H e a d a c h e a n d An e u r y s m

O-Ki Kwon, MD, PhD

KEYWORDS
 Aneurysm  Headache  Pathophysiology  Trigeminal nerves  Upper spinal nerves

KEY POINTS
 No pain from the aneurysm develops without pain nerves.
 The pain nerves involved in headache are the trigeminal nerve and high cervical spinal nerves (C1,
2, and 3).
 The pain nerves for intradural structures are present on blood vessel (mainly artery) walls.
 Various types of stimulation to the arterial walls producing pain include compression, distension,
traction, chemicals, and simple touching.
 With the basic knowledge, the mechanism of the headache from cerebral aneurysms can be better
understood.

INTRODUCTION fibers terminate in caudal and interpolar divisions

of the spinal trigeminal nucleus. The sensory fibers
Headache requires a wider definition than just a of cervical spinal nerves terminate in the dorsal
pain in the head.1,2 In this article, a narrow concept horns of the spinal cord. Small fibers of the general
of headache (a pain) is used. It is a basic concept somatic afferent system of cranial nerve VII
that headache develops from peripheral pain (through parts of the nervus intermedius), IX (tym-
nerve fibers. No headache develops without pain panic nerve, nerve of Jacobson), and X (auricular
nerves. Brain does not have pain nerve fibers.3 nerve, Arnold nerve) also have nociception but
Therefore, as seen in awake brain surgery, direct the sensing area is limited to ear structures. The
surgical manipulation of the brain does not pro- cell bodies that receive these pain senses are
duce pain. Structures that have pain fibers are also in the trigeminal nucleus. The central nervous
dura (pachymeninges), major arteries, and veins. system itself contributes to relation, perception,
The entire dura does not sense pain. Pain is and modulation of the headache. Centrally pro-
perceived only in dural parts with pain nerve fibers. duced pain such as thalamic pain, in which no acti-
Likewise, the other source of intracranial pain- vation of peripheral nerve fibers is necessary for
cerebral vessels can also produce pain only generating pain, exists but it is not a typical form
when they have pain fibers. of headache. The brain stem itself may also have
headache-producing structures,5,6 but it is not
thought to be a mainstay mechanism of headache
CONTENT
development. Stimulation or modulation of the tri-
Nerves that innervate intracranial vessels are auto- geminal nucleus and its connections may be a
nomic (sympathetic and parasympathetic) and pain-producing mechanism in this situation.
sensory nerves. Direct innervation from fibers of The exact mechanisms that cause major pri-
the brain may be present4 but its function is not mary headaches like migraines, tension head-
aches, and cluster headaches are still not clearly
neuroimaging.theclinics.com

yet fully determined. The pain nerves involved in

headache are trigeminal nerve (and its 3 divisions) understood. Proposed theories are divided into
and high cervical spinal nerves (dorsal [sensory] peripheral origin (arteries and accompanying tri-
roots of C1, 2, and 3). The sensory trigeminal nerve geminal or cervical spinal nerves) and central

Department of Neurosurgery, Seoul National University Bundang Hospital, Gumiro 173 Beongil, Bundanggu,
Seongnamsi, Gyeonggido 463-707, South Korea
E-mail address: [email protected]

Neuroimag Clin N Am - (2019) -–-

https://doi.org/10.1016/j.nic.2019.01.004
1052-5149/19/Ó 2019 Elsevier Inc. All rights reserved.
2 Kwon

