Arterial variations and hemodynamic impact in the upper limb: Insights from an observational study

Abstract

BACKGROUND:

The incidence of arterial variations in the upper limb is variable among ethnic groups. However, there are only a few studies on the Asian population, particularly in China.

OBJECTIVE:

This research provided the first large data series on arterial variations in the upper limb of Chinese adults.

METHODS:

In this observational study, the arteries in the upper limb of consecutive patients were analyzed between July 2020 and June 2021, and the hemodynamic variables of each patient were collected.

RESULTS:

The brachial artery deviated in 6.60% of upper limbs (11.89% of patients), and the brachioradial artery (BRA) was the most frequent variation. In the wrists of all patients, the volume flow (VF) of the BRA was lower than that of the radial artery (RA). Besides, the VF of the BRA in patients with end-stage renal disease (ESRD) was lower than that in those without ESRD in the wrist. Additionally, in the forearms of patients without ESRD, the VF of the BRA was lower than that of the RA. In the upper arm of patients with ESRD, the VF of the brachial artery in patients with BRA was significantly lower than that in patients with RA.

CONCLUSION:

The incidence of arterial variations in the upper limb of Chinese adults was 6.60% (limbs) or 11.89% (patients) in this study. In our investigation, the BRA was the most common high bifurcation of the brachial artery type. Furthermore, the Chi-squared test revealed significant differences in the distribution, which was common in the right upper limb but not in sex.

Keywords

Arterial variation hemodynamic influence upper limb

1. Introduction

The incidence of arterial variations in the upper limb is estimated to range from 8% to 25%, with variations among ethnic groups [1, 2, 3, 4]. Nonetheless, there are only a few studies on arterial variations in the upper limb in the Asian population, particularly in China. Although recent large-sample autopsy anatomical studies [1, 5] have been conducted, they have not elucidated the corresponding hemodynamic changes. Additionally, many researchers point out that the pattern of arterial variations in the upper limb results in uncertain surgical prognoses [6, 7, 8]. For instance, some researchers believe that fistulas created within a high bifurcation of the brachial artery (HBBA) may lead to non-maturation or early fistula failure [9, 10]. In addition, recent studies have further explored the impacts of arterial variations in the upper limb on clinical practice. According to studies from the past three years, certain arterial variations are associated with an increased risk of surgical complications. For example, Haimov et al. (1975) found that patients with HBBA were more likely to experience complications following arteriovenous fistula surgery [11]. These studies have suggested that understanding the anatomical variations of the upper limb arteries is crucial for improving surgical outcomes. Recently, hemodynamic analysis has become an essential tool for studying arterial variations in the upper limb. In 2022, Weinberg conducted a study using computational fluid dynamics models to analyze blood flow distribution under different arterial variation patterns. They also found that wall shear stress was significantly influenced by arterial bifurcation and curvature [12]. This study has demonstrated that hemodynamic parameters are valuable in assessing the clinical impact of arterial variations. To further explore this issue, we collected comprehensive and systematic data on arterial variations in the upper limb of Chinese adults and recorded their hemodynamic changes. In this observational study, data from 917 consecutive patients hospitalized in the vascular surgery department were collected between July 2020 and June 2021. Color doppler ultrasound (CDUS) examinations were performed to assess variations in the branching pattern of the main arteries in both upper limbs. This approach allowed us to record the incidence of each variation type and its corresponding hemodynamic characteristics in detail. Moreover, factors, including age, gender, and medical history, were considered to evaluate their impact on arterial variations and hemodynamic changes. As reported in the study, older patients are more prone to arterial stiffness. With aging, arterial elasticity decreases, and the arterial walls become stiffer, leading to arteriosclerosis. This may further impact the hemodynamic characteristics of arterial variations [13].

