Visuospatial Changes after Clipping of Anterior Communicating Artery Aneurysms

Abstract

Introduction A series of symptoms are commonly seen after anterior communicating artery (ACoA) aneurysm clipping. Previous studies designated it as ACoA syndrome, a condition in which symptoms like amnesia, confabulation, and personality changes are observed. The present study investigates visuospatial impairments associated with ACoA aneurysm rupture followed by subarachnoid hemorrhage (SAH) and clipping procedure.

Methods 31 patients who underwent surgical clipping of the ACoA after SAH were evaluated prospectively at three, six, and twelve months after the surgery. Hooper Visual Organization test (HVOT), Judgment of Line Orientation test (JLOT), and Stroop-I test were used to evaluate visual organization, visual orientation perception, and visual attention, respectively.

Results Regarding the HVOT, the mean score observed in each observation was at three, six, and twelve months, respectively: 20.2 (SD ± 4.4), 21.5 (SD ± 4.7), and 20.9 (SD ± 4.6). The JLOT, in turn, presented the following results at the same respective time frames: 19.0 (SD ± 4.9); 19.7 (SD ± 4.3); 21.2 (SD ± 4.7). Finally, for the Stroop-I test, a similar pattern was found: 18.35 (SD ± 5.8); 18.00 (SD ± 6); 17.00 (SD ± 4.4). Of all the tests above, only Stroop-I test scores did not follow a normal distribution.

Conclusion Visuospatial and visuoperceptual abilities can also present impairments after SAH following ACoA aneurysm rupture and clipping, although it is commonly a mild symptom. Therefore, diffuse symptomatology, rather than the stricter ACoA syndrome described in the literature, may be seen. Moreover, positive outcomes are expected twelve months after postoperatively.

Resumo

Introdução Uma série de sintomas é comumente observada após a clipagem de aneurismas da artéria comunicante anterior (ACoA). Estudos anteriores denominaram essa condição como síndrome da ACoA, em que sintomas como amnésia, confabulação e alterações de personalidade são frequentemente observados. O presente estudo investiga os déficits visuoespaciais associados à ruptura de aneurisma da ACoA, seguida por hemorragia subaracnoide (HSA) e clipagem.

Método 31 pacientes que foram submetidos à clipagem cirúrgica da ACoA após HSA foram avaliados prospectivamente aos três, seis e doze meses após a cirurgia. Foram utilizados o Teste de Organização Visual de Hooper (HVOT), o Teste de Julgamento de Orientação de Linhas (JLOT) e o Stroop-I para avaliar, respectivamente, a organização visual, a percepção de orientação visual e a atenção visual.

Resultados Em relação ao HVOT, a pontuação média observada em cada momento foi de três, seis e doze meses, respectivamente: 20,2 (DP ± 4,4), 21,5 (DP ± 4,7) e 20,9 (DP ± 4,6). O JLOT, por sua vez, apresentou os seguintes resultados nos mesmos períodos: 19,0 (DP ± 4,9); 19,7 (DP ± 4,3); 21,2 (DP ± 4,7). Finalmente, para o Stroop-I, foi encontrado um padrão semelhante: 18,35 (DP ± 5,8); 18,00 (DP ± 6); 17,00 (DP ± 4,4). De todos os testes mencionados, apenas os escores do Stroop-I não seguiram uma distribuição normal.

Conclusão Habilidades visuoespaciais e visuoperceptivas também podem apresentar comprometimentos após HSA decorrente da ruptura de aneurisma da ACoA e sua subsequente clipagem, embora sejam comumente sintomas leves. Portanto, uma sintomatologia difusa, em vez da síndrome da ACoA mais restrita descrita na literatura, pode ser observada. Além disso, são esperados desfechos positivos doze meses após o procedimento cirúrgico.

Keywords

subarachnoid hemorrhage - anterior communicating artery - intracranial aneurysm - visuospatial changes - visuospatial abilities - visual impairment

Palavras-chave

hemorragia subaracnóidea - artéria comunicante anterior - aneurisma intracraniano - alterações visuoespaciais - habilidades visuoespaciais - deficiência visual

Introduction

Intracranial aneurysms are present in ∼5% of the population.[1] Known risk factors associated with the abnormal dilation of blood vessel walls include advanced age, hypertension, alcoholism, diabetes mellitus, atherosclerosis, family history of the disease, hormonal and ethnic factors, and smoking.[1] [2] [3] These factors, directly or indirectly, increase hemodynamic stress on the vessel walls. Arterial hypertension is, in fact, considered one of the main causes of subarachnoid hemorrhage (SAH) resulting from aneurysm rupture, facilitated by the weakening of vessel walls.[1] [4] Clinical manifestations are severe and include headache, nausea, vomiting, hemiparesis, and altered consciousness.[5]

The system of vessels formed by the anterior communicating artery (ACoA) and its perforating branches is the most prone to the development and rupture of intracranial aneurysms, causing aneurysmal subarachnoid hemorrhage (SAH).[6] [7] [8] [9] It is estimated that 18% of aneurysms are located in this system, and women are more likely to develop them.[5] Etiological factors include trauma, infections, or congenital defects.[10] [11] The bifurcations and taperings typical of the vessels in this system are morphological variables associated with aneurysm development.[5]

