Extracardiac Complications in Intensive Care Units after Surgical Repair for Congenital Heart Disease: Imaging Review with a Focus on Ultrasound and Radiography

Abstract

Pediatric patients show various extracardiac complications after cardiovascular surgery, and radiography and ultrasound are routinely performed in the intensive care unit to detect and evaluate these complications. This review presents images of these complications, sonographic approach, and timing of occurrence that are categorized based on their extracardiac locations and include complications pertaining to the central nervous system, mediastinum, thorax and lung parenchyma, diaphragm, liver and biliary system, and kidney along with pleural effusion and iatrogenic complications. This pictorial review will make it easier for medical doctors in intensive care units to identify and manage various extracardiac complications in pediatric patients after cardiovascular surgery.

Keywords

complication - pediatric - cardiovascular surgery

Introduction

Various extracardiac complications have been reported in pediatric patients after cardiovascular surgery.[1] These patients should receive early and appropriate interventions to prevent a prolonged stay in the intensive care unit.[2] [3] [4] Radiography and ultrasound are routinely performed at patients' bedside by pediatric physicians, cardiologists, intensivists, or radiologists to detect these complications and evaluate the patients' condition while they are admitted to the intensive care unit.[3] [5] [6] [7]

To the best of our knowledge, although some previous reports have focused on the risk factors for the occurrence of these complications and their prognosis, there are no reports focusing on the image findings of these complications. The purpose of this review is to show the image findings of these complications using radiography and ultrasound.[2] [8] [9] [10] This pictorial review will help doctors in intensive care units to more easily identify and manage various extracardiac complications in pediatric patients after cardiovascular surgery.

Classification Based on the Location of the Extracardiac Organ

The extracardiac complications occurring after cardiovascular surgery are classified based on the locations of occurrence. [Tables 1] and [2] show locations and types of these complications ([Table 1]: locations and types of complications and intrathoracic and diaphragmatic complications, and [Table 2]: locations and types of complications and intra-abdominal and other locations' complications). Although their incidence and timing of onset vary depending on the underlying congenital heart diseases, treatments or institutions' comprehensive data pertaining to these complications are important for daily management and evaluation of pediatric patients after cardiovascular surgery in the intensive care unit.

Table 1 Locations and types of complications: intrathoracic and diaphragmatic complications

Location	Types	Incidence (number of occurrence/total number)	Interval between surgery and diagnosis average ± SD (range)	Comments	Ref.
Mediastinum	Hemorrhage/hematoma	10% (6/54)			[115]
		N/A	16 (12–22) days	3 cases	[9]
		4.1% (5/121)		Only patients who underwent mechanical aortic valve replacement were included	[116]
		N/A	1 and 10 days	2 cases	[12]
		11–40%		Variable bleeding rate depending on the implanted durable devices	[117]
	SSI	2.2% (9/412) 5.8% (24/412)		Organ/space infection DII or SWI	[2]
		2.4% (27/1,117) 0.1% (1/1,117) 0.9% (10/1,117)		Organ/space infection DII SWI	[118]
		0.8% (7/826) 1.5% (12/826)		Organ/space infection DII and SWI	[119]
		N/A	17.2 (6–30) days 5 and 10 days	6 cases with DII and SWI 2 cases with organ/space infection	[120]
		6.3% (384/6,127) 1.8% (107/6,127)		Wound infection with delayed sternal closure Mediastinitis with delayed sternal closure	[121]
	Mediastinitis (organ/space infection)	1.1% (29/2,675)	10 (5–27) days		[122]
		N/A	27.3 (7–53) days		[9]
		0.2% (17/7,616)	14 (6–50 days) days		[18]
		0.85% (57/6,705)	13 days		[123]
		5% (10/202)			[124]
		1.4% (19/1,405)	32 days (5 days–9 months)		[125]
		1.7% (64/3,650)	13.4 (4–37) days		[126]
		8.3% (3/36)	8.8 (5–14) days	Only neonate (under 4 weeks of age) were included	[127]
Pleural effusion	Pleural effusion	N/A
	Hemothorax	N/A
	Chylothorax	5% (57/1,135)	0–10 days		[23]
		5% (12/238)		Chylothorax or plastic bronchitis. All cases with Fontan procedure were included.	[30]
Thorax	Pneumothorax	N/A
Lug parenchyma	Atelectasis	N/A
Lung infection	Pneumonia Respiratory infection upper Respiratory infection lower	0.7% (3/412) 1.7% (7/412) 0.5% (2/412)			[2]
Diaphragm	Diaphragmatic paralysis	1.5% (25/1,656)		Plication rate was 44%, and the procedure was performed 2–3 weeks after operation	[128]
		0.46% (47/10,200)		Plication rate was 79%, and the procedure was performed 24 ± 14 days after the operation	[41]
		2.1% (19/891)		Plication rate was 79%	[40]
		4.9% (152/3,071)		Plication rate was 1.3%, and the procedure was performed 17.8 ± 3.6 days after the operation	[39]
		4.8% (24/500)		Plication was performed in all cases	[129]

Abbreviations: DII, deep incisional infection; N/A, not available; Ref., reference; SD, standard deviation; SSI, surgical site infection; SWI, superficial wound infection.

