Interpolated Paramedian Forehead Flaps

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Interpolated Paramedian Forehead Flaps

Introduction

Median forehead flaps were first described in an Indian medical treatise, the Sushruta Samita, in approximately 700 BC.13 The operation was performed by members of a caste of potters known as the Koomas. The need for this operation arose from the common Indian practice of amputating the tip of the nose as punishment for a variety of crimes ranging from robbery to adultery.4,5 The first reported use of the median forehead flap outside of India was by Antonio Branca of Italy. Based on an Arabic translation of the Sushruta Samita, Branca performed a nasal reconstruction using the midforehead flap in the 15th century.6,7 In the 16th and early 17th centuries, little advancement was made in the use of the median forehead flap because plastic and reconstructive surgery fell into disrepute.4,5,7 The flap had a revival in 1794, when J. C. Carpue read an editorial in the Gentleman’s Gazette of London describing the flap’s use for nasal reconstruction.810 Initially, Carpue practiced the median forehead flap operation on cadavers. Twenty years passed before he performed the operation on two patients. He reported his successful results in a monograph entitled “An Account of Two Successful Operations for Restoring a Lost Nose from the Integuments of the Forehead.” His article was widely circulated throughout Europe and served to popularize the operation.6,9 In the 1830s, Ernst Blausius (Chief of Ophthalmologic Surgery of Berlin), Johann Friedrich Dieffenbach (Chief of Surgery at Munich Hospital), and Natale Petrali of Milan simultaneously reported on uses and variations of the median forehead flap for reconstruction of the face and nose. On the basis of their influence as respected surgeons at large European teaching hospitals, the use and popularity of the forehead flap grew.6 In the late 1830s, use of the median forehead flap for nasal and facial reconstruction crossed the Atlantic when J. M. Warren performed the operation in the United States.4,11

By the early 1900s, the forehead flap was used to reconstruct losses of the nose secondary to battle, scrofula, syphilis, and cancer. Many American surgeons, such as Pancoast, Mutter, Buck, Davis, and Fomon, wrote about the use of the forehead flap in nasal reconstruction. Little modification of flap design, use, harvest, or donor site closure occurred until articles authored by Kazanjian appeared in the plastic surgery literature of the 1930s. This pioneer plastic surgeon was the first to determine that the primary blood supply of the flap is from the supratrochlear and supraorbital arteries. Kazanjian described a forehead flap designed precisely in the midline, allowing primary closure of the donor site. This technical modification minimized the forehead donor scar, which up to that point represented the major morbidity of the operation. Before Kazanjian’s modification, the donor site of the forehead flap had either been skin grafted or left open to heal secondarily by granulation and wound contraction. This practice commonly left the patient more scarred and disfigured than before the reconstructive surgery.12

Kazanjian carried incisions from the hairline to a point immediately above the level of the nasofrontal angle. By his time, surgeons had recognized that the use of unlined forehead flaps to repair full-thickness nasal defects predictably resulted in contraction of the flap and compromise of the nasal passage. The contour of the external nose also deformed as the airway constricted from progressive contracture of scar developing on the undersurface of the flap. In response to this, surgeons developed a number of modifications in the design of the forehead flap to achieve additional length so the flap could be folded on itself for internal lining. These designs included oblique and horizontally oriented flaps. Gillies13 described a U-shaped flap with an ascending and descending component that he called the up-and-down flap. The ascending portion of the flap was positioned over the axis of the supraorbital artery on one side and the descending portion over the contralateral supraorbital artery. Converse14 harvested lateral forehead skin based on a long pedicle of hair-bearing scalp, which became known as the scalping flap. The designs by Gillies and Converse circumvented the need to include hair-bearing scalp to provide additional length so that the flap could be folded on itself. Unfortunately, these modifications of the original design of the median forehead flap left marked deformities of the forehead. It also became apparent that folding the flap on itself created a great deal of tissue bulk that caused the nose to collapse. In addition, partial necrosis of the portion turned internally was common.

