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How to safely and effectively locate, select and dissect the perforator vessels is the biggest difficulty in the preparation of DIEP flap. Preoperative CTA was used to evaluate the perforators of the DIEP flap. The CTA data were imported into the image analysis software to select the dominant perforators of the flap before operation, and to determine the anatomical information such as the diameter of the perforator vessel, the course of the perforator in the muscle, and the location of the perforator exit point, so as to guide the operation. In summary, CTA technology can accurately provide detailed anatomical information of perforator vessels, facilitate surgical design, reduce intraoperative perforator selection and dissection time, reduce the risk of secondary surgical exploration, and have a high imaging and surgical consistency rate, especially for patients with a history of abdominal surgery, CTA is of higher value. Therefore, CTA examination is worthy of clinical application in delayed DIEP breast flap reconstruction.
Department of Thyroid and Breast Surgery, Xiaogan Hospital Affiliated to Wuhan University of Science and Technology, Xiaogan, Hubei, China
Pan Dai
Department of Ultrasound, Xiaogan Hospital Affiliated to Wuhan University of Science and Technology, Xiaogan, Hubei, China
Xu Hua
Department of Plastic Surgery, Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China
*Address all correspondence to: 443430731@qq.com
1. Introduction
Breast reconstruction is becoming more popular under the basis of tumor safety. The rate of immediate or delayed reconstruction following breast cancer surgery has grown dramatically [1, 2]. Deep inferior epigastric perforator (DIEP) flap has become the gold standard in autologous breast reconstruction due to low donor site problems and significant abdominal esthetic improvement [3]. While DIEP flap surgery has become commonplace, the anatomy of the deep inferior epigastric artery perforator is very diverse, and flap perforator selection remains difficult. Color Doppler ultrasonography was the first approach used to evaluate perforators in DIEP [4]. Nevertheless, due to its strong subjectivity, time-consuming nature, high false positive rate of preoperative perforator evaluation, and lack of local anatomical features, its applicability is limited to some extent. Till date, computed tomography angiography (CTA) has been an essential assessment approach prior to DIEP surgery [5, 6]. CTA can provide more detailed preoperative anatomical information than color Doppler ultrasound examination, which can help to better select the dominant perforator of the flap before surgery, clarify the diameter of the perforator vessels, the characteristics of the perforator vessels in the muscle, and the location of the perforator point, so as to effectively guide the operation process [7].
This study has collected clinical data from 298 female patients undergoing breast reconstruction surgery following breast cancer surgery, ranging in age from 25 to 67 years (mean age 42.2 ± 8.28 years). Before undergoing reconstructive surgery, all patients had conventional tumor therapy and were in a stable disease phase. In January 2016 and January 2018, 92 patients (US group) had their data gathered. Prior to surgery, these patients were subjected to a color Doppler ultrasound examination to examine abdominal vascular perforators using a GE Logiq 700 ultrasonography machine with a probe frequency of 10–13 MHz and a color Doppler frequency of 7.5 MHz, with a maximum velocity of 2 cm/s. The focus of the examination was to accurately detect where the target perforator vessels exited the deep fascia and entered the subcutaneous fat layer, and then to label the matching surface projection. As the observation group, data from 206 patients was gathered between January 2018 and January 2021 (CTA group). These patients underwent abdominal vascular perforator evaluation prior to surgery using a Philips Brilliance 256i CT scanner, which used a non-ionic iodine contrast agent (iopromide) with a volume of 90–100 mL and an injection rate of 4 mL/s, introduced via a vein on the back of the hand or at the elbow. The following CTA settings were employed with a single high-pressure injector: 120 kVp, 250 mA, detector 128 × 0.625 mm, pitch 0.977, 512 × 512 matrix, and a 350 mm field of view.
2.2 CTA image data processing
The HOROS software was used to evaluate the data and establish the location and trajectory of perforator vessels, which were then marked on the patient’s body surface.
2.3 Research indexs
Baseline data were collected for both groups and compared, including age, body mass index (BMI), history of hypertension or diabetes, history of tumor chemotherapy, chest wall radiation history, abdominal surgery history, smoking history, and single/double pedicle flap blood supply. In addition, intraoperative and postoperative evaluation indices were statistically analyzed. Intraoperative evaluation indices included the number of perforators located preoperatively, the number of perforators utilized during the surgery, the decision-making time for perforators, perforator dissection time, flap harvesting time, flap total weight, and total operation time. The postoperative evaluation indices included abdominal incision infection rate, fat necrosis rate, re-exploration rate, and complete flap necrosis rate.