This study aimed to provide valuable information for clinicians in surgical planning and prognostic evaluation through understanding the incidence and hemodynamic characteristics of arterial variations in the upper limb. Also, this research was designed to improve surgical success rates and reduce the incidence of complications. Further research and data accumulation are expected to provide scientific evidence for the standardized classification and assessment of arterial variations, ultimately benefiting a wide range of patients.

2. Materials and methods

2.1 Groups

There were 691 patients (73.54%) with end-stage renal disease (ESRD) in our study. They were from various regions of China, and the majority of their initial construction and repair of hemodialysis (HD) access were completed at local hospitals. For patients with established HD access, only the hemodynamic parameters of the non-access upper limb were recorded due to consequent changes in the hemodynamic status after the fistula creation. The hemodynamic status could be modified because of the dilation and thickening of the artery and vein used for HD access creation [14]. Additionally, HD access to arterial beds provided low-resistance outflow, with only spectral broadening and diastolic flow throughout the artery [15]. Moreover, the branching pattern of the BRA was similar to that of the RA in the forearm. To compare hemodynamic differences between the RA and BRA as objectively as possible, participants were divided into four groups according to the presence or absence of ESRD. The four groups were as follows: Group A: hemodynamic parameters of the RA in the upper limb of patients without ESRD; Group B: hemodynamic parameters of the BRA in the upper limb of patients without ESRD; Group C: hemodynamic parameters of the RA in the upper limb (without HD access) of patients with ESRD; and Group D: hemodynamic parameters of the BRA in the upper limb (without HD access) of patients with ESRD.

2.2 Definitions

HBBAs are classified into six types based on the published literature [16]. A high origin of the radial artery (RA) or ulnar artery (UA), with a healthy course along the forearm to the hand, is considered a brachioradial artery (BRA) (Fig. 1A) or brachioulnar artery (BUA) (Fig. 1B). Additionally, if this high origin of the RA or UA courses over the superficial forearm flexor muscles, it is defined as a superficial brachioradial artery (SBRA) (Fig. 1C) or superficial brachioulnar artery (SBUA) (Fig. 1D). The brachioulnoradial artery (BURA) (Fig. 1E) is an HBBA that divides at the elbow level into radial and ulnar arteries, besides coexisting with the brachial artery (BA), which continues as the healthy interosseous artery. The brachiointerosseous artery (BIA) (Fig. 1F) is defined by a high origin of the interosseous artery with a healthy BA that divides 1 cm distal to the elbow joint into radial and ulnar arteries.

Figure 1.

High bifurcation of the brachial artery.

2.3 Ultrasound protocol

A Mindray M7 ultrasound scanner (Shenzhen Mindray Bio-Medical Electronics Co., Ltd.; Shenzhen, China) equipped with a 6–11 MHz frequency linear transducer was adopted to perform brightness mode, color, and pulsed-wave Doppler ultrasonography. Each patient was instructed to lie in the supine position, with the arm turned externally and extended from the body at a 45-degree angle. In addition, an HBBA could originate from the subclavian artery, axillary artery (AA), or proximal, middle, and distal thirds of the BA. First, the arterial scan was performed from the axillary fossa to the transverse carpal crease for an overall appreciation of the arterial anatomy. If the origin of the HBBA was not found, the arterial-scan starting line was changed to the midclavicular line. Second, the inside diameter (ID) of the following arteries was measured: the BA (middle of the upper limb), RA or HBBA in the forearm (1 cm distal to the cubital crease), and RA or HBBA in the wrist (1 cm proximal to the transverse carpal crease). Finally, the arterial scan probe was returned to the middle of the upper limb, and its view was rotated longitudinally. To avoid measurement errors, the Doppler sample volume was set to fit the entire vessel diameter, and the Doppler angle was maintained at $<$ 60^∘. Doppler color flow imaging was used as a guide for the placement of the pulsed-wave Doppler sample volume. Calculated by a software package incorporated into the ultrasound, we recorded the volume flow (VF) of the BA in the upper arm (middle of the upper limb), the VF of the RA or HBBA in the forearm (1 cm distal to the cubital crease), and in the wrist (1 cm proximal to the transverse carpal crease).