Table 2 Locations and types of complications: intra-abdominal and other locations' complications

Location	Types	Incidence (number of occurrence/total number)	Interval between surgery and diagnosis average ± SD (range)	Comments	Ref.
CNS	IVH Cerebral infarction	0.9% (5/543) 1.7% (9/543)			[49]
	IVH	17% (6/34)	4 hours after the surgery (routine examination)	Arterial switch operation in neonates	[50]
	Subdural hemorrhage	0.1% (1/706)			[47]
Liver and biliary system	Acute liver failure (liver insufficiency)	15% (8/54)		This study focused on the NEC. Neonates with and without NEC were included.	[70]
	Debris within biliary system	N/A	19th day	Case report	[130]
Intestine	NEC	11% (8/73)			[70]
		18% (9/43)		Hypoplastic left heart syndrome	[68]
		13% (14/108) 12% (8/66) 14% (7/50)	25 ± 17 (days of life) 36 ± 19 (days of life) 22 ± 15 (days of life)	Indomethacin (performed 4 ± 3 days of life) Indomethacin and ligation (11 ± 8 days of life) Ligation (9 ± 13 days of life) Treatment for PDA in premature neonates;	[73]
		11.0% (8/65) 5.8% (3/49)		Only neonates performed the Norwood procedure were included and using different protocol of enteral feeding	[131]
		14/52 (27%) 3/46 (6.5%)		Hypoplastic left heart syndrome after the Norwood procedure and using different protocol of enteral feeding	[71]
		N/A	21 postoperative hours (1 case) 1 postoperative day (2 cases)	3 cases reports	[69]
		1.7% (19/1120)			[67]
	Paradoxical hypertension result in postcoarctectomy syndrome or mesenteric arteritis	56% (14/25)		After repair of coarctation of the aorta	[86]
		6% (9/145)	4 (3–6) days	After repair of coarctation of the aorta	[72]
	Gastroenteritis	0.08% (1/1120)			[67]
Kidney	AKI	90% (53/59)		Using ECMO during cardiovascular surgery	[132]
		54% (352/613)	2 (1–6) days	AKI remained stable until 4th postoperative days	[133]
		62% (76/122)	Progression of AKI within 48 hours after surgery	Only neonates were included	[8]
		35% (33/125)	1 postoperative day in 57% of cases (1–27 days)	Most cases resolved within 24 hours (65% of cases)	[94]
		26% (51/194) 14% (28/201)		<2 years ≥2years	[134]
		17% (53/311)	Sever AKI (receipt of acute dialysis)		[137]
		51% (234/458)	Usually within 48 hours after surgery		[135]
	UTI	3.6% (15/412)			[2]
Vascular complication[a]	Phlebitis associated PICC[a]	13% (83/654)	86 hours (12–286 hours after insertion)		[105]
	Venous thromboembolism	2% (65/2,718)			[136]
	Thrombosis	15% (8/53) 16% (6/37)	4.8 ± 3.7 days 5.1 ± 3.6 days	With heparin With placebo	[106]

Abbreviations: AKI, acute kidney injury; CNS, central nervous system; ECMO, extracorporeal membrane oxygenation; IVH; Intraventricular hemorrhage; N/A, not available; NEC, necrotizing enterocolitis; PDA, patent ductus arteriosus; PICC, peripheral inserted central catheter; SD, standard deviation; UTI, urinary tract infection.

^a Catheter-associated complications: there were no previous reports focusing on pediatric patients after cardiovascular surgery; therefore, these incidences were reported from studies targeting pediatric patients.

Approach Methods Using Ultrasound for Various Complications

In clinical settings, abdominal or cardiac ultrasound is usually performed, whereas in intensive care units, ultrasound is performed for various sites ([Fig. 1]). The approach for nonfamiliar sites may differ across physicians; therefore, a schematic guideline to demonstrate the approach methods for nonfamiliar target organs, such as the cranium, trachea, mediastinum, lungs, and diaphragm, is necessary.[3] [11] [12] [13] [14] [15] Vascular complications can be found at any location; hence, point-of-care ultrasound is useful.

Fig. 1 Schematic presentation of the standard scanning approach. (A) Correct placement of the transducer for cranial approach via posterior fontanelle to obtain the coronal or sagittal view. (B) Schematic presentation of coronal view via the posterior fontanelle. Transducer is located at the line B in [Fig. 1A] ([Fig 2A]). (C) Schematic presentation of sagittal view via the posterior fontanelle. Transducer is located at the line C in the [Fig. 1A] ([Fig 2B]). (D) Tracheal tube evaluation using axial view at above the suprasternal approach (line 1) ([Fig 26]). Mediastinum evaluation using axial view at the suprasternal (line 1), transsternal (line 2), or subxiphoid approach (line 3). (E) Mediastinum evaluation using sagittal view at the parasternal approach (line 4) ([Figs. 3] [4] [5]). (F) Lung evaluation by using ultrasound. Intercostal or parasternal approach is used. Each thorax is divided into some areas and almost the entire area of the lung can be evaluated (upper lung, line 5; middle lung, line 6; base lung, line 7 ([Fig. 12B] and [12D]). (G) Posterior paraspinal approach is useful for to the posterior lung parenchyma (medial side, line 8; lateral side, line 9). (H) Diaphragmatic motion of both right- and left-side evaluation using axial view at the subxiphoid (line 10). Movement of the mediastinum can be also evaluated ([Fig 13D]). (I) Diaphragmatic motion evaluation using longitudinal view at the posterior axially line on each side (line 11 [[Fig 13B]] and 12 [[Fig 13C]]). (J) Vascular complications are evaluated in the affected vessel. Innominate vein is visualized using the at suprasternal approach (line 13; [Fig 23B]). The subclavian vein and proximal side of the common carotid vein are visualized at the supraclavicular approach (line 14; [Fig 23A]).

