Introduction: The aim of the study was to investigate the clinical characteristics, surgical treatment, and long-term efficacy of primary right heart tumors. Methods: This study is retrospective analysis of the clinical data of 70 patients with primary right heart tumors admitted to our department between 1980 and 2022 (observation group) and 70 patients with left heart tumors during the same period (control group). The surgical treatment was performed under cardiopulmonary bypass after differential diagnosis by echocardiography, cardiac CTA, and PET-CT before the surgery. The perioperative characteristics, recurrence rate, and long-term survival rates of right heart tumor versus left heart tumor were compared. Results: The most common pathological types of right heart tumors were myxoma (60%), lipoma (8.57%), and papillary elastofibroma (7.14%). During the perioperative period, there were 1 case of systemic embolism in the observation group, compared with 6 in the control group (p = 0.026), 13 cases of malignant tumor in the observation group versus 1 in the control group (p = 0.01). During the follow-up period, there were 15 cases of tumor recurrence and 17 cases of death in the observation group versus 4 (p = 0.002) and 7 in the control group (p = 0.006), comparatively. Conclusion: Compared with left heart tumors, primary right heart tumors had a higher incidence of malignant tumors and a lower risk of systemic embolism during perioperative period. During the follow-up period, primary right heart tumors had a higher rate of tumor recurrence and a lower long-term survival rate.

Primary cardiac tumors are rare, with an incidence of 0.02% (0.001–0.5%) at routine autopsy, of which 75% are benign [1, 2]. Myxoma is the most common type of primary benign heart tumor, accounting for more than 50% of the total number [3]. Most of the benign heart tumors occur in the left atrium, while the right atrial myxoma accounts for only 8–20% of atrial myxomas. However, studies have shown that the proportion of primary cardiac malignant tumors in right heart tumors is significantly higher than that of the left heart [4, 5].

The mass of cardiac tumors can cause various cardiovascular complications, including hemodynamic disorders, vascular embolism, and heart failure. The mass in different chambers has different clinical characteristics, treatment strategies, and long-term prognosis. Thus, the investigation of cardiac tumors in different chambers plays an important role in the clinical diagnosis and treatment of the disease. Due to the low incidence of heart tumors, previous reports of primary right heart tumors are mostly of case reports. In addition, there are currently no standardized guidelines for the diagnosis and treatment of the disease. This study retrospectively analyzed the clinical characteristics of 70 patients with primary right heart tumors who were admitted to the Department of Cardiovascular Surgery of our hospital from January 1980 to January 2022, and the clinical manifestations, perioperative complications, tumor recurrence rate, and long-term survival rate were compared with patients with left heart tumors, which may help the establishment of a more comprehensive and standardized plan for the disease diagnosis and treatment.

Patients

In this study, 71 patients initially diagnosed with primary right heart tumors who underwent surgical treatment in our department in 1980∼2022 were included, and 1 patient with postoperative diagnosis of secondary (metastatic) cardiac tumors was excluded; therefore, the total number of patients with primary right heart tumors with the inclusion criteria was 70 patients (observation group). Exclusion criteria were as follows: (1) Secondary cardiac tumors; (2) patients without surgical treatment; (3) patients with postoperative pathological results suggesting that the resected tissue was non-tumor or without pathological results. This study protocol was reviewed and approved by the Xinqiao Hospital, Army Medical University, approval number 2020-No.010-01. Written informed consent was obtained from all adult patients to participate in the study and from the participants’ legal guardian for all minor patients.

The data from 70 patients with right heart tumors were used as the observation group and 70 patients with left heart tumors in the same period were included in the control group using the European Scoring Criteria (EuroSCORE II) [6]. The general condition, surgery, mortality, ventilator assist time, intensive care unit time, and other complications of the two groups were compared, and the long-term tumor recurrence rate and survival rate were evaluated based on the follow-up results.

Surgery

After intravenous compound anesthesia and endotracheal intubation, the patients received the complete tumor removal, assisted by extracorporeal bypass. Most of the patients adopted cardiac arrest with median chest incision, and several patients received the surgery through right anterolateral chest incision or with no cardiac arrest. The aorta was blocked as soon as possible during the operation, avoiding unnecessary movement or touching of the heart. Then the superior and inferior vena cava were free and blocked after the stop of cardiac perfusion, reducing the risk of embolism caused by tumor detachment.

