Pediatric Microsurgery and Free-Tissue Transfer

Abstract

Advancements in microsurgery, along with increased microsurgical experience in pediatric patients, have made free-tissue transfer a reliable modality for pediatric bone and soft tissue reconstruction today. Free-tissue transfer is most commonly used in children for the coverage of large or complex defects resulting from traumatic, oncologic, or congenital etiologies. While flap success and complication rates between pediatric and adult populations are similar, special considerations must be taken into account within the pediatric population. In this article, we will describe common indications, technical nuances, and clinical considerations for the management of the pediatric free-tissue transfer patient.

Pediatric free-tissue transfer dates back to the 1970s when Harii and Ohmori published successful outcomes using free groin flaps in two pediatric patients for lower extremity defect repairs. ¹ A minimum anastomotic diameter of 0.7 mm was initially established by Gilbert as the smallest vessel size safe for microvascular anastomosis. ² This lower limit, along with a concern for vessel size mismatch and a proposed tendency for vasospasm, led to hesitancy of free-tissue transfer for pediatric patients. ² However, successful outcomes for free-tissue transfer in children in vessels as small as 0.3 mm led to the acknowledgment that success rates were not necessarily tied to anastomotic size but rather surgical skill and experience. ^{2 3 4 5 6}

Despite initial concerns and increased technical challenges, pediatric free flap success and complication rates are comparable to those seen in adult free-tissue transfer. ^{4 7 8 9 10 11 12 13 14 15 16} The literature reports a high survival rate of 88 to 100% for free flaps in pediatric reconstruction ( Table 1 ). ^{17 18} Advancements in microsurgery and supermicrosurgery, alongside greater microsurgical experience with pediatric patients, have made free-tissue transfer a reliable modality for pediatric bone and soft tissue reconstruction today. ¹⁹ Free-tissue transfer is most commonly employed in pediatrics for the reconstruction of large or complex defects that are a result of trauma, oncologic, or congenital etiologies ( Table 2 ). ²⁰

Table 1. Pediatric free-tissue transfer success and complication rate.

	Year	Flaps	Recipient site	Avg. age (years)	Flap success rate (%)	Complication rate (%)
Parry et al 60	1988	N  = 22	UE—7 LE—15	9.6	96	9
Canales et al 4	1991	N  = 106	UE—45 LE—36 H&N—25	9	88	43
Devaraj et al 5	1991	N  = 43	–	5.4	93	7
Serletti et al 23	1996	N  = 20	UE—2 LE—16 H&N—2	10	100	20
Rinker et al 38	2005	N  = 28	LE—28	13 (median)	88	62
Upton and Guo 7	2008	N  = 433	UE—141 LE—108 H&N—165 Trunk—19	0.3–16 (range)	99.8	9
Aboelatta and Aly 6	2013	N  = 28	UE—7 LE—16 H&N—4 Trunk—1	8.8	89	32
Alkureishi et al 16	2018	N  = 48	UE—6 LE—15 H&N—17 Trunk—4	8.4	94	40
Liu et al 15	2019	N  = 135	H&N—135	14.6	95.6	7

Abbreviations: H&N, head and neck; LE, lower extremity UE, upper extremity.

Table 2. Etiology of defects in pediatric free-tissue transfer.

	Year	Flaps	Congenital (%)	Trauma (%)	Oncologic (%)
Parry et al 60	1988	N  = 22	–	–	–
Canales et al 4	1991	N  = 106	23	55	22
Devaraj et al 5	1991	N  = 43	32.2	51.1	16.7
Serletti et al 23	1996	N  = 20	5	65	25
Rinker et al 38	2005	N  = 28	0	100	0
Upton and Guo 7	2008	N  = 433	–	–	–
Aboelatta and Aly 6	2013	N  = 28	10.7	85.7	3.6
Alkureishi et al 16	2018	N  = 48	79	14	7
Liu et al 15	2019	N  = 135	6.9	7.7	85.4

While flap success and complication rates between pediatric and adult populations are similar, special considerations must be taken into account during pediatric free-tissue transfer. These considerations include future growth of both the donor and recipient site, psychosocial burden, anesthetic exposure, and postoperative compliance. ^{4 7 15 16 19} Herein, we describe indications for pediatric microsurgical intervention, technical aspects of microsurgery in this subpopulation, and the nuances in perioperative management of the pediatric free-tissue transfer patient.

