The microsurgical anatomy of the paracentral lobule artery: a cadaveric series

doi:10.21203/rs.3.rs-4903088/v1

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The microsurgical anatomy of the paracentral lobule artery: a cadaveric series

https://doi.org/10.21203/rs.3.rs-4903088/v1

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Purpose

The paracentral lobule artery (PLA) is a typically present branch of the distal anterior cerebral artery (ACA), irrigating the homonymous lobule. The PLA origin is either a pericallosal portion of the ACA or a prominent branch of the ACA termed callosomarginal (CMA). In addition to the paracentral lobule, the PLA irrigates the cingulate gyrus in the medial hemispheric surface, and the superior portion of the precentral and postcentral gyri in the lateral hemispheric surface. The present cadaveric case series aimed at establishing previously unreported morphometric estimates of the PLA, including its length according to its site of origin, its supplying branches according to its distribution area, as well as its anastomoses.

Methods

Seventeen colored latex-injected cadaveric heads were studied with a surgical microscope and microsurgical instruments.

Results

The PLA was invariably present and most commonly originated from the A4 (n = 15 hemispheres, 50%) segment of the ACA. Other PLA origins were the CMA (n = 10, 30%), the A3 (n = 5, 16.7%) and the A5 (n = 1, 3.3%) segments. When the PLA originated from the A4, its mean (SD) overall length was 7.6 (17.9) mm and its mean (SD) diameter was 0.88 (0.26) mm. The PLA supplied the paracentral lobule, cingulate gyrus and post central gyrus with a mean (SD) of 28.07 (13.4), 8.53 (4.27), 5.92 (4.4) branches respectively and the precentral gyrus with a median [IQR] of 2 [0–6] branches. The most common anastomoses of the PLA in the medial and the lateral hemispheric surface involved the ipsilateral posterior internal frontal artery and the branches of the middle cerebral artery, respectively. There were no significant differences between genders or hemispheric sides for the anatomical features of the artery analyzed.

Conclusion

The present study established previously unreported morphometric estimates for the PLA by considering all possible PLA variant origins and morphological variants. Given that variable pathologies have been previously detected in the areas supplied by the PLA, a better understanding of its anatomy can aid surgical planning and approaches.

Paracentral lobule

distal anterior cerebral artery

vascular anatomy

microsurgical anatomy

The paracentral lobule artery (PLA) is a terminal branch of the anterior cerebral artery (ACA). According to Fischer, the commonly used classical segmentation scheme divides the ACA into 5 segments [1, 2]. The A1 segment is proximal to the anterior communicating artery (AComA), and the A2 segment extends from the origin of the AComA to the junction between the rostrum and the genu of the corpus callosum. The A3 segment winds around the genu of the corpus callosum and ends where the artery turns posteriorly above the genu. The A4 and A5 segments are located above the corpus callosum, and the border between these two segments is the projection of the coronal suture onto the midline. The origin of the PLA reported in previous cadaveric and angiographic studies shows variation. Thus, some studies indicate that one of the three pericallosal segments of the ACA (A3, A4 or A5) is the most common origin of the PLA. In contrast, others indicate the callosomarginal artery (CMA) as its most common origin [2–9]. The CMA corresponds to the prominent ACA branch coursing in or around the cingulate sulcus [2, 7, 8]. Previous anatomical descriptions of the PLA’s course, indicate that the vessel usually runs within the cingulate sulcus in the medial surface of the hemisphere and then upwards supplying the cingulate gyrus and the homonymous (paracentral) lobule [3, 10]. In many cases, the vessel continues its course on the lateral hemispheric surface and gives off branches to the upper part of the premotor, motor and sensory cortex [2, 3, 5, 6]. According to most studies, the PLA supplies a functionally important neocortex area and is rarely absent[2–5, 8, 10, 11]. Of note is that duplication or even triplication of this artery has been reported [10, 11].

Only a few studies have previously provided morphometrical data on the PLA, such as the distance of the artery from the origin of the AComA and its diameter [2–8, 11]. Moreover, Ciliers and Page (2017) identified gender and age differences in the distance of the PLA from the AcomA and its diameter, respectively [11]. Nevertheless, anatomical features such as the anastomoses of the PLA and the number of its supplying branches have not been established in previous studies.