For patients with benign tumors, the endocardium and surrounding 1.0∼1.5 cm normal myocardial tissue at the attachment of the tumor pedicle were resected as much as possible, and the atrial septum or wall was repaired with mesh if necessary. After the tumor was removed, the heart cavity was rinsed with a large amount of normal saline, and the pedicle attachment was appropriately cauterized with argon knife to reduce the recurrence of implantation. If the tumor was attached to the tricuspid valve, and a large area of the valve leaflet was missed, autologous pericardial sheet or bovine pericardial mesh could be used for repair. For tricuspid valve orifice obstructed by tumor, which could cause annular dilatation, tricuspid annular contraction or appropriate tricuspid valve ring insertion could be operated. Before evacuating cardiopulmonary bypass, esophageal ultrasound was routinely used to explore the multiple or residual tumors, the alignment and regurgitation of the tricuspid valve, and the residual obstruction of the superior and inferior vena cava.

For patients with malignant tumors, the scope of resection was expanded as much as possible on the basis of ensuring the safety of surgery. The atrial wall, blood vessel wall, and valve were repaired with autologous pericardial film or artificial materials. The “radical resection” should not be blindly pursued, avoiding the occurrence of uncontrollable hemorrhage, damage to important structures, or excessive turnaround time.

Statistical Analysis

The data of this study were analyzed by IBM SPSS (Statistics version 21). The perioperative data conforming to the normal distribution of measurement data are expressed as “mean ± standard deviation,” and comparisons are made using t tests; enumeration data are expressed as “number (percentage),” and comparisons are made using χ2 tests. Kaplan-Meier survival analysis was analyzed using GraphPad Prism 8.4. p < 0.05 was regarded as statistically significant.

Clinical Characteristics

A total of 70 primary right heart tumors were included in this study as the observation group, with 30 males and 40 females. The age of the patients ranged from 5 to 79 years old (average 45.6 ± 15.6 years). The weight of the patients ranged from 20 to 69 kg (average 54.7 ± 10.2 kg). The course of disease was 1∼17 months, with an average of 6.7 ± 2.4 months. The control group included 70 patients with primary left heart tumors. There were 32 males and 38 females in the control group. The patients were aged from 3 to 73 years old (average 47.5 ± 14.5 years) and weighted from 12 to 75 kg (average 53.5 ± 12.1 kg). The clinical characteristics of the patients were shown in Table 1.

Table 1.

Clinical characteristics and measurements before and during the surgery in the observation and control groups

Characteristics and measurementsObservation (n = 70)Control (n = 70)P
Age, years 45.6±15.6 47.5±14.5 0.573 
Male, n (%) 30 (42.9) 32 (45.7) 0.835 
BMI 25.7±7.2 24.8±6.5 0.606 
Acute surgery 0.171 
Reoperation 0.562 
Extracorporeal circulation time, x ± s, min 85.2±23.7 53.1±19.4 0.198 
Aorta block time, x ± s, min 84.7±22.3 52.6±20.1 0.213 
COPD, n (%) 3 (4.3) 5 (7.1) 0.562 
History of diabetes, n (%) 2 (2.8) 2 (2.8) 0.868 
History of ischemic stroke, n (%) 2 (2.8) 5 (7.1) 0.324 
History of chronic kidney disease, n (%) 2 (2.8) 3 (4.3) 0.545 
Smoking, n (%) 10 (14.3) 12 (17.1) 0.692 
Ejection fraction, n (%) 56.1±13.5 55.7±14.8 0.137 
LVDD, x ± s, mm 51.6±8.7 53.5±9.1 0.475 
History of angina, n (%) 3 (4.3) 4 (5.7) 0.778 
Pulmonary embolism, n (%) 3 (4.3) 0 (0) 1.0 
Characteristics and measurementsObservation (n = 70)Control (n = 70)P
Age, years 45.6±15.6 47.5±14.5 0.573 
Male, n (%) 30 (42.9) 32 (45.7) 0.835 
BMI 25.7±7.2 24.8±6.5 0.606 
Acute surgery 0.171 
Reoperation 0.562 
Extracorporeal circulation time, x ± s, min 85.2±23.7 53.1±19.4 0.198 
Aorta block time, x ± s, min 84.7±22.3 52.6±20.1 0.213 
COPD, n (%) 3 (4.3) 5 (7.1) 0.562 
History of diabetes, n (%) 2 (2.8) 2 (2.8) 0.868 
History of ischemic stroke, n (%) 2 (2.8) 5 (7.1) 0.324 
History of chronic kidney disease, n (%) 2 (2.8) 3 (4.3) 0.545 
Smoking, n (%) 10 (14.3) 12 (17.1) 0.692 
Ejection fraction, n (%) 56.1±13.5 55.7±14.8 0.137 
LVDD, x ± s, mm 51.6±8.7 53.5±9.1 0.475 
History of angina, n (%) 3 (4.3) 4 (5.7) 0.778 
Pulmonary embolism, n (%) 3 (4.3) 0 (0) 1.0 