Timing of Examination

In the guideline for after surgical repair for congenital heart disease, if a change in clinical status or new concerning signs or symptoms are detected, computed tomography (CT) and radiography could be recommended.[16] In the guideline, however, transesophageal echocardiogram is included but ultrasound targeting the abdomen or other organs is not included.[16] The timing of examination could be varied based on the kinds of complication and of modality used for the diagnosis. Therefore, the timing of occurrence of each complication and strategy, including the modality for diagnosing the complications, was stated in each below section of complications.

Locations and Types of Complications: Intrathoracic and Diaphragmatic Complications

Mediastinum

Information regarding mediastinal complications, including surgical site infection (mediastinitis) and hemorrhage, is important to ensure appropriate intervention ([Table 1]).

Timing of Occurrence and Strategy for the Diagnosis

The complications in the mediastinum include hemorrhage or surgical site infection. Mediastinal hemorrhage usually occurs within 1 week after intrathoracic surgery.[9] [17] [18] [19] The surgical site infection (organ/space infection [mediastinitis]) usually occurs 1 week after intrathoracic surgery.[9] [17] [18] [19] Computed tomography is reported to be a useful modality for diagnosing mediastinitis; however, this modality requires radiation exposure and cannot be performed at a patient's bedside; ultrasound is reported to be useful for diagnosing mediastinitis.[5] [12] [20] If the circulation status is stable to undertake the ultrasound, ultrasound is used to detect the retrosternal fluid correction at the patients' bedsides. If fluid correction is detected, further examinations, such as CT, were recommended.[9] [12] [19] Color Doppler ultrasound is useful for evaluating the intrathoracic structure and differentiating a pseudoaneurysm from the fluid correction.[5] [12]

• Mediastinal hematoma/hemorrhage: Hematoma or bleeding at the surgical site is a critical complication during and after surgical procedures, and it is a common complication that requires reoperation.[1] Hematoma results in an unstable circulation status, necessitating rapid surgical intervention. Management of hematomas may be difficult and should be based on each patient's condition. In addition to vital sign and laboratory data, image findings may be useful to diagnose this complication ([Fig. 2]).[12]

• Surgical site infection (incisional or organ/space [mediastinitis]): surgical site infection is classified into following three types based on the depth of the infection: (1) superficial wound infection, (2) deep incisional infection, and (3) organ/space infection. Mediastinitis is classified as an organ/space infection, and it causes critical complications, has a high mortality rate, and requires adequate surgical intervention ([Figs. 3] and [4]).[2] [9]

Fig. 2 Mediastinal hematoma. A 4-month-old female who underwent cardiovascular surgery for coarctation of the aorta and ventricular septal defect. The patient showed a decreased red cell blood count, and mediastinal hematoma is diagnosed. (A) Chest radiograph on the day of the operation. The width of the mediastinum is normal (double heads arrow). (B) Chest radiograph on the day after the operation. The width of the mediastinum is larger than that in [Fig. 2A] (double heads arrow). Hematoma is suspected. (C) Sagittal sonogram shows fluid collection behind the retrosternal space (arrows). It has complex echogenicity. R, ribs.

Fig. 3 Surgical site infection (deep incisional infection). Images obtained 20 days after surgery for transposition of the great arteries in a 1-month-old female infant. (A) Sagittal sonogram showing a hyperechoic area in the subcutaneous fat tissue (arrows). Fluid collection behind the sternum is not detected. Presence of superficial wound infection is suspected. (B) Axial computed tomography showing absence of fluid collection behind the sternum; there is low attenuation in the subcutaneous tissue and anterior chest wall (arrows). The infection progressed to a deep incisional infection. S, separated sternal ossifications.

Fig. 4 Images of surgical site infection (organ/space infection; mediastinitis) that were obtained 21 days after surgery for a ventricular septal defect in a 22-month-old female child. (A) Fluid collection detected behind the sternum (arrows). Parasternal hyperechogenicity is present (arrowheads). The infection progressed to an organ/space infection (mediastinitis). (B) Sagittal computed tomography shows fluid collection with capsular enhancement (arrows) and an air bubble within the collection. Organ/space infection (mediastinitis) is diagnosed. R, the ribs.

Sonographic Evaluation

Ultrasound was recently reported to be useful in the evaluation of mediastinitis.[5] [12] Retrosternal fluid collection and parasternal hyperechogenicity are usually detected in cases of mediastinitis.[12] [19] Superficial wound infection and deep incisional infection are detected as parasternal or subcutaneous hyperechogenicity ([Fig. 3]), and organ/space infection is detected as retrosternal fluid collection ([Fig. 4]).[5] [12] Although these findings have high–negative predictive value for diagnosing mediastinitis, cases with hematoma may show these findings ([Fig. 2]).[9] [12] [19] In addition, Hosokawa et al reported that the two cases with mediastinitis having retrosternal simple fluid correction.[12] There are various CT reports that the cases with mediastinitis had various degree of enhancement and various timing when the mediastinitis occurred.[9] [17] [19] Echogenicity within the retrosternal fluid correction might be varied based on the degree of inflammation, period between the examination and onset of mediastinitis, and treatment before the examination.