Anatomically, the ACoA is a small vessel located in the anterior portion of the Circle of Willis, which is responsible for most of the blood supply to the brain. The ACoA connects the two anterior cerebral arteries, and several smaller arteries (called perforators) project from it, classified according to the brain regions they supply (e.g., subcallosal, hypothalamic, and chiasmatic). Cortical and subcortical structures relevant to cognition, including the fornix, cingulate gyrus, and basal forebrain, are supplied by the perforators,[12] [13] which explains the cognitive deficits found in nearly 50% of patients following vascular accidents in this region.[14] [15] [16] [17] [18]

In addition to neurological damage, the rupture is also associated with severe neuropsychological and psychiatric repercussions. These impairments may result from the brain insult caused by the aneurysm rupture, the pathophysiological consequences of the hemorrhage (e.g., blood toxicity, brain edema, ischemic lesions or infarction typically associated with vasospasm, increased intracranial pressure due to bleeding, and hydrocephalus), and/or iatrogenic effects (e.g., side effects of anesthesia and unavoidable surgical damage to areas adjacent to the aneurysm, including perforators, the rectus gyrus, and limbic structures, among others). Iatrogenic effects may result either from malpractice or the necessity of accessing the frontobasal region.[15] [17]

Vasospasm, a phenomenon characterized by the narrowing of blood vessels, typically occurs around five days after the hemorrhagic event[19] [20] and has been identified as an important predictor of long-term cognitive deficits.[21] More recent studies, however, suggest that although vasospasm is common, it does not seem to have a significantly strong association with postoperative cognitive damage, unless it leads to brain tissue death (ischemia followed by infarction).[22]

There is ongoing debate surrounding the two main surgical modalities used to treat aneurysms—embolization and clipping—regarding the cognitive risks associated with each. Evidence suggests that patients undergoing the latter may be more prone to cognitive sequelae, mainly due to the higher risk of structural brain damage during the procedure.[9] [11] It has been suggested that cognitive sequelae may depend more on the characteristics of the aneurysm (e.g., location and volume of the aneurysm sac) than on the type of treatment used.[20]

Neurocognitive domains commonly affected by the disease and/or treatment seem to result from lesions in respective neuroanatomical regions (mainly front-frontotemporal), although this association is not always clear or direct. These include domains of memory, language, executive functions (EF), and personality changes.[23] [24] [25] Confabulation and its rarer variant, fabulism, may also be observed following ACoA hemorrhage.[10]

The pattern of symptoms triggered by aneurysm rupture and possibly exacerbated by surgical treatment has been termed “ACoA syndrome”[26] [27] [28]. However, there is no consensus on the accuracy of this entity due to the distinct patterns of deficits found in different studies, both in terms of the cognitive domains affected, their severity, and the transience or permanence of the sequelae.[18]

Recent studies have increasingly emphasized the decline in patients' performance in attention tasks (focused, divided, and alternating) compared with healthy controls.[9] It is acknowledged that, as an “input function,” attention impairment is expected to secondarily affect other cognitive domains. Lezak[29] asserts that the quality of attentional focus is a prerequisite for good performance in various neuropsychological tests. Although not always detected by standardized tests, attentional decline is reported by patients and their families.[18]

Deficits in domains associated with posterior brain regions, particularly visual processing (VP), are less commonly reported. VP depends on highly specialized neural networks in different cortical and subcortical pathways responsible for its subcomponents, namely visuospatial (VSE), visuoperceptive (VPE), and visuoconstructive (VCE) abilities. VSE, associated with the dorsal stream (occipitoparietal pathway), refers to the ability to judge the orientation and position of visual stimuli, as well as topographical orientation. VPE, associated with the ventral stream (occipitotemporal pathway), refers to the ability to identify or recognize the identity or nature of visually presented stimuli (the ability to discern what something is or what it is for). Finally, VCE, also associated with the dorsal stream, represents the interaction between visual and motor domains, allowing tasks such as graphomotor execution (e.g., copying figures) or constructive tasks (e.g., assembling blocks based on diagrams or models).[30] Vascular accidents are among the main etiological factors for disturbances in these functions, which include visual agnosias, hemispatial neglect, difficulties navigating familiar environments, constructive disabilities, and other rarer, debilitating, and usually chronic conditions.[31]

One of the few studies that extensively evaluated the cognitive profile of these patients[32] found no significant differences in visuospatial task performance between the group of operated patients and healthy controls. The same was true when comparing the performance of patients treated with clipping to those treated with embolization.[32] Two decades earlier, the same author described the neuropsychological profile of five patients with “ACoA syndrome,” none of whom showed significant visuospatial impairments.[27] Diamond's[33] encyclopedic review also pointed to the absence or mild impairment of VSE associated with ACoA aneurysms.