The comparison between the two groups is statistically significant, with p < 0.05 indicating a significant difference. Conversely, it indicates no difference.

BMI, body mass index; COPD, chronic obstructive pulmonary disease; LVDD, left ventricular end diastolic dimension.

Perioperative Data Comparison

There were no significant differences between the observation group and the control group in terms of death cases, time to endotracheal intubation, length of intensive care unit stay, hypocardiac syndrome, cardiac arrest, gastrointestinal bleeding, and new dialysis cases during the perioperative period (p = 0.05, Table 2). In terms of malignant tumors, the cases in the observation group (13, 18.6%) were significantly higher than those in the control group (1, 1.4%; p = 0.01). However, 1 (1.4%) patient in the observation group has nerve damage, which was significantly less than those in the control group (6, 8.6%; p = 0.026).

Table 2.

Postoperative complications in the observation and control groups

ComplicationsObservation (n = 70)Control (n = 70)p value
Death, % 3 (4.3) 1 (1.4) 0.137 
Endotracheal intubation time, x ± s, h 59.3±31.2 56.1±17.1 0.868 
ICU time, x ± s, d 3.78±4.1 3.35±1.4 0.324 
Malignant tumors, n (%) 13 (18.6) 1 (1.4) 0.01 
Hypocardiac syndrome, n (%) 4 (5.7) 2 (2.9) 0.692 
Cardiac arrest, n (%) 2 (2.9) 3 (4.3) 0.137 
Nerve damage, n (%) 1 (1.4) 6 (8.6) 0.026 
Gastrointestinal bleeding, n (%) 3 (4.3) 5 (7.1) 0.778 
New dialysis, n (%) 7 (10.0) 5 (7.1) 1.0 
ComplicationsObservation (n = 70)Control (n = 70)p value
Death, % 3 (4.3) 1 (1.4) 0.137 
Endotracheal intubation time, x ± s, h 59.3±31.2 56.1±17.1 0.868 
ICU time, x ± s, d 3.78±4.1 3.35±1.4 0.324 
Malignant tumors, n (%) 13 (18.6) 1 (1.4) 0.01 
Hypocardiac syndrome, n (%) 4 (5.7) 2 (2.9) 0.692 
Cardiac arrest, n (%) 2 (2.9) 3 (4.3) 0.137 
Nerve damage, n (%) 1 (1.4) 6 (8.6) 0.026 
Gastrointestinal bleeding, n (%) 3 (4.3) 5 (7.1) 0.778 
New dialysis, n (%) 7 (10.0) 5 (7.1) 1.0 

The comparison between the two groups is statistically significant, with p < 0.05 indicating a significant difference. Conversely, it indicates no difference. Hypocardiac syndrome was defined as postoperative monitoring of cardiac index (CI) <2 L (min*m2) by radial arterial thermodilution, accompanied by systemic hypoperfusion manifestations, including oliguria, decreased blood pressure, and increased lactate. Nerve damage included delayed awakening after cardiac surgery (>24 h), delirium, ischemic hypoxic encephalopathy, new limb and peripheral nerve dysfunction, etc.

The postoperative pathology reports showed that among the 70 cases in the observation group, there were 42 cases of myxoma, 6 lipomas, 3 papillary elastofibromas, 2 cavernous hemangiomas, 2 intravenous leiomyomass, 5 angiosarcoma, 2 low-grade malignant angioendothelial cell tumors, 2 epithelioid angioendothelial cell tumors, 1 malignant solitary fibroma, 1 rhabdomyosarcoma, and there remaining 4 cases of other malignant tumors (Fig. 1). Among the 70 patients in the control group, there were 38 myxomas, 8 lipomas, 7 papillary elastofibromas, 3 cavernous hemangiomas, 3 venous leiomyomas, 4 angiosarcomas, 1 low-grade malignant hemangioendothelioma, 2 epithelioid hemangioendothelioma, 1 malignant solitary fibroma, 1 rhabdomyosarcoma, and 2 other malignant tumors.