New surgical approaches and appropriate planning for the paracentral lobule area demand an understanding of the relation of this artery with structures such as the corpus callosum and the upper surface of the hemisphere. The paracentral lobule is a trapezoid-like area in the medial surface of hemispheres between the frontal and parietal lobes [12]. The anterior border of this lobule lies behind the end of the medial frontal gyrus, its posterior border is the marginal ramus of the cingulate sulcus, its inferior is usually the cingulate sulcus, while its superior is the upper edge of the medial surface of the hemisphere. It can be classified according to its morphology as continuous, partial and segmented [13]. It forms part of the so-called central lobe with the pre-central, post-central and subcentral gyrus [12]. The paracentral lobule is responsible for motor and sensory control of the perineum and contralateral lower limb. It can also be divided into an anterior and a posterior segment by the indentation of the central sulcus, a division which also has a functional role as the anterior segment is the motor cortex and the posterior sensory with cytoarchitectonic differences between them [13, 14]. Aside from the homonymous artery, the paracentral lobule is also supplied by the posterior internal frontal artery and the superior internal parietal artery [12]. It drains via paracentral veins to the superior sagittal sinus[12].

The present study aims at describing the detailed microanatomy of the PLA. It provides previously unreported anatomical features, including the length of the artery according to its site of origin, its anastomoses, as well as the number of its proximal branches in the medial and outer cerebral surface. Moreover, the present study tested the hypothesis that anatomical features of the PLA display significant differences between genders or between the two hemispheres (anatomical asymmetry).

For the present study, 17 cadaveric formalin-fixed human heads (Science Care, USA) without known brain pathology, were used, which had been injected with intravenous/intra-arterial colored latex. Microneurosurgical equipment and a Carl Zeiss (Oberkochen, Germany) Meditec AG OPMI Pico Surgical Microscope were used in the dissection. Any hemisphere with poor quality vessel latex or brain parenchyma was excluded from the study.

Dissection Procedure

The brain together with its meninges was extracted via a circumferential craniectomy with the use of a craniotome (Midas Rex®, Medtronic USA). A bilateral parafalcine c-shaped dura incision was carried out and the pedicles were reflected in the midline. At this stage, the presence of arterial anastomoses between the two hemispheres (interhemispheric branches) was assessed. Then, the dura was removed with scissors. The hemispheres were split with a sagittal transection of the corpus callosum (CC). The ACA branching pattern was determined in the medial surface of each hemisphere about the distribution area. For the ACA, the Fischer classification [1] was used and the CMA was defined as absent or present according to Cavalcanti et al. [7] who defines the CMA as the longest vessel that courses in or above the cingulate sulcus, giving rise to at least 2 cortical branches.

Starting from the medial surface, the branches of ACA were dissected, and the arachnoid was carefully peeled along its course toward the external surface. The paracentral lobule was identified as the area between the marginal ramus of the cingulate sulcus, the cingulate sulcus, the medial frontal gyrus and the upper edge of the medial surface of the hemisphere.

Morphological and morphometrical data

The PLA origin was identified, and its diameter was measured with the use of a Vernier digital calliper (Würth Group, Künzelsau, Baden-Württemberg, Germany). The branches along its course and any possible anastomoses in the ipsilateral hemisphere (intrahemispheric anastomosing branches) were carefully investigated under the surgical microscope. The vessel’s trajectory in the medial surface was defined as the distance from the origin to the superior hemispheric point where it turns to the lateral/outer surface, with the vessel in its natural position and shape. The vessel’s trajectory in the lateral/outer surface was defined as the straight-line distance from the origin to the visible end of the vessel. On the other hand, the length of the vessel was calculated as the distance from the origin to its end point with the vessel dissected and straightened with non-toothed forceps. The areas of distribution were also noted. Then the same measurements were applied separately to the external/lateral surface. In addition, each hemisphere's medial surface rostrocaudal length was measured as the longest distance between the frontal and the occipital poles at the mid-sagittal level of each hemisphere. The distance of the PLA origin from the splenium and from the superior part of medial surface was also determined. The distance of the origin of PLA from the superior edge of the hemisphere at the mid sagittal level was calculated as the vertical length from the origin of the artery to the horizontal line that passes from the superior edge of the hemisphere. The distance of the origin of the PLA to the splenium was calculated as the horizontal length from the origin of the PLA to the vertical line passing from the posterior border of the splenium.

