypertension
into the cavernous sinus and compresses the cranial nerves passing through the cavernous sinus, which can cause cavernous sinus syndrome [4, 6]. After the cavernous sinus is filled with the aneurysm, the aneurysm expands the cavernous sinus dura; then, the aneurysm can break a weak part of the cavernous sinus dura, which is presumably related to passages of cranial nerves. Thereafter, if the aneurysm ruptures, bleeding from the aneurysm results in ASDH. Hence, all the reported five patients, including the present patient, with a ruptured cavernous ICA aneurysm causing ASDH had both giant aneurysms and preceding cranial nerve signs. Symptoms of these reported patients at the rupture of the aneurysm were sudden-onset headache and/or consciousness disturbance [1–3, 7]. Although life-threatening events were seldom reported in the previous studies [4, 6], when a patient with a cavernous ICA giant aneurysm showing a preceding cavernous sinus syndrome experiences sudden-onset headache and/or consciousness disturbance, rupture of the aneurysm resulting in ASDH should be differentiated. Considering that two of the five reported patients died of ASDH, early surgery to prevent rerupture from an aneurysm must be performed in patients with an ASDH [2, 3]. The preceding symptoms were observed in all five patients [1–3, 7], suggesting that surgery should not be performed in patients with an asymptomatic cavernous ICA aneurysm to prevent ASDH [4, 6]. In the three patients undergoing surgery, ICA occlusion was selected to treat the aneurysms [1, 7]. In two patients without bypass surgery, transient hemiparesis caused by cerebral infarction occurred after the ICA occlusion [1, 7]. High-flow bypass associated with ICA occlusion is necessary to prevent ischemic complication when a poor collateral flow has been observed on preoperative angiograms. In terms of endovascular therapy for a symptomatic cavernous ICA aneurysm, intraaneurysmal coil embolization, with or without stent assist, can seldom obtain complete improvement of the cavernous sinus syndrome [8]. Recently, a flow diverter stent has been reported to treat an unruptured giant symptomatic cavernous ICA aneurysm effectively [10]; however, early aneurysm rupture after treatment has been described [11]. In case of a ruptured aneurysm, because of both
continuous blood flow into the aneurysm without intraaneurysmal pressure reduction immediately after device deployment [9] and the necessity of antiplatelet use during the perioperative period, prompt prevention of the aneurysmal rerupture could not be obtained. Therefore, ICA occlusion with high-flow bypass seems to be the first choice treatment for ruptured giant cavernous ICA aneurysms. Patient consent-case reports The patient consented to submission of this case report to the journal. Conflict of interest All authors certify that they have no affiliations with or involvement in any organization or entity with any financial interest (such as honoraria; educational grants; participation in speakers’ bureaus; membership, employment, consultancies, stock ownership, or other equity interest; and expert testimony or patent-licensing arrangements), or non-financial interest (such as personal or professional relationships, affiliations, knowledge or beliefs) in the subject matter or materials discussed in this manuscript.
References 1.
2.
3.
4.
5.
6.
7.
Andaluz N, Tomsick TA, Keller JT, Zuccarello M (2006) Subdural hemorrhage in the posterior fossa caused by a ruptured cavernous carotid artery aneurysm after a balloon occlusion test. Case report. J Neurosurg 105:315–319 Barr HWK, Blackwood W, Meadows SP (1971) Intracavernous carotid aneurysms. A clinical-pathological report. Brain 94:607– 622 Hodes JE, Fletcher WA, Goodman DF, Hoyt WF (1988) Rupture of cavcavernous carotid artery aneurysm causing subdural hematoma and death. Case report. J Neurosurg 69:617–619 Kupersmith MJ, Hurst R, Berenstein A, Choi IS, Jafar J, Ransohoff J (1992) The benign course of cavernous carotid artery aneurysms. J Neurosurg 77:690–693 Lee AG, Mawad ME, Baskin DS (1996) Fatal subarachnoid hemorrhage from the rupture of a totally intracavernous carotid artery aneurysm: case report. Neurosurgery 38:596–599 Linskey ME, Sekhar LN, Hirsch WL Jr, Yonas H, Horton JA (1990) Aneurysms of the intracavernous carotid artery: natural history and indications for treatment. Neurosurgery 26:933–938 McLaughlin MR, Jho HD, Kwon Y (1996) Acute subdural hematoma caused by a ruptured giant intracavernous aneurysm: case report. Neurosurgery 38:388–392
1116 8.
9.
10.
Acta Neurochir (2015) 157:1113–1116 Morita K, Sorimachi T, Ito Y, Nishino K, Jimbo Y, Kumagai T et al (2011) Intra-aneurysmal coil embolization for large or giant carotid artery aneurysms in the cavernous sinus. Neurol Med Chir (Tokyo) 51:762–766 Schneiders JJ, VanBavel E, Majoie CB, Ferns SP, van den Berg R (2013) A flow-diverting stent is not a pressure-diverting stent. AJNR Am J Neuroradiol 34:E1–E4 Szikora I, Berentei Z, Kulcsar Z, Marosfoi M, Vajda ZS et al (2010) Treatment of intracranial aneurysms by functional reconstruction of the parent artery: the Budapest
experience with the pipeline embolization device. AJNR Am J Neuroradiol 31:1139–1147 11. Turowski B, Macht S, Kulcsár Z, Hänggi D, Stummer W (2011) Early fatal hemorrhage after endovascular cerebral aneurysm treatment with a flow diverter (SILK-Stent): do we need to rethink our concepts? Neuroradiology 53:37–41 12. van Rooij WJ, Sluzewski M, Beute GN (2006) Ruptured cavernous sinus aneurysms causing carotid cavernous fistula: incidence, clinical presentation, treatment, and outcome. AJNR Am J Neuroradiol 27:185–189
Copyright of Acta Neurochirurgica is the property of Springer Science & Business Media B.V. and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.