(brain) origin. Unlike primary headaches, the head- exquisitely sensitive to stimuli but were progres-
ache associated with aneurysms has a definite pe- sively less sensitive over the convexity.10,11 In
ripheral origin, the aneurysm. In general, cerebral awake brain surgery, neurosurgeons confirmed
aneurysms arise from major cerebral arteries on that pain-sensitive structures are the dura of the
which pain nerve fibers are present. These nerves skull base, falx cerebri, and the leptomeninges of
are branches from the trigeminal nerve (almost all the sylvian fissure and neighboring sulci.9 Some
from V1, the ophthalmic division) and the upper 3 sensory fibers reach opercular or proximal cortical
cervical spinal nerves. segments of MCA.
All of the 3 trigeminal divisions have sensory Several types of stimulation on cerebral arteries
nerves. Their main sensing structures are dura. produce pain, including dilatation (distension),
The ophthalmic division of the trigeminal nerve traction, chemical, thermal, and electrical stimula-
(V1) innervates the anterior cranial fossa and falx tion.10–12 Among these, dilation of intracranial and
through the anterior and posterior ethmoidal extracranial arteries has been studied exten-
nerves. The tentorial nerve is the first branch of sively.12,13 Balloon inflation of cerebral arteries
the ophthalmic nerve. It takes a recurrent course caused headaches, which disappeared immedi-
to innervate the superior surface of the tentorium ately with balloon deflation.12 Stent-assisted coil-
and posterior falx. The maxillary nerve (V2) inner- ing caused headache more than simple
vates part of the dura of the anterior and middle coiling.14,15
cranial fossa. The mandibular nerve (V3) also in- Simpler manipulation like just touching of the ar-
nervates part of the anterior and middle cranial teries can also produce pain. Experience from
fossa dura. awake brain surgery has provided information
In general, these nerves use vessels (mainly ar- about pain-sensitive structures.8 In most cases,
teries) to reach dura (via meningeal arteries) and just touching causes pain. The pain from these
intracranial structures (via internal carotid artery). structures was described as sharp, acute, intense,
Sympathetic nerves also use a similar pathway. and brief. When the touching stopped, the pain
Supratentorial intradural structures are inner- disappeared. The pain from large aneurysms or
vated mainly by branches of V1. It enters the intra- tumors could be explained by just touching
dural space along with the ICA. It begins from (compression with low pressure) of neighboring
cavernous sinus and dura around the ICA level. pain-sensitive structures.
On the surface of the ICA, the fibers go along Displacement of the ICA also produces pain.16
into the middle cerebral artery (MCA) and anterior Frequent development of frontal and periorbital
cerebral artery (ACA) as with the ICA course. The pain after stent-assisted coiling of ICA aneurysms
exact level at which they end seems to vary. can be explained by ICA stretching and
Posterior cranial fossa dura and intradural struc- displacement.17
tures, mainly arteries, are innervated by C1, C2, As with other sensory neurons, activation
and C3. The cervical spinal nerve 1 (C1) is unique. of pain fibers is influenced by temporal and spatial
Unlike other spinal nerves that have both motor summation. The number of nociceptive receptors
and sensory fibers, only about half of C1 has sen- and neurons can be related with pain
sory fibers.7 It enters the skull with the hypoglossal strength.18,19 Low-intensity stimulation for a short
nerve. duration may not produce pain. Likewise, slowly
How far and how many these pain nerves reach forming aneurysms may not induce headache.
on the dura seem to vary. Distribution of pain Acute tearing dissection20 or acute formation of
sense is not uniform over the dura. A study of a daughter sac or a pseudoaneurysm from a pre-
awake brain surgery showed that the intensity of existing aneurysm could produce sudden severe
pain differed by location. The intensity of the pain headache. This headache may disappear if there
caused by touching the temporal part of the skull is no further acute change or it may persist if other
base dura was 7.9 out of 10 (range, 0–10), falx subsequent arterial changes, such as rupture, that
and tentorium was 4.2 (range, 0–9), and perisylvian newly stimulate pain nerve fibers on the arterial
leptomeninges was 6.6 (range, 0–10).8 Convexity wall occur.
dura has less pain. Stimulation of some parts of In addition, neural adaptation could affect pain
the dura does not induce pain. Likewise, large production and its intensity, so the intensity of
areas of posterior fossa dura over rostral and pain caused by long-lasting low-grade stimulation
lateral convexities of the cerebellum were insensi- may decrease over time despite pain sensation,
tive to pain by stimulation.9 especially via C-type nociceptive fibers, adapts
The proximal portions of arteries have more slowly. New headaches can develop after coiling
abundant sensory innervation than distal. Proximal or stent-assisted coiling, probably caused by
arterial segments near the circle of Willis were stretching of arterial walls, and generally are of
 Headache and Aneurysm 3