Statistical analysis

All variables were tested for normal distribution with the Shapiro-Wilk test. The measured PLA anatomic variables were assessed for statistically significant differences between hemispheres and sexes. Normally distributed variables were expressed as mean value and standard deviation [mean, (SD)], whereas variables with non-normal distribution were expressed as median value and interquartile range [median (IQR)]. If the normality assumption was satisfied for the comparison of means between 2 groups, Student’s t tests were used. In contrast, the Mann-Whitney U test was used for non-normally distributed variables.

For the diameter and length of duplicated PLAs each vessel was counted as separate while for the branches of duplicated PLA a cumulative count was obtained. Pearson’s correlation coefficient was used to explore the association of 2 continuous variables with normal distribution. A correlation coefficient of 0.1 to 0.3 was considered low, 0.31 to 0.5 moderate, and > 0.51 was high. The chi-squared test was used to examine differences between categorical values. All reported P values were 2 tailed, and statistical significance was set at p-value < 0.05. Analysis was carried out using SPSS Statistics (IBM Corp. Released 2019. IBM SPSS Statistics for Windows, Version 26.0. Armonk, NY: IBM Corp).

Sample demographics

Our study population included 30 hemispheres (13 bilateral, 1 single right and 3 single left) from 17 human white subjects (8 Male, 9 Female) with a mean age (SD) of 69 (13) years.

PLA anatomical characteristics

The PLA was present in all hemispheres (100%, 30/30). The CMA (present in 76.7% of cases) was the artery of the origin of the PLA in 30% (n = 10) of hemispheres. The A4 segment in 50% (n = 15), the A3 in 16.7% (n = 5) and the A5 in 3.3% (n = 1). When the PLA originated from segments A3-A5 (21 cases), the CMA was present in 66.7% and absent in 33.3%. On the right side, A4 was the artery of origin of the PLA in 43% (n = 6) of the hemispheres, the CMA in 35% (n = 5), the A3 segment in 20% (n = 3). On the left side, A4 was the artery of origin of the PLA in 56% (n = 9) of the hemispheres, the CMA in 25% (n = 4), the A3 in 12.5% (n = 2) and A5 in 6.2% (n = 1). There was no significant association between the PLA origin and gender or side. Moreover, 3 hemispheres (10%) had a duplicated PLA. Interestingly, all cases of PLA duplication were observed in female cadavers. After its origin, the PLA ran within the cingulate and paracentral sulci in 86% of the hemispheres (N = 26) before turning sharply to the external surface where it coursed along the central sulcus in 58% of the hemispheres (N = 17). The PLA extended to the external cerebral surface in 90% of the hemispheres (N = 27).

The origin of PLA was found at a mean distance (SD) of 34.92 (8.7) mm vertically downwards from the upper edge of the hemisphere in the medial surface when the PLA originates from CMA, at a mean (SD) distance of 40.18 (8.48) mm, 34.39 (6.4) mm when the PLA originates from, respectively, the A3 and A4 and at a distance of 32.93 mm when PLA originates from A5 (single hemisphere). Also, the origin of PLA is located at a mean (SD) distance of 54.14 (12.68) mm anterior to the edge of the callosal splenium when originating from CMA, at 69.05 (7.91) mm when originating from Α3, at 48.49 (7.26) mm when originating from Α4 and at 27.3 mm when originating from Α5. The PLA’s mean (SD) external diameter was measured at 0.91 (0.28) mm at the site of origin. The PLA mean (SD) diameter on the right side was 0.96 (0.28) mm, while on the left side 0.87 (0.27) mm. There was no significant difference in the diameter of the PLA when the vessel originated from PrcA or CMA (0.88 mm vs 0.9 mm respectively).