Pleural Effusion, Thorax, and Lung Parenchyma

Atelectasis, pneumonia, or pleural effusion associated with mechanical ventilation may occur in pediatric patients after cardiovascular surgery.[2] These complications are caused by mechanical support modalities such as ventilation or extracorporeal membrane oxygenation (ECMO).[21] Lung ultrasound is typically used to evaluate these complications in intensive care units.[6] [22]

Timing of Occurrence and Strategy for Diagnosis

Hemothorax or atelectasis may occur during operation or in the intensive care unit. After ECMO, lung opacity for lung rest usually occurred within 24 hours, and may last only a few days or as long as 4 to 6 weeks depending on the patients' pulmonary condition.[21] The duration between thoracic duct injury and development of chylothorax is usually 0 to 10 days.[23] Pleural effusion is diagnosed by combination of clinical symptom, radiography, and ultrasound. Based on the species of pleural effusion, further recommended examination is changed. If the chylothorax suspected, lymphoscintigraphy is usually recommended.[24] [25] [26]

1. Pleural effusion without or with complex echogenicity

Pleural effusion is commonly observed after cardiovascular surgery. Ultrasound is a useful modality to evaluate the characteristics of this effusion ([Figs. 5] and [6]).[6] [22]

Fig. 5 Pleural effusion. A 17-day-old female patient with total anomalous pulmonary venous connection. Surgical repair was performed 7 days after birth. The effusion is characterized by serous fluid, not accumulation of chyle nor hemothorax, via the drainage tube. (A) Bilateral pleural drainages are shown in the chest radiograph. (B) Sagittal sonogram demonstrates pleural fluid at the right lung base (arrow). It does not have internal echoes or separations.

Fig. 6 Hemothorax. A 3-month-old male who underwent the Blalock–Taussig shunt. (A) Left pleural drainage is shown in the chest radiograph. (B) Axial sonogram demonstrates pleural fluid at the left lung base. It had hyper- and low-echoic density within the pleural cavity (arrows), representing hemothorax.

Sonographic Evaluation

The echogenicity within the effusion is different for the varying etiologies of pleural effusion.[27] Transudative pleural effusion is anechoic ([Fig. 5]), while exudative pleural effusion showed septation or nonseptation and is anechoic.[27] Hemothorax occurs frequently after cardiovascular surgery. Blood in the pleural cavity shows a complex echogenicity, including hyper- to low-echoic density ([Fig. 6]).[28] [29]

2. Chylothorax

Chylothorax refers to the accumulation of the chyle in the pleural cavity that usually develops after disruption of the thoracic duct during intrathoracic surgery ([Fig. 7]).[23] Chylothorax after cardiovascular surgery is a not-so-rare complication and is related to the duration of hospitalization.[23] [30] Various modalities, such as lymphoscintigraphy, lymphangiography, and magnetic resonance lymphography, have been used to evaluate this condition and select appropriate treatment.[24] [25] [26] However, traumatic events resulting in chylothorax are usually obvious, minor surgical trauma has also been noted to result in chylothorax. Therefore, the lymphoscintigraphy procedure is important for diagnosing chylothorax. This examination is easy compared with lymphangiography because it is performed only after injection of 99 mTc-HAS-DTPA into the subcutaneous tissue of the bilateral dorsum pedis.[31] [32] The first treatment usually was total parenteral nutrition instead of the nutrition per mouth until chyle drainage decreases. Octreotide intravenous infusion is added in patients who do not show a response to these treatments.[23] In cases showing no response to conservative treatment, including surgical ligation, lymphatic-venous anastomosis, and embolization at the leakage, point system might be performed.[23] [24] [33]

Fig. 7 Chylothorax. A 2-year-old male who underwent surgical repair for congenital heart disease. After surgical repair, accumulation of the chyle continued in the left pleural cavity. Since the patient did not respond to conservative treatment, further studies were performed. (A) Left pleural drainage is shown in the chest radiograph. (B) Radioisotope lymph scintigraphy shows abnormal tracer accumulation in the left pleural cavity (arrow). (C) Anteroposterior lymphangiogram shows lymph node as a subtle nodular stain (arrowhead). The leakage point into the left pleural cavity is revealed (arrow). (D) Coronal reconstructed computed tomography after lymphangiography shows the cisterna chyli to the leakage point (arrow).

3. Pneumothorax

Pneumothorax can be demonstrated or excluded with a high degree of accuracy using ultrasound ([Figs. 8] and [9]).[6] [22] Artifacts, such as the comet-tail sign or bands, of reverberating echoes are normally seen at the junction of the pleura and the ventilated lung.[6] [22]

Fig. 8 Pneumothorax. Images of a 25-day-old female neonate who underwent the Blalock–Taussig shunt. Transverse sonogram shows the absence of a B-line as a comet-tail artifact (arrows), leading to a diagnosis of pneumothorax. On the left side of the pneumothorax, the presence of comet-tail artifacts (arrowheads) indicates the presence of lung parenchyma. R, ribs.

Fig. 9 Normal case without pneumothorax. Images of a 23-day-old female neonate with Blalock–Taussig shunt 1 week postoperatively. (A) On the chest radiograph, the left lung appears more radiolucent than the right lung. (B) Ultrasound shows an A-line (arrows) and a B-line as a comet-tail (arrowheads). Therefore, pneumothorax is not present in this case. R, ribs.

Sonographic Evaluation

The detection of lung point, which represents the physical limit of pneumothorax, is important to diagnose the pneumothorax ([Fig. 8]).[34] The area with absence of lung sliding or movement of B-line, that is, comet tail–like artifact extending from pleural line to the bottom of the screen obliterating, is the area of affected pneumothorax ([Figs. 8] and [9]).[34] [35]

4. Atelectasis

Lung atelectasis is a common finding in the intensive care unit. Aspiration, prolonged bed rest, or iatrogenic factors may result in the atelectasis. In addition, atelectasis caused by lung rest usually occurs after ECMO ([Fig. 10]).[21] In patients undertaken the ECMO, the lungs show progressive opacification on radiograph. The etiology of these changes is unclear, but multifactor, such as varying degrees of widespread atelectasis and pulmonary edema, was influenced.[21] [36] Lung ultrasound was reported to be able to differentiate the atelectasis, lung edema, and pleural effusion.[6] [11] [22] [34] Therefore, ultrasound may be useful morality to evaluate the lung status after ECMO.