In the 1960s, Millard11,15 designed a large modified median forehead flap called the seagull flap, in which lateral extensions were used to cover the nasal alae. Incisions for the pedicle of the flap extended below the bony orbital rim to gain additional flap length. Millard also described methods of donor site repair and techniques for constructing nasal support, all of which improved the outcome of nasal reconstruction.

Labat7,16 was the first surgeon to design a median forehead flap with the base centered over a unilateral supratrochlear artery. He curved the incisions of the proximal pedicle so the base of the flap rested immediately above the medial brow and canthus on one side. This reduced the standing cutaneous deformity resulting from pivoting of the flap and increased the effective length, making more tissue available for reconstruction. Millard shifted the entire vertical axis of the central forehead flap to a paramedian position, demonstrating that the flap could survive without including the central glabellar skin in the pedicle.7 Menick modified Millard’s design of the paramedian flap by making the pedicle narrower.7 This offered a greater freedom of tissue movement, a smaller standing cutaneous deformity, and a longer effective length to the flap.

In the 1980s, Burget and Menick1719 found that extending incisions for the pedicle of the paramedian flap below the bony orbital rim provided additional flap length. This often avoided the need to extend the flap to hair-bearing scalp for sufficient length to reach the nasal tip. They noted that the end arterioles of the supratrochlear artery are located immediately under the dermis, superficial to the frontalis muscle. The authors determined that the frontalis muscle could be safely removed from the distal flap without impairing the vascularity of the skin.1

Studies by Mangold, McCarthy, and Shumrick better defined the vascular anatomy of the forehead. In 1980, Mangold et al20 demonstrated that the blood supply to forehead skin is from the dorsal nasal (a terminal branch of the angular artery), supratrochlear, supraorbital, and superficial temporal arteries. Each of these vessels provides a primary blood supply to a particular region of the forehead, but all demonstrate numerous interconnecting anastomoses. Mangold’s injection studies and dissections of cadavers showed that the forehead could be divided into regions based on their predominant vascular supply (Fig. 13-1). On the basis of these vascular regions, Mangold determined that median and paramedian vertically oriented forehead flaps are nourished primarily by the supratrochlear artery and secondarily by the dorsal nasal and supraorbital arteries. McCarthy and others21,22 confirmed Mangold’s work in clinical experiences with patients. McCarthy injected the facial artery after ligation of the supraorbital and supratrochlear arteries and showed sufficient filling of the forehead vasculature to supply vertically oriented flaps in the region of the central forehead.21 This suggested that a paramedian forehead flap could survive even when the supratrochlear artery on the side of the flap is not present.

In 1992, Shumrick and Smith10 performed detailed anatomic studies of the forehead using techniques of latex injection, radiography, and microdissection to determine the precise vascular anatomy of the central forehead. Examination of the radiographic data confirmed a clinically apparent fact: the forehead region contains an intricate system of anastomosing vessels among the angular, supratrochlear, supraorbital, and superficial temporal arteries (Fig. 13-2). The paired supratrochlear arteries connected with each other by several horizontal unnamed arteries that cross the midline. Moreover, the supratrochlear arteries consistently demonstrated anastomotic branches with the angular and supraorbital arteries in the medial canthal region. Microdissection of the forehead vasculature confirmed these radiographic findings. The supratrochlear artery was consistently found to exit the superior medial orbit approximately 1.7 to 2.2 cm lateral to the midline and continued its course vertically in a paramedian position approximately 2 cm lateral to the midline. This position closely corresponds to the location of the medial border of the eyebrow. The supratrochlear artery was found to exit the orbit by piercing the orbital septum, passing under the orbicularis oculi and over the corrugator supercilii.10 At approximately the level of the eyebrow, the artery passes through the orbicularis and frontalis muscles and continues superiorly in the superficial subcutaneous tissue. This transition of the artery from a deeper to a more superficial tissue plane was confirmed by histologic examination of cross sections of forehead skin at various levels. Doppler examinations of healthy volunteers helped confirm the findings of the cadaver studies.10