The mean (SD) length of PLA in the medial hemispheric surface was 68.72 (28.69) mm [right side 63.75 (32.24) mm vs left side 73.35 (25.17) mm] and its mean (SD) trajectory was 49.72 (18.52) mm [right side 47.64 (21.68) mm vs left side 51.42 (16.06) mm]. These results are depicted in Table 1. At the lateral hemispheric surface, the PLA has a median length (IQR) of 30.06 (25.61–39.29) mm [left side 30.4 (20.88–45.14) mm vs right side 30 (17.7-52.65) mm] and a median trajectory (IQR) of 20.37 (10.2-26.95) mm [left side 20.4 (12.74–26.6) mm vs right side 22.2 (8-44.3) mm]. The PLA in the medial hemispheric surface had a mean (SD) length of 95.77 (19.52) mm and a mean (SD) trajectory of 67.27 (10.01) mm when it originated from A3. When it originated from the A4 it had a mean (SD) length of 71.6 (17.9) mm and a mean (SD) trajectory of 49.49 (11.35) mm. In the single case where it originated from the A5, its length was 48.3 mm and its trajectory 36 mm. These results can be summarised in Table 2. The difference in length (71.75 mm vs 73.32 mm) and trajectory (52.31 mm vs 49.53 mm) between PLA with CMA and non CMA origin was not statistically significant. The was no significant correlation between PLA length or trajectory with hemispheric rostro-caudal distance. The mean (SD) rostro-caudal distance (frontal to occipital pole) of the hemispheres was 155 (9.5) mm [right side 156 (10.4) mm vs left side 154.2 (9) mm].

Table 1

The morphometric characteristics of the PLA in total and according to side (left and right). All values are reported in mm and as means (SD) for normal distribution or median (IQR) for non-normal distribution.
	Total	Left	Right	p-value
Diameter	0.91 (0.28)	0.87 (0.27)	0.96 (0.28)	0.418
Length (Medial surface)	68.72 (28.69)	73.35 (25.17)	63.75 (32.24)	0.378
Trajectory (Medial surface)	49.72 (18.52)	51.42 (16.06)	47.64 (21.68)	0.594
Length (Lateral surface)	30.06 (25.61–39.29)	30.4 (20.88–45.14)	30 (17.7-52.65)	0.759
Trajectory (Lateral surface)	20.37 (10.2-26.95)	20.4 (12.74–26.6)	22.2 (8-44.3)	0.364

Table 2

The morphometric characteristics of the PLA according to its origin. All values are reported in mm and as means (SD) for normal distribution or median (IQR) for non-normal distribution.
	Total	Left	Right	p-value
Diameter	0.91 (0.28)	0.87 (0.27)	0.96 (0.28)	0.418
Length (Medial surface)	68.72 (28.69)	73.35 (25.17)	63.75 (32.24)	0.378
Trajectory (Medial surface)	49.72 (18.52)	51.42 (16.06)	47.64 (21.68)	0.594
Length (Lateral surface)	30.06 (25.61–39.29)	30.4 (20.88–45.14)	30 (17.7-52.65)	0.759
Trajectory (Lateral surface)	20.37 (10.2-26.95)	20.4 (12.74–26.6)	22.2 (8-44.3)	0.364
Table 1. The morphometric characteristics of the PLA in total and according to side (left and right). All values are reported in mm and as means (SD) for normal distribution or median (IQR) for non-normal distribution.
	Length	Trajectory	Distance from hemisphere upper edge (medial surface)		Distance from callosal splenium edge
CmA origin	71.75 (30)	52.31 (19.8)	40.18 (8.48)		54.14 (12.68)
A3 Origin	95.77 (19.52)	67.27 (10.01)	40.18 (8.48)		69.05 (7.91)
A4 Origin	71.6 (17.9)	49.49 (11.35)	34.39 (6.4)		48.49 (7.26)
A5 Origin	48.3	36	32.93		27.3

In the medial surface, the PLA supplied, by definition, the paracentral lobule invariably with a mean (SD) of 28.07 (13.4) branches [right side 27.14 (15.15) branches vs left side 28.88 (12.01) branches]. The PLA also supplied the cingulate gyrus in all but one specimen with a mean of 8.53 (4.27) branches [right side 7.57 (3.7) branches vs left side 9.38 (4.67) branches]. On the external surface, PLA typically supplied the upper part of postcentral gyrus in 83% of the hemispheres and the precentral gyrus in 54% of the hemispheres with a mean (SD) of 5.92 (4.4) branches [right side 6.58 (9) branches vs left side 2.58 (4.23) branches] and a median (IQR) of 2 (0–6) branches [right side 5.5 (3.08–9.75) branches vs left side 5.5 (3.16–7.67) branches] respectively. The results are summarized in Table 3. No significant differences between sexes or sides regarding branches to paracentral lobule or cingulate sulcus were noted.