Indications for Pediatric Microsurgery

Congenital Reconstruction

For severe congenital anomalies, microsurgical free-tissue transfers are effective options for restoring both aesthetic appearance and functional outcomes. Common congenital anomalies that are treated with free-tissue transfer include Mobius syndrome, Parry–Romberg syndrome, congenital hand malformations, and vascular malformations, among others.

Mobius syndrome includes bilateral absence of the facial nerve resulting in facial paralysis, with treatment strategies focusing on the enhancement of dynamic facial movement and expression. ^{21 22} Previously, the temporalis muscle and other static measures were employed for addressing bilateral facial paralysis. ²¹ In 2009, Coombs et al pioneered an approach that involves the use of the local masseteric nerve for innervation of a free gracilis muscle to restore a functional, voluntary smile, and is still used today. ^{22 23 24} Cross-facial nerve grafting may also be implemented prior to free gracilis muscle transfer in the setting of trauma or oncologic resection when an intact unilateral facial nerve remains. ²⁵

Parry–Romberg syndrome involves progressive, unilateral atrophy of the hard and soft tissues of the face. As Parry–Romberg only affects one side, it can create significant asymmetry and disfiguration. In cases of severe deformity with large-volume defects, fasciocutaneous flaps (i.e., anterolateral thigh, scapular flap) can be used to augment the atrophied soft tissues of the face and restore symmetry. ^{26 27} The fasciocutaneous flap is contoured to the underlying defect and secured by the fascia so that migration due to gravity is minimal. ^{26 28}

Congenital hand malformations requiring free-tissue transfer include conditions such as constriction ring syndrome with loss of fingers and cleft hand. Radial longitudinal deficiency (RLD), commonly referred to as radial clubhand, is characterized by radial bowing and thumb hypoplasia, and microsurgical intervention may be helpful in its most severe presentation. ²⁹ Vilkki et al have used the second toe with the metatarsophalangeal joint to reconstruct support on the absent radius side of the wrist with some success. ^{30 31} Free fibula transfer with the vascularized physis may offer a treatment option for severe RLD, as it has the potential for continued long bone growth and therefore longevity of results. ^{29 32}

Vascular malformations, including arteriovenous malformations (AVM), may manifest anywhere in the body and are most often encountered in the head, neck, and extremities. ^{33 34 35} AVMs may require radical extirpation necessitating free-tissue transfers for adequate soft tissue defect coverage. ^{34 36}

Trauma and Oncologic Reconstruction

Pediatric trauma and oncologic reconstruction aim to restore form and function, with continued growth of the transferred tissue throughout the course of the child's life ( Figs. 1 and 2A , B ). Pediatric trauma cases which most often require the use of free-tissue transfer include wounds from all-terrain vehicle accidents to gunshots ( Figs. 3 and 4 ). ^{37 38 39} The overall incidence of lower extremity Gustilo type III trauma is less common in the pediatric population compared to the adult population, given relative bony pliability and height in relation to trauma. ⁴⁰ It is particularly rare in the upper and middle 1/3 of the lower extremity, though foot and ankle injury requiring microsurgical reconstruction is relatively common. ^{38 40}

Fig. 1.

View of 5-year-old male's scalp after total avulsion in dog attack; scalp was not available for replantation.

Fig. 2.

( A ) View of “chimeric” subscapular axis flap with parascapular skin flap, latissimus dorsi muscle flap, and serratus anterior flap all on a single pedicle for coverage. ( B ) View after anastomosis to the left temporal vessels with only partial scalp coverage.

Fig. 3.

View of latissimus dorsi muscle and serratus anterior muscle flap on single pedicle from the right side of the chest to cover remaining skull.

Fig. 4.

Posterior view of reconstruction 6 months postoperatively.

The most predominant malignancies requiring free-tissue transfer in a child are osteosarcomas, which can occur in the head and neck region, lower extremities, and humerus. ^{17 41} Resection and reconstruction may need to be conducted in a staged fashion to ensure clear margins but should be accomplished sooner rather than later. The vascularized free fibula can be harvested with its intact physis, preserving growth potential in its new heterotopic location, which is important for patients who have epiphyseal damage to an extremity long bone due to oncologic involvement. ^{42 43} Postoperative fibular growth with a physis transfer has been sited at 78 to 96% of normal with 0.54 to 1.72 cm of longitudinal growth per year in pediatric extremity reconstruction patients. ^{43 44 45 46} Besides immediate reconstruction following tumor extirpation, free-tissue transfer may be performed later in life for growth-related deficiencies or long-term effects of radiation in the oncologic pediatric population.