2.4 Parameters

The demographic and comorbidity information of patients was recorded. This included sex, age, upper arm length (from the axillary furrow to the cubital crease), forearm length (from the cubital crease to the transverse carpal crease), and disease etiology (ESRD, arteriosclerosis obliterans, varicose veins, aneurysm, venous thromboembolism, and others). For anatomic HBBA data, we collected data on the type, origin, and distribution of arterial variations. The ID and VF of the BA in the upper arm and the RA, or HBBA, in the forearm and wrist were then measured.

2.5 Statistical analysis

An analysis of variance was used to compare continuous normally distributed variables between groups. Continuous variables are expressed as the mean $\pm$ standard deviation. The Kruskal-Wallis test was applied to compare continuous non-normally distributed variables, and the Nemenyi test was employed to assess group comparisons. Continuous non-normally distributed variables are expressed as medians (first quartiles, third quartiles). Comparisons of nominal variables; which were analyzed via the Chi-squared test or Fisher’s exact test, are expressed as frequencies and percentages. Additionally, comparisons between groups were tested with the Bonferroni correction test ( $\alpha=$ 0.0125). Statistical significance was defined as $P<$ 0.05. Statistical analysis was performed by SPSS 25.0 for Windows (SPSS Inc.; Chicago, IL, USA).

PASS 15.0 was employed to calculate the sample size required to achieve statistical significance in the analysis of variance, with alpha set at 0.05, power at 0.80, and group assignment set at “Equal.” Consequently, 48 limbs were included in the sample to achieve statistical significance (actual power $=$ 0.8323).

3. Results

We examined the upper limbs of consecutive patients admitted to our inpatient department. Men and women exhibited similar baseline characteristics, except that men had significantly longer upper arms and forearms than women (Table 1).

Table 1
Patient baseline characteristics

	Men	Women	$P$ -value	Total
Number of patients (limbs)	601 (1,202)	316 (632)		917 (1,834)
Age (years, quartiles)	62.00 [49.00, 70.50]	63.00 [47.00, 71.00]	0.615
Etiology of disease
ESRD	446	245	0.295	691
Arteriosclerosis obliterans	42	12	0.055	54
Varicose veins	67	35	1.000	102
Aneurysm	10	6	0.795	16
Venous thromboembolism	4	7	0.054	11
Others	32	11	0.251	43
Length of arm
Upper arm (cm, quartiles)	20.00 [19.00, 21.00]	18.70 [18.00, 19.50]	0.000
Forearm (cm, quartiles)	25.30 [24.50, 26.00]	23.50 [23.50, 24.10]	0.000

ESRD, end-stage renal disease.

Table 2

The characteristics of high bifurcation of the brachial artery

Incidence
	Men	Women	$P$ -value	Total
Patients (%)	68 (11.31)	41 (12.97)	0.455	109 (11.89)
Limbs (%)	76 (6.32)	45 (7.12)	0.553	121 (6.60)
Origination
Subclavian artery	12	11	0.189	23
Axillary artery	25	12	0.863	37
Proximal 1/3 segment of brachial artery	33	16	0.879	49
Middle 1/3 segment of brachial artery	5	3	1.000	8
Distal 1/3 segment of brachial artery	1	3	0.121	4
Distribution
Left arm	21	15	0.374	36
Right arm	39	22	0.782	61
Bilateral	8	4	1.000	12
$P$ (left/right)	–	–	0.024	–

The origin and distribution of HBBAs were presented in Table 2. The Chi-squared test revealed no statistically significant differences in the origin and distribution of HBBAs by sex. However, HBBAs occurred more frequently in the upper right limb.