low intensity and spontaneously disappeared days nucleus in the brain stem. Some patients did not
or weeks later.14,15 perceive any headache with the balloon inflation,
Patients have pulsatile or throbbing headache which indicates that not all major arteries, or not
with increased intracranial pressure. Increased all parts of major arteries, have pain fibers, and
pulsatility of the whole dura can be a mechanism the number of pain receptors may vary by location
for headache. Increased arterial pulsatility can and among individuals. Stimulation of the superfi-
also contribute to headache.21–23 Likewise, the cial temporal and middle meningeal arteries and
pulsatile motion of aneurysms may be a source the large intracranial venous channels can also
of headache. Conditions with high pulsatile move- produce similar referred pain.10,11,31,32 Therefore,
ment, such as large size and thin wall, may be fac- it is natural to think that the precise localization
tors of headache development. The pulsatile of arterial pain cannot be determined from the
motion can be reduced or removed by treatment. location of the pain. One obvious point is a ten-
Disappearance of headache after coil packing dency for carotid headaches to be located anteri-
of aneurysmal sacs can be explained by this orly and vertebrobasilar-associated headaches to
mechanism.21 Many reports have showed that be located posteriorly.10,33
headache had substantial reductions after treat- Likewise, pain develops at the posterior neck
ment, including surgery and coiling.24–29 when the posterior fossa dura is stimulated. It is
Acute severe stimulation, such as abrupt arterial innervated by the upper 3 cervical spinal nerves.
tearing or distension of major cerebral arteries, But trigeminal fibers can reach the rostral part of
causes a sudden intense headache such as thun- the basilar artery via the posterior communicating
derclap headache. Vasospasm, also produces se- artery. The pain from the rostral part of the basilar
vere pain from the uncontrollable smooth muscle artery therefore can be referred to the orbital,
contraction and compensatory dilatation. The retro-orbital, and frontal areas. Of interest, sen-
same one can be the mechanisms of pain associ- sory signal from the C1 spinal nerve may enter
ated with reversible cerebral vasoconstriction syn- the trigeminal caudal neucleus.34,35 The nucleus
drome (RCVS). is located from the medulla to the C2 level of
Long-lasting stimulation with constant intensity the spinal cord, where it continues with the dorsal
could have diverse results. Pain fiber activation horn of the spinal cord. The spinal trigeminal tract
may decrease with adaptation, or, in some situa- is also analogous to the Lissauer tract of the spi-
tions, temporal summation can provoke more se- nal cord. One study showed that C1 stimulation
vere headache. Prolonged intensive headache produced periorbital and frontal pain.36 Simulta-
from subarachnoid hemorrhage or bacterial men- neous sensitization or interaction between
ingitis or bearable headache from chronic increase neurons may be the mechanism of common
of intracranial pressure can be examples. occurrence of both headache and neck pain.37
When the meningeal artery is stimulated, the Accordingly, pain from the vertebrobasilar sys-
pain location varies depending on the innervating tem can be perceived as orbital–retro-orbital
nerves. All 3 divisions of the trigeminal nerve take and frontal pain.37 Cases of frontal or retro-
part in dural innervation.30 But for intracranial ar- orbital headaches associated with vertebrobasi-
teries, V1 is the main innervating nerve. In general, lar dissection38 and posterior fossa tumor39
pain from stimulating intracranial arteries is have been reported. Similarly, sensory fibers
referred to the ipsilateral temporal, retrorbital and from the upper cervical spinal nerve can also
frontal regions. The pain caused by stimulation of reach the distal ICA and neighboring arteries,
the superior surface of the tentorium, torcular, or so pain from the anterior circulation system may
straight sinus is also referred to the ipsilateral fore- also be felt in the posterior neck.37 In addition,
head and periorbital region because this part is midline crossing fibers that innervate the contra-
innervated by the tentorial nerve from V1.30 lateral side have been noted in both trigeminal
In a study on balloon inflation of cerebral ar- and spinal nerves.40
teries, balloon inflation produced pain and its loca- Patients with giant aneurysms have plausible
tion was reproducible. Inflation in the proximal reasons for a high incidence of headaches. They
MCA stem produced pain primarily in the ipsilat- have more chance to compress adjacent pain-
eral temple. Ballooning in the middle of the MCA sensitive structures, including the dura and the
stem produced pain referred primarily retro- artery.41,42 Traction, compression, and displace-
orbitally, and inflation in the distal MCA stem pro- ment of adjacent arteries produce pain. Pulsatile
duced pain referred primarily to the forehead.12 motion of a large aneurysm sac, thrombus forma-
These findings show that there are patterns of tion within the sac, and extravasation of the
pain fiber distribution. Anatomically it is also thrombin followed by inflammation can also be
related to localization of cells of the trigeminal factors.
4 Kwon

