Effects of ankle pump exercise frequency on venous hemodynamics of the lower limb

Abstract

PURPOSE:

The purpose of this study was (1) to compare the effects of ankle pump exercise(APE) frequency on hemodynamics of the common femoral vein(CFV) and (2) to analyse the relationship between APE duration and lower limb fatigue.

METHODS:

Twenty-seven males and thirty-three females performed APE. Among them, there were thirty participants with non-lower limb fracture (N-LLF) and thirty participants with lower limb fracture (LLF).The colour doppler ultrasound was used to record the time-averaged mean velocity (TAMV) of common femoral venous flow when the participants at rest and move at different frequencies of 6 times/min, 10 times/min, 30 times/min, 60 times/min. The ratings of perceived exertion (RPE) was used to assess the lower limb fatigue of the participants when performing APE at the frequency of 60 times/min after 1 min, 2 mins, 3 mins, 4 mins and 5 mins.

RESULTS:

With the increase of frequency, TAMV increased significantly in both the participants with N-LLF and LLF (p < 0.01). The TAMV were 19.82±3.86, 33.78±8.76, 37.06±8.67, 43.82±10.40, 52.18±10.53, respectively in the participants with N-LLF and 16.98±3.01, 22.20±4.96, 24.01±5.78, 29.20±7.05, 35.75±9.28, respectively in the injured limb of patients with LLF when at rest and moving at the frequency of 6 times/min, 10 times/min, 30 times/min, 60 times/min. There was a positive correlation (p < 0.01) between lower limb fatigue and exercise duration.When the RPE was 16 points (the corresponding fatigue degree is “tired”), the exercise duration of the participants with N-LLF was 3 mins and that of the injured limb of patients with LLF was 2 mins.

CONCLUSIONS:

Both fast and slow-frequency APE can promote venous blood return in the lower limb. Despite of the equivalent APE duration, fast-frequency APE can promote venous blood return more effectively. When the frequency of APE was 60 times/min, participants with N-LLF can exercise for 3 mins, and the injured limb of patients with LLF can exercise for 2 mins.

Keywords

Ankle pump exercise requency duration common femoral vein hemodynamics

Abbreviations

APE

Ankle pump exercise

CFV

Common femoral vein

N-LLF

Non-lower limb fracture

LLF

Lower limb fracture

RPE

Ratings of perceived exertion

TAMV

Time-averaged mean velocity

TRTB

Time from the end of the ankle pump exercise to the time-averaged mean velocity of common femoral venous blood flow returns to the baseline

DVT

Deep vein thrombosis

PTE

Pulmonary thromboembolism

THA

Total hip arthroplasty

1 Introduction

Deep vein thrombosis (DVT) is a common complication in hospitalized patients,with high incidence and great harms. In severe cases, it can cause pulmonary thromboembolism (PTE) leading to death of patients. Therefore, DVT prevention becomes particularly important. Virchow, a German biologist, put forward three major factors of DVT as early as 1856: slow blood flow, hypercoagulable state of blood and vascular intimal injury [1]. In view of the above three factors, three measures to prevent DVT were formulated, including basic prevention, physical prevention and drug prevention. There are already standardized practices for drug prevention and physical prevention, such as the use of anticoagulants and antithrombotic pump [2]. Ankle pump exercise (APE) makes the calf muscles contract and relax rhythmically through the movement of ankle joint and squeezes the venous plexus to achieve the purpose of promoting the venous blood return in lower limbs [3, 4]. It is one of the important measures of basic prevention recommended by relevant guideline [5] and has been widely used in clinical practice.However, there has been much debate about the most effective method of APE [6]. Standardized APE has not been established yet. Therefore,the purpose of this study is to analyze the effects of different APE frequency on the hemodynamics of the common femoral vein (CFV) and the effect of different exercise duration on lower limb fatigue.So as to form a suitable APE plan and provide a theoretical basis for the clinical practice guidance.

2 Methods

2.1 Participants

Sixty participants were enrolled in the study using convenient sampling (Table 1). Among them, there were thirty participants with non-lower limb fracture (N-LLF) (all of them were with upper limbs damaged) and thirty participants with lower limb fracture (LLF) (6 patients with femoral shaft fracture were treated with closed reduction and intramedullary nail fixation; 11 patients with femoral neck fracture were treated with closed reduction and screw internal fixation, 3 patients with femoral neck fracture were treated with open reduction and plate internal fixation; 10 patients with femoral trochanteric fracture were treated with closed reduction and intramedullary nail fixation; all patients with lower limb fracture were in bed).This study was approved by the hospital ethics committee.