Fig. 10 Atelectasis. A 1-month-old female receiving extracorporeal membrane oxygenation after surgical repair for congenital heart disease. (A) Extracorporeal membrane oxygenation was introduced. Bilateral pleural effusion is suspected. (B) Transverse sonogram on the left base lung shows hepatization with air bronchograms in the central area of the lung (arrows) and without air bronchograms in the peripheral area of completely deaerated lung (arrowheads). (C) Chest radiograph taken after 2 weeks with lung physical therapy. (D) Transverse sonogram shows decreased area of hepatization in the left lung. In the peripheral area of the lung, air bronchogram is more clearly detected than that in B (arrowheads).

Sonographic Evaluation

Lung aeration can be classified as well aerated, partially aerated, or completely deaerated.[35] [37] The well-aerated lung is seen as A-line; this is seen as parallel lines in the intercostal space that descend to the bottom of the screen ([Fig. 9]). Dynamic sliding of the pleura is clearly detected in real time. The partially aerated lung is seen as B-line; this is seen as a comet tail–like artifact, extending from the pleural line to the bottom of the screen ([Fig. 8]). Increased numbers of B-line are seen in interstitial lung disease or edema.[37] [38] The deaerated lung, as in lung consolidation, has a shredding appearance on the air bronchogram ([Fig. 10]).

Diaphragm

Phrenic Nerve Paralysis

Timing of Occurrence and Strategy for Diagnosis

Phrenic nerve paralysis may occur during surgery. Surgical treatment, such as diaphragmatic plication, is usually performed at least 2 weeks after operation.[39] [40] [41] This complication is suspected in routine radiograph and ultrasound is usually recommended to evaluate the motion of diaphragm.[3] [13] [22] [39] [42] While fluorography is also a useful morality to diagnose this complication, this procedure cannot be performed at a patient's bedside.[42]

Phrenic nerve paralysis after cardiovascular surgery is associated with prolonged hospitalization ([Fig. 11]).[39] Radiographic findings showing the differences on each side of the diaphragm are important to suspect the presence of phrenic nerve paralysis.[42] Based on this suspicion, movement of the diaphragm is evaluated using ultrasound or fluorography.[3] [13] [22] [39] [42] M-mode ultrasonography in a longitudinal view of the diaphragm is performed by positioning the probe on the posterior axillary line on one side with the transducer notch pointing 12 o'clock toward axilla.[3] Paradoxical movement of the diaphragm or weak movement of the affected diaphragm is observed in cases with this complication.[39] [43]

Fig. 11 Phrenic nerve paralysis. Images obtained 1 week after surgery for transposition of the great arteries in a 17-day-old female neonate. (A) Chest radiograph shows that the left diaphragm is higher than the right. (B) M-mode sonogram showing normal diaphragmatic movement during spontaneous ventilation. The movement of the right diaphragm during inspiration is toward the transducer with an excursion of more than 4 mm (arrow). (C) M-mode sonogram showing paradoxical diaphragmatic movement during spontaneous ventilation. The movement of the left diaphragm is away from the transducer during inspiration (arrowheads). (D) The position of the left diaphragm (arrowheads) has not changed during inspiration and expiration. The right diaphragm (arrows) shows normal movement. The descending aorta is located more toward the right during expiration than during inspiration. (E) Using fluoroscopy, mediastinum is seen toward the right during inspiration, with the left diaphragm (arrowheads) at a higher position. The right diaphragm (arrows) shows normal movement. Ao, descending aorta; M, mediastinum.

Sonographic Evaluation

Normal movement of the diaphragm is defined as movement toward the transducer during inspiration with an excursion of more than 4 mm and a difference of less than 50% between the movements of the two hemidiaphragms ([Fig. 11]). Paretic movement is defined as an amplitude of less than 4 mm and a difference of more than 50% between the movements of the two hemidiaphragms. Paradoxical movement is defined as diaphragmatic movement away from the transducer during inspiration ([Videos 1] and [2]; available in the online version).[3] [44] [45]

Video 1 The position of the left diaphragm is unchanged during inspiration and expiration. The right diaphragm demonstrates normal movement. The descending aorta is located more toward the right during expiration than during inspiration. Therefore, paradoxical movement of diaphragm was diagnosed. Ao, descending aorta.

Video 2 Fluoroscopic examination of the diaphragm. The right normal hemidiaphragm descends with inspiration. The left hemidiaphragm demonstrates paradoxical upward movement with inspiration. The mediastinum is located more toward the right during expiration than during inspiration.