Preoperative Considerations

Flap Selection

The literature reports a high survival rate of 95.2 to 98% for free flaps in pediatric reconstruction with several studies citing complication rates of less than 15% and a re-exploration rate of less than 7%. ^{17 18 46 47} Even in oncologic cases, 95% success rates are reported despite neoadjuvant therapies such as chemotherapy and radiation. ¹⁸ Some studies even report higher success in pediatric cohorts compared to the adult patients operated on by the same surgeon. ¹⁴ This is likely accounted for by lack of comorbidity, virgin anatomical planes, and overall higher functional reserve in a younger population.

In theory, most flaps described and utilized in an adult patient may also be harvested in a pediatric population. There are, however, some nuances that may make one flap better than the other. An ideal flap choice in this population would be one with optimal pedicle size and length, limited donor site morbidity, and growth capacity with the child. The most used soft tissue flaps in children are the latissimus dorsi and anterolateral thigh flap for large defects, the free gracilis for innervated muscle transfer, and the anterolateral thigh flap for head and neck ( Fig. 5 ). ^{38 46 48} Disadvantages for the use of fasciocutaneous flaps includes the possibility of aesthetic deformity, as these flaps retain their native ability to gain fatty tissue with patient weight gain, as seen in anterolateral thigh flaps. ¹⁹ In all flaps, incisions should be carefully planned to limit prominent scars, and radial forearm flaps should be avoided in this pediatric population if feasible to prevent visible donor site deformity.

Fig. 5.

Child with Moebius syndrome and bilateral facial palsy. View of gracilis muscle on face prior to insetting and anastomoses of vessels and nerve to masseter.

Larger bony defects may require microvascular bone transfer, which in children some flaps may be transferred with the vascularized physis for continued bone growth such as in toe transfers and free fibulas. ^{7 15 49} Microvascular bone flaps can be taken with or without a cutaneous component for soft tissue coverage and can be used for defects involving soft tissue and bone loss. ^{13 15} Vascularized fibula transfer has been successfully used for upper extremity (humerus, radius, ulna), lower extremity (femur, tibia), trunk (spine, pelvis), and craniofacial (maxilla, mandible) bony defects in children. ^{50 51 52 53}

Anesthesia

Since its application in surgical practice, general anesthesia has been a remarkable achievement in modern medicine, enabling immobilization and pain control during operations with seemingly safe implications. Nevertheless, recent evidence from studies involving nonhuman primates has established a link between commonly used anesthetic agents and brain neurotoxicity. ^{54 55} Furthermore, observational studies have indicated a potential correlation between early exposure to anesthesia and subsequent neurocognitive deficits later in life. ^{56 57 58} The U.S. Food and Drug Administration (FDA) convened to address concerns regarding neurological sequelae from anesthetic agent exposure. ⁵⁹ While immediate modification of current pediatric anesthesia practices was deemed unnecessary due to insufficient data, the FDA recommended avoiding elective procedures in children under 3 years and reducing overall exposure time. ⁵⁹

Pediatric free-tissue transfer is an intricate procedure that demands substantial time investment ranging from 6 to 8 hours, which surpasses the recommendations of the FDA. ^{60 61 62} However, we must take into account the opportunity to avoid future operations which may be necessary in other forms of reconstruction, such as skin grafting. Nonetheless, proactive measures should be implemented to optimize efficiency and lower overall operative time. ⁶³ Interdisciplinary communication and preoperative planning can optimize surgical efficiency and minimize exposure time to anesthetic agents. A two-team approach can help to decrease overall operative times.