Table 1
Baseline characteristics of the participants

Participants with N-LLF (n = 30) Participants with LLF (n = 30)

Age (years) 45.70±11.49 Age (years) 40.80±13.90

Range 20–60 Range 21–60

Sex Sex

Male 18 Male 18

Female 12 Female 12

Height (cm) 169.17±7.40 Height (cm) 170.33±5.17

Weight (kg) 67.33±11.74 Weight (kg) 65.17±10.65

Body mass index (kg/m²) 21.92±3.62 Body mass index (kg/m²) 22.37±3.17

Participants with N-LLF	(n = 30)	Participants with LLF	(n = 30)
Age (years)	45.70±11.49	Age (years)	40.80±13.90
Range	20–60	Range	21–60
Sex		Sex
Male	18	Male	18
Female	12	Female	12
Height (cm)	169.17±7.40	Height (cm)	170.33±5.17
Weight (kg)	67.33±11.74	Weight (kg)	65.17±10.65
Body mass index (kg/m²)	21.92±3.62	Body mass index (kg/m²)	22.37±3.17

Values are means±SE, N-LLF Non-lower limb fracture, LLF lower limb fracture.

Inclusion criteria:

Aged from 18 to 60 years old;

Have clear consciousness, be able to perform APE according to instruction;

Understand the assessment methods of RPE;

Volunteer to participate in the study;

Patients with LLF were required to have unilateral LLF;

Patients with LLF were confined to bed for no more than 24 hours.

Exclusion criteria:

With a history of lower limb vascular disease;

With heart and lung disease;

Operational history of chest, abdomen and pelvis;

Swelling or scarring of the groin.

2.2 Experimental design

This study was divided into two parts. The first part detected the effects of APE frequency on the common femoral venous hemodynamics; the second part analyzed the effects of exercise duration on the fatigue of the lower limb. In this study, two groups of subjects were included: one group was subjects with N-LLF, the other group was subjects with unilateral LLF. For subjects with N-LLF, the study randomly selected one side of the femoral vein to measure its hemodynamic indexes and fatigue degree; for subjects with unilateral LLF, the study was conducted to measure the hemodynamic indexes and fatigue degree of the injured limb and the healthy limb respectively. The test group is shown in Table 2.

Table 2
Test group

Group At rest (baseline) 6 times/min 10 times/min 30 times/min 60 times/min

N-LLF (Group A) A0 A1 A2 A3 A4

LLF Injured limb BI0 BI1 BI2 BI3 BI4

(Group BA)

(Group B) Healthy limb BH0 BH1 BH2 BH3 BH4

(Group BH)

Group	At rest (baseline)	6 times/min	10 times/min	30 times/min	60 times/min
N-LLF (Group A)	A0	A1	A2	A3	A4
LLF	Injured limb	BI0	BI1	BI2	BI3	BI4
	(Group BA)
(Group B)	Healthy limb	BH0	BH1	BH2	BH3	BH4
	(Group BH)

N-LLF Non-lower limb fracture, LLF Lower limb fracture.

Part 1: To detect the effects of APE frequency on the hemodynamics of CFV in participants with N-LLF and participants with LLF. Every participant took part in five trials in random order. Asked the participants to lie on the bed, after baseline measurement performing APE according to the requirements. The frequency of APE was 6 times/min, 10 times/min, 30 times/min and 60 times/min respectively. The time-averaged mean velocity (TAMV) of the common femoral venous blood flow and the time from the end of the ankle pump exercise to the time-averaged mean velocity of common femoral venous blood flow returns to the baseline (TRTB) were recorded after exercising for 1 min at the above four frequencies.

Part 2: After finishing the data analysis of the exercise frequency, the experiment about exercise duration was planned. According to the results of the first part, it was concluded that the TAMV of common femoral venous blood flow was the fastest when the APE frequency was 60 times/min. Therefore, in this part, the frequency of the APE was set to 60 times/min, and the exercise duration was set to 5 minutes for participants with N-LLF. The ratings of perceived exertion (RPE)was recorded when the participants at rest, exercised for 1 min, 2 mins, 3 mins, 4 mins, 5 mins. Considering the effect of pain on participants with LLF, the APE was performed at the frequency of 60 times/min, when RPE reached 16 points (corresponding fatigue level was “tired”), stop exercising and record the duration of the exercise.