Given the discussion around the involvement of higher visual processing aspects, particularly VSE, this study aims to investigate and discuss the potential impact on visual and visuospatial abilities in a group of 31 patients who underwent surgical clipping to repair SAH secondary to ACoA aneurysm rupture. The patients' performance was analyzed using two neuropsychological tests (line judgment and Hooper) at three points over 12 months. Theoretical considerations about prognostic variables will also be addressed.

Method

This is a prospective study in which 31 patients who underwent surgical clipping for repair of SAH secondary to ACoA aneurysm rupture were evaluated between 2006 and 2010 at the vascular neurosurgery outpatient clinic of the Hospital das Clínicas, Faculty of Medicine, University of São Paulo (HCFMUSP). This project was approved by the ethics committee under no. 0272/10.

The patients, consisting of 13 women and 18 men aged between 20 and 75 years, underwent cognitive evaluation using the Hooper Test, Line Judgment Test, and Stroop Test at three-time points: 3, 6, and 12 months after surgery. Illiterate patients had multiple aneurysms, or had comorbidities affecting the brain were excluded from this study.

To assess visual and visuospatial functions, the Hooper Visual Organization Test (VOT), which evaluates visuospatial ability and was originally designed for assessing adults with neurological damage, was used. It consists of 30 figures of common objects, drawn on cards and cut into two or more parts, forming a puzzle. The figures are presented individually, and the patient is asked to identify and name the object shown on each card.[34] The Judgment of Line Orientation Test (JLO)[35] was also used to assess visuospatial orientation, emphasizing visual perception. It consists of 30 items presented in increasing order of difficulty and evaluates the ability to visually identify the angular positions of 11 lines arranged in a semicircle (0° to 180°).[34]

Visual attention was investigated using the Stroop Test to exclude attentional deficits as a primary cause of other potential deficits. The Stroop Test assesses sustained attention, selective attention, and cognitive flexibility.[29] Visual attention was evaluated using the first card, which measures sustained visual attention. The patient was asked to name the colors of 24 colored rectangles. The time taken to complete each task was timed, and both correct and incorrect responses were recorded.[36]

Descriptive statistical analyses were performed for age, gender, and education. The Kolmogorov-Smirnov test was used to determine the normality of the distribution (Gaussian curve), aiding in the choice of statistical tests for subsequent analyses. The parametric ANOVA (Analysis of Variance) test for repeated measures was applied to the Hooper Test and Line Judgment Test scores. For the Stroop Test, the non-parametric Friedman test was used. Multiple comparisons using Tukey's test were conducted to examine differences between the time points (2 × 2 comparisons).

Results

The present sample included N = 31 patients who underwent surgical clipping for the treatment of ruptured ACoA aneurysms. As shown in [Table 1], there was a variation in age (mean 47.4 years, SD ± 11.4), with 58.1% of the sample being male and 41.9% female. The mean level of education for these patients was 6.9 years (SD ± 3.7).

Table 1 Descriptive statistics of Age, Years of Schooling, and Sex

	AGE	YEARS OF SCHOOLING
Mean	47,4	6,9
Median	48,0	5,0
Minimum	20	3
Maximum	75	15
Standard deviation	11,4	3,7
n	31	31
Sex	N	%
F	13	41,9
M	18	58,1
Total	31	100,0

[Table 2] presents the results of the normality test for numerical variables to determine the appropriate statistical test for each. The Kolmogorov-Smirnov normality test was applied.

Table 2 Normality test results

	Kolmogorov-Smirnov
	Statistic	df	Sig. (p)
Hooper 3M	0,078	31	0,200
Hooper 6M	0,104	31	0,200
Hooper 12M	0,089	31	0,200
Judgment of Line 3M	0,111	31	0,200
Judgment of Line 6M	0,097	31	0,200
Judgment of Line12M	0,134	31	0,164
Stroop 3M	0,205	31	0,002
Stroop 6M	0,149	31	0,079
Stroop 12M	0,162	31	0,037

[Table 3] presents the statistical analyses, with the time between surgery and the three neuropsychological evaluations being 3, 6, and 12 months. Performance on the visuoperceptive Hooper Test followed a normal distribution, with mean scores of 20.2 (SD ± 4.4), 21.5 (SD ± 4.7), and 20.9 (SD ± 4.6) for the respective periods, with a significant difference observed between 3 and 6 months.

Tabela 3 Comparativos entre 3 momentos: 3 meses, 6 meses e 12 meses segundo as 3 variáveis numéricas de interesse: Hooper, Julgamento de linhas

		3 months	6 months	12 months	Repeated Measures ANOVA or Friedman Test (p)	Multiple 2 × 2 Comparisons	Result
Hooper	Mean	20,2	21,5	20,9		3m × 6m - p = 0,043*	3m < 6m
	Median	20,5	22,0	21,5	0,023*	3m × 12m - p = 0,496	3m = 12m
	Standard deviation	4,4	4,7	4,6		6m × 12m - p = 0,343	6m = 12m
	n	31	31	31
Judgment of Line	Mean	19,0	19,7	21,2		3m × 6m - p = 0,747
	Median	19,0	20,0	22,0	0,002*	3m × 12m - p = 0,007*	3m = 6m < 12m
	Standard deviation	4,9	4,3	4,7		6m × 12m - p = 0,053
	n	31	31	31

Performance on the visuospatial Benton Line Judgment Test also followed a normal distribution, with mean scores of 19 (SD ± 4.9), 19.7 (SD ± 4.3), and 21.2 (SD ± 4.7) for the respective periods, with a statistically significant difference observed between the results at 3 and 12 months.

