Ultrasound in pediatric surgery; intraoperative applications of the growing technology

Ultrasonography is increasingly used in pediatric surgery. Intraoperatively, ultrasonography can be used to confirm the preoperative diagnosis, guide the surgical approach, and enhance decision-making. We aimed to report our experience with intraoperative ultrasonography in different neonatal and pediatric procedures. So, a retrospective study was designed. It included all pediatric patients who had intraoperative ultrasound between January 2018 and October 2020 in a single center. We used intraoperative ultrasonography in 208 pediatric patients for various types of surgery. The authors compared ultrasound-guided central line insertion (n = 139) to the landmark method (n = 153). The number of trials was significantly lower in the ultrasound-guided method (P < 0.001). Conversion to cut-down was significantly lower with the ultrasound-guided technique (4 (2.8%) vs. 13 (8.5%); P = 0.047) and insertion-related complications were lower with ultrasound (0 vs 13 (8.5%); P < 0.001). We used ultrasound-guided sclerotherapy for cystic hygroma in 15 patients. Nine patients had successful treatment with a single injection (60%). The application of intraoperative ultrasound in pediatric patients is increasing in our institution. The technique is safe and could effectively reduce central line insertion complications and enhance cystic hygroma sclerotherapy’s success with a single injection. Ultrasonography should be an essential part of residents’ and fellows’ training in pediatric surgery.


Background
The use of intraoperative ultrasonography (IOUS) in pediatric surgery is growing. There are several benefits of ultrasonography in this field, yet its incorporation into daily practice is slow [1]. Ultrasonography produces realtime imaging in different clinical settings, including bedsides, outpatient clinics, and operating rooms.
It is essential to understand the basics of ultrasonographic physics for proper image interpretation and diagnosis. The ultrasound's transducer emits and receives sound waves [2]. The most frequently used ultrasonographic mode is the two-dimensional B-mode. The images produced by this mode are black and white and can be modified by changing the probe's shape and size and the waves' frequencies [3].
Sound waves are reflected more from the solid medial because of their dense particles [4]. Solid tissues are echogenic (white), and fibrous tissues appear white with shadows, and bones appear white without shadows. Fluids are anechoic (black), and soft tissues appear gray [5]. Air reflects sound waves and appears hyperechoic with while lines that prevent visualization of deeper structures [6]. These white lines are the reverberation artifacts, and they are very useful for the diagnosis of intraperitoneal free air.
Intraoperatively, ultrasonography can be used to confirm the preoperative diagnosis, guide the surgical approach, and enhance decision-making. Several ultrasound-guided methods have been adopted, such as hepatic lesion mapping during resection. Ultrasonography has proven safety, and proper ultrasound use in the operating room could reduce the intervention time and improve patient outcomes. This technology has changed the operative management of central venous catheter insertion by reducing the complication rate and the total number of cannulation trials [7].
The use of ultrasonography has been expanded to include trauma, endocrine, breast, and vascular surgery [8]. In pediatric surgery, ultrasonography can be used to diagnose pyloric stenosis and acute appendicitis and in several interventions such as central line [9,10] and port-a-cath insertion [11].
The increasing role of ultrasound in pediatric surgery motivated us to perform this study to evaluate the role of intraoperative ultrasonography and report our experience with it in different procedures for children and neonates.

Design and patients
This retrospective study included 208 pediatric patients who had intraoperative ultrasound between January 2018 and October 2020 in a single center. The Institutional Review Board approved the study, and the need for the patients' consent to participate in the research was waived.

Data collected
We highlighted some of the procedures in which intraoperative ultrasonography was used.
We extracted the data required for this study from the electronic and paper charts. The obtained data included age, the indication of the procedure, and the operative times. Study endpoints were the success of using the ultrasound-guided approach, conversion to open approach, and postoperative complications.

Ultrasonography techniques
We used probes with different frequencies depending on the target tissues. Tissue penetration is higher with lowfrequency probes, while the penetration is lower with high-frequency probes, but they have better resolution. Therefore, we used low-frequency probes (2)(3)(4)(5) to evaluate the deep structures and in obese patients and high-frequency probes (6-13 MHz) for superficial structures.
We washed the scan head with alcohol before use and placed sterile gel into a long sterile plastic sleeve. We introduced the transducer wire over this plastic sleeve and secured it with rubber bands povidone-iodine or sterile gel is used as the coupling agent.

Statistical analysis
We described the continuous data as mean and standard deviation and categorical data as number and percent. Continuous data were compared using the t test and categorical data with the Chi-square or Fisher exact test when appropriate. SPSS version 26 (IBM Corp., Armonk, NY, USA) was used to perform the descriptive statistics.

Ultrasound and cystic hygroma
We used ultrasound-guided sclerotherapy for cystic hygroma in 15 patients. The most common site was the neck. Nine patients had successful treatment (complete resolution) with a single injection (60%) ( Table 1).