According to the HBBA type, BRAs were found in 49 men unilaterally (33 right, 16 left) and in 8 men bilaterally. Besides, BRAs were discovered in 34 women unilaterally (19 right, 15 left) and in 4 women bilaterally. A BRA was more common in the right upper limb, and the Chi-squared test revealed remarkable differences in the distribution but not in sex. BUAs were found unilaterally, and there were no noticeable differences in their distribution or by sex. SBUAs were also found unilaterally, similar to BIAs; whereas a SBRA or BURA was not observed (Table 3).

Table 3

The type of high bifurcation of the brachial artery

Type	BRA	BUA	SBRA	SBUA	BURA	BIA
Men/women (patients)	57/38	7/3	–	1/0	–	3/0
$P$ (patients)	0.254	1.000	–	–	–	–
Left/right (limbs)	43/64	4/6	–	1/0	–	0/3
$P$ (limbs)	0.046	0.753	–	–	–	–
Total (limbs)	107	10	0	1	0	3
% (limbs)	5.83%	0.55%	0.00%	0.05%	0.00%	0.16%

BRA, brachioradial artery; BUA, brachioulnar artery; SBRA, superficial brachioradial artery; SBUA, superficial brachioulnar artery; BURA, brachioulnoradial artery; BIA, brachiointerosseous artery.

CDUS was conducted on 226 patients without ESRD to record the main artery branching pattern in 452 upper limbs; and 16 BRAs were discovered. However, four women without a HBBA refused the assessment of their arterial hemodynamic parameters. Moreover, CDUS was performed on 691 patients with ESRD (77 patients with bilateral HD access, 489 patients with unilateral HD access, and 125 patients without HD access) to record the branching pattern of the main arteries from 1,382 upper limbs; A total

Table 4

Arterial hemodynamic parameters of the upper limb

Group	Etiology of disease	Variation	ID of BA in the upper arm (mm)	VF of BA in the upper arm (mL/min)	ID of artery in the forearm (mm)	VF of artery in the forearm (mL/min)	ID of artery in the wrist (mm)	VF of artery in the wrist (mL/min)
A	Non-ESRD	Non-HBBA	4.10 [3.45, 4.55]	41.85 [29.20, 58.80]	2.75 [2.30, 3.20]^∗	23.59 [17.70, 30.93]^∗	2.10 [1.80, 2.50]^∗	18.26 $\pm$ 8.42^∗
		( $n=$ 428)
B		HBBA	4.08 [3.73, 4.51]	34.65 [24.20, 51.20]	2.20 [2.01, 2.95]^∗∗	17.70 [7.22, 22.20]^∗∗	1.95 [1.76, 2.64]^∗∗	12.72 $\pm$ 3.14^∗∗
		( $n=$ 16)
C	ESRD^∗∗∗	Non-HBBA	3.90 [3.40, 4.80]	42.70 [29.10, 59.80]	2.65 [2.25, 3.05]^∗	13.49 [13.08, 17.30]^∗	2.10 [1.73, 2.40]^∗	9.76 $\pm$ 4.22^∗
		( $n=$ 660)
D		HBBA	3.85 [3.50, 4.50]	29.65 [26.04, 32.27]	2.10 [1.97, 3.23]^∗∗	13.15 [9.84, 17.20]^∗∗	2.00 [1.65, 2.50]^∗∗	6.39 $\pm$ 2.90^∗∗
		( $n=$ 65)
$P$	Groups A and B		0.998	0.296	0.121	0.003	0.521	0.009
	Groups A and C		0.016	0.432	0.004	0.000	0.037	0.000
	Groups C and D		0.268	0.000	0.000	0.382	0.501	0.000
	Groups B and D		0.252	0.319	0.569	0.265	0.639	0.000

^∗: The arterial hemodynamic parameter of the RA; ^∗∗: The arterial hemodynamic parameter of the BRA; ^∗∗∗: The arterial hemodynamic parameter from the upper limb without HD access. ID, inside diameter; BA, brachial artery; VF, volume flow; ESRD, end-stage renal disease; HBBA, high bifurcation of the brachial artery.

of 105 HBBAs were discovered (91 BRAs, 10 BUAs, 1 SBUA, and 3 BIAs). In addition, 26 HD accesses were created through the BRAs, and all of them were BRA-cephalic vein arteriovenous fistulas. We also measured arterial hemodynamic parameters in 739 upper limbs (660 non-HBBAs, 65 BRAs, 10 BUAs, 1 SBUA, and 3 BIAs) without HD access.