[Table 4] shows that Stroop-I scores did not follow a normal distribution, and no significant difference was observed across the three-time points of the study. The sample's mean scores were 18.35 (SD ± 5.82), 19.06 (SD ± 5.94), and 18.3 (SD ± 4.39). Based on the sample's demographic profile and the reference values from the test manual, the mean reference values from the manual for individuals aged 40 to 49 years and 50 to 59 years with 5 to 8 years of education are 19.12 and 18.25, respectively. The average performance on Stroop-I suggests that the deficient performance in visual domains is not secondary to attentional impairment, a domain that does not appear to be compromised in these patients.

Table 4 Comparisons across 3 time points: 3 months, 6 months, and 12 months for the 3 numerical variables of interest: Stroop

		3 months	6 months	12 months	Friedman Test (p)	Result
Stroop	Mean	18,35	19,06	18,03
	Median	17,00	18,00	17,00	0,738	3m = 6m = 12m
	Standard deviation	5,823	5,944	4,385
	n	31	31	31

Discussion

The neuropsychological profile of patients undergoing surgery for the treatment of SAH due to ACoA aneurysm rupture has been sparsely investigated for several decades, with most studies reporting that cognition is impacted either by the disease or by the surgical treatment, which, depending on the type, may be invasive. The first recorded changes included focal declines in memory functions (particularly delayed recall), executive functions, awareness (confabulation), and behavioral changes (personality alterations), a condition that became known as “ACoA syndrome”[26] [27].

The refinement of neuropsychological (NP) methods and instruments has led to more sensitive and accurate investigations of cognition, making it possible to identify impairments in domains that were previously undetected. Attention and executive functions (EF), for instance, were not initially included among these impairments.[10] [26] However, more recent studies have revealed a different scenario, with findings showing that patients perform worse on attention tasks compared with healthy controls.[9] [18] In our study, the performance classified as average by patients on focused and selective attention tasks (Stroop) in the three postoperative NP assessments suggests the absence of impairment in this domain.

On the other hand, our results showed impacts on EF, a rarely reported finding in the literature. Despite the somewhat hierarchical relationship between attention and other cognitive domains, our data suggest that EF was not impacted secondarily by attention, which was preserved. Neural networks more closely related to visuospatial functioning may have been affected by the SAH and treatment.

In Beeckman et al.'s recent study,[9] 35 operated patients and 20 healthy controls were evaluated on tasks of attention (sustained, divided, and alternating), memory (auditory-verbal and visuospatial), executive functions (verbal fluency, abstract reasoning, planning, and problem-solving), and visuospatial functions (visuospatial judgment and visuospatial construction). The authors noted significantly worse performance of patients on sustained, divided, and alternating attention tasks, but not on visuospatial functions. Regarding EF and memory, their findings confirmed previous studies, with impairments in these domains being cardinal signs of “ACoA syndrome.” However, memory impairment was more severe than previously reported, with declines identified in both immediate and delayed recall tasks, as well as in tasks of both auditory-verbal and visual nature. Previous studies, such as those by DeLuca[26] and Ravnik et al.,[18] had reported relative preservation of short-term memory systems for this group of patients, with greater impact on long-term systems.

Beeckman et al.[9] argued that such discrepancies stem from methodological issues. According to the authors, some biases may have compromised the identification of other affected domains in previous studies, such as the absence of more sensitive instruments for assessing skills like visual and visuospatial abilities. Therefore, we recommend the adoption of diverse and specific instruments for these functions in future studies with this patient group, as our findings suggest alterations in these functions. It is worth noting that we were unable to investigate these functions in greater depth in our study due to the research design, which involved adopting the institution's NP protocol. Indeed, the initial aim of the group was to conduct a more global investigation of cognition based on literature findings pointing to “ACoA syndrome” rather than analyzing specific functions or domains. For this same reason, it was also not possible to investigate more deeply some physiological variables that have been generically suggested as possible causes or aggravators of cognitive impairments.

Regarding EF, Beeckman et al.,[9] as mentioned above, did not detect a decline in these patients. Our results suggest otherwise. In the instruments dedicated to evaluating visual synthesis ability (Hooper test) and visuospatial orientation and perception (line judgment), many patients scored below the expected age average. In the Hooper, the mean score of our group was 20.2 (SD ± 4.4), 21.5 (SD ± 4.7), and 20.9 (SD ± 4.6) in assessments conducted three, six, and twelve months after surgery. The instrument's manual establishes, for score ranges of 16–18, 19–20, and 21–22, high, moderate, and low deficit probabilities, respectively. Considering the SD, it can be observed that some patients remained in the most severe classification range even after the longer postoperative period.

