Effects from vascular changes and tumors on cerebral function, and specifically for this review, on the cranial and cervical nerves comprising the spinal accessory nerve plexus, have been extensively discussed in neurology texts (43). In addition, the voluminous neurosurgical literature is a rich source of clinical experience recorded to identify nerves making up the spinal accessory nerve plexus both intra- and extracranially. It contains many reports of anatomic studies, only a few being cited here, which are meant to be helpful in getting into the much wider literature. As already stated, they are usually focused on a clinical problem in a specific area. For example, the vagal nuclei have been investigated as part of a study of brain stem dysfunction and malformation (44). Also, in general, most of these papers say little of the intracranial connections of individual nerves to each other or of the specific blood supply to each individual nerve. Rather, they address, for example, the blood supply to an entire area or a group of nerves as a whole with an occasional exception (14, 45, 46).
Normal neural anatomy and vascular anatomy, both arterial and venous in relation to brain and cord structures of the entire posterior fossa, however, are described and shown in elegant colored photographs of dissections painstakingly done by Rhoton and collaborators (47). The emphasis in these writings is on the safest surgical approaches to the posterior fossa structures, accomplished by combining anatomic relationships to incisions.
Studies of vessels such as the above when injected with latex into deceased subjects have the advantage of retracting little on solidification. That property, along with the ability to color latex, makes it relatively easy to identify and measure the actual caliber of the injected vessels. This advantage has been noted previously by others (48). Also, the caliber of vessels relative to each other may be measured on x-ray film after injection of radio opaque substances (48). In clinical practice, radiologists commonly measure the size of such injected vessels on film, the caliber often being very close to the true size.
The intracrania1 region of the brainstem is very compactly arranged, with important neural and vascular structures that may be described in levels, but which in reality are very close to each other. As examples of writings about the brain stem at three levels dorsally to ventrally, one study detailed the bridging veins on the tentorial surface of the cerebellum in close proximity dorsally to the lower four cranial nerves. The writing points out the serious risks to those veins and the cerebellum from traction on them when operating in this area (49). At a level a bit more ventrally, Person et al. (45) did 59 microdissections of the medullospinal junction, noting the great variability of the posterior inferior cerebellar artery in relation to the lower four cranial nerves. They held that the lack of landmarks necessitated complete angiographic studies for each patient to avoid iatrogenic operative injury to these vessels and nerves (45). Work in the dissecting laboratory also illustrates the vagaries of anatomic landmarks (39), reemphasizing the need clinically to be circumspect in identifying as many anatomic relationships as possible for more certain identity. Katsuka et al. (18), studying more ventrally at the skull base, described microsurgical anatomy and surgical approaches to the jugular foramen, the exit for the glossopharyngeal, vagus, and spinal accessory nerves. This report complements an earlier detailed study by Lang et al. (50).
Vascular or direct nerve compression of the glossopharyngeal in this area with attendant glossopharyngeal neuralgia, attributed to atherosclerosis and architectural changes, may be amenable to surgical relief by decompression (51, 52). Bejjani et al. (53), studying still more ventrally, reported on the extradural foraminal exit from the skull base of cranial nerves, among them the lower four and the facial nerve, into the infratemporal fossa. The latter, in their terminology, was the area under the middle fossa of the skull base. They point out that cranial nerves are at risk when exposing neoplasia in this confined and difficult area. As a result, they too point out that important landmarks must be observed to identify relationships of nerves both to each other and to major cerebral vessels before proceeding (53). Another study investigated the relationship of the vertebral artery to the foramen magnum and the upper cervical vertebrae for suboccipital craniectomy (54). In still another study, this one concerning more actual deficiency in cerebral blood supply, Koboyashi et al. (55) point out their use of the transverse cervical artery to revascularize the internal carotid artery in two patients.