Studies of the vascular anatomy of the forehead confirm that the supratrochlear artery serves as the axial blood supply of median and paramedian vertically oriented forehead flaps. The studies also confirm a rich anastomotic network in the medial canthal region. Surgical techniques that preserve this regional blood flow have allowed surgeons to harvest paramedian forehead flaps based on pedicles narrower than those used for median forehead flaps. The narrower pedicle provides the flap with greater freedom of transposition about its pivotal point and greater effective length. The pedicle may be as narrow as 1.2 cm, reducing deformity of the inferior forehead area and always enabling the surgeon to achieve primary closure of the lower half of the donor defect (Fig. 13-3).7,23

Paramedian Forehead Flap

Midforehead flaps, which include the median and paramedian flaps and their many variations, have proved to be dependable flaps for midfacial reconstruction.2,3,24 However, the paramedian forehead flap based on a single supratrochlear artery has replaced the median forehead flap for nasal reconstruction because it has a more axial design, narrower base, and greater effective length. The design also enables the simultaneous or sequential use of two vertically oriented forehead flaps. The paramedian flap has an abundant blood supply, providing for revascularization of cartilage and bone grafts covered by the flap. Removal of muscle and subcutaneous fat from the distal portion can make the paramedian forehead flap thin, pliable, and easily contoured to fit any defect of the nose. Maintaining the attachment of the frontalis muscle to the flap is occasionally useful when more bulk is required to fill defects of considerable depth.25 In most instances, however, freeing the flap from the frontalis muscle and most of its subcutaneous fat is essential when the forehead flap is used as covering for the nose. Proper thinning of the flap will ensure that the shape and contour of the underlying nasal framework are visually manifested. Flap thinning may be accomplished without concern for compromise of the flap’s vasculature because the supratrochlear artery travels superiorly in the subcutaneous/subdermal tissue plane from a point 1 cm superior to the level of the eyebrow.10 The superficial location of the artery enables thinning of the distal portion of the flap by removal of the fascia and frontalis muscle and, if necessary, nearly all of the subcutaneous tissue. The ability to modulate the thickness of a flap so that it may exactly match the thickness of the nasal defect at the recipient site greatly enhances the aesthetic result.25

Paramedian forehead flaps used as interpolated flaps for nasal reconstruction require a second operation to separate the pedicle.26 The pedicle may safely be detached as soon as 10 to 14 days after flap transfer. The author prefers a 3-week interval between the time of flap transfer and flap inset for all patients, especially those who use tobacco products. At 3 weeks, the distal portion of the flap has developed sufficient collateral blood supply from the nose to allow thinning and sculpturing of the more proximal portion of the flap left attached to the recipient site. If the nasal defect is small, the portion of the forehead flap covering the defect may be completely thinned at the time of initial transfer.

A minor disadvantage of the paramedian forehead flap is the donor site scar and the necessity for a two-stage procedure. However, forehead scars are rarely unsightly because primary wound closure is easily achieved in the inferior portion of the forehead owing to the narrow pedicle required (Fig. 13-4). Although the narrow pedicle enables primary repair of the inferior aspect of the donor site wound, the width of the superior portion of the flap may be several centimeters, precluding complete wound approximation. In general, flaps wider than 4.5 cm are too large to allow complete primary closure of the donor site. In such circumstances, the superior portion of the donor site wound must, in part, be left to heal by secondary intention. Fortunately, the resulting midline or paramedian scar in the superior portion of the forehead is extremely forgiving and only occasionally requires revision. The acceptable scar is related to the immobile skin and convex contour of the superior central forehead (Fig. 13-5).