Each participant was trained to do APE within 24 hours after being admitted to hospital and explained the self- assessment method of the RPE to them. In order to eliminate the residual effects of the previous exercises on hemodynamics and lower limb fatigue, participants were required to rest in bed for 30 minutes before each round of the trial. In order to avoid the impact of intra-abdominal pressure, breathing, and other parts’ activities on the results, participants were required to empty the bladder before the experiment, to keep breathing at a constant speed, to avoid talking, coughing, and other parts except the ankle were forbidden to move.

2.3 Method of APE

The participants took the supine position with slight abduction and external rotation of the lower limb,relaxed the thigh and the ankle was padded with a small cotton pad. Then hooked the foot (the toes face ourself), and next stretched the foot (the toes away from ourself). The frequency of movement of group A1 is 6 times/min, the dorsiflexion and plantarflexion stayed for 5 seconds; the frequency of movement of group A2 is 10 times/ min, the dorsiflexion and plantarflexion stayed for 3 seconds; the frequency of movement of group A3 is 30 times/min, the dorsiflexion and plantarflexion stayed for 1 second; the frequency of movement of group A4 is 60 times/ min, the dorsiflexion and plantarflexion be performed continuously. The angle of dorsiflexion and plantarflexion was the maximum angle that can be achieved at the specified frequency, and the maximum angle was maintained during stay. The frequency of the movement was controlled by a timer.

2.4 Self-assessment method of RPE

The RPE is divided into 15 grades. Each grade has corresponding scores, which represents different fatigue levels. After the exercise, the fatigue degree of the moving limb is given and the corresponding value of the subject is the RPE [7].

2.5 Measurement of TAMV and RPE

Bilateral common femoral venous hemodynamics were measured using the color doppler ultrasound. To avoid confounding effects from operation difference, all the measurements were performed by one operator who has been trained for the use of ultrasound before. During the test, the participants took supine position, the leg being examined relaxed. Adjusted the parameters of the ultrasound to maintain the angle between the sound beam and the derection of blood flow at 60°,the sampling volume was set to 1/2–2/3 of the diameter of the venous lumen. The detection value was automatically calculated by the computer of the Doppler system and displayed on the screen.

At the end of the exercise, the participants gave a corresponding RPE score based on their perceived fatigue of the moving limb.

2.6 Statistical analysis

Data was inserted into an SPSS database and analysed using SPSS 21.0.The data presented is regarded as being normal in distribution and the results are presented as mean±SD (x±s). T test was used for comparison between two independent samples. For comparison between multiple independent samples, LSD analysis of variance (ANOVA) was used for comparison if the homogeneity test of variance was satisfied, and Tanhane ANOVA was used for comparison if the homogeneity test of variance was not satisfied. Pearson correlation coefficient was used to express the correlation between two variables P-value is 0.05, values smaller than this are regarded as significant and values larger than this as nonsignificant.

3 Results

3.1 Effects of APE frequency on hemodynamics of CFV in participants with N-LLF

The TAMV of the common femroal venous blood flow was higher in group A1(33.78±8.76), A2(37.06±8.67), A3(43.82±10.40) and A4(52.18±10.53) than in group A0(19.82±3.86) (P < 0.01)(see Table 3). TAMV was positively correlated with the frequency of APE (P < 0.01), the faster the frequency the larger the TAMV (see Table 4).Compared with the group A0 the increase of TAMV were 70.43%,86.98%,121.09%,163.27% respectively.

Table 3
Effects of APE frequency on hemodynamics of CFV in participants with N-LLF (n = 30)

Group TAMV (cm/s) TRTB (s)

At rest 19.82±3.86 —

6 times/min 33.78±8.76^* 21.08±5.68

10 times/min 37.06±8.67 33.75±8.11^*

30 times/min 43.82±10.40^* 44.92±10.64^*

60 times/min 52.18±10.53^* 59.83±12.82^*

F 113.052 173.473

P-value 0.000 0.000

Group	TAMV (cm/s)	TRTB (s)
At rest	19.82±3.86	—
6 times/min	33.78±8.76^*	21.08±5.68
10 times/min	37.06±8.67	33.75±8.11^*
30 times/min	43.82±10.40^*	44.92±10.64^*
60 times/min	52.18±10.53^*	59.83±12.82^*
F	113.052	173.473
P-value	0.000	0.000

Values are mean±SE, APE Ankle pump exercise, CFV Common femoral vein, N-LLF Non-lower limb fracture, TAMV Time-averaged mean velocity, TRTB Time from the end of the ankle pump exercise to the time-averaged mean velocity of common femoral venous blood return to the baseline; ^*P < 0.05 compared to the previous group.