The statistical comparison of hemodynamic parameters between Groups A and B revealed that the VF of the BRA was evidently lower than that of the RA in the forearm. Similarly, the VF of the BRA was remarkably lower than that of the RA in the wrist. In comparison between Groups A and C, the ID of the BA in patients with ESRD was statistically smaller than that in non-ESRD patients, which was similar to the ID of the RA (both in the forearm and the wrist). Furthermore, the VF of the RA (both in the forearm and the wrist) in patients with ESRD was significantly lower than that in non-ESRD patients. Comparing Groups C and D, the VF of the BA in the upper arm with the BRA variant was substantially lower than that with the RA. Additionally, the ID of the BRA was markedly lower than that of the RA in the forearm. In the wrist, the VF of the BRA was substantially lower than that of the RA. In addition, the comparison between Groups B and D exhibited that the VF of the BRA (in the wrist) in patients with ESRD was considerably lower than that in non-ESRD patients. The Kruskal-Wallis test manifested no significant differences as opposed to the other arterial hemodynamic measures (Table 4).

4. Discussion

In the upper limb, the AA continues to the BA, which begins at the distal border of the teres major muscle tendon and divides into the RA and UA 1 cm distal to the elbow, where the BA terminates [5]. Although the RA is slightly shorter than the UA, it appears to be a more direct continuation of the BA in the forearm. In addition, arterial variants were discovered in the entire upper limb (BRA, BUA, SBUA, and BIA), and no arterial variants limited to the sole upper arm or forearm were discovered. In this study, the branching patterns were individually examined based on the presence of various types of arterial variations. In our investigation, the BRA was the most common HBBA type, and it was observed unilaterally in the right upper limb more often than in the left, with significant differences (Table 3). Furthermore, the BRA started from the BA rather than from the AA, and more frequently from the upper third of the BA, followed by the middle and lower thirds. These findings were consistent with previous results [16]. Our results displayed no remarkable differences in BRA occurrence by sex (Table 3). In our research, the incidence of the BUA (Fig. 1B), defined as a high origin of the UA coexisting with a BA with common divisions, such as the radial and interosseous trunk, was lower than that of the BRA. Additionally, there were no significant differences in sex or the distribution (Table 3). The BUA was more frequently derived from the upper third of the BA than from the subclavian artery, followed by the AA. The SBUA occurrence was confirmed in our study to be the lowest, only present in a man’s left arm, originating from the upper third of his BA. Moreover, the BIA, previously reported as a rare variation [17], was observed in three men, originating from the upper third of the BA in the right arms. A SBRA or BURA was not found, despite being common BA variations. Based on our research findings, the incidence rate of deviations from the healthy pattern of the BA in Chinese adults was 6.60% (11.89% of patients). This rate was lower than the incidence rates reported in the literature for foreign populations, which ranged from 8% to 25% [18]. Studies have reported various rates of BA variations, such as 8% in Nasr’s study [19] and 9.2% in Haładaj’s study [20]. Moreover, Poiseuille stated that the flow resistance (R) through a narrow tube was determined by the length (l) and radius (r) of the tube, as well as the fluid viscosity ( $\eta$ ), which was defined as R $=8\eta l/(\pi r^{4})$ . When the liquid viscosity was under certain conditions, the flow resistance was inversely proportional to the fourth power of the tube radius, which explained the significant influence of the tube radius on the flow resistance. The BRA started more frequently in the upper third of the BA, where it was much higher than the origination of normal RA. Meanwhile, the ID of the BRA in the forearm was statistically smaller than that of the RA, making the increase in the flow resistance evidently higher in the BRA than that in the RA. Furthermore, the ID of the BA in the upper arm of patients with ESRD was statistically lower than that of patients without ESRD. In patients with ESRD, the ID of the RA in the forearm and wrist was significantly lower than that of patients without ESRD (Table 4). Therefore, the impact of ESRD on the arterial wall may result in an inability to achieve effective arterial dilation and accommodate the increased flow resistance, especially in the BRA of patients with ESRD. In addition, the Kidney Disease Outcomes Quality Initiative guidelines recommend [21], if available, a RA-cephalic vein arteriovenous fistula configuration at the wrist, which should be created first as the preferred initial HD access for patients with ESRD. Since the BRA and BA have similar alignment in the forearm and their arterial pulsations can be palpated at similar sites, the BRA is frequently confused with the RA. In our study, there were 10 immature BRA-cephalic vein arteriovenous fistulas (38.46%). This may be attributed to the statistically smaller ID of the BRA in the forearm relative to the RA and the higher origination of the BRA as opposed to the RA. Consequently, the increase in the flow resistance of the BRA was significantly higher than that of the RA, resulting in the VF of the BRA in the wrist being lower than that of the RA in patients with ESRD (Table 4).