Periorbital pain with ptosis from an aneurysm Sentinel headache, which is similar to that of
compressing the third nerve is a well-known symp- subarachnoid hemorrhage, characterized by sud-
tom. Posterior communicating artery aneurysm is den severe headache, has been thought to be
the most common cause.21,43,44 The occulomotor caused by a small amount of hemorrhage from
nerve has parasympathetic fibers and motor fibers the aneurysm. When a patient has SAH and the
for eye movement. When a posterior communi- patient has a history of sudden severe headache
cating artery aneurysm compresses the third nerve hours, days, or months before, physicians can
from above, ptosis develops because motor fibers consider the previous one to be a sentinel head-
for the levator palpebra muscle are located super- ache. If cerebral aneurysms that will rupture soon
ficially. The third nerve does not have sensory could be detected and treated before catastrophic
function, so theoretically pain should not be a SAH using this warning sign, many patients could
symptom unless the pain fibers on the ICA wall is be saved.53 However, real causes of the head-
stimulated. However, studies have shown that fi- aches could be various, including migraine, vaso-
bers from V1 of the trigeminal nerve may join and spasm, inflammation, or just tension headache.
travel with the third nerve at the level of the lateral Other mechanisms, such as acute expansion of
wall of the cavernous sinus, which accounts for the the aneurysm, acute formation of a daughter sac,
periorbital pain with third nerve compression.42 and hemorrhage into the aneurysm wall, can also
Some patients with unruptured intracranial be considered to be aneurysm-associated sudden
aneurysms present with trigeminal neuralgia. severe headache.
Compression or distortion of trigeminal nerves at Perimesencephalic SAH, a distinct form of SAH
various levels could be a mechanism. Many aneu- with a benign clinical course, is characterized by
rysm locations have been reported, including the a small amount of SAH around the midbrain.
ICA, posterior cerebral artery, superior cerebellar Angiograms show no source of the bleeding.
artery, anterior and posterior inferior cerebellar ar- The cause is thought to be venous or small arte-
tery, and basilar artery.45–47 Typical trigeminal rial bleeding.54 Headache characteristics are not
neuralgia involves the V2 and V3 divisions.48 How- distinct from conventional SAH, which suggests
ever, in cases of posterior communicating artery that the real mechanism that produces a sudden
aneurysm associated with trigeminal neuralgia, it severe headache is not necessarily high-
mainly occurs in the V1 and V2 area. It is explained pressure bleeding, a large artery rupture hole, or
by the anatomic location of V1 fibers, which are a large subarachnoid hemorrhage. Regardless of
distributed superiorly and medially in the trigemi- pressure, sudden severe headache can develop
nal nerve and posterior communicating artery at the time of rupture of vessels that have pain
compression of the cavernous sinus from nerve fibers.
above.48,49
The hallmark of subarachnoid hemorrhage SUMMARY
(SAH) is a sudden, severe headache. It is often
described as head explosion or thunderclap. It is The pain from an unruptured cerebral aneurysm
very intense and severe, so many patients can occur if it develops in proximal cerebral ar-
describe it as unbearable, or the worst headache teries in which pain fibers are present. These ar-
of their lives. Typically, it peaks within minutes teries can be the ICA, proximal ACA and MCA,
and last hours or days.50 In a report, about 50% vertebrobasilar arteries, and proximal posterior
of the headaches reached a maximum instanta- cerebral artery. Aneurysms at distal arteries do
neously. In the others, it took 1 to 5 minutes or not produce headache unless they stimulate
longer.51 In terms of pain location, 70% of the other pain-sensitive structure. The exact level
headaches are bilateral. In cases of bilateral head- which pain nerve fibers reach on the vessel
ache, generalized headache is most common in walls varies between individuals, so some distal
66%. In the case of lateralized headache, frontal aneurysms may produce pain. Slowly formed
and frontoparietal locations are common.50 Given aneurysms may not induce pain. Rapidly
that a frequent location of ruptured aneurysms is growing or forming aneurysms can cause pain.
the circle of Willis (anterior circulation) and the sub- Acute changes to preexisting aneurysms or ar-
arachnoid space is an open space with bilateral teries can produce pain. Stimulation of larger
communication, these findings are expected. arterial areas (large aneurysms) possibly causes
Meningeal irritation signs, such as nuchal rigidity more pain than small aneurysms.55 Pain location
and the Kernig sign, do not clearly develop at the and characteristics from the aneurysm can
onset. They take 2 or 3 days to become apparent52 be various and nonspecific. The pain-sensing
because development of meningeal inflammation nerves for intracranial structures are the
from blood degradation products takes time. ophthalmic nerve (V1 of the trigeminal nerve)
 Headache and Aneurysm 5