3.1 Preoperative localization of DIEP flap perforator
Patients in the US group had US examinations the day before the surgery, with the US group getting surface markings of perforator arteries directly under color doppler ultrasound guidance. CT vascular imaging examinations were done in the CT room for the CTA group, and the physician duplicated the DICOM files and loaded them into the HOROS program on their mobile phone or a personal computer. The imaging processing system was used to determine the dominant perforator, and the position of the chosen dominant perforator was written on the body surface centered on the level of the umbilicus.
3.2 Preoperative scribing
Based on the shape of the patient’s contralateral breast, the reconstruction of the breast fold and the separation area of the inner and outer sides of the affected breast were marked on the body surface prior to surgery.
3.3 Receiving area pretreatment
During surgery, the patient was positioned supine, and the scar tissue on the chest wall was addressed, as well as the cavity of the breast flap divided. The third rib cartilage was regularly resected to reveal the recipient vessels within the chest wall.
3.4 Preparation of the donor site
A DIEP flap was harvested and dissected after a perforator site close to the marked area was identified. The power of the electric scalpel was lowered to measure and mark the target perforator vessel again with the center at the level of the umbilicus on the anterior sheath surface. The perforator vessel was carefully dissected and separated, and the DIEP flap was obtained. The upper and lower abdominal wall tissues were freed, the abdominal wall was reshaped, the umbilical hernia was reconstructed, and the abdominal incision was closed.
3.5 Microvascular anastomosis and breast reconstruction
The recipient artery and vein were dissected and reserved, with the distal ends being ligated and the proximal ends being clamped. The blood vessels within the chest wall were trimmed. The flap was moved to the breast defect site and temporarily fixed, and the veins and arteries below the abdominal wall were trimmed. Microscopic vascular anastomosis was performed using 9-0 or 10-0 prolene suture thread. The patency of the anastomosis was checked. After the flap blood supply was established, the shape of the breast was formed.
4.1 Comparison of preoperative baseline data between the two groups
Among 298 patients undergoing delayed DIEP flap breast reconstruction, the overall survival rate of the flap was 99.33% (296/298). There were no significant differences between the two groups in age, BMI, history of underlying diseases, history of tumor chemotherapy, history of chest wall radiotherapy, history of abdominal surgery, history of smoking, and blood supply of the flap (uni/bi-pedicle) (P > 0.05) (Table 1).
Factors
CTA group
US group
F/χ2
P value
Age/year
41.78 ± 9.06
40.94 ± 8.61
1.25
0.27
BMI
24.34 ± 3.20
24.21 ± 2.86
0.71
0.40
Basic disease
0.098
0.754
With
25
10
Without
181
82
Chemotherapy
0.281
0.596
With
168
69
Without
48
23
Chest wall radiotherapy
0.001
0.977
With
72
32
Without
134
60
Abdominal surgery
0.264
0.608
With
82
36
Without
124
56
Smoking
0.017
0.895
Yes
4
2
No
202
90
Blood supply of flap
0.128
0.720
Unipedicle
85
40
Bipedicle
121
52
Table 1.
Comparison of baseline data between two groups.
4.2 Comparison of intraoperative and postoperative outcome indexes between the two groups
In the observation group, the number of preoperative location perforations was (2.90 ± 1.13), while that in the control group was (3.21 ± 1.46), and the difference was statistically significant. In terms of perforator decision time and perforator anatomy time, the observation group was shorter than the control group (P < 0.001), as shown in Table 2. The acquisition time of donor flap was (50.05 ± 10.94) min in the observation group and (84.8 ± 15.44) min in the control group. Donor site flap acquisition time was shorter in the observation group, and the difference was statistically significant (P < 0.001). There was no significant difference in the total operation time between the two groups (P = 0.809) (Figure 1). The total weight of the flap was (730.62 ± 127.31) g in the observation group and (718.25 ± 129.36) g in the control group, showing no difference.