Ultrasound-guided central line insertion
Ultrasound-guided central line insertion was performed in 139 patients (Fig. 1). We compared these patients to 153 patients who had line insertion through the landmark method. There were no differences in the baseline data between both approaches. The number of trials was significantly lower in the ultrasound-guided method ( Table 2). Conversion to cut-down was significantly lower with the ultrasound-guided technique (4 (2.8%) vs. 13 (8.5%); P = 0.047) and insertion-related complications were lower with ultrasound (0 vs 13 (8.5%); P < 0.001). There were no differences in other complications, including bleeding, pneumothorax, arterial injury, and infection between groups (Table 3).

Discussion
Improving the surgical vision and enhancing the diagnosis will improve the surgical outcomes. Ultrasonography is a widespread technique with proven safety that is already in use in several medical specialties. This technique's application has expanded to include intraoperative use in thyroid surgery [12], hepatobiliary surgery [13], and neurosurgery [14].
The technique was introduced to pediatric surgery and became of utmost importance in several procedures. Intraoperative ultrasonography can be used during liver tumor resection. It effectively shows the surrounding vessels and tumor margins, and depth. Its imaging accuracy was comparable to the preoperative computed tomography scan. Additionally, intraoperative ultrasonography provides real-time feedback during surgery, and it can be repeated several times to provide continuous feedback to the surgeon. This application's potential benefits are reducing bleeding, operative time, and performing complete surgical resection. In a previous study, intraoperative ultrasonography in pediatric surgery decreased the rate of positive surgical margins [15].
Another application of ultrasonography in pediatric surgery is central line insertion. Traditionally, the central line is inserted through the landmark method. This method may increase the number of trials before successful insertion and the insertion-related complications [16]. Like other studies, we reported fewer puncture trials in the ultrasound-guided method and lower insertion-related complications, such as neck hematoma and carotid artery puncture [7]. The efficacy and safety of ultrasound-guided vascular puncture have been demonstrated in several studies [17]. Ultrasound-guided insertion demonstrated a higher success rate than the landmark method in a multicenter study [18]. The main barrier to the generalization of ultrasound-guided  [19].
Although several studies have demonstrated the potential advantage of ultrasound use in pediatrics, several limitations exist. Several centers around the globe had initiated ultrasonography training programs for pediatric surgery residents and fellows. These training programs did not replace the conventional radiological methods with ultrasonography but used them to enhance each other's success.
Ultrasonography needs a learning experience and repeated use to improve the learning curve. Additionally, probes suitable for neonates and infants are not widely available. Currently, small and portable ultrasonography devices with high resolution are available for use in pediatric patients. These small machines were incorporated into pediatric patients' daily care, and some centers reported an improvement of the surgical outcomes with this technology [20].
Another drawback of ultrasonographic use in pediatric surgery is the medicolegal aspect. Pediatric surgeons are not well-trained to perform a comprehensive radiological assessment as the trained radiologists. However, ultrasonography is used as an adjunct to the physical examination, and radiological consultation is always available for complex cases. Additionally, the training can be enhanced with hands-on experience on simulators and manikins. The training programs should familiarize the fellow with the components of ultrasound machines and include an introduction to ultrasound physics in the curriculum. The training experience can be enhanced by comparing the preoperative CT images to the intraoperative ultrasound images.
Ultrasonography is not a screening tool only; it has proven interventional and therapeutic benefits [21]. The use of ultrasonography during surgical interventions decreases the procedure's invasiveness, time, and complications [3]. The use of ultrasound may decrease the need for further diagnostic work-up. Real-time imaging provided intraoperatively may lead to early detection and prevention of several complications. The transition to this technology requires a national initiative that makes ultrasound machines readily available for all pediatric surgeons, moreover, incorporates a formal ultrasound training curriculum in many surgical residencies [22]. The technology is cost-effective compared to other imaging modalities such as intraoperative MRI. Therefore, intraoperative ultrasound is the optimal imaging tool that should be adopted worldwide [23].

Study limitations
The study has several limitations, including the retrospective nature of the study and the limited number of most of the applications other than central venous catheter (CVC) insertion and the cystic hygroma.

Conclusion
The application of intraoperative ultrasound in pediatric patients is increasing in our institution. The technique is safe and could effectively reduce central line insertion complications and enhance cystic hygroma sclerotherapy's success with a single injection. Ultrasonography should be an essential part of residents' and fellows' training in pediatric surgery. Authors' contributions OB and OAB made the study design. OAB did extensive literature review, analyzed, and interpreted the patient data regarding the intraoperative ultrasound for children. OAB and OB performed the data collection and was a major contributor in writing the manuscript. OAB and OB did the final revision and correction of the manuscript. Both authors contributed to the conception or design of the work and/or the acquisition, analysis, and interpretation of data. Drafts were revised critically for important intellectual content and the final version approved by all. Both agree to be accountable