and upper cervical spinal nerves. Maxillary 11. Penfield W, McNaughton F. Dural headache and
nerves, mandibular nerves, and other minor innervation of the dura mater. Arch Neurol Psychiatr
nerves from VII, IX, and X have sensory function 1940;44:43–75.
but mainly innervate dura and ear structures. 12. Nichols FT 3rd, Mawad M, Mohr JP, et al. Focal
Therefore, pain from supratentorial structures headache during balloon inflation in the internal ca-
is felt in the orbitofrontal area and that from rotid and middle cerebral arteries. Stroke 1990;
infratentorial structures is felt at the posterior 21(4):555–9.
neck. Pain occurs mostly on the ipsilateral side 13. Nichols FT 3rd, Mawad M, Mohr JP, et al. Focal
but some fibers cross-innervate, so bilateral headache during balloon inflation in the vertebral
perception may be possible.21 A sudden severe and basilar arteries. Headache 1993;33(2):87–9.
headache possibly indicates that an acute 14. Choi KS, Lee JH, Yi HJ, et al. Incidence and risk fac-
pain-producing stimulation has occurred. They tors of postoperative headache after endovascular
could include a variety of situations such coil embolization of unruptured intracranial aneu-
as rupture of vessels or cerebral aneurysms, rysms. Acta Neurochir (Wien) 2014;156(7):1281–7.
tearing (dissection), acute expansion (daughter 15. Hwang G, Jeong EA, Sohn JH, et al. The character-
sac formation), spasm and dilatation (RCVS), istics and risk factors of headache development af-
embolism (sudden imbedding or stretching of ter the coil embolization of an unruptured aneurysm.
major cerebral arteries by emboli), and migraine. AJNR Am J Neuroradiol 2012;33(9):1676–8.
Pain location does not provide decisive informa- 16. Fay T. Atypical facial neuralgia, a syndrome of
tion. Diagnosis still depends on the physician’s vascular pain. Ann Otol Rhinol Laryngol 1932;41:
clinical suspicion and work-up. 1030–62.
17. Baron EP, Moskowitz SI, Tepper SJ, et al. Headache
REFERENCES following intracranial neuroendovascular proced-
ures. Headache 2012;52(5):739–48.
1. International Study of Unruptured Intracranial Aneu- 18. Price DD, McHaffie JG, Larson MA. Spatial summa-
rysms Investigators. Unruptured intracranial tion of heat-induced pain: influence of stimulus area
aneurysms–risk of rupture and risks of surgical inter- and spatial separation of stimuli on perceived pain
vention. N Engl J Med 1998;339(24):1725–33. sensation intensity and unpleasantness.
2. Raps EC, Rogers JD, Galetta SL, et al. The clinical J Neurophysiol 1989;62(6):1270–9.
spectrum of unruptured intracranial aneurysms. 19. Staud R, Koo E, Robinson ME, et al. Spatial summa-
Arch Neurol 1993;50(3):265–8. tion of mechanically evoked muscle pain and painful
3. Lebedeva ER, Gurary NM, Sakovich VP, et al. aftersensations in normal subjects and fibromyalgia
Migraine before rupture of intracranial aneurysms. patients. Pain 2007;130(1–2):177–87.
J Headache Pain 2013;14:15. 20. May A, Buchel C, Turner R, et al. Magnetic reso-
4. Edvinsson L. Calcitonin gene-related peptide nance angiography in facial and other pain: neuro-
(CGRP) in cerebrovascular disease. ScientificWorld- vascular mechanisms of trigeminal sensation.
Journal 2002;2:1484–90. J Cereb Blood Flow Metab 2001;21(10):1171–6.
5. Veloso F, Kumar K, Toth C. Headache secondary to 21. Rodriguez-Catarino M, Frisen L, Wikholm G, et al. In-
deep brain implantation. Headache 1998;38(7): ternal carotid artery aneurysms, cranial nerve
507–15. dysfunction and headache: the role of deformation
6. Goadsby PJ, Lipton RB, Ferrari MD. Migraine–cur- and pulsation. Neuroradiology 2003;45(4):236–40.
rent understanding and treatment. N Engl J Med 22. Drummond PD, Lance JW. Extracranial vascular
2002;346(4):257–70. changes and the source of pain in migraine head-
7. Tubbs RS, Loukas M, Slappey JB, et al. Clinical ache. Ann Neurol 1983;13(1):32–7.
anatomy of the C1 dorsal root, ganglion, and ramus: 23. Arndt JO, Klement W. Pain evoked by polymodal
a review and anatomical study. Clin Anat 2007;20(6): stimulation of hand veins in humans. J Physiol
624–7. 1991;440:467–78.
8. Fontaine D, Almairac F. Pain during awake crani- 24. Schwedt TJ, Gereau RW, Frey K, et al. Headache
otomy for brain tumor resection. Incidence, causes, outcomes following treatment of unruptured intracra-
consequences and management. Neurochirurgie nial aneurysms: a prospective analysis. Cephalalgia
2017;63(3):204–7. 2011;31(10):1082–9.
9. Wolff DL, Naruse R, Gold M. Nonopioid anesthesia 25. Qureshi AI, Suri MF, Kim SH, et al. Effect of endovas-
for awake craniotomy: a case report. AANA J cular treatment on headaches in patients with unrup-
2010;78(1):29–32. tured intracranial aneurysms. Headache 2003;
10. Ray B, Wolff H. Experimental studies on headache. 43(10):1090–6.
Pain sensitive structures of the head and their signif- 26. Kong DS, Hong SC, Jung YJ, et al. Improvement of
icance in headache. Arch Surg 1940;41:813–56. chronic headache after treatment of unruptured
6 Kwon