Indicators
CTA group
US group
F/χ2
P value
Number of preoperative location perforations
2.90 ± 1.13
3.21 ± 1.46
6.46
0.012
Number of intraoperative choice perforations
2.26 ± 0.92
2.49 ± 0.96
0.907
0.342
Perforation choice time (min)
9.14 ± 3.38
26.73 ± 6.54
49.42
<0.001
Perforation anatomy time (min)
40.92 ± 9.98
58.11 ± 14.44
19.64
<0.001
Donor site flap acquisition time (min)
50.05 ± 10.94
84.8 ± 15.44
15.56
<0.001
Flap weight (g)
730.62 ± 127.31
718.25 ± 129.36
0.005
0.942
Total operation time (min)
294.20 ± 68.51
328.74 ± 68.69
0.058
0.809
Abdominal incision infection
0.199
0.656
Yes
3
2
No
203
90
Fat necrosis
0.404
0.525
Yes
6
4
No
200
88
Secondary surgical exploration
11.501
<0.001
Yes
6
12
No
200
80
Complete flap necrosis
Yes
0
2
0.095
No
206
90
Table 2.
Comparison of intraoperative and postoperative indicators between two groups.
Figure 1.
Comparison of key intraoperative indicators.
In the comparison of postoperative complications between the two groups, there were no statistical differences in abdominal incision infection rate, fat necrosis rate and flap complete necrosis rate (P > 0.05). In the comparison of secondary surgical exploration rate, the CTA group was lower than the US group (P < 0.001) (Figure 2).
Figure 2.
Comparison of key postoperative indicators.
4.3 Patients in the two groups were stratified according to whether there was a history of abdominal surgery
Stratified comparisons were made with or without a history of abdominal surgery. The experimental data were divided into four groups: ① CTA + NAS (non-abdominal surgery); ② CTA + AS; ③ US + NAS; ④ US + AS. The results showed that the time and total operation time of the flap were increased in both the CTA group and the US group in patients with a history of abdominal surgery (P < 0.05). For patients with a history of abdominal surgery, the time and total operation time of the flap in the CTA group were lower than those in the US group (P < 0.05). For patients with no history of abdominal surgery, the time of flap resection in CTA group was lower than that in US group (P < 0.05), and there was no significant difference in total operation time (P > 0.05) (Table 3).
Groups
Perforation anatomy time(min)
P value
Total operation time(min)
P value
① CTA + NAS
32.06 ± 7.96
0.023a
288.46 ± 58.34
0.040e
② CTA + AS
42.36 ± 10.06
<0.001b
300.06 ± 60.29
0.018f
③ US + NAS
50.98 ± 13.02
<0.001c
304.78 ± 64.58
0.248g
④ US + AS
68.30 ± 15.08
0.012d
332.03 ± 70.28
0.014h
Table 3.
Stratification analysis according to the history of abdominal surgery between two groups.
Note: Comparison of perforation anatomy time between different groups: a is ①vs②comparison; b is ③vs④ comparison; c is ①vs③ comparison; d is ②vs④ comparison. Total operation time (min): e is ①vs②comparison; f is ③vs④ comparison; g is ①vs③ comparison; and h is ②vs④ comparison.
4.4 Analysis of consistency rate of imaging surgery
Among 206 flaps in the observation group, the perforator selection in 200 flaps was related to CTA, and the consistency rate of imaging operation was 97.09%; among 92 flaps in the control group, the perforator selection in 40 flaps was related to US, and the consistency rate of imaging operation was 43.48%, with statistical significance (P < 0.001) (Table 4).
Groups
Total number of cases
Conformed cases
Accordance rate (%)
P value
US
92
40
43.48
<0.001
CTA
206
200
97.09
Table 4.
Comparison of the consistency rate of imaging surgery between two groups.