The forehead provides a source of skin with an excellent color and texture match to the nasal skin. The paramedian forehead flap may be designed with sufficient size and length to provide covering for the entire nose. For patients who have a low anterior hairline or a widow’s peak, the surgeon may not be able to design the flap with adequate length to reach the columella or tip without transferring hair-bearing skin to the nose. When flap extension to hair-bearing scalp is necessary, the distal flap is thinned sufficiently to expose hair follicles. Under magnification, each hair follicle is meticulously cauterized either at the time of transfer or at the time of pedicle division. In patients with a high concentration of hair follicles in the distal portion of the flap, it is usually not possible to eradicate all hair at the time of initial transfer or subsequent pedicle detachment. Two to 3 months after division of the pedicle and inset of the flap, another procedure is performed to eliminate the hair. The portion of the flap bearing hair is elevated in the subdermal plane where the follicles of scalp hair are located. Exposed follicles are removed or cauterized with a fine-tip needle cautery, with use of magnification to assist in visualization. A third depilation may sometimes be required. Even with this persistent approach, a few hair follicles may survive and are treated individually with electrolysis. The hair bulb that is responsible for hair regeneration is located in the subcutaneous fat just beneath the dermis. In some instances, remnants of the bulb may be left in the dermis after removal of the follicle during surgical depilation. These remnants may have sufficient germinating potential to cause breakthrough hair growth in spite of aggressive removal of exposed hair follicles.

The fine vellus hair that is prominent in some patients just in front of the forehead hairline is even more difficult to eliminate from a forehead flap because the hair follicles are not visible by the human eye and are located in the dermis rather than in the subdermal plane. This hair may be treated by electrolysis with limited success. The best treatment is to have the patient periodically use a depilatory cream for removal. Laser hair removal may be used in place of electrolysis for dark-pigmented scalp hair, but it is not effective for vellus hair.

To avoid multiple procedures directed at depilation, paramedian forehead flaps should be designed not to include scalp hair whenever possible. Avoiding scalp hair may be possible by extending the incision for the pedicle through the eyebrow to the level of the bony orbital rim. The pedicle is skeletonized on the soft tissue surrounding the supratrochlear artery as it exits the orbit. This requires complete sectioning of the corrugator supercilii to achieve free tissue movement. If this step is unlikely to lend sufficient length to the flap, another helpful approach is to obliquely angle the flap from the midline laterally toward the temporal recession just beneath the hairline (Fig. 13-6).27,28 This modification in design of the paramedian forehead flap is possible only for smaller flaps measuring less than 3 cm in maximum width. Harvesting of flaps 3 cm or greater in width from the lateral portion of the forehead may occasionally cause more apparent scars than centrally located donor sites. It may also cause excessive upward displacement of the central portion of the eyebrow on the donor side. Thus, flaps wider than 3 cm are usually extended to the hair-bearing scalp rather than designed in an oblique fashion when the necessary length of the flap requires such extensions (Fig. 13-7). When the oblique forehead design is used, the distal portion of the flap does not have the advantage of an axial vascular pattern. However, the author has been successful in transferring forehead skin based on a supratrochlear artery but positioned several centimeters lateral to the axis of the artery. This success is related to the rich vascular anastomotic network of forehead skin.

Historically, the paramedian forehead flap has been used for reconstruction of larger defects of the nose. It is the preferred method for covering nasal defects too large to be repaired with full-thickness skin grafts, nasal cutaneous flaps, composite auricular grafts, or interpolated melolabial flaps.4,5,12 In general, nasal defects larger than 2 cm in width in the horizontal axis are best repaired with a paramedian forehead flap (see Fig. 13-7).12 In addition, this flap is best for repair of nasal defects with exposed bone and cartilage deficient of periosteum or perichondrium and in instances in which the central face has been irradiated.5,12

Reconstruction of a nasal defect with a paramedian forehead flap requires planning and preparation. Preoperative assessment includes measurement of the defect and consideration of the required length and width of the flap. Attention is given to the height of the anterior hairline and degree of forehead skin laxity. Patients are counseled concerning their appearance during the staged reconstruction. They are shown photographs of patients who have had similar surgery after the first stage and after flap inset. Wound care of the pedicle, donor site, and recipient areas and information about realistic expectations and goals of the reconstructive procedure are discussed.