intracranial aneurysms. Headache 2007;47(5): 42. Hahn CD, Nicolle DA, Lownie SP, et al. Giant cavernous
693–7. carotid aneurysms: clinical presentation in fifty-seven
27. Li H, Zhang X, Zhang QR, et al. Resolution of cases. J Neuroophthalmol 2000;20(4):253–8.
migraine-like headache by coil embolization of a 43. Lanzino G, Andreoli A, Tognetti F, et al. Orbital pain and
primitive trigeminal artery aneurysm. Pain Med unruptured carotid-posterior communicating artery
2014;15(6):1052–5. aneurysms: the role of sensory fibers of the third cra-
28. Choxi AA, Durrani AK, Mericle RA. Both surgical nial nerve. Acta Neurochir (Wien) 1993;120(1–2):7–11.
clipping and endovascular embolization of unrup- 44. Kojo N, Lee S, Otsuru K, et al. A case of ophthalmo-
tured intracranial aneurysms are associated with plegic migraine with cerebral aneurysm. No Shinkei
long-term improvement in self-reported quantitative Geka 1988;16(5 Suppl):503–7 [Japanese].
headache scores. Neurosurgery 2011;69(1): 45. Di Stefano G, Limbucci N, Cruccu G, et al. Trigemi-
128–33 [discussion: 133–4]. nal neuralgia completely relieved after stent-
29. Gu DQ, Duan CZ, Li XF, et al. Effect of endovascular assisted coiling of a superior cerebellar artery aneu-
treatment on headache in elderly patients with un- rysm. World Neurosurg 2017;101:812.e5-9.
ruptured intracranial aneurysms. AJNR Am J Neuro- 46. Ildan F, Gocer AI, Bagdatoglu H, et al. Isolated tri-
radiol 2013;34(6):1227–31. geminal neuralgia secondary to distal anterior infe-
30. Wirth FP Jr, Van Buren JM. Referral of pain from dural rior cerebellar artery aneurysm. Neurosurg Rev
stimulation in man. J Neurosurg 1971;34(5):630–42. 1996;19(1):43–6.
31. Penfield W. A contribution to the mechanism of intra- 47. Mendelowitsch A, Radue EW, Gratzl O. Aneurysm,
cranial pain. Assoc Res Nerv Ment Dis 1932;15: arteriovenous malformation and arteriovenous fistula
399–416. in posterior fossa compression syndrome. Eur Neu-
32. Feindel W, Penfield W, Mc NF. The tentorial nerves rol 1990;30(6):338–42.
and localization of intracranial pain in man. 48. Sindou M, Leston J, Howeidy T, et al. Micro-vascular
Neurology 1960;10:555–63. decompression for primary trigeminal neuralgia
33. Edmeads J. Vascular headaches and the cranial (typical or atypical). Long-term effectiveness on
circulation–another look. Headache 1979;19(3): pain; prospective study with survival analysis in a
127–32. consecutive series of 362 patients. Acta Neurochir
34. Le Doare K, Akerman S, Holland PR, et al. Occipital (Wien) 2006;148(12):1235–45 [discussion: 1245].