This study had some limitations. First, the participants were consecutive patients. Although their diseases had no effect on their arterial branching patterns in the upper limb, other underlying systemic diseases, besides the renal condition, might have impacted arterial hemodynamic parameters. Second, patients with ESRD were from various regions of China. It would be a great inconvenience for them to provide their relevant surgical records. Therefore, we could not compare the site of anastomosis and the criteria for venous diameters. Finally, a SBRA or BURA was not observed in our study, indicating that the number of research participants was relatively insufficient, which would result in bias in the incidence estimates of arterial variations in Chinese adults. Future studies need to encompass a more diverse ethnic population to better understand the global incidence of arterial variations. Additionally, we plan to measure additional hemodynamic parameters to gain a more comprehensive understanding of the impact of arterial variations in the future. Furthermore, we will adopt a longitudinal study design to track and monitor changes in arterial hemodynamics over time, particularly in the development of diseases such as ESRD. Designing intervention studies to explore the effects of medical or surgical treatments on the hemodynamics of patients with arterial variations, particularly those with ESRD, will also help evaluate treatment effectiveness. Incorporating data on surgical outcomes for patients with arterial variations to assess the clinical relevance of these anatomical differences is also important. Therefore, in future studies, these data will be considered for collection and analysis to provide a more comprehensive clinical assessment.

5. Conclusions

The incidence of arterial variations in the upper limb of Chinese adults was 6.60% (limbs) or 11.89% (patients) in this study. Moreover, the BRA was the most common HBBA type in our investigation. In addition, the Chi-squared test revealed significant differences in the distribution, which was common in the right upper limb but not in sex. Finally, a further study is required to clarify the relationships among the diameter, the threshold of hemodynamic parameters of the variant vessels, and the maturity of the arteriovenous fistula established based on the variant arteries.

Funding

The authors report no funding.

Ethical approval

The study protocol was established based on the ethical guidelines of the Declaration of Helsinki and was approved by the Human Ethics Committee of Beijing Tongren Hospital, Capital Medical University (TRECKY2020-101). All participants were informed of the goal and method of our study, and their written informed consents were obtained. This study has been registered in a protocol registration and results system (Protocol ID: NCT04613115).

Data availability

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Footnotes

Acknowledgments

The authors would like to acknowledge the ethics committee and institutional review board of Beijing Tongren Hospital, Capital Medical University.

Conflict of interest

The authors declare that they have no conflict of interest.

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