Surgical Technique

The paramedian forehead flap is usually harvested with use of a combination of a short-acting local anesthetic (lidocaine 1% with epinephrine 1:100,000 concentration), long-acting local anesthetic (bupivacaine 0.25%), and intravenous sedation. Thirty minutes before skin incision, a prophylactic antistaphylococcal antibiotic of the surgeon’s choice is administered intravenously if a cartilage or bone graft is required. The patient is placed supine on the operating room table in 20° to 30° of a reverse Trendelenburg position. This position decreases venous pooling, causing less intraoperative blood loss during flap harvest and transfer. The eyes are protected by covering them securely with moist eye pads. The full face and scalp, from the mid vertex to the submental area, are prepared with a sterilization solution of the surgeon’s choice. A sterile head drape is placed, and full-body draping is completed in the usual sterile fashion.

The flap may be designed with the assistance of a Doppler probe to localize the supratrochlear artery, but the author has not found this to be necessary. The base of the pedicle is usually centered over the supratrochlear artery on the same side as the majority of the nasal defect for which the flap is intended for repair. The vertical axis of the supratrochlear artery is 2 cm lateral to the midline, which corresponds to the medial border of the eyebrow in the majority of patients. Therefore, the base of the flap is centered over the medial border of the eyebrow. The width of the pedicle is designed 1.5 cm wide, and the base is not flared as this restricts the pivotal movement of the flap.

The cutaneous defect is outlined by squaring off the corners of the defect with a skin marker. Giving the defect angular rather than curvilinear borders reduces the propensity for development of trap-door deformity (see Fig. 13-5). If the defect occupies more than 50% of the surface area of a convex-shaped nasal aesthetic unit (tip and alae), the remaining skin of the unit is marked for removal (Fig. 13-8). When a unilateral cutaneous defect encompasses half or less of the surface area of the nasal tip, the defect is usually enlarged only to the degree that the enlargement creates a hemi-tip defect (Fig. 13-9). This will limit the size of the forehead flap necessary for reconstruction, which in turn minimizes the deformity of the forehead. The aesthetic result of resurfacing a heminasal defect with a paramedian forehead flap is as pleasing as resurfacing the entire nasal tip, provided the remaining nasal skin is of thin or medium thickness.

An exception to the rule of resurfacing the entire nasal unit when the defect occupies half or more of the surface area of the unit is the dorsum. When cutaneous defects occur on the dorsum, the thin skin of the rhinion is never removed unless it is required for tumor ablation. In most patients, the intrinsic thickness of forehead skin is greater than that of the native skin covering the rhinion. Even with removal of all the subcutaneous tissue from a forehead flap, the thickness of the flap will not match the thinness of the in situ skin and muscle of the rhinion. In this region, contour outweighs the advantage of placing the borders of the flap along the junction of aesthetic units. It is wiser to leave this skin intact and to resurface only the caudal dorsum than to resurface the entire dorsal nasal aesthetic unit (Fig. 13-10). The same principle applies to skin of the superior nasal sidewall, which is very thin and is not replaced with forehead skin unless the defect involves this region of the nose.

Similar to the rhinion, the skin of the nasal facets is delicate and thin. It is supported only by fibroconnective tissue. Forehead skin cannot replicate the delicate nostril margin in this area of the nose. Nasal tip defects requiring a forehead flap as a cover should be enlarged only to a line along the upper border of the facet (Fig. 13-11). This line corresponds to the caudal border of the intermediate crura of the lower lateral cartilages.

A three-dimensional template exactly duplicating the surface area and contour of the region to be resurfaced is fashioned from foil or a thin sheet of foam rubber. The author prefers foam rubber because it has the flexible qualities of skin and easily conforms to the convex and concave contours of the nasal topography (Fig. 13-12). The final defect to be resurfaced is marked on the nasal skin, outlining additional skin removal to square off the defect or to remove the remaining cutaneous portions of the aesthetic unit. The template is designed before the defect is enlarged because once the additional skin is removed, the wound will spread and the defect will appear larger than it is. For this reason, if the nasal defect involves an aesthetic unit that has an intact counterpart, the intact unit is used to design the template because it will give a more accurate measurement of surface area. The template is then reversed to design the flap. When the defect involves an aesthetic unit that is unpaired, the template is designed as an ideal size for the specific patient. In dealing with large surface defects, it is helpful to suture the rubber foam template to the margins of the defect to fashion the template more precisely (see Fig. 13-12). Cartilage grafts are required to replace missing framework, and the template is designed after the grafts are in place. Templates should not be oversized but tailored exactly.