In the case of line judgment, the mean score of our group was 19 (SD ± 4.9), 19.7 (SD ± 4.3), and 21.2 (SD ± 4.7), under the same temporal conditions mentioned above. The best possible score of 25.9 (i.e., 21.2 + 4.7) corresponds, according to the instrument manual, to the 56th percentile. Score ranges of 23–24, 21–22, and 19–20 correspond to the 40th, 22nd, and 9th percentiles, respectively.

Statistically, a decline followed by improvement in average performance can be observed in both the visual synthesis test (Hooper) particularly in the second evaluation, six months after surgery—and the visuoperceptive test (line judgment), especially in the third evaluation, twelve months after surgery, evidencing the expected transitory nature of this sequela. The improvement in both tests allows us to conclude, first, that the impacted function resulted from the cerebrovascular event and/or treatment, second, that it was not secondary to any possible attentional impairment (whose performance, as reiterated, remained constant and within average throughout the period), and third, that this sequela tends to present a good prognosis within a year after the clipping operation.

The line judgment test was also used by Beeckmans et al.[9] and DeLuca.[26] The average score obtained by Beeckmans' 19 patients, evaluated three months after surgery, was higher than that obtained by our 31 patients evaluated 12 months post-surgery (24.4 × 21.2). DeLuca's patients tested a few days post-operation, also performed better than those in our sample (24.6 × 21.2).

It is noted that visuospatial functioning impairments are not always identified by studies, either through testing or by the subjective reports of patients or their caregivers. Likely, this domain is not significantly affected, at least in many cases, to the point of guaranteeing its detection, nor does it impact patients' functionality in everyday tasks requiring such skills, a hypothesis that could be explored in future research.

There has been a debate about whether the pattern of post-surgical cognitive sequelae manifested by SAH patients in the ACoA follows a focal or diffuse logic. DeLuca[26] found evidence supporting the former hypothesis, noting, in one sample, the preservation of global IQ but impaired performance on delayed recall and executive functioning tasks (constituting the “ACoA syndrome”). His study compared the performance of 11 SAH patients in the ACoA (experimental group) with that of 13 controls who had SAH in other vessels. Relative to the control group, the experimental group exhibited worse performance limited to delayed recall tasks (e.g., logical memory test) and EF (e.g., persevering errors on the Wisconsin test). On the other hand, the experimental group performed better on attentional and visuospatial tasks and had higher IQs than the controls. The author suggested that focal damage might be associated with focal lesions in anterior brain regions (e.g., basal forebrain).

Similarly, Ravnik et al.[18] found that, regarding the process of memory and learning, patients with SAH in the ACoA experience more difficulties in certain stages rather than exhibiting a global decline in this domain. In their case, greater impairment was observed in the recall stage than in the ability to store information (suggesting a possible overlap of executive functioning, necessary for the ability to retrieve content from long-term memory systems). Both DeLuca[26] and Ravnik et al.[18] suggest that the disruption of connections between frontal and limbic areas due to lesions in perforating branches of the ACoA accounts for the reduced recall ability, while the limbic structures traditionally associated with memory are preserved.

The fact that our results revealed impairments in functions less related to anterior regions, such as visual processing skills (e.g., EF and visual synthesis ability), may be evidence of the second hypothesis (i.e., a diffuse pattern of cognitive damage). It is likely that, due to the association between cognition and physiological phenomena (e.g., vasospasm, blood toxicity, neuroinflammation, brain edema), and not only the disruption of the connection between frontal and limbic areas, the brain's lesions are not confined to specific areas but rather affect the entire brain. Some studies that concluded in favor of the diffuse hypothesis were cited by Ravnik et al.,[18] demonstrating that the debate remains unresolved. We reiterate that, due to research design issues, our study did not include the analysis of surgical or physiological variables.

Ravnik et al.[18] suggested that blood toxicity in contact with parenchyma and surgical treatment are factors that can generate cognitive impacts from a more localized perspective (EF and verbal and visual recall) but recognized studies that showed more diffuse impairments. The pharmacotoxic effects of anesthesia may also account for the diffuse cognitive decline in these patients. The effects of anesthesia on cognition have been gaining relevance in recent years, although still at an early stage.

To our knowledge, no specific studies have investigated anesthetic side effects as a potential risk factor for cognitive decline in this patient population. However, Ancelin et al.[37] reported impairment of various cognitive functions, including EF, in patients undergoing orthopedic surgeries. According to them, neuronal changes related to aging can be exacerbated by the pharmacotoxic effects of anesthetic substances. Such substances could, for example, promote the acceleration of mild neurocognitive disorders toward forms of dementia. Furthermore, they noted that visuospatial functioning is a particularly vulnerable aspect of cognition in normal aging, in addition to being a hallmark of vascular-type neurocognitive disorder. In this sense, anesthesia could initiate or accelerate subcortical vascular lesions, culminating in more permanent declines, especially in visuospatial functions. If this conclusion applies to orthopedic patients, it is highly likely that it also applies to neurological patients.