4.5 Typical cases
The female patient, 65 years old, was admitted to hospital due to “left breast defect 10 years after left breast cancer surgery.” Specialized physical examination on admission showed: chest: postoperative changes of left breast cancer, absence of left breast, surgical scar about 15.0×1.0 cm in length visible on left chest wall, good healing, no skin ulceration, nodules and other abnormalities. There was mild drooping of the right breast, no obvious abnormal nodules in it, no obvious enlarged lymph nodes in the bilateral axilla and the upper and lower clavicular region. Abdomen: The patient’s abdomen was slightly elevated, and the longitudinal surgical scar about 10.0*1.0 cm in length was visible in the lower abdomen. Preoperative images are shown inFigure 3A. After admission, the general condition assessment was completed, and no obvious contraindications were found, so the left breast reconstruction with DIEP flap was performed under general anesthesia. Before surgery, the patients underwent CTA examination first, and then abdominal ultrasound examination. The body surface identification of the dominant perforator was performed in the blind state, respectively, as shown in Figure 3B. Before surgery, the location of the dominant perforator on the left and right sides was calculated in horizontal, coronal and sagittal positions with the umbilical level as the center, respectively, as shown in Figure 4. During the operation, CTA navigation technology was combined to accurately locate the corresponding perforator vessels, as shown in Figure 5. The perforator vessels of both sides of the flap and DIEP flap were completely free for flap shaping and breast shaping, as shown in Figure 6. The surgery was successful. The chest drainage tube was removed 3 days after surgery, and the abdominal drainage tube was removed 5 days after surgery.
Figure 3.
Preoperative thoracic and abdominal images of the patient. (A) Preoperative image, and (B) In the preoperative positioning image, the black arrow shows the vessel perforator located by CTA, and the red mark in the red circle is the vessel perforator location point evaluated by preoperative ultrasound.
Figure 4.
CTA images of perforator vessels. (A) The left perforator was in the shape direction of the flap, (B) The exit point of the left perforator flap, (C) Vertical distance between sagittal perforating branches and the center of the umbilicus, and (D) Vertical distance between left and right perforating branches and the center of the umbilicus.
Figure 5.
Perforator vessel image-real comparison. (A) The red arrow shows the left and right perforations respectively, and (B and C) The actual right and left perforations calculated according to CTA during the operation respectively.
Figure 6.
A panoramic view of DIEP flap and immediate postoperative images.
The DIEP flap has numerous benefits in breast restoration, including big tissue acquisition, tissue similarity in the donor region, full preservation of rectus abdominis and anterior sheath tissue, and so on. It can also help with abdominal wall reconstruction in individuals who have abdominal fat accumulation. DIEP is currently the favored flap for autologous tissue breast surgery. However, due to its technological complexity, lengthy operation time, convoluted intraoperative links, and high postoperative complications, the operation of the DIEP flap is limited to some degree [8]. The choosing of flap perforator vessels and non-invasive anatomy are critical in DIEP surgery. There were, however, substantial variations in the starting position, diameter, and intramuscular course of flap perforator vessels between people or between lateral perforator vessels of the same individual. In traditional surgery, the main perforator is determined by a thorough assessment of each perforator during intraoperative anatomical investigation. The procedure is time-consuming, inefficient, and needs the physician to have extensive personal experience. Furthermore, perforator vessels have a smaller diameter, a wide range of form and location variability, which adds to the complexity and danger of operation [9].
During the development of DIEP flap for more than 30 years, a variety of methods and means for detecting and locating perforator vessels of flap have appeared in clinic. The commonly used methods include: portable ultrasonic Doppler examination: it was first used in 1975 to locate vascular perforator in flap surgery. Its advantages of simple operation, convenient portability and low cost can be used for preliminary vascular evaluation before surgery. However, studies have shown that its high false positive rate reduces the actual clinical guidance value [10]. Color Doppler examination: compared with portable ultrasonic Doppler, color Doppler can provide more detailed hemodynamic information, such as the origin, caliber, intramuscular shape, peak flow rate, resistance index, etc., so as to judge the vascular quality [11]. At present, it has been reported in the literature that color Doppler can detect perforator vessels with a diameter of about 0.7 mm, with an accuracy comparable to that of CTA. If combined with contrast-enhanced ultrasound examination, the effect of vascular development can be further improved [12]. High-resolution magnetic resonance angiography (MRA) examination, conventional MRA resolution is low, although with the emergence of high-resolution MRI and corresponding sequences, MRA can display perforator vessels with a diameter of 1 mm, and can even partially replace CTA examination, but its economy, practicability and scanning time are worth considering [13]. CTA examination: In 2006, Masia et al. [14] first used CTA to locate the inferior abdominal perforator vessel before surgery and selected the dominant perforator for breast reconstruction, and the imaging consistency rate of CTA reached 100%. CTA can provide accurate anatomical information on the perforating point, number, caliber and course of the perforating vessel of DIEP flap. Compared with other examinations, CTA is not susceptible to the influence of the patient’s body type, vascular variation and deformity.