The template is used to design the flap on the forehead skin (see Fig. 13-12). The center of the template is positioned approximately 2 cm lateral to the midline. At a minimum, the upper border of the template is positioned at the frontal hairline unless the patient has a receding hairline or frontal balding. The length of the flap is measured by a length of suture extending from the distal end of the positioned template to the level of the medial eyebrow. Holding it at the eyebrow, the suture is rotated 180° in the coronal plane toward the midline to the most distal recipient site on the nose. If the suture does not reach this point, the template must be repositioned higher on the forehead or the pedicle must be lowered by extending it below the level of the eyebrow. By use of this method of determining flap length, a decision can be made concerning the necessity of placing a portion of the template over hair-bearing scalp. The flap is then precisely outlined on the forehead with a skin marker, following the exact shape of the template (see Fig. 13-12).

Cutaneous defects that involve the nose and significant portions of the medial cheek or upper lip are reconstructed in stages. The first surgical stage is directed toward repair of the cheek to provide a stable foundation for subsequent reconstruction of the nose. The surgical plan of first restoring the foundation on which to place the constructed nose, before initiating nasal reconstruction, is used whenever a sizeable full-thickness defect of the cheek or lip is associated with a full-thickness nasal defect. For example, when there is a full-thickness loss of the ala or columella and adjacent upper lip, it is prudent to delay reconstruction of the nose until the lip is repaired and scars have contracted to their maximum propensity.

In contrast to full-thickness nasal defects, defects of the nose that are not full thickness and that extend into the lip or cheek can usually be reconstructed concurrently. This is because there is less scar contracture surrounding the nose during the healing stages compared with repair of full-thickness defects and thus fewer problems with distortion of the constructed segments of the nose. Keeping with the principles of repairing each portion of a defect involving multiple facial aesthetic regions with an independent covering flap, individual flaps are used to reconstruct the cheek, nose, and lip if all three aesthetic regions are involved by the defect. The most common circumstance leading to defects involving the nose, lip, and cheek is a skin malignant neoplasm arising from the ala and extending into the alar-facial sulcus with subsequent growth into the medial cheek and upper lip. Another common circumstance is for the malignant neoplasm to arise from the nasal sidewall and extend across the nasofacial sulcus into the medial cheek. The cutaneous defect resulting from resection of this type of neoplasm should be reconstructed with two independent flaps. In such instances, the cheek defect is typically reconstructed with a cheek advancement flap. The flap is advanced medially to the nasofacial sulcus. The leading border of the flap is secured to the periosteum of the ascending process of the maxilla to prevent the flap from migrating laterally during the healing process. The cheek flap is secured in place first before a template is designed for the paramedian forehead flap that is used to resurface the nasal sidewall. If periosteal sutures are inadequate to hold the advancement flap in place, holes are drilled in the exposed bone along the piriform aperture. These holes are used for anchoring sutures placed along the advancing border of the cheek flap.

Figures 13-13 and 13-14 show two examples of cutaneous defects that extend from the nasal sidewall into the cheek. The patient shown in Figure 13-13 had a limited extension of the cutaneous defect into the cheek. The adjacent cheek skin was advanced and secured to the nasofacial sulcus without the necessity of making incisions in the cheek skin. Small standing cutaneous deformities resulting from advancement of the cheek skin were removed in the nasofacial sulcus superiorly and alar-facial sulcus inferiorly. In contrast, the patient shown in Figure 13-14 suffered a more extensive defect of the cheek necessitating an incision that was made inferior to the defect, paralleling the melolabial crease. In both cases, the remaining skin of the nasal sidewall involved with the defect was removed to resurface the entire aesthetic unit. Likewise, the remaining skin of the nasal dorsum was removed from the nose of the patient shown in Figure 13-14 so that the aesthetic unit could be covered with the paramedian forehead flap used to reconstruct the nose.