Fig. 1.

Distribution of tumor types in the observation group (n = 70).

Fig. 1.

Distribution of tumor types in the observation group (n = 70).

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Follow-Up Data Comparison

Except for the 4 deaths in the perioperative period, the remaining 136 cases had a follow-up rate of 100% and a total of 1–137 (60.19 ± 35.20) months of follow-up. There were 19 recurrent cases during the follow-up period, including 15 (22.4%) in the observation group and 4 (5.8%) in the control group (recurrent mass lesions in the heart were defined as recurrent cases shown with cardiac ultrasound or coronary computed tomography angiography). The Kaplan-Meier survival analysis by recurrence showed that the recurrence rate in the observation group was significantly higher than that in the control group during the follow-up period (Mantel-Cox test, χ2 = 7.49, p = 0.0062; Breslow-Wilcoxon test, χ2 = 9.791, p = 0.0018) (Fig. 2b).

Fig. 2.

Results of survival analysis during the follow-up period. a Blue indicated the survival rate in the observation group, black indicated the survival rate in the control group (p = 0.006). b Blue indicated the recurrent rate in the observation group, black indicated the recurrent rate in the control group (p = 0.002). When p < 0.05, it indicates a significant difference between groups.

Fig. 2.

Results of survival analysis during the follow-up period. a Blue indicated the survival rate in the observation group, black indicated the survival rate in the control group (p = 0.006). b Blue indicated the recurrent rate in the observation group, black indicated the recurrent rate in the control group (p = 0.002). When p < 0.05, it indicates a significant difference between groups.

Close modal

A total of 24 deaths were counted during the follow-up period, including 17 (25.4%) cases in the observation group and 7 (10.1%) cases in the control group. Kaplan-Meier survival analysis by death showed that during the follow-up period, mortality in the observation group was significantly higher than in the control group (Mantel-Cox test, χ2 = 5.66, p = 0.0174; Breslow-Wilcoxon test, χ2 = 7.573, p = 0.0059). The median survival time in the observation group was 112 months, meaning that patients in this group had a 50% survival rate at month 112, even though the median survival time in the control group was longer (Fig. 2a).

The study retrospectively analyzed the perioperative and follow-up data of 70 patients with primary right heart tumor who underwent surgical resection, aiming to explore the clinical characteristics, treatment process, and long-term efficacy of right heart tumors. Although myxoma is the most common type of benign right atrial tumor, with a total of 42 myxomas (60%) in the observation group, it rarely occurs in the right atrium. It occurs from subendocardial tumor precursor cells, including polygonal cells and pluripotent mesenchymal cells histologically [7, 8]. About 10% of the patients have a family history and are autosomal dominant inheritance [9], knowing as Carney’s syndrome – a neuroendocrine cardiac syndrome characterized as the following: (1) familial recurrent myxomas; (2) pigmented skin lesions, schwannomas, and multiple recurrent mucocutaneous mucormycosis; (3) hyperendocrine tumors [5]. One young female patient in this study had multiple recurrences and multiple mucocutaneous myxomas, with no clear family history. Neuroendocrine system lesions were further excluded after endocrinology consultation. Most of the right atrial myxomas are asymptomatic and often discovered incidentally during physical examination or treatment of other diseases. The proportion of vascular embolism is significantly lower than that of left heart myxomas. The perioperative data showed that there were 10 (14.3%) cases of systemic embolism in the control group, while only 4 (5.7%) cases of pulmonary embolism occurred in the observation group. However, in order to avoid serious complications including pulmonary embolism and hemodynamic disorders, the right atrial myxoma should be surgically resected once found, using cardiac ultrasound, cardiac computer tomography angiography, and positron emission tomography/computed tomography, to evaluate tumor morphology and CT value and exclude metastatic lesions before the surgery. The recurrence of right atrial myxoma may be related to multiple tumor growth, incomplete resection of surgery, disseminated implantation of tumor fragments, familial myxoma, and abnormal DNA. The recurrence rate of cardiac myxoma reported in the previous publication was 1-2% [10], while the recurrence rate of right atrial myxoma in this study was 2 cases (4.8%), all of which were ectopic recurrence.