Locations and Types of Complications: Intra-abdominal and Other Locations' Complications

Central nervous System

The incidence of acute neurologic complications after cardiovascular surgery in pediatric patients is reported to be 2 to 25%.[46] [47] Although the anterior fontanelle typically closes between the ages of 12 and 18 months, ultrasound via the fontanelle is useful to evaluate hemorrhage ([Table 2]).[48]

Timing of Occurrence and Strategy for Diagnosis

Central nervous system complications are associated with hypoperfusion, cardiac arrest, or thromboembolism, or treatment such as anticoagulant therapy.[46] [47] [49] Therefore, these complications may be encountered during cardiovascular surgery. Intracranial hemorrhage can be found 4 hours postoperatively using ultrasound.[50] However, cranial ultrasound is useful to diagnose this complication, in case with after closure of the anterior fontanelle, CT, or magnetic resonance imaging is needed to diagnose this complication.[51] Magnetic resonance imaging does not have need of radiation exposure, but it needs the relative longer time for examination compared the CT. The values of the resistive index, peak systolic, end diastolic, and time-averaged velocities of intracranial artery are determined by using Doppler techniques, and that is useful for the diagnosis, follow-up, and management of brain damage.[52] [53]

• Hemorrhage: hemorrhage is associated with anticoagulant therapy or prematurity ([Fig. 12]).[47] [48] Ultrasound via the anterior fontanelle is useful to evaluate this complication.[48] It is important to distinguish the choroid plexus hemorrhage from the normal choroid plexus, which is also echogenic. The echogenicity anterior to the caudothalamic groove represents blood as the choroid plexus finishes at the caudothalamic groove, and the choroid plexus hemorrhage is diagnosed sonographically when the affected side is enlarged, or irregular in contour as compared with the contralateral nonaffected side.[51] [54] [55] [56] Sequelae, such as hydrocephalus and brain atrophy, can also be evaluated using ultrasound.[48] [57]

Fig. 12 Hemorrhage. An 18-day-old neonate with transposition of the great arteries. Surgical intervention with percutaneous cardiopulmonary support was performed 7 days after birth. Subsequently, intraventricular hemorrhage is detected by ultrasound examination via the anterior fontanelle. (A) Coronal sonogram shows a high-echoic mass in the right and left ventricles (arrows) without ventricular dilation. (B) Sagittal sonogram shows intraventricular hemorrhage (arrow). (C) T1-weighted magnetic resonance image shows blood with iso- to high-signal intensity in bilateral ventricles (arrows) without ventricular dilation.

Liver and Biliary System

Liver dysfunction in pediatric patients with congenital heart disease is associated with congestion and low cardiac output.[58] Liver complications after the Fontan procedure are known to be chronic in nature.[59] Acute liver failure after cardiovascular surgery is usually associated with low cardiac output during the operation.[60] [61] In addition, fatty liver or accumulation of debris within the biliary system may be caused by using medication or total parenteral nutrition.

Timing of Occurrence and Strategy for Diagnosis

Acute liver failure or liver sufficiency is usually accompanied with low cardiac output during operation and acute renal failure.[60] [61] Therefore, circulation status during the operation is important. The ultrasound should be the first method of diagnostic imaging used for inflammation of biliary system and differentiate from other liver diseases.[62] The contrast-enhanced CT or magnetic resonance imaging may be recommended to evaluate etiology of inflammation of biliary system, such as causative stone in the gallbladder or bile duct, if the etiology is not detected clearly buy ultrasound.[62]

• Acute liver failure (liver sufficiency): patients with acute liver failure usually show evidence of low cardiac output and acute renal failure ([Fig. 13]).[60] [61] Acute liver failure after cardiovascular surgery may occasionally present with marked prolongation of the prothrombin time, which is associated with failure of hemostasis and hypoglycemia.[60] [61]

• Fatty liver: fatty liver is a rare disease in pediatric patients ([Fig. 14]). However, it may appear in these patients as a result of medications or total parenteral nutrition.[63] [64] Liver disorder in the intensive care unit is occasionally caused by fatty liver.

• Accumulation of debris within the biliary system: some drugs or total parenteral nutrition may result in the accumulation of debris within the biliary system ([Fig. 15]).[65] [66] In some cases, this complication required appropriate treatment.[66] Ultrasound is a useful modality to evaluate this condition.[65]

Fig. 13 Live sufficiency. A 1-year 3-month-old male with the tetralogy of Fallot: surgical repair was performed 20 days previously. Hepatic vein is dilated (arrows) due to congestion and low output circulation status.

Fig. 14 Fatty liver. A 1-year 3-month-old male with the tetralogy of Fallot: surgical repair was performed 20 days previously. Liver shows hyperechogenicity rather than normal echogenicity.

Fig. 15 Accumulation of debris within the biliary system. A 28-day-old male with the tetralogy of Fallot: surgical intervention was performed 10 days previously. (A) Transverse sonogram demonstrates debris within the common hepatic duct (arrow). (B) Transverse sonogram demonstrates debris within the common bile duct (arrow).

Intestine

Gastrointestinal complications after cardiovascular surgery are associated with longer hospitalization periods.[67] These gastrointestinal complications include necrotizing enterocolitis, vocal cord paralysis, gastrointestinal bleeding, ileus, or enteritis.[1] [10] [67] [68] Necrotizing enterocolitis is reported to be the most common event.[67] [68] To prevent these complications, various enteral feeding programs are tested.[69] [70] [71]

Timing of Occurrence and Strategy for Diagnosis

Congenital heart disease is one of the risk factors for necrotizing enterocolitis. In addition, paradoxical hypertension may be occurred after repair of the coarctation of aorta.[72] The necrotizing enterocolitis occurs even before surgery or 1 day after surgery.[69] [70] [73] [74] The diagnosis of necrotizing enterocolitis is usually performed based on the radiograph according to Bell's staging criteria.[75] [76] [77] [78] The ultrasound provides the additional information to diagnose the necrotizing enterocolitis, therefore ultrasound is recommended as the next examination.[77] Paradoxical hypertension after repair of the coarctation of aorta was reported to be usually occurred 48 hours after operation. Clinical diagnosis could usually made based on the clinical sign.[72]