Table 4

Correlation analysis between the frequency and duration of APE and outcome measures

Outcome measures	r	P-value
APE frequency/TAMV of participants with N-LLF	0.700	0.000
APE frequency/TRTB of participants with N-LLF	0.797	0.000
APE frequency/TAMV of participants with LLF	0.672	0.000
APE frequency/TRTB of participants with LLF	0.673	0.000
APE duration/RPE of participants with N-LLF	0.826	0.000

APE Ankle pump exercise, N-LLF Non-lower limb fracture, LLF Lower limb fracture, RPE Ratings of perceived exertion, TAMV Time-averaged mean velocity, TRTB Time from the end of the ankle pump exercise to the time-averaged mean velocity of common femoral venous blood return to the baseline.

The TRTB was longer of group A4 than that of group A1, A2 and A3. It was still positively correlated with APE frequency (P < 0.01) (see Table 4).The TRTB of groupA1, A2, A3 and A4 were 21.08±5.68, 33.75±8.11, 44.92±10.64, 59.83±12.82, respectively (see Table 3).

3.2 Effects of APE frequency on hemodynamics of CFV in participants with LLF

The statistical analysis results of the injured limbs of participants with LLF were the same as that of participants with N-LLF. The TAMV was positively correlated with frequency of APE(P < 0.01)(see Table 4). With the increased of APE frequency, TAMV showed an upward trend. The TAMV of group BI0,BI1, BI2, BI3 and BI4 were 16.98±3.01, 22.20±4.96, 24.01±5.78, 29.20±7.05, 35.75±9.28, respectively (see Table 5).Compared with group BI0, the increase of TAMV were 30.74%, 41.40%, 71.97% and 110.54%.

Table 5
Effects of APE frequency on TAMV of common femoral venous blood flow in participants with LLF (cm/s) (n = 30)

At rest 6 times/min 10 times/min 30 times/min 60 times/min F P-value

Healthy limbs (n = 30) 18.78±4.04 34.84±8.30^* 36.03±9.60 43.15±9.12^* 52.36±11.69^* 57.720 0.000

Injured limbs (n = 30) 16.98±3.01 22.20±4.96^,^† 24.01±5.78^† 29.20±7.05^, † 35.75±9.28^*, † 37.780 0.000

t 2.707 12.516 5.442 6.096 5.689

P-value 0.011 0.000 0.000 0.000 0.000

	At rest	6 times/min	10 times/min	30 times/min	60 times/min	F	P-value
Healthy limbs (n = 30)	18.78±4.04	34.84±8.30^*	36.03±9.60	43.15±9.12^*	52.36±11.69^*	57.720	0.000
Injured limbs (n = 30)	16.98±3.01	22.20±4.96^*,^†	24.01±5.78^†	29.20±7.05^*, †	35.75±9.28^*, †	37.780	0.000
t	2.707	12.516	5.442	6.096	5.689
P-value	0.011	0.000	0.000	0.000	0.000

Values are mean±SE, APE Ankle pump exercise, TAMV Time-averaged mean velocity LLF Lower limb fracture, ^*P < 0.05 compared to the previous group, ^†P < 0.05 compared to healthy limbs.

The TRTB was longer in group BI4 than that in group BI1, BI2 and BI3. It was still positively correlated with APE frequency (P < 0.01) (see Table 4). The TRTB of group BI0,BI1, BI2, BA3 and BI4 were 21.08±5.68, 33.75±8.11, 44.92±10.64, 59.83±12.82, respectively(see Table 6).