afferent activation of second order neurons in the tri- 49. Sindou M, Howeidy T, Acevedo G. Anatomical ob-
geminocervical complex in rat. Neurosci Lett 2006; servations during microvascular decompression for
403(1–2):73–7. idiopathic trigeminal neuralgia (with correlations be-
35. Bartsch T, Goadsby PJ. Stimulation of the greater oc- tween topography of pain and site of the neurovas-
cipital nerve induces increased central excitability of cular conflict). Prospective study in a series of 579
dural afferent input. Brain 2002;125(Pt 7):1496–509. patients. Acta Neurochir (Wien) 2002;144(1):1–12
36. Johnston MM, Jordan SE, Charles AC. Pain referral [discussion: 12–3].
patterns of the C1 to C3 nerves: implications for 50. Al-Shahi R, White PM, Davenport RJ, et al. Subarach-
headache disorders. Ann Neurol 2013;74(1):145–8. noid haemorrhage: lumbar puncture for every nega-
37. Piovesan EJ, Kowacs PA, Tatsui CE, et al. Referred tive scan? Authors’ reply. BMJ 2006;333(7567):550.
pain after painful stimulation of the greater occipital 51. Linn FH, Rinkel GJ, Algra A, et al. Headache charac-
nerve in humans: evidence of convergence of cervi- teristics in subarachnoid haemorrhage and benign
cal afferences on trigeminal nuclei. Cephalalgia thunderclap headache. J Neurol Neurosurg Psychi-
2001;21(2):107–9. atry 1998;65(5):791–3.
38. Berger MS, Wilson CB. Intracranial dissecting aneu- 52. Sarner M, Rose F. Clinical presentation of ruptured
rysms of the posterior circulation. Report of six intracranial aneurysm. J Neurol Neurosurg Psychia-
cases and review of the literature. J Neurosurg try 1967;30:67–70.
1984;61(5):882–94. 53. Polmear A. Sentinel headaches in aneurysmal sub-
39. Kerr RW. A mechanism to account for frontal head- arachnoid haemorrhage: what is the true incidence?
ache in cases of posterior-fossa tumors. A systematic review. Cephalalgia 2003;23(10):
J Neurosurg 1961;18:605–9. 935–41.
40. Kimmel DL. Innervation of spinal dura mater and 54. van Gijn J, van Dongen KJ, Vermeulen M, et al. Peri-
dura mater of the posterior cranial fossa. Neurology mesencephalic hemorrhage: a nonaneurysmal and
1961;11:800–9. benign form of subarachnoid hemorrhage.
41. Goedee HS, Depauw PR, vd Zwam B, et al. Superfi- Neurology 1985;35(4):493–7.
cial temporal artery-middle cerebral artery bypass 55. Ji W, Liu A, Yang X, et al. Incidence and predictors
surgery in a pediatric giant intracranial aneurysm of headache relief after endovascular treatment in
presenting as migraine-like episodes. Childs Nerv patients with unruptured intracranial aneurysms. In-
Syst 2009;25(2):257–61. terv Neuroradiol 2017;23(1):18–27.