1. Necrotizing enterocolitis

Necrotizing enterocolitis more frequently occurs in pediatric patients with prematurity or those presenting with shock ([Figs. 16] and [17]).[68] Radiographic signs include a dilated intestine without peristalsis, intramural air, or portal venous gas.[69] Although radiography is a useful modality to evaluate these findings, ultrasound can more easily detect the portal venous gas and other findings such as the need for an urgent surgical intervention.[79] [80] [81]

Fig. 16 Necrotizing enterocolitis. A 20-day-old male with atrioventricular septal defect who underwent surgical intervention 1 week previously. (A) Radiograph shows the absence of free air and portal venous gas. Intestinal pneumatosis located transverse colon is suspected. (B) Ultrasound image shows hyperechoic foci in the liver parenchyma in left lobe due to accumulation of gas (arrows). (C) Hyperechoic foci (arrows) are seen moving from splenic vein to portal vein. (D) Hyperechoic foci (arrows) are observed in the middle and left colic vein, moving from the transverse and descending large colon. (E) Pneumatosis intestinalis was detected at transverse colon (arrows). Free air and echogenic ascites are not detected and pneumatosis intestinalis was confined to the large colon. Therefore, this case was diagnosed as benign type of pneumatosis intestinalis and surgical intervention was not needed.

Fig. 17 Necrotizing enterocolitis. A 12-day-old female with pulmonary atresia. Pulmonary artery banding was performed. (A) Radiograph shows massive portal venous gas (arrows). (B) Ultrasound image showing many hyperechoic foci in the liver parenchyma (arrows). (C) Hyperechoic foci are observed in the wall of the small intestine (arrowheads).

Sonographic Evaluation

It is important to evaluate the necessity of urgent surgical intervention in the presence of necrotizing enterocolitis. Presence or absence of intra-abdominal free air and echogenic ascites are important findings to recommend surgical intervention.[79] [80] [81] [82] [83] There are some reports that the cases with pneumatosis intestinalis confined to the colon had better prognosis than that extended to the small intestine, therefore evaluation for location of pneumatosis intestinalis could be useful.[79] [84] Portal venous gas, when detected, can be traced to its origin by following the hyperechoic foci in the portal vein along its branches with real-time ultrasound ([Fig. 16C] and [16D]; [Videos 3] [4] [5]; available in the online version).[81]

Video 3 Ultrasound image showing hyperechoic foci moving in the portal vein.

Video 4 Hyperechoic foci seen moving from the splenic vein to portal vein.

Video 5 Hyperechoic foci (arrows) seen in the inferior mesenteric vein, moving from the transverse and descending large colon. Free air and echogenic ascites are not detected and pneumatosis intestinalis is confined to the large colon. Therefore, this case was diagnosed as benign type of pneumatosis intestinalis and surgical intervention was not needed.

2. Paradoxical hypertension results in postcoarctectomy syndrome or mesenteric arteritis

The coarctation of aorta is a little different from other congenital heart diseases. First, intra-abdominal of coarctation might be associated with occurrence of intestinal ischemia.[85] Second, paradoxical hypertension might be occurred after surgical repair of coarctation of the aorta.[72] [86] [87] The etiology is unclear but there appears to be a direct relationship to the hypertension that is observed in the postoperative period in these cases.[72] [86] [87] This complication might be result in abdominal pain, mesenteric arteritis, or arterial aneurysm.[72] [87] [88] [89] [90] Recognition of this complication and early treatment for this hypertension by using antihypertensive drugs will shorten the duration of symptoms.[72] [88] [89] Angiographic findings of this complication showed arterial segmental constriction, dilatation, or aneurysm.[87] [91] Ultrasound or CT was reported to be able to show the arterial lumen; therefore, these findings may be detected by ultrasound or CT.[92] [93]

Kidney

Renal dysfunction, renal infectious disease, or drug-induced renal dysfunction may occur in pediatric patients after cardiovascular surgery.[1] Higher morbidity and mortality are associated with more severe acute kidney injuries, and this complication is also associated with a longer intensive care unit stay.[8] [94]

Timing of Occurrence and Strategy for Diagnosis

Onset of acute kidney injury is 1 to 27 days after operation.[94] In neonates, progression of acute kidney injury can occur within 48 hours after surgery[8]. However, acute kidney disease is diagnosed based on the clinical data such as serum creatine, not imaging modality, ultrasound might provide the information about presence or absence of urinary tract obstruction.[95] [96] [97] Doppler technique is useful to evaluate the resistivity index and it is important information about renal parenchymal damage and prediction of clinical outcomes.[97] [98] [99]

• Acute kidney injury: the sonographic findings for acute kidney injury are not specific but ultrasound may show enlargement or high echogenicity of the renal parenchyma ([Fig. 18]).[97] Doppler ultrasound may be useful to predict renal function.[8]

• Nephrocalcinosis: nephrocalcinosis may be caused by furosemide that is usually an important medication in intensive care units ([Fig. 19]). Foci with high echogenicity are easily detected by using ultrasound, and the presence or absence of hydronephrosis can be evaluated.[100]

• Urinary tract infection: urinary tract infection is one of the most frequent infectious foci in pediatric patients after cardiovascular surgery ([Figs. 20] and [21]).[1] [2] Ultrasound is reported to be useful in detecting the presence of hydronephrosis and to diagnose it as pyelonephritis or acute focal bacterial nephroma.[101]

Fig. 18 Acute kidney injury. A 16-day-old female with truncus arteriosus communis. Pulmonary banding. Echogenicity of the renal cortex is slightly high. In addition, Doppler ultrasound demonstrates reversed diastolic flow (arrow), as well as a highly resistant arterial flow.

