The PCoA arises from the posteromedial surface of the communicating segment of ICA and courses medially and inferiorly such that it bisects the ICA into an ophthalmic segment and a communicating segment. Typically, 2–14 perforators arise from the PCoA during its course [8, 21], and such arteries are called the anterior thalamoperforating arteries. Among them, the PMA is generally the largest and the most frequently seen perforating branch that penetrates the paramedian perforating substance, which is a triangular space limited by the mammillary body and tuber cinerum medially, the optic tract anterolaterally, and the cerebral peduncle posterolaterally [8, 24]. PMA, also called as the tuberothalamic artery, is known to supply the posterior hypothalamus, the mammillothalamic tract, the anterior thalamus (nucleus ventralis anterior, ventrolateral and dorsomedial nucleus, and reticular nucleus), the anteromedial part of the optic tract, the inferomedial tip of the head of the caudate nucleus, the genu, and a part of the posterior limb of the internal capsule [8, 12]. Further, it is known that the PMA originates from the superior and lateral surface of the PCoA, that it courses superiorly, laterally, and posteriorly, and that the majority of the PMAs originate from the middle segment of PCoA [1, 8, 12, 20, 21].
Only a few reports have described PMA infarction after PCoA aneurysm clipping. Even though Tanabe et al. have reported outcomes from 183 patients who had undergone microsurgical clipping of a PCoA aneurysm, a majority of these patients (60.1%) presented with subarachnoid hemorrhage, which is in contrast to the patients in our cohort. Furthermore, of the 183 patients who underwent PCoA aneurysm clipping in that study, 22 patients (12%) suffered infarction in a perforator originating from the PCoA , and among unruptured PCoA aneurysm patients, 2 out of 73 patients (2.7%) experienced perforator infarction after clipping. This small sample size of the perforator infarction group precluded detailed analysis of associated risk factors. Also, in patients with subarachnoid hemorrhage, infarction may occur due to vasospasm secondary to hemorrhage, rather than other than factors such as aneurysm characteristics, PCoA type, or clipping strategy; hence, it is difficult to clearly determine risk factors of PMA infarction after clipping of unruptured PCoA aneurysm from the study of Tanabe et al. In our cohort, the overall incidence of PMA infarction after microsurgical clipping for unruptured PCoA aneurysm was about 5%, and among them, while 22 patients were asymptomatic, five showed postoperative motor weakness and four patients had postoperative confusion; thus, the incidence of symptomatic PMA infarction was about 1.5%. Further, symptomatic patients tended to have a wider infarction area with corticospinal tract involvement. Presumably, in cases of asymptomatic infarction, blood vessels other than the PMA, such as the lenticulostriate artery or the anterior choroidal artery, form anastomoses with the internal capsule or basal ganglia, implying a relatively smaller extent of infarction. Additionally, while Tanabe et al. excluded patients treated with a fenestration clip for an aneurysm with the fundus projecting posteromedially, we show that medial aneurysm direction and large size significantly increased risk of infarction.
Generally, during microsurgical clipping of a PCoA aneurysm, the origin of the PCoA is often difficult to see and only the knuckle of the artery proximal to the aneurysm neck can be seen. Further, if the origin of PCoA is low, it is difficult to expose the entire neck in the surgical field of a general pterional approach. The origin of the PCoA is also difficult to identify in some cases; in such cases, an anterior clinoidectomy or cutting of the anterior petroclinoid ligament is performed, as needed. We prefer an extradural anterior clinoidectomy because it permits easier identification of the anatomical orientation, has a shorter procedure time, and can protect intradural structures [30, 31].
In the PCoA aneurysm in medial direction, the origin of PCoA tends to be located more posteriorly and medially. And in these patients, the origin of PCoA, also known as the “knuckle”, is almost invisible, and the origin of the PMA is almost hidden by the ICA (Figure 5). Nevertheless, the origin of the PMA can be verified by carefully rotating the ICA after temporary clipping (Figure 6). However, if the aneurysm is large or there is atherosclerosis in the proximal artery, special caution is needed when using this technique. In patients with a large aneurysm or atherosclerosis in the proximal artery, premature aneurysmal rupture, or parent artery dissection can also occur. Hence, in large aneurysms that are medial in direction, the surgeon applies the clip by targeting the area presumed to be the neck of the aneurysm; however, as the origin cannot be clearly identified, both PCoA and PMA flow from the ICA may be occluded or stenosis may occur. Additionally, the course of the PCoA often coincides with the direction of the aneurysm, which may cause the PCoA and the aneurysm to adhere, and if clipping is performed without complete dissection, PCoA torsion will occur, resulting in perforator infarction. Therefore, it is important to ensure patency through various spaces even if the surgeon judges that the clip has been accurately placed. Flow should also be checked near the neck of the aneurysm and in the opticocarotid triangle because the patency of PCoA can be checked using doppler and ICG. However, doppler measurement results may vary depending on arterial diameter, vessel wall thickness, and probe-vessel angle. Additionally, even if flow is seen during ICG video angiography, it may actually be backflow from the posterior cerebral artery, implying that the results from these methods alone cannot guarantee efficient blood supply to all the perforating arteries of the PCoA . When unsure of the relationship between the tip of the blade and perforators, the surgeon can alternatively use an endoscope [6, 11, 13, 22]. Yoshioka et al. have suggested that the endoscope can reveal the medial aspect of the aneurysm and enable perforator dissection, even at dead angles of the microscope, during PCoA aneurysm surgery .