Table 6

Effects of APE frequency on TRTB of participants with LLF(s) (n = 30)

	6 times/min	10 times/min	30 times/min	60 times/min	F	P-value
Healthy limbs (n = 30)	22.83±4.68	32.50±6.53^*, †	42.50±8.48^†	61.67±9.94^*, †	140.470	0.000
Injured limbs (n = 30)	11.00±3.57	14.50±4.61^*, †	18.83±4.87^†	25.17±8.56^*, †	34.148	0.000
t	10.186	12.584	12.158	13.720
P-value	0.000	0.000	0.000	0.000

Values are mean±SE, APE Ankle pump exercise, TRTB Time from the end of the ankle pump exercise to the time-averaged mean velocity of common femoral vein return to the baseline, LLF Lower limb fracture, ^*P < 0.05 compared to the previous group, ^†P < 0.05 compared to healthy limbs.

There was no significant difference in TAMV between the healthy and injured limbs when at rest (P > 0.05). When doing APE at the same frequency, the TAMV and the TRTB were higher in the healthy limb than in injured limb(P < 0.01) (see Tables 5 and 6).

3.3 Effects of APE duration on lower limb fatigue

The RPE of participants with N-LLF after exercising for 1 min (14.43±0.57), 2 mins (15.10±0.66), 3 mins (15.73±0.74), 4 mins (16.63±0.72) and 5 mins (17.53±0.57) were significant different (P < 0.01). The longer the exercise time, the more obvious the fatigue of the lower limb (P < 0.01) (see Table 4). When the exercise time was 3 mins, the RPE was 15.73 for participants with N-LLF. When the RPE of the patients with LLF was 16 (the corresponding lower limb fatigue level was “tired”), the exercise time was 110 (90–157.5) s.

4 Discussion

In this study, by analyzing the effects of APE frequency on the hemodynamics of the CFV and the effects of APE duration on the fatigue of the lower limbs, we came to a conclusion different from the traditional concept. Traditionally, it has been believed that slowing down the exercise frequency can strengthen the contractile force of calf muscles and promote the blood flow return more effectively. Experts have proposed to do plantar flexion and dorsiflexion for 5–10 seconds (3–6 times/min) in some academic forums. But the results of this study found that the faster the APE frequency, the faster the blood flow velocity. Besides, it was also found that exercise for 10–20 mins each time,which prescribed in the past is impractical for clinical practice. We found that the participants could do APE for no more than 5 mins, because of the long- term continuous contraction of the muscles.

4.1 Principles of APE to promote venous blood return in lower limbs

The negative pressure produced by diastolic heart and inspiratory movement is the main motive power for venous blood return to ventricles. In addition, the contraction of skeletal muscle also plays an important role in promoting venous blood return of the lower limbs, especially the calf muscles. The calf muscle pump is a closed chamber composed of skeletal muscle, venous sinus, superficial and deep veins,which wrapped by fascia. It has rich blood volume, the contraction of normal calf muscle can discharge 60–90 ml blood at one time [8], which can effectively squeeze the blood from intermuscular and intramuscular veins to the proximal.While, the APE is to drive the contraction of calf muscle through the movement of ankle joint, so as to achieve the purpose of promoting venous blood return of lower limbs.

4.2 Fast-frequency APE can promote venous blood return in the lower limbs more effectively

Kaori et al proved that APE can speed up the return velocity of venous blood and increase the quantity of reflux [9]. The results of this study also showed that the TAMV of the common femoral venous blood flow was higher when performing APE than at rest, indicating that regardless of the frequency of APE, it can promote the venous blood return of the lower limbs. Moreover, this study further proved that fast- frequency APE can promote the venous blood flow more effectively. Compare the TAMV among the four frequencies, it was found that when the frequency was 60 times/min, the TAMV was faster than 30 times/min and faster than 6–10 times/min, which indicated that the faster the frequency, the faster the blood flow velocity. The results subvert the traditional idea that set the frequency at 3–6 times/min.

Traditionally, the plantarflexion and dorsiflexion required to be maintained for 5–10 s, but it has the opposite effect. Because the long-term muscle contraction keeps the veins in a continuous clamping state, causing the blood stasis in the distal vein, which is not conducive to the return of venous blood.

Through the ultrasound we found that the intermuscular veins of the lower limbs could be clamped by different intensity of muscle contraction (different frequency of APE).That is to say the blood flow through the same cross section is the same for each contraction of the calf muscle pump. The faster the contraction frequency, the more blood flow through the same section in unit time. According to the inertia theorem, the more blood flow through in the unit time, the larger the blood’s inertia, the longer time it takes for blood flow velocity to return to baseline, the longer the exercise effect will stay. As shown in the results of this study, when the exercise frequency is increased, the TRTB will also be prolonged.