Neuroinflammatory effects may also account for part of the postoperative cognitive decline. According to Saxena & Maze,[37] natural defensive reactions of the body are triggered by tissue injury or infections, a phenomenon involving a complex interaction between the immune system and the brain. This is an essential organic response for the body's self-repair, but it can, under certain conditions (e.g., advanced age, low cognitive reserve, insulin resistance, obesity), produce deleterious effects, including on cognition, by favoring excessive inflammatory responses. One of the reasons for cognitive damage, according to the authors, is that inflammatory processes can impact synaptic plasticity, which underpins cognitive processes such as learning and memory. Although the authors referred only to memory components, it is possible that others, such as EF, are also impacted by chronic neuroinflammatory states.

It is worth noting that tissue damage is invariably inevitable during the treatment of ruptured aneurysms through the clipping method. Depending on clinical variables, more invasive methods may be necessary, increasing the extent of lesions, the inflammatory response, and possibly the cognitive sequelae. However, some authors, such as Hadjivassiliou et al.[38] concluded that the cognitive sequelae exhibited after treatment are more associated with complications from SAH, i.e., the cerebrovascular disease, than with the chosen treatment modality. In any case, it is recommended that future research investigate the association between neuroinflammatory aspects and cognitive deficits in patients operated on for SAH in the ACoA.

Surgical resection of a small portion of the gyrus rectus, for example, may be necessary in some cases. This surgical maneuver aims to facilitate access and visualization of the frontobasal region, where the ACoA and its perforating branches are located. Some studies assume that it is a safe technique from the perspective of cognitive sequelae.[17] Joo et al.[17] investigated this hypothesis based on cognitive screening conducted in a group of 39 patients, 15 and 44 days after surgery. Although they only used the Mini-Mental State Examination, the authors did not observe significant differences in cognitive performance between the group of patients who had the gyrus rectus resected (∼65% of the sample) and the group where this maneuver was not necessary. The researchers observed a slight trend toward better performance by the second group (the “non-resected” patients). During the first evaluation, resected patients showed, on average, poorer performance, especially in verbal and executive domains, with improved scores obtained in the second evaluation.

Another potential risk factor for cognitive sequelae mentioned by some studies is vasospasm. Kreiter et al.[39] investigated predictive factors of cognitive impairment in a group of 113 patients affected by hemorrhagic stroke (not restricted to the ACoA but mostly located in anterior regions) three months after surgery. Overall, the sample's performance was below the population average in eight neuropsychological domains: global mental state, visual memory, verbal memory, reaction time, psychomotor functioning, executive functioning, visuospatial functioning, and language.

Regarding vasospasm, the authors concluded that the phenomenon does not appear to correlate clearly with the cognitive decline observed in these patients, contrary to what had been suggested in earlier studies. According to Kreiter et al.[39] the recent development of medications used in vasospasm management, such as nimodipine, suggests that other sources of infarction or ischemia (e.g., procedural complications) are likely more responsible for cognitive damage than vasospasm itself.

Determining which cognitive functions and to what extent they are potentially impaired by the disease and/or treatment leads to the issue of determining the transience or permanence (or the transience of some and permanence of others) of sequelae, something that remains uncertain.[9] Clarifying this issue could help optimize neuropsychological rehabilitation programs that are more effective for the profile of these patients, suggesting the implementation of predominantly restorative strategies for potentially transient damage or predominantly compensatory strategies for permanent conditions.

Methodological difficulties justify the scarcity of research on patients operated on after a considerably long period following surgery. The present study followed the evolution of 31 patients at three moments (three, six, and twelve months) after surgery. Other studies limited the observation of their respective samples to similar or, occasionally, slightly longer intervals,[9] [18] [26] which represents a limitation of those studies.

Some studies, however, observed the evolution of patients over a longer period. Nassiri et al.,[9] for example, mapped, albeit generically, the global cognitive functioning and quality of life of 32 of these patients approximately eight years after surgery. Standardized tests were not used. Cognitive complaints (in the domains of memory, perception, and motor functioning) in daily life activities were reported by participants from all three groups. Overall, six (19%), all belonging to the clipping groups, scored in a way that suggested cognitive impairment, with worse performance on the instruments assessing cognition. Eight years after surgery, the patients continued to report cognitive complaints, with better performance in the group of patients treated by embolization.

We emphasize that, although the results of this study found visuospatial impairment, the initial objective of this work was to investigate the different cognitive functions and not only the altered abilities. For this reason, we suggest the conduction of further studies that utilize a greater quantity and diversity of instruments for visuospatial functions, as well as more specific and sensitive tests for attentional abilities.

Our findings directly contribute to the discussion about “ACoA syndrome,” particularly concerning visuospatial functions, which have so far been less explored in the literature. The significant improvement in patients' performance on visual orientation and organization tests over 12 months suggests that initially observed deficits may be transient and not necessarily permanent, as suggested in previous studies.[9] [26] This reinforces the hypothesis that, although “ACoA syndrome” involves severe neuropsychological impairment, some cognitive functions, especially visuospatial ones, may show progressive recovery over time, opening new perspectives for rehabilitation approaches focused on these specific domains.