Technical Considerations

Vessels

In a child, the pedicle has a larger size to flap volume ratio than found in an adult. Further, lack of vascular disease and comorbidity may lead to a more favorable outcome. On the contrary, overall small vessel size leads to a more technically challenging operation. Successful free-tissue transfers have been reported with anastomoses as small as 0.3 mm; however, those under 0.5 mm are generally cautioned against. ³ Aboelatta and Aly point out in their large review that patients under the age of 5 years had a greater risk for flap failure likely as a result of smaller vessel size, likely reflective of the increased technical challenge seen with smaller vessels. ⁶

The tendency for vasospasm in pediatric vessels has been widely debated and remains a point of contention within pediatric microsurgery, with evidence both for and against. ^{19 40 64} Parry et al speculated that the underdeveloped muscularis layer in the vessels of children might be responsible for a less likely vasospasm. ⁶⁰ Additionally, pediatric vessels have the microsurgical advantage of relatively undisturbed intima compared to their adult counterparts, who often present with comorbidities such as diabetes, atherosclerosis, smoking, and resultant vascular disease. ⁷ Nonetheless, topical antispasmodic agents and technical finesse should be implemented to prevent spasm during pediatric microsurgery. ^{5 7 19} Most authors recommend microsurgical anastomosis of vessels with 9-0 or 10-0 nylon in an interrupted fashion for both the artery and the vein. ¹⁹ Though surgeons should implement the technique they feel most comfortable, a study evaluating outcomes in pediatric microsurgery revealed increased complications when running suture or couplers were implemented. ¹⁸

The use of anticoagulation in pediatric microsurgery is also debated. Few authors recommend routine postoperative anticoagulation, but rather limit use for specific patients, such as those undergoing redo operations, with intraoperative evidence of thrombus noted, or in an irradiated field. ^{6 15 16 23 65} Commonly implemented agents include heparin, low molecular weight heparin, and aspirin.

Growth

Perhaps one of the greatest questions surrounding that of pediatric microsurgery is that of growth. Will there be a restriction in growth for the donor site? Recipient site? Anastomosis?

Regarding the donor site, there has been no evidence to date that supports a postoperative functional deficit, with many studies reporting outcomes from long-term follow-up from 49 months to 14.9 years. ^{6 66} Additionally, the Pediatric Outcomes Data Collection Instrument, a patient-reported outcome measure on patient perception of their surgery, satisfaction, residual pain, dysesthesia, and disfigurement, found no excessive morbidity noted at the donor site, with all parents reporting that they would have their child undergo the same operation again. ^{16 66}

Similarly, large studies have failed to show any growth restriction at the recipient site for free-tissue transfer. ^{15 16 17 60} Radiation may, however, result in asymmetry at the recipient site. Transfer of muscle flaps without restoration of innervation will result in atrophy of the muscle. ^{7 38} These flaps will, however, continue to grow in accordance with skeletal growth without contraction. ⁷ Nonetheless, caution should be taken when transferring deinnervated muscle to areas of rapid growth. Free bony transfer can be conducted with or without the growth plate. It has historically been thought that no growth will occur in the maxilla or mandible when growth centers (physis) are not included. ^{51 52} However, the senior author at our institution has documented several cases of postoperative growth in patients who did not receive physis transfer, likely due to inadvertent distraction from growth of the contralateral, normal mandible. ^{67 68} The vascularized fibula epiphyseal flap was first used in 1998 for proximal humeral reconstruction. ⁶⁹ It is supplied by the recurrent epiphyseal branch from the anterior tibial artery and musculopereosteal perforators. The vascularized fibula epiphyseal flap can result in adequate growth in many cases of the upper extremity ( Figs. 6 7 8 9 ). ⁶⁹ However, risk of transient or permeant peroneal nerve palsy is common, and fracture of the reconstructed extremity may occur, especially in the early postoperative period. ⁵¹

Fig. 6.

7-year-old female with osteosarcoma of proximal humerus.

Fig. 7.

Fibula harvested with proximal physis, note peroneal nerve branches over fibular neck, and distal anterior tibial vessels coming off the fibula for anastomosis.

Fig. 8.

Radiograph at 5 months.

Fig. 9.

Radiograph at 2 years.