The incidence of lipomas in benign heart tumors is second only to myxoma [11], and a total of 6 (8.6%) cases were lipomas in this study. The lipomas are composed of mature adipocytes, containing connective tissue components, and complete capsule [3]. The lipomas have a low radiodensity and a CT value of about −50 to +150 HU, which can be used as a key indicator for preoperative differential diagnosis. Intracardiac lipomas are often asymptomatic with small size. However, they can lead to arrhythmias or the obstruction of inflow and outflow tracts of the heart after grown up (Fig. 3). The prognosis for lipomas is good after surgical resection. In this study, 6 patients with lipoma resection had stable perioperative condition and no recurrence or death during follow-up period.

Fig. 3.

Patient with lipomyoma (case 1). a Cardiac ultrasound, with the arrow indicating that large pulmonary valve tumor blocked right ventricular outflow tract. b Tumor resected during surgery (10*5.5*4.5 cm3) growing from the pulmonary valve, with the arrow indicating the pulmonary valve. MPA, main pulmonary artery; AO, aorta; RPA, right pulmonary artery; LPA, left pulmonary artery.

Fig. 3.

Patient with lipomyoma (case 1). a Cardiac ultrasound, with the arrow indicating that large pulmonary valve tumor blocked right ventricular outflow tract. b Tumor resected during surgery (10*5.5*4.5 cm3) growing from the pulmonary valve, with the arrow indicating the pulmonary valve. MPA, main pulmonary artery; AO, aorta; RPA, right pulmonary artery; LPA, left pulmonary artery.

Close modal

Papillary elastofibroma is common in middle-aged and elderly patients, which often involve valve dysfunction and cause cardiac insufficiency. Papillary elastofibroma tends to occur in the left heart system and is prone to partial tumor detachment or embolism. In 2019, we summarized the clinical characteristics of 11 heart valve tumors, of which 5 were papillary elastofibromas and all occurred in the left heart system. In addition, there were no recurrences or deaths within 5 years after surgical resection [12]. Among the 70 cases in this study, there were 2 cases (2.9%) of papillary elastofibromas, located in tricuspid valve and pulmonary valve, respectively (Fig. 4). After surgical resection and simultaneous valvuloplasty, there were no recurrence or death during follow-up period.

Fig. 4.

Patient with papillary elastofibroma (case 2). a Cardiac CTA, with the arrow indicating the space-occupying lesion located in the right atrium. b Intraoperative pictures, with the arrow indicating the tumor. RA, right atrium; RV, right ventricle; DAO, descending aorta; LA, left atrium; LV, left ventricle; RAA, right atrium appendage; PTS, posterior tricuspid leaflet.

Fig. 4.

Patient with papillary elastofibroma (case 2). a Cardiac CTA, with the arrow indicating the space-occupying lesion located in the right atrium. b Intraoperative pictures, with the arrow indicating the tumor. RA, right atrium; RV, right ventricle; DAO, descending aorta; LA, left atrium; LV, left ventricle; RAA, right atrium appendage; PTS, posterior tricuspid leaflet.

Close modal

Venous leiomyoma mostly occurs in young and middle-aged women, aged 35–50 years before menopause. Venous leiomyoma is a proliferation of smooth muscle cells occurring in the vein, which can protrude into the uterus or pelvic vein, extending to the inferior vena cava and right atrium. Although it is benign histologically, the growth pattern is similar to malignant tumors [13]. In the study, one 41-year-old female with intravenous leiomyoma underwent total uterus, bilateral appendages, and pelvic mass resection during the surgery. After the incision of the middle of chest, the inferior vena cava, right atrium, and pulmonary artery incisions were made, respectively, and the full-length tumor cord was carefully separated and dragged out (Fig. 5a). The tricuspid valve was slightly to moderately regurgitated 16 months after the surgery.

Fig. 5.

Patient with intravenous leiomyoma and angiosarcoma (cases 3 and 4). a Thoracoabdominal aortic CTA, with the arrow indicating the space-occupying lesion located in the inferior vena cava. b Cardiac CTA, with the arrow indicating the tumor located from the right ventricular wall to the tricuspid annulus (a RK, right kidney; LK, left kidney; DAO, descending aorta; LV, lumbar vertebra) (b RA, right atrium; RV, right ventricle; LV, left ventricle; TV, thoracic vertebra; IVS, interventricular septum; DAO).