Conclusion

We conclude that, indeed, several cognitive functions are impaired by cerebrovascular disease (SAH in ACoA) and by the surgical treatment for its correction. However, contrary to the extensive literature pointing to an “ACoA syndrome” (memory, executive functions, alterations in consciousness, and personality), we observed that a group of functions anatomically “more distant” from the frontotemporal regions may also be impaired, albeit more subtly, as is the case with visuospatial and visuoperceptual abilities. This impairment is apparently followed by a positive prognosis within a year after surgery, considering the increasing performance of our samples in the tests dedicated to these abilities. By comparing our data with recent, though sparse, studies that have investigated the association between certain physiological phenomena and cognitive impairment, we hypothesize that such factors may have, to some extent, contributed to this decline. It is worth noting that these phenomena (vasospasm, bleeding, anesthetic toxic effects, among others) represent threats to the brain from a diffuse perspective, while the ACoA stroke and its respective treatment are more circumscribed to the frontotemporal region, explaining the heterogeneity of neuropsychological profiles in these patients.

Conflict of Interest

None.

• References

• 1 Seibert B, Tummala RP, Chow R, Faridar A, Mousavi SA, Divani AA. Intracranial aneurysms: review of current treatment options and outcomes. Front Neurol 2011; 2: 45
• 2 Figueiredo EG. Aneurismas cerebrais - Prof. Dr. Eberval Gadelha Figueiredo. São Paulo: Sociedade Brasileira de Neurocirurgia; 2017 [accessed 2021 Feb 13]. Available from: http://portalsbn.org/portal/aneurismas-cerebrais-prof-dr-eberval-gadelha-figueiredo
• 3 Galvão J, Lima DD, Haas LJ. Prevalência de aneurismas cerebrais incidentais entre homens e mulheres. Saúde Pesqui 2020; 13 (02) 309-316
• 4 Adamson J, Humphries SE, Ostergaard JR, Voldby B, Richards P, Powell JT. Are cerebral aneurysms atherosclerotic?. Stroke 1994; 25 (05) 963-966
• 5 Rabelo NN, Pereira VHH, Sant'Anna MAF, Dias Jr LA, Dias LA, Pereira CU. Anterior communicating artery aneurysms: analysis of case studies. J Bras Neurocir 2016; 27 (04) 295-300
• 6 Hernesniemi J, Dashti R, Lehecka M. et al. Microneurosurgical management of anterior communicating artery aneurysms. Surg Neurol 2008; 70 (01) 8-28 , discussion 29
• 7 Nassiri N, Sheth SA, Amans MR. et al. Cognitive outcomes in treated and untreated cerebral aneurysms: a systematic review and meta-analysis. J Neurosurg 2018; 128 (03) 768-778
• 8 Gomez-Andres A, Suades A, Cucurell D, de Miquel MA, Juncadella M, Rodríguez-Fornells A. Electrophysiological correlates of feedback processing in subarachnoid hemorrhage patients. Neuroimage Clin 2019; 24: 102075
• 9 Beeckmans K, Crunelle CL, Van den Bossche J. et al. Cognitive outcome after surgical clipping versus endovascular coiling in patients with subarachnoid hemorrhage due to ruptured anterior communicating artery aneurysm. Acta Neurol Belg 2019; 119 (04) 461-468
• 10 Diamond BJ. Anterior communicating artery. In: Kreutzer JS, DeLuca J, Caplan B. editors Encyclopedia of clinical neuropsychology. 2018 ed.. New York: Springer International Publishing; 2018. . p. 260-6
• 11 Beeckmans K, Vancoillie P, Michiels K. Neuropsychological deficits in patients with an anterior communicating artery syndrome: a multiple case study. Acta Neurol Belg 1998; 98 (03) 266-278
• 12 Chan A, Ho S, Poon WS. Neuropsychological sequelae of patients treated with microsurgical clipping or endovascular embolization for anterior communicating artery aneurysm. Eur Neurol 2002; 47 (01) 37-44
• 13 Mugikura S, Kikuchi H, Fujii T. et al. MR imaging of subcallosal artery infarct causing amnesia after surgery for anterior communicating artery aneurysm. AJNR Am J Neuroradiol 2014; 35 (12) 2293-2301
• 14 Kreiter KT, Copeland D, Bernardini GL. et al. Predictors of cognitive dysfunction after subarachnoid hemorrhage. Stroke 2002; 33 (01) 200-208
• 15 Ravnik J, Starovasnik B, Sesok S. et al. Long-term cognitive deficits in patients with good outcomes after aneurysmal subarachnoid hemorrhage from anterior communicating artery. Croat Med J 2006; 47 (02) 253-263
• 16 Egeto P, Loch Macdonald R, Ornstein TJ, Schweizer TA. Neuropsychological function after endovascular and neurosurgical treatment of subarachnoid hemorrhage: a systematic review and meta-analysis. J Neurosurg 2018; 128 (03) 768-776