The question also exists as to the growth potential of the anastomotic site and whether inflow may become restricted over time. A rat study by Chen et al established that the circumferential anastomosis continued to grow proportionately 6 months postoperatively, without restriction in flow. ⁷⁰ Though no studies evaluate longer follow-up than 6 months, it is likely that an inflow issue beyond this time point would be less concerning in the setting of the flap's innate ability to revascularize through collateral flow. ⁷⁰

Postoperative Considerations

General Considerations

As stated by Upton et al, four factors produce vasoconstriction and are thus enemies of the microsurgeon: fear, cold, pain, and dehydration. ^{7 65} These general considerations found in the adult population should also be recognized in a pediatric population, with some additions. ^{71 72 73}

Pediatric patients should be admitted to the pediatric intensive care unit (PICU) in the immediate postoperative period for close flap monitoring. ^{14 47 74} A subpopulation of patients may benefit from continued intubation and paralysis in the immediate postoperative period in instances such as difficult anatomical locations, that is, head and neck, or behavioral issues. Efforts should be made in the preoperative period to elicit behavioral issues that may compromise later flap success. ^{71 74} Blood pressure should be maintained, and the use of inotropes should be limited. ^{6 40} Volume status should be maintained with intravenous fluids at 1 to 1.5x the patient's calculated maintenance infusion rate in order to optimize flap perfusion in the immediate postoperative PICU stay. ⁷⁵ At our institution, postoperative transfusion is pursued in patients with a hematocrit less than 27%, as levels below this lead to poor oxygen perfusion. ^{73 76} Caution should be used in overtransfusion as higher hematocrit levels lead to thicker viscosity, and therefore higher risk of thrombosis.

Additional environmental factors that contribute to vasospasm such as excessive stimulation, pain, and room temperature should be minimized as much as possible. ^{6 8 65} Extremity nerve blocks and epidural anesthesia for indicated patients are useful options for both the donor and recipient sites. ^{18 66}

Flap Monitoring

Standard protocol at the author's institution includes hourly flap checks for the first 24 hours and every 4 hours thereafter until discharge. Historically, the gold standard for flap monitoring is a clinical assessment at the bedside for flap color, skin turgor, surface temperature, capillary refill, and handheld Doppler signal. ^{75 77 78} Today, flap monitoring has evolved with the advent of implantable dopplers, such as the Cook–Swartz catheter. This, however, may only be utilized in vessels greater than 2 mm, as vessels smaller than this are at risk of anastomotic disruption with Doppler probe motion and removal. ^{78 79 80} Further, the risk of accidental wire pulling in the postoperative period must be taken into account in a younger, less compliant population.

Sedation and Intubation

Management of the airway following head and neck reconstruction is challenging. ^{46 75} Cameron et al developed a scoring system for the need for tracheostomy following oropharyngeal tumor resection. ⁸¹ Patients who undergo bilateral neck dissection, mandibulectomy, and free-tissue transfer score the highest and require tracheostomy. ^{75 81} In our experience, most head and neck free flap patients have tracheostomy placement at the time of tumor resection/reconstruction in order to preserve the upper airway postoperatively. The tracheostomy tube should be sutured in place to avoid mechanical compression in the neck, which may cause kinking or tension on the pedicle. ^{81 82} Extubation is determined by the PICU team and ENT, and in our experience, patients are typically extubated on postoperative day 2 or 3, as swelling subsides.

Elevation/Immobilization

Postoperative elevation of the flap in the immediate postoperative period is important for limiting swelling and venous congestion. ^{7 40} For head and neck reconstruction patients, the patient's head should be maintained in a neutral position, with the head of the bed elevated to 45 degrees in order to minimize swelling. ^{15 75} Extremity flaps should be elevated to at least 45 degrees and can be elevated even higher if tolerated by the patient. ^{38 40 83} Plaster splinting with a monitoring window is a useful adjunct to aid in postoperative immobilization and elevation, especially in lower extremity free flaps. ^{40 83}

Anticoagulation

The use of postoperative anticoagulation in pediatric free-tissue transfer patients remains a controversial topic in microsurgery. ^{3 4 6} At our institution, therapeutic anticoagulation is not routinely necessary in uncomplicated pediatric free-tissue transfer patients. Patients who acquire a venous thrombosis or require venous anastomotic revision are treated with low molecular weight heparin at a pediatric dose of 150 IU/kg/d. All patients, however, are prescribed an antiplatelet in the form of 81 mg of acetylsalicylic acid taken daily for 2 weeks postoperatively.

Conclusion

In summary, the field of pediatric microsurgery has undergone significant progress in free-tissue transfer techniques since its inception in the 1970s. These advancements have paved the way for pediatric microsurgical reconstruction to be successfully employed in congenital, traumatic, and oncologic defects. Microvascular free-tissue transfers have proven highly effective in addressing these defects without apparent effect on either donor or recipient growth.

Funding Statement

Funding None