Surgeons often use the curved clip or the j-shaped clip for complete occlusion of a PCoA aneurysm as the slight curve of the clip helps eliminate a “dog-ear” adjacent to the ICA . However, in patients with a medial aneurysm, the use of a curved clip is likely to be a factor in the occlusion of the PCoA or the PMA. A fenestration clip is sometimes used when the aneurysm is large and the aneurysm sac is oriented in the posterior medial direction, i.e., opposite to the surgical field of view. Importantly, greater attention is required in such cases. If the parent artery displays atherosclerotic change, the diameter of the ICA itself, as well as that of the PCoA origin, may be narrowed after clipping. Occasionally, the origin of the anterior choroidal artery is also narrowed and a wide range of ischemic insults may occur (Figure 4).
SEP evaluation during clipping surgery monitors the dorsal column pathway responsible for proprioception and vibration sensation among somatosensory sensations and it is sensitive enough to detect changes in the motor nervous system . However, as SEP monitors the posterolateral tract of the thalamus, it is possible that infarctions in the anterior thalamus may not be apparent intraoperatively. Thus, we hypothesized that SEP change would not have been observed in patients, except for patient#15, who only showed a transient SEP change. In contrast, intraoperative MEP monitoring can detect neurophysiological changes in the motor cortex and in corticospinal tract function, and because monitoring changes in sensory function is more difficult than evaluating changes in motor function, surgeons usually pay attention to motor function monitoring during aneurysm surgery. In our cohort, two patients (#8 and #27) showed false-negative results during EP monitoring and we have previously reported the incidence of false positive cases (0.99%) and false negative cases (0.53%) . Mechanisms underlying false-negative EP observations include (1) direct stimulation of deeper structures within the subcortical motor pathway that bypass the ischemic lesion, (2) motor weakness from a lesion that is not located in the corticospinal pathway, and (3) motor weakness without a neurophysiological change in the axons of the corticospinal pathway.
An infarction in the anterior thalamus, which is mainly supplied by the PMA, can lead to abulia, apathy, decrease in general intelligence, impairment of anterograde memory, and disorientation [9, 18, 23]. This could have contributed to the observed increase in the length of hospitalization in the PMA infarction group. Further, depending on individual anatomical variations, only a part of the internal capsule could be supplied, which may manifest as a specific neurologic deficit and a significant difference in GOS at discharge. However, as the results of this study showed no significant difference in GOS at 6 months, permanent morbidity due to PMA infarction could be less serious than other perforator injuries, such as an anterior choroidal artery or lenticulostriate artery, probably because the PMA can supply a portion of the anterior choroidal territorial or lenticulostriate artery territory, which can then form collaterals with the existing anterior choroidal artery or the lenticulostriate artery. However, apart from prominent motor deficits such as hemiparesis, behavioral symptoms, such as inactivity and depression, persisted in most patients despite adequate rehabilitation. Moreover, disturbances in verbal memory or learning have been reported, which make it difficult to return to work [2, 15].
There are some limitations in our study. First, selection biases inherent to a single-center, retrospective analysis are applicable. Next, the rapid growth of endovascular treatment technology during the 13 years of data collection may have led to differences in enrollment criteria for microsurgical clipping between the beginning and the end of the study. However, overall, about 15% of the 5000 patients who were treated with microsurgical clipping in our center had a PCoA aneurysm. This is similar to the incidence (about 10-15%) of PCoA aneurysms [28, 29], indicating that that selection bias is probably relatively small. Second, given that PMA infarction induces symptoms such as abulia and apathy, rather than weakness, the modified Rankin scale and GOS, which are often used as prognostic evaluations, may not accurately reflect prognosis. Symptoms associated with PMA infarction can be evaluated more objectively through other tools, such as the Mini-Mental state examination, Wechsler adult intelligence scale, apathy evaluation scale [4, 16] and the Lille apathy scale . In this study, these evaluations could not be performed due to a lack of records. Thus, multicenter, prospective studies and objective evaluation of outcomes using the above-mentioned evaluation tools are needed.