• 17 Joo MS, Park DS, Moon CT, Chun YI, Song SW, Roh HG. Relationship between gyrus rectus resection and cognitive impairment after surgery for ruptured anterior communicating artery aneurysms. J Cerebrovasc Endovasc Neurosurg 2016; 18 (03) 223-228
• 18 Cullum CM, Rossetti HC, Batjer H, Festa JR, Haaland KY, Lacritz LH. Cerebrovascular disease. In: Morgan JE, Ricker JH. editors Textbook of clinical neuropsychology. 2nd ed.. New York: Routledge; 2018. . p. 350-86
• 19 Weir B. Vasospasm. In: Spetzler RF. editor Cerebral aneurysms. Baltimore: Williams & Wilkins; 1995. . p. 401-20
• 20 Stenhouse LM, Knight RG, Longmore BE, Bishara SN. Long-term cognitive deficits in patients after surgery on aneurysms of the anterior communicating artery. J Neurol Neurosurg Psychiatry 1991; 54 (10) 909-914
• 21 Guaresi JR, Iung TC, Branco LTO, Medeiros MS, Sakae TM. Sequelas em pacientes com hemorragia subaracnóide por ruptura de aneurisma intracraniano. Arq Catarin Med 2011; 40 (02) 91-96
• 22 Pena MCS, Sobreira EST, Souza CP, Oliveira GN, Tumas V, do Vale FAC. Visuospatial cognitive tests for the evaluation of patients with Parkinson's disease. Dement Neuropsychol 2008; 2 (03) 201-205
• 23 Bolognani SAP, Covre P, Landucci-Moreira D, Rivero TS, Brucki SMD, Bueno OFA. Neuropsychological rehabilitation in a patient with ruptured anterior communicating artery aneurysm: 48 month outcomes. Dement Neuropsychol 2007; 1 (04) 407-411
• 24 Santos CB, Carvalho SC, Figueiredo EG, Teixeira MJ. Neurophysicological findings after anterior communicant artery aneurysm surgery (AcomA): a literature review. Braz Neurosurg 2011; 30 (01) 14-18
• 25 Bauer RM. Visuospatial, visuoperceptual, and visuoconstructional disorders. In: Parsons MW, Hammeke TA. editors Clinical neuropsychology: a pocket handbook for assessment. 3rd ed.. American Psychological Association; 2014. . p. 291-318
• 26 DeLuca J. Cognitive dysfunction after aneurysm of the anterior communicating artery. J Clin Exp Neuropsychol 1992; 14 (06) 924-934
• 27 Molino I, Cavaliere C, Salvatore E, Quarantelli M, Colucci L, Fasanaro AM. Is anterior communicating artery syndrome related to fornix lesions?. J Alzheimers Dis 2014; 42 (Suppl. 03) S199-S204
• 28 Ogden JA, Mee EW, Henning M. A prospective study of impairment of cognition and memory and recovery after subarachnoid hemorrhage. Neurosurgery 1993; 33 (04) 572-586 , discussion 586–587
• 29 Lezak MD. Neuropsychological assessment. 5th ed.. New York: Oxford University Press; 2012
• 30 Strauss E, Sherman EMS, Spreen O. A compendium of neuropsychological tests: administration, norms, and commentary. 3rd ed.. New York: Oxford University Press; 2006
• 31 Ancelin ML, de Roquefeuil G, Scali J. et al. Long-term post-operative cognitive decline in the elderly: the effects of anesthesia type, apolipoprotein E genotype, and clinical antecedents. J Alzheimers Dis 2010; 22 (Suppl. 03) 105-113
• 32 Saxena S, Maze M. Impact on cognitive function of inflammatory response to surgery, the role of anesthesia, and other factors. Minerva Anestesiol 2018; 84 (04) 517-528
• 33 Hadjivassiliou M, Tooth CL, Romanowski CA. et al. Aneurysmal SAH: cognitive outcome and structural damage after clipping or coiling. Neurology 2001; 56 (12) 1672-1677
• 34 Riina HA, Lemole Jr GM, Spetzler RF. Anterior communicating artery aneurysms. Neurosurgery 2002; 51 (04) 993-996 , discussion 996
• 35 Kreiter KT, Rosengart A, Claassen J. et al. Predictors of cognitive dysfunction after subarachnoid hemorrhage. Stroke 2014; 35 (08) 2002-2007
• 36 Mortimer AM, Saunders T, Cook JL, Cross JJ. Endovascular treatment of unruptured anterior communicating artery aneurysms: outcomes and mid-term follow-up. Clin Radiol 2015; 70 (05) 522-530
• 37 Saxena S, Kruys V, Vamecq J, Maze M. The Role of Microglia in Perioperative Neuroinflammation and Neurocognitive Disorders. Front Aging Neurosci 2021; 13: 671499 10.3389/fnagi.2021.671499
• 38 Hadjivassiliou M, Tooth CL, Romanowski CAJ. et al. Aneurysmal SAH: cognitive outcome and structural damage after clipping or coiling. Neurology 2001; 56 (12) 1672-1677 10.1212/WNL.56.12.1672
• 39 Kreiter KT, Copeland D, Bernardini GL. et al. Predictors of cognitive dysfunction after subarachnoid hemorrhage. Stroke 2002; 33 (01) 200-208 10.1161/hs0102.101629

Publication History

Received: 14 October 2024

Accepted: 27 December 2024

Article published online:
27 March 2025