At present, CTA imaging technology is more and more widely used in the field of flap repair abroad, especially in the application of abdominal DIEP flap for breast reconstruction after breast cancer surgery [15, 16, 17]. However, there are few domestic reports on the clinical application of CTA in delayed breast reconstruction after breast cancer surgery. In traditional DIEP breast reconstruction surgery, the perforator is usually evaluated by color Doppler. However, the accuracy of perforator localization is affected by false positive ultrasonography and operator’s subjectivity to some extent. With the wide application of imaging technology, CTA can clearly display the anatomical information of perforator vessels with a diameter > 0.3 mm before surgery. As a “rehearsal” before surgery, surgeons can accurately conduct preoperative clinical operation simulation according to the picture [7]. In recent years, our center has conducted preoperative imaging evaluation for patients who plan to undergo delayed DIEP breast reconstruction. Combined with the different imaging evaluation methods in our hospital before and after 2018, this paper attempts to analyze the application value of CTA in delayed DIEP breast reconstruction surgery.
As a non-invasive, rapid, high image resolution, high accuracy and high specificity preoperative perforator vessel imaging method, CTA examination has been widely used in preoperative localization of perforator vessels of DIEP flap [15, 18]. In this study, we compared baseline data, intraoperative observed indicators, and incidence of postoperative complications between the CTA group and the US group. Among them, the CTA group was significantly better than the preoperative ultrasound localization group in choosing the time of perforator and the anatomic time of perforator. The time required to obtain the same mass flap was significantly shorter in CTA group than in ultrasound group (p < 0.001). This conclusion is consistent with most foreign studies [5, 6, 15]. All CTA data in this experiment were identified and read DICOM files by the surgeon himself through HOROS software in the mobile phone or computer. It can objectively evaluate and locate the number of perforator vessels before surgery, and perform a good preoperative operation simulation. At the same time, it is convenient for preoperative communication between doctors and patients, and can also play a positive role in promoting scientific research and teaching. On the other hand, CTA examination can get rid of the dependence of clinical surgeons on radiologists to a certain extent. Previous studies have shown that the agreement between surgeons and radiologists is 67.3%, and surgeons have higher accuracy of preoperative perforator localization [3, 17, 19].
In all cases of CTA, the surgeon can read, measure, draw and mark the intended surgical treatment cases anytime and anywhere in advance, regardless of the limitation of time and space, which is especially convenient for the formulation of remote consultation surgery plans for clinicians. In the CTA group, the operation time and cost can be saved when the skin flap is obtained. According to the study of Haddock et al. [3], compared with the group without preoperative CTA, the time to obtain the flap and the total operation time were longer. However, in the comparison of total operation time in this study, there was no significant statistical difference between the CTA group and the US group. Analysis of this reason may be due to: First, this study was bounded by time nodes. From January 2016 to January 2018, the perforator vessel was evaluated by ultrasonic localization, and from January 2018 to January 2021, the perforator vessel was evaluated by CTA. In the early stage (US group), the operator team paid more attention to the flap resection process. With the further improvement of surgical skills and surgical instruments, surgeons spent more energy on the flap shaping process in the later period (CTA group), which reduced the difference of total operation time between the two groups to a certain extent. Second, 92 cases were included in the US group and 206 in the CTA group in this study. The mismatch in the number of cases may bias the experimental results to a certain extent. In addition, the results of this study indicated that, in the comparison of total operating time between the CTA group and the US group, the mean net operating time of the CTA group was shortened by 34 min. Although it did not translate into statistical P value difference, different results may occur with the matching or increasing of the number of cases. Third, in this study, the CTA group contained more patients with double pedicle reconstruction than the US group (58.7 vs. 56.5%), which increased the operation time to a certain extent. In addition, the preoperative evaluation of color Doppler ultrasound in the control group has a certain guiding value for the localization of perforator branches.