Fig. 5.

Patient with intravenous leiomyoma and angiosarcoma (cases 3 and 4). a Thoracoabdominal aortic CTA, with the arrow indicating the space-occupying lesion located in the inferior vena cava. b Cardiac CTA, with the arrow indicating the tumor located from the right ventricular wall to the tricuspid annulus (a RK, right kidney; LK, left kidney; DAO, descending aorta; LV, lumbar vertebra) (b RA, right atrium; RV, right ventricle; LV, left ventricle; TV, thoracic vertebra; IVS, interventricular septum; DAO).

Close modal

Angioendotheliomas can be divided into epithelioid angioendothelioma and angiosarcoma, which are the most common subtypes and accounting for about 1/3 of primary malignant cardiac tumors. Epithelioid angioendothelioma generally occurs in the skin and soft tissues of the liver, lung, and extremities and very rarely occurs in the heart [14]. It is low-grade malignant and has the potential for metastasis. For heart angiosarcoma, it often occurs in the right atrioventricular sulcus and invades the right atrial wall and pericardium, presenting with pericardial effusion-induced tamponade, vena cava obstruction, or right heart failure (Fig. 5b). The survival time for untreated angiosarcomas is only 6 to 9 months [15]. In this study, there were 5 cases of angiosarcoma and 2 cases of epithelioid angioendothelioma. One case died of postoperative liver and kidney failure in the perioperative period after the surgical resection, 4 cases relapsed within 20 months, and the remaining 1 case recurred 36 months after surgery even received radiotherapy and chemotherapy intermittently after the surgery. Malignant cardiac tumors remain a challenge in treatment, and complete resection is the only management that could improve the prognosis, when preoperative positron emission tomography/computed tomography suggests no or limited metastases [16]. However, since it was often asymptomatic or had only non-specific symptoms in the early stage, distant metastasis has often occurred when it was discovered, making difficult for complete resection [17]. Even after complete resection, the vast majority of patients relapse and die from metastasis. The overall median survival of malignant heart tumors was about 6–18 months [18]. In more than 500 primary malignant heart tumors, Oliveira et al. [19] reported a median survival time of 10 months. The combined management including surgery, chemoradiotherapy, immunotherapy, and other comprehensive treatments is the best treatment to prolong the survival of patients with primary cardiac malignancies [20]. In this study, there were 13 cases (18.6%) of malignant tumors, among which 3 cases died in the perioperative period, and the recurrence rate was 100% during the follow-up period, except for 1 case lost to follow-up. Postoperative survival ranged from 0.5 to 36 (12.7 ± 8.7) months, among which 5 patients survived more than 10 months, and 3 patients received chemoradiotherapy or immunotherapy, with survival of more than 12 months.

This study described the clinical characteristics of primary right heart tumors through comparison with left heart tumors. Compared with left heart tumors, primary right heart tumors have a higher incidence of malignant tumors and a lower risk of systemic embolism during perioperative period. In addition, primary right heart tumors have a higher rate of tumor recurrence and a lower long-term survival rate.

This study protocol was reviewed and approved by the Xinqiao Hospital, Army Medical University, approval number 2020-No.010-01. Written informed consent was obtained from all adult patients to participate in the study and from the participants’ legal guardian for all minor patients.

There are no potential conflicts of interest to disclose.

This study was funded by the Chongqing Natural Science Foundation project, CSTB2022NSCQ-MSX0200.

T.L. is the guarantor of integrity of the entire study, study concepts and design, definition of intellectual content, literature research, and manuscript preparation and editing; C.L. is responsible for the data acquisition and analysis and statistical analysis; X.P. is responsible for the clinical studies, experimental studies, data analysis, and statistical analysis; S.Z. is responsible for the clinical studies, data analysis, and statistical analysis; S.G. is responsible for the data acquisition; W.P. is responsible for the experimental studies; and Y.W. is the guarantor of integrity of the entire study, literature research, and manuscript review. All authors read and approved the final manuscript.

All data generated or analyzed during this study are included in this article. Further inquiries can be directed to the corresponding author.

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