Fig. 19 Nephrocalcinosis. A 28-day-old female with total anomalous pulmonary venous return who underwent surgical repair on the birthday. Diuretic treatment was continued. Nephrocalcinosis by renal ultrasound evidenced by increased pyramidal density (arrows) associated with acoustic shadowing.

Fig. 20 Urinary tract infection. A 21-day-old female with hypoplastic left heart syndrome that underwent pulmonary artery banding 2 days previously. (A) Ultrasound demonstrates a dilated proximal ureter with a thickened ureter wall (arrows). (B) Debris appears within the dilated distal ureter (arrow).

Fig. 21 Urinary tract infection. A 5-month-old male patient with atrioventricular septal defect who underwent surgical intervention 20 days previously. A transverse sonogram shows focal hyperechogenicity in the right kidney (arrows) with a focal loss of corticomedullary differentiation. Acute focal bacterial nephroma is present.

Vascular Complications Associated with Inserted Catheter and Drainage Tube Location

The risk of venous thrombotic events is higher in pediatric patients admitted to intensive care units.[102] The presence of a central venous catheter increases this risk.[102] Catheter-associated bloodstream infection is an important complication of care in children hospitalized with complex congenital heart disease.[103] In addition, phlebitis and osteomyelitis caused by thrombophlebitis have been reported.[104] Regardless of these potential complications, venous cannulation in intensive care units is usually unavoidable.

Timing of Occurrence and Strategy of Diagnosis

The timing of occurrence of thrombosis or phlebitis associated with catheter insertion is approximately 3 to 5 days after insertion.[105] [106] Physical examination is important to suspect thrombosis or phlebitis associated with catheter insertion.[107] In addition, ultrasound is a useful modality to evaluate these complications.[105] [106] If these complications are suspected to occur at intrathoracic vein or difficult location by using ultrasound, contrast-enhanced CT could be recommended.[108] Color Doppler is useful technique to detect the vessel and thrombosis.[105] [106] [109]

• Thrombosis (thrombophlebitis): venous thrombosis could be caused from an inserted catheter and patient conditions such as an underlying disease, or inadequate prophylaxis ([Figs. 22] and [23]).[102] [104] Pulmonary embolism or thrombophlebitis caused by venous thrombosis may be critical for pediatric patients.[110] [111] [112] Ultrasound is usually used to evaluate the presence of thrombosis and its complications.[109]

• Catheter migration: prevention of catheter migration is essential to avoid the complications associated with catheters ([Fig. 24]).[113] Ultrasound is a useful modality to guide cannulation and evaluate catheter migration.[113]

• Arrangement of the location of the drainage tube: ultrasound is useful to evaluate the location of the catheter or drainage tube ([Fig. 25]). The location may be changed based on the findings obtained in ultrasound evaluations.

• Endotracheal intubation: intubation-related issues are critical for pediatric patients in intensive care units. Repeated endotracheal intubation may be sometimes needed because of various underlying diseases ([Fig. 26]). Ultrasound has been reported to be useful for safe endotracheal intubation.[14] [114]

Fig. 22 Thrombophlebitis. A 1-month-old male who underwent balloon atrial septostomy. (A) Radiograph shows the PICC (arrows) is inserted in the left lower leg. (B) Oblique sonogram shows the intraluminal hyperechoic thrombus (arrows) within the left external iliac vein. Hyperechogenicity is present around the thrombus due to inflammation (arrowheads). PICC, peripheral inserted central catheter.

Fig. 23 Thrombosis. A 1-month-old male who underwent balloon atrial septostomy. (A) Intraluminal thrombus (arrow) is revealed within the internal carotid vein. (B) Thrombus (arrow) is located near the junction of the common carotid and innominate vein.

Fig. 24 Migration of catheter. A 15-day-old female who underwent pulmonary artery banding 2 weeks previously. (A) Chest radiograph shows the PICC inserted from the left upper arm (arrows). Presence or absence of migration cannot be judged from the radiograph. (B) Sagittal sonogram shows the catheter is located within the vessel (arrows). (C) Pulse-wave Doppler sonogram shows the vessel, and the catheter located within it, had arterial flow (arrow). PICC, peripheral inserted central catheter.

Fig. 25 Arrangement showing the location of the drainage tube. An 18-day-old male with pulmonary atresia. After pulmonary banding, necrotizing enterocolitis occurred and additional surgical intervention was needed. (A) The drainage tubes are located in the subphrenic space and pelvis. (B) There is no fluid collection around the drainage tube (arrows) located in the pelvis. Therefore, this tube was judged unnecessary. (C) Fluid collection (arrow) is detected in the left subphrenic space and it is not located around the drainage tube. The location of the drainage tube tip is arranged for drainage fluid collection.

Fig. 26 Endotracheal intubation. A 1-month-old female after surgical repair for congenital heart disease. (A) Before endotracheal intubation, normal trachea (arrow) and esophagus are observed. (B) Axial sonography after endotracheal intubation showed bilaminar hyperechoic appearance appearing into the trachea (arrow). In addition, the empty esophagus can be seen to the left of the trachea. Eso, esophagus.

Conclusion

Various complications may occur after cardiovascular surgery. Radiography and ultrasound are important modalities to evaluate and manage these complications.

Conflict of Interest

None declared.

Ethical Approval

This research was performed in accordance with the tenets of the Declaration of Helsinki. This review article was approved by the ethics committee of our institution, and informed consent was waived.

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Publication History

Received: 03 June 2020

Accepted: 24 June 2020

Article published online:
09 September 2020