Table 3

The areas of distribution of PLA branches with reference to Brodmann areas in brackets. Branches are demonstrated as means and [SD] for normal distribution ones or as median and [IQR] for non-normal distribution ones.
PLA-supplied areas by frequency and branches
Paracentral lobule (4, 5, 3, 2, 1)	100%	28.07 [13.4]
Cingulate gyrus (23, 24, 31, 32)	96.6%	8.53 [4.27]
Post-central gyrus (5,7)	83%	5.92 [4.4]
Pre-central gyrus (4,6)	54%	2 [0–6]

The present study did not find anastomoses of the PLA with arteries from the opposite hemisphere. PLA had intra-hemispheric anastomoses at the medial surface in 50% of cases (n = 15 hemispheres) as shown in Fig. 2. The most common anastomoses were with the posterior internal frontal artery (PIFA, 36.6%) followed by the SIPA (30%), and the PrCA (6.6%). At the lateral surface, anastomoses with the terminal branches of the middle cerebral artery were found in 3 cases (12.5%).

Anatomical Variability

The anatomical characteristics of the PLA determined in the present study in comparison to those in previous pertinent studies are shown in Table 4.

Table 4

Anatomic parameters regarding PLA in literature. N/A: not applicable. The most frequent origin of PLA in each study is bold.
	Perlmutter (1978)	Gomes (1986)	Stefani (2000)	Kakou (2000)	Ugur (2006)	Cavalcanti (2010)	Kedia (2013)	Cilliers (2016)	Present study
Sample size (n)	50	60	76	46	100	30	30	121	30
Presence (%)	90	98.3	97	N/A	100	N/A	100	100	100
Duplication/Triplication (%)	N/A	N/A	N/A	N/A	N/A	N/A	N/A	31.4, 0,8	10, 0
Origin (%)
CmA	26	16.9	N/A	50	66	53.6	94.3	8.7	30
A3	18	-	N/A	50	12	N/A	-	16.8	16.7
A4	32	33.8	N/A	-	18	N/A	6.6	42.4	50
A5	14	49.1	N/A	-	0	N/A	-	24.8	3.3
Other	N/A		N/A	-	2% IFA, Opposite A4 2%	N/A	-	-	-
Diameter (mm)	1.3 (0.7-2)	1.1	1.2 +/- 0.3	N/A	1.4 (0.55–2.02)	1.02 +/- 0.16	0.29	1.3	0.9 +/- 0.3

According to all studies to date, the PLA is a stable artery, nearly always present with duplication having been reported in 2 studies. According to Cilliers et al, it is the most frequently duplicated amongst other branches of distal ACA [11].

In the present study, the A4 segment of ACA was the most common site for the origin of the PLA, followed by the CMA. These findings are in line with those of Perlmutter and Rhoton [3] and Cilliers et al [11]. Other authors have previously reported the CMA as most common site of origin [2, 5, 7, 8], while Kakou et al., reported equal frequency between CMA and A3 [6]. Of note, the anatomical definition of the CMA in the aforementioned studies shows substantial variation and thus their reported rates should be interpreted cautiously.

Previous morphometric studies on the PLA have only reported the length of the origin of the PLA from the AcomA with mean values ranging from 71.9 to 84.8 mm [3, 5, 11]. In the preset study we provide a detailed analysis of the length and trajectory of the PLA according to its site of origin and indicate that these two measures show (in the medial hemispheric surface), mean values ranging between 48 to 96 mm and 36 to 67 mm, respectively. The mean diameter of the PLA established in the present study is consistent with previous findings [2–5, 7, 9].

Perlmutter and Rhoton first described the distribution areas of the PLA artery, with Brodmann areas 1, 2, 3, 4, 5, 6, 7, 32, 24, 23, 31. These refer to the paracentral lobule, parts of the cingulate gyrus and motor, premotor and somatic sensory areas [3]. In accordance this description and that of other investigators [2, 5, 6], we also confirmed the areas above of distribution for the PLA. Moreover, in the present study we provide for the first-time data on the number of proximal branches through which the PLA supplies different areas of the medial hemispheric surface along its course.