In addition to the role of APE in accelerating venous blood return to the heart, it is still important that when the blood flow speeds up, vortexes can form in the blood vessels, which has a scouring effect on the blood vessel wall [10, 11]. There is a tangential viscous resistance between the fluid layers of the blood. When blood flows at a uniform speed, the velocity in the center of the blood vessel is the largest, and the closer to the tube wall the slower the velocity. As a result, the visible components of blood will be easy to adhere to the tube wall, leading to the formation of thrombus [12 –14]. Moreover, rhythmic contraction can pulse the flowing blood [15]. By oscillating against the vessel wall to reduce the formation of deposits. This is consistent with the principle of flushing and sealing the venous catheter [6].

4.3 TAMV of common femoral venous blood flow in the injured limb is lower than that in the healthy limb

Considering the complicated clinical condition and injury mechanism of patients, in order to expand the scope of the results of this study and ensure the scientificity of the results, this study conducted clinical studies on participants with LLF, including their injured limb and healthy limb. Because of the pain, operation and other factors, the exercise effect of the injured limb is poor. As shown in the results, the TAMV of the common femoral venous blood flow of the injured side was lower than that of the healthy side at any frequency. When the frequency of APE was 60 times/min, the increase of TAMV of the healthy side was 178.81%, which was significantly higher than that of the injured side (110.54%).

But regardless of the frequency, as long as the APE is performed, the venous blood velocity of the lower limbs will increase. This finding also reminds us: no matter what kind of clinical patients are targeted, compared with the overemphasis on increasing the strength of dorsiflexion and plantarflexion, the effect of increasing the frequency of APE to promote the venous blood return will be better. [17] have once suggested that for patients receiving total hip arthroplasty(THA) moving at 60 times/min could obtain optimal venous blood flow.

4.4 Effects of APE duration on lower limb fatigue

With the extension of exercise time, the fatigue degree of the lower limbs increased gradually, which is related to the muscle stimulation caused by anaerobic digestion and accumulation of lactate [18].

This study found that when the frequency of APE was 60 times/min and the exercise time reached 3 mins, the RPE of people with N-LLF was 15.73 points and the corresponding fatigue was close to “tired”. At this time most patients said “ they don’t want to continue”. For the injured limb of patients with LLF, when the RPE score was 16 points, that is the fatigue is “tired”, the exercise time was about 2 mins. If we continue to extend the exercise time, most of the patients said that they were suffering from pain and weakness and could not insist on it, and they did not want to cooperate with this study. Therefore, from the perspective of comprehensive consideration of exercise effect and compliance, this study suggests that the exercise time should better be 3 mins for patients with N-LLF and 2 mins for patients with LLF.

In conclusion, no matter what kind of people, compared with the slow frequency APE, the fast frequency APE can promote the venous blood flow of the lower extremity more effectively. But, prolonging exercise time will increase the lower limb fatigue and reduce the compliance of patients. Therefore, we advocate that the frequency of APE should be controlled at 60 times/min. For participants with N-LLF, the exercise duration should be controlled at 3 mins, and for patients with LLF, the exercise duration should be controlled at 2 minutes.

This study regulated the frequency and duration of APE, and provided theoretical basis for guiding patients to carry out APE in clinic, but it also had some limitations. Due to the poor tolerance to fatigue and poor clinical compliance of the elderly, this study did not include elderly patients. Besides, this study only included patients with proximal LLF. About which exercise method is more effective for patients with distal LLF further research is needed. In addition, this study only analyzed the influence of APE frequency on the hemodynamics of lower extremity vein. Whether fast frequency APE can prevent the occurrence of venous thromboembolism more effectively remains to be studied in large sample clinical trials.

Funding

Government-funded clinical talent training program.

Conflict of interest

None.

Ethics approval

Approval was obtained from the ethics committee of The Third Hospital of Hebei Medical University. The procedures used in this study adhere to the tenets of the Declaration of Helsinki.

Footnotes

Acknowledgments

The authors are grateful for the equipment and technical support provided by the director Qingmao Fang of the ultrasound department of the Third Hospital of Hebei Medical University.

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