At the end of the nineteenth century, Quenu and Lejars (56) changed the thinking of the time by stating that "the arterial circulation of nerves is at the same time very rich and very regular". They also described the rich blood supply of the brachial plexus (56). Without specifically mentioning that plexus, they implicated circulatory disturbances, including those from atheromata, as causes of neuralgia, functional disorders, and many vascular accidents of peripheral nerves. A clinico-pathological study nearly a half century ago (57) and a recent study in the anatomical laboratory (39) confirm that the blood supply to the lower four cranial and the cervical nerves, although usually very rich, is not constant. The recent laboratory study also suggested that the deprived blood supply might be the cause of dysfunction, often painful. Parenthetically, the brachial plexus, formed from cervical nerves, is intimately connected with the spinal accessory nerve plexus and its blood supply (1). In the dissecting room, the blood supply to the brachial plexus was observed to be deficient, particularly in older people, mostly from atherosclerotic vessel narrowing or occlusion. This relative ischemia is theorized to be the cause of otherwise unexplained shoulder pain that has been commonly observed in the author’s clinical experience. In the laboratory, this ischemia was observed not only in the brachial plexus, but in the lower four cranial nerves as well. In the case of the lower four cranial nerves, neuroforaminal occlusion obstructing blood flow was believed to be the cause of ischemia. In addition, severance of blood vessels at operation may be an iatrogenic cause for ischemia. Logically, ischemia would result in dysfunction. The mechanism may be similar to the generally accepted view that atherosclerosis usually is the cause of a painful ischemic dysfunction in the lower extremity, i.e., intermittent claudication. In the same way, ischemia of the lower four cranial nerves from these causes as suggested by the same anatomic studies (39) theoretically could cause some otherwise unexplained swallowing dysfunction in elderly patients. The mechanism could be by impairing the highly coordinated swallowing mechanism which is dependent on these nerves at the pharyngo-esophageal sphincter (43). These theoretical considerations would be in agreement with observations of others (41, 56, 57). More evidence is needed, however, to conclusively show a clinical correlation between painful ischemic dysfunction of the brachial plexus or of the lower four cranial nerves or swallowing dysfunction and the deficient blood supply observed in our laboratory (39).Beside the above disadvantage of atherosclerosis, Robbins et al. (58) in a recent review article pointed out another hazard from significant carotid artery atherosclerosis, namely, that it increases the chance of stroke with head and neck cancer surgery. Vascular imaging procedures, especially duplex ultrasonography, usually a reliable screening technique to detect such problems preoperatively, may miss a high-grade (80%) internal carotid artery stenosis. This error may occur with a densely calcified carotid bifurcation. Wixon et al. (59) term this error the "Gibraltar Sign". In these circumstances, magnetic resonance angiography or selective cerebroangiography are needed to assist in diagnosis (59). Parenthetically, these laboratory and clinical observations give some of the reasons why studies on more ways to impede atherosclerosis are urgently needed.
Interruption of the essential blood supply to the spinal accessory nerve may occur from other causes. Vessels must change caliber to maintain cerebral blood flow with the rise and fall of cerebrospinal fluid pressure because the rigid skull requires the intracranial content to remain constant, i.e., the Monro (1783) Kellie (1824) law (60). In this light, additional study is required of an intriguing but undocumented theory. This theory is based on the fact that vessels in the brain may differ structurally from each other, as for example when they are abnormally large, tortuous, or pulsating or have atheromatous changes (14). These structural differences might account in part for variations in blood supply under changing conditions in the brain. This thesis may well have been part of what Hofmökl had in mind when in 1875 he wrote on the subject of the ratio of blood vessel pressure in the large and small circulations (61). Similarly, it is worth considering the theory that both cellular factors of blood vessels as well as blood flow in the vessels themselves may be important in nerve healing. The evidence that vascular endothelial cells supply trophic and mitogenic factors to injured nerves (62) is one instance illustrating this idea. In fact, recovery of nerve and vessel function in peripheral nerves may be mutually dependent on one another. For example, the nerve’s microarteriolar smooth muscle altered reactivity might contribute to vascular disturbances in vivo after nerve damage or surgical denervation (63). Specifically, in this review regarding the spinal accessory nerve plexus, the degree of plasticity of the injured central nervous system is probably of critical importance, along with circulation, for its recovery. Plasticity here has the connotation of the capacity of the central nervous system to alter sensory and motor representation. Without this plasticity, the ability to relearn sensibility may be impaired because the central nervous system representation of a recovered injured nerve may differ from that prior to injury (64, 65).
The anatomy of the cervical sympathetic plexus and the operative risks to it (in this review, in surgery involving the spinal accessory nerve plexus) were well documented by Collins in 1991 (23). She pointed out that most of the major risks as, for example, causing a Horner’s syndrome from stellate ganglion injury come when operating beneath the deep cervical fascia. In the author’s clinical experience, this has seldom been the case in head and neck cancer surgery; but he agrees that exceptions may occur as when deep structures as the carotid artery have been invaded by tumor. It is unclear whether the numbness, pain, and dysesthesia sometimes following surgical neck dissection are also due in part to severance or injury to the cervical sympathetic branches penetrating the deep cervical fascia and connected to the spinal accessory nerve plexus. This question requires further study.