Moreover, to the best of our knowledge, this is the first study that focused on the anastomotic network of PLA. In this context, anastomoses with ipsilateral branches of the ACA and MCA were observed in 50% of the hemispheres. This highlights the presence of a reserve supply network for the important paracentral lobule in case of distal occlusion of ACA. This appears consistent with the findings of a computational blood flow study in ACA stroke models indicating that there was low probability of infarction to the paracentral lobule due to “bailout” anastomoses with the MCA and leptomeningeal arteries [15]. Preservation of this network is crucial when approaching the area for oncological or vascular lesions.

Clinical Considerations

The paracentral lobule represents a cerebral area where a variety of pathologies have been observed. Due to its crucial position as the junction between motor and sensory functions, a thorough understanding of its microsurgical anatomy including its arterial supply is a prerequisite for successful surgical approaches.

Gliomas can occur in this eloquent area and previous studies have indicated that this location is a strong independent risk factor of epileptogenicity [16, 17]. Attempting a resection in this region may result in serious neurological complications and in this regard, the surgeon should be familiar with the anatomy of the area.

Also, an fMRI study showed that the interaction between paracentral lobule and amygdala may have a role in suicidal ideation of patients with mood disorders [18]. This may indicate a possible functional target for the future. In addition, abnormalities in the cortical thickness of this area have been associated with vulnerability to psychopathology in at-risk mental state patients [19].

AVMs in the central lobe have been reported with their management being challenging due to proximity with eloquent areas. The AVMs related to the medial surface usually receive their feeders from the ACA[12, 20, 21].

Infarction of the ACA territory is rare, representing only 0.5–35 of all ischaemic strokes. Stroke in the paracentral lobule typically results in contralateral leg paresis and urinary/faecal incontinence [12, 22, 23]. This can take place when coagulating in the interhemispheric fissure branches of the PrcA or the CMA. Otherwise, this area is thought not to be vulnerable to infarction due to its rich anastomotic network[15].

Limitations

We acknowledge the main limitation of the present cadaveric study was the relatively small size of the studied cohort and thus any significant differences (or lack of) in measured anatomical parameters, should be interpreted cautiously. We nevertheless provide previously unreported anatomical characteristics of the PLA such as length and trajectory size of this vessel according to its site of origin, number of irrigating branches according to supply area and anastomoses.

In the present cadaveric study, we provide estimates of previously unreported anatomical characteristics of the PLA, namely its length and trajectory according to its site of origin, supplying branches according to its area of distribution and anastomoses with branches of the ACA and MCA. In the era of microneurosurgery, a thorough understanding of the anatomy of the PLA can aid surgical approaches in regions supplied by the PLA, including the eloquent homonymous lobule, where a wide range of lesions have been previously observed.

ACA Anterior cerebral artery

AComA Anterior communicating artery

CMA Callosomarginal artery

CC Corpus Callosum

MCA Middle cerebral artery

PLA Paracentral lobule artery

PrcA Pericallosal artery

SIPA Superior internal parietal artery

Acknowledgments

The authors sincerely thank those who donated their bodies to science so that anatomical research could be performed. Results from such research can potentially increase mankind's overall knowledge which can then improve patient care. Therefore, these donors and their families deserve our highest gratitude.

Disclosure

Authors’ Contribution

All authors contributed to the project development. The data collection and analysis were performed by G. Georgountzos (G.G.) and T. Kalamatianos (T.K.). T.K. and George Triantafyllou (G.T) made the revision of the manuscript. All authors read and approved the final manuscript.

Data Availability

All the data are available upon request to the corresponding author.

Conflict of interest

None.

Ethical Approval

The research was conducted ethically following The Code of Ethics of the World Medical Association (Declaration of Helsinki). The cadavers belonged to Department of Neurosurgery, School of Medicine, National and Kapodistrian University of Athens.

Funding

None.

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No competing interests reported.

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The microsurgical anatomy of the paracentral lobule artery: a cadaveric series

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Abstract

Purpose

Methods

Results

Conclusion

Figures

Introduction

Materials and Methods

Dissection Procedure

Morphological and morphometrical data

Statistical analysis

Results

Sample demographics

PLA anatomical characteristics

Discussion

Anatomical Variability

Clinical Considerations

Limitations

Conclusion

Abbreviations

Declarations

References

Additional Declarations

Status:

Version 1