The presence of scar in previous abdominal surgery may affect the effect of DIEP flap reconstruction, because scar tissue may affect the normal distribution of blood supply in the abdominal flap, and in severe cases affect the normal shape of perforator vessels, thus increasing the difficulty of surgical anatomy [20, 21]. However, preoperative CTA examination can clearly show the integrity and shape of the deep vessels and perforator vessels under the abdominal wall, which is of greater reference value for patients with surgical history. The present study was stratified according to whether there was a history of accompanying abdominal surgery. The results showed that: for patients with a history of abdominal surgery, the time of flap resection and total operation time in CTA group were lower than those in US group (P < 0.05). For patients with no history of abdominal surgery, the time of flap resection in CTA group was lower than that in US group (P < 0.05), and there was no significant difference in total operation time (P > 0.05). Therefore, it is of great significance to strengthen preoperative CTA examination for patients with a history of abdominal surgery.
In the comparison of postoperative complications between the two groups, 92 patients in the US group had complete necrosis of the skin flap, and 206 patients in the CTA group had all survived. Although the difference between the two groups was not statistically significant, the CTA group may have a higher flap survival rate. To this end, we again compared the rate of secondary surgical exploration between the two groups, the US group was 13.04% (12/92) and the CTA group was 2.91% (6/206), the difference was statistically significant (P < 0.001), and CTA could reduce the risk of secondary surgical exploration to a certain extent. As for the consistency comparison between the intraoperative perforator and the dominant perforator evaluated based on imaging data, the consistency rate of imaging surgery was 97.09% (200/206) in the CTA group and 43.48% (40/92) in the US group, the difference was statistically significant (P < 0.001). Therefore, CTA examination can more accurately select, measure and locate the dominant perforator before surgery.
CTA examination is not only limited to the application of perforating branches of abdominal flaps, but also can further evaluate the conditions of blood vessels in the chest receiving area (internal arteriovenous) during the preoperative thoracoabdominal joint examination. Especially for some patients with radiation ulcers, reasonable selection of blood vessels in the receiving area can further increase the probability of successful surgery [22]. In addition, in some patients with a history of abdominal surgery, CTA can be better used to evaluate the conditions of abdominal perforator vessels, so as to guide the selection of surgical methods. However, as with any form of imaging, preoperative CTAs are inevitably subject to unexpected findings. Literature reported that the incidence of accidental discovery was 13–75% in CTA studies on DIEP flap program [16]. Wagner et al. suggested that among the 350 patients who met the criteria, 56.9% of the patients found lung nodules and abdominal diseases without special intervention in preoperative imaging examination, 12.9% of the patients received additional imaging examination, and 4.0% of the patients received additional intervention, such as puncture biopsy of lung tumors. In addition, abdominal CTA examination is conducive to the selection of donor skin flap during breast reconstruction surgery, and preoperative CTA evaluation is especially important for patients who plan to undergo SIEA skin flap operation [23, 24]. However, CTAs also have some disadvantages: patients need to be exposed to radiation, which may trigger a certain risk of cancer; In addition, the use of iodine contrast media may cause a small number of people allergic reactions, kidney damage and other unpredictable unexpected conditions.
In summary, CTA technology can accurately provide detailed anatomical information of perforator vessels, facilitate surgical design, reduce intraoperative perforator selection and dissection time, reduce the risk of secondary surgical exploration, and have a high imaging and surgical consistency rate, especially for patients with a history of abdominal surgery, CTA is of higher value. Therefore, CTA examination is worthy of clinical application in delayed DIEP breast flap reconstruction.
In delayed DIEP flap breast reconstruction, CTA can significantly shorten the choice time of flap perforation and anatomy time, reduce the risk of secondary surgical exploration and has a high rate of image surgery consistency, which can effectively guide the operation.
Xu yuanbing: thesis design, writing, modification, and data proofreading, Pan dai: imagine data measurement and statistics, paper revision, Xu hua: thesis design and revision. The author(s) read and approved the final manuscript. This work was supported by funding from a special fund in the field of major health of the Science and Technology Department of Hubei Province (2022BCE041) and the Natural Science Foundation of Xiaogan City (XGKJ2022010006).
The copyright of this academic study belongs to the “Chinese Journal of Cancer.” We thank the editor and reviewers of the Journal for their guidance and assistance in the Chinese submission. The English version is the translation of the Chinese version. Please point out if there are any improper points.
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Written By
Xu Yuanbing, Pan Dai and Xu Hua
Submitted: 06 April 2023Reviewed: 17 August 2023Published: 06 September 2023
Open access peer-reviewed chapter