According to Brierley and Field (66), connection of cerebrospinal fluid to cervical lymphatics was first shown by Schwalbe in 1869 (67). Brierley and Field traced researches done in this area up to 1948, including their own work. Even though incompletely understood, the connection of the spinal subarachnoid space to the cervical lymphatics at that time was generally accepted, as was the idea that cervical lymph nodes may be filled with cerebrospinal fluid under physiological conditions (66). The possible routes of metastatic spread of cancer to peripheral nerves from the central nervous system and vice versa via the cerebrospinal fluid, as well as the role of cerebrospinal fluid in normal nutrition of nerves, are important topics, but are beyond the scope of this review. Similarly, the entire feedback mechanism involved in cerebrospinal fluid pressure, arterial pressure, baroreceptors, and chemoreceptors discussed by others (68) also are beyond the scope of this review. These latter mechanisms may also have clinical significance, with cerebrospinal fluid pressure changes affecting head and neck lymphatic metastases.
Several papers quoted here, nevertheless, review the literature on the importance of cervical lymphatics in head and neck cancer (69–73). They omit reference to the possible role of cerebrospinal fluid pressures in cervical metastases. These clinical papers also usually do not add appreciably to knowledge of the normal gross anatomy of cervical lymphatics. Perhaps part of the reason for this relative paucity of research is the difficult and painstaking laboratory techniques involved in laboratory dissections (74).
From a clinical perspective, Kraus (69) retrospectively reviewed the incidence of supraspinal accessory lymph node metastases in 47 supraomohyoid neck dissections. He concluded that; 1.) Dissection of these nodes exposed the patient to trapezius muscle paralysis from spinal accessory nerve injury, which could be avoided since 2.) Dissections of those nodes could be safely omitted without changing prognosis since metastatic spread to those nodes is very uncommon. This statement is another indication of the trend toward more conservative surgery when the spinal accessory nerve plexus is involved. Neck dissections other than for cancer, as for example, carotid endarterectomy for atherosclerotic stenosis, also expose the spinal accessory nerve plexus to injury. Fortunately, many injuries to these nerves from stretching or scarring are only temporary (75, 76). Restenosis of the carotid artery also might expose the spinal accessory nerve plexus again to ischemic injury. In this regard, Archie (77) pointed out that applying proper geometric dimensions in reconstruction after carotid endarterectomy is important in preventing restenosis. Also, stretching of the spinal accessory nerve from heavy lifting may injure that nerve. For one patient with a partially torn nerve from such an injury, a cable graft replacing only the torn part of the nerve was reported to give good results (78). Conversely, mixed results have been reported for surgical repair following complete transection of the spinal accessory nerve. Generally, in those circumstances, the repaired nerve either by direct suture or nerve cable graft gives less satisfactory function, often much less, than the nerve gave prior to injury (79–81). The same may be said for shoulder and arm function after muscle transfer performed for patients where nerve repair could not be done or when earlier nerve repair gave unsatisfactory results (82, 83). When the spinal accessory nerve has been transected at the base of the skull, others suggest reinnervation of the trapezius muscle with cervical and thoracic nerves (84). Still others suggest reinnervation of the trapezius muscle with the entire cervical plexus following transection and removal of the spinal accessory nerve (85). When so many different methods for repair are offered, it suggests to the author that no method is completely satisfactory. From the viewpoint of a neurobiologist, a discussion of the few known factors favoring nerve regeneration after repair and the many daunting factors against nerve regeneration may also help to explain these mixed results (86). A recent review of the immunologic response to injury may also give pertinent insights here as to why so many failures occur with nerve repair (87).
The same line of reasoning may be applied to injury and recovery in the central nervous system from the effects of endocrine, systemic, inflammatory, and infectious stimuli on blood-brain communication. Studies of these factors suggest that proinflammatory cytokines released from the myeloid cell lineage on presentation of an antigen set off a cascade of events involving mitogen-activating factor protein, janus kinase/signal transducer, and signaling molecules of vascular-associated cells of the central nervous system. These cells in turn induce fever and autonomic functions to restore homeostasis (88). Experimental evidence for this hypothesis is strong in animals, but more work is needed to establish its exact role clinically.