Paramedian forehead flaps are usually dissected with use of local anesthetic and intravenous sedation. Lidocaine 0.5% with 1:100,000 concentration of epinephrine mixed in equal parts with bupivacaine 0.25% without epinephrine is injected circumferentially and deeply about the surgical defect. The entire forehead from the level of the lateral canthus to its counterpart is injected with 15 mL of similar anesthetic solution. The skin along the entire length of the supraorbital bony rims is infiltrated to the level of the periosteum. Particular attention is given to a broad vertical band of skin in the axes of the supratrochlear and supraorbital nerves. The anesthetic is injected into the subcutaneous tissue plane because this is the location of the nerves and vessels supplying the forehead skin. The base of the flap and skin over the root of the nose are also injected. Dolasetron (Anzemet) is administered intravenously to control postoperative nausea commonly associated with the procedure. A template used to design the forehead flap is constructed as previously described. The margins of the nasal defect are made perpendicular with a scalpel. If indicated, the remaining skin of the aesthetic unit is removed to the level of the perichondrium or periosteum. Until the pedicle of the flap is detached and the flap is inset, it is not necessary to excise the skin of the more extreme cephalic portion of the dorsum and sidewall aesthetic units when defects involve these units. The skin bordering the nasal defect is undermined below the muscle layer for 1 to 2 cm. Undermining of adjacent nasal skin may help prevent trap-door deformity.

The template is centered over the axis of the supratrochlear artery on either side of midline. With use of the template, the flap is outlined with a skin marker (Fig. 13-15). To avoid oversizing the flap, incisions are made inside the lines of the designed flap. The flap is incised through the skin, subcutaneous tissue, muscle, and fascia. The flap is elevated from superior to inferior in the subfascial plane, just superficial to the periosteum of the frontal bone. Rapid dissection may be performed in this plane until the corrugator supercilii muscle is encountered, at which point the muscle is dissected away from the underlying periosteum bluntly with scissors or a periosteal elevator. If it is necessary to extend incisions of the pedicle below eyebrow level, it is accomplished with a scalpel cutting through skin only. Blunt dissection by spreading tissue with a hemostat is then performed to mobilize the pedicle away from the medial bony orbit. The supratrochlear artery may sometimes be visually identified in the area on the deep surface of the frontalis muscle just as it exits over or through the corrugator supercilii muscle and before passing deep to the orbicularis oculi muscle to enter the orbit. Adequate flap mobilization usually requires complete sectioning of the corrugator muscle to achieve sufficient flap length. Blunt and sharp dissections are used to continue flap elevation downward into the root of the nose (see Fig. 13-10) or until sufficient pedicle length and flap mobility have been attained to allow tension-free wound closure. Hemostasis along the border of the flap is achieved with an electrocautery applied judiciously.

The forehead flap is covered with a damp sponge and reflected downward to allow repair of the donor site. Donor site closure is accomplished by extensive undermining of the forehead skin in the subfascial plane from the anterior border of one temporalis muscle to the other (see Figs. 13-11 and 13-15G). A few parallel vertical galeotomies 2 to 3 cm apart may be made to facilitate primary repair of the superior portion of the donor site if the donor defect is large. Galeotomies should be made just through the galea to the level of the muscle and removed from the vertical corridor of the supraorbital and supratrochlear nerves. The deep branch of the supraorbital nerve can readily be seen through the galea as it travels superiorly just medial to the temporal line, and it should be protected when galeotomies are performed.

Horizontal incisions along the hairline to facilitate closure of the donor site are not performed. This would increase anesthesia of the anterior scalp by cutting through the distal branches of the supraorbital nerves and create an additional visible scar on the forehead. As the wound edges are advanced, a standing cutaneous deformity of scalp tissue occurs at the superior apex of the flap donor site defect. This is excised completely by extending an incision sufficiently superiorly in the scalp to enable excision of the tissue cone (see Fig. 13-15).

The muscle and galea of the forehead are approximated as a single layer with 2-0 polyglactin suture. These are left untied until all have been placed (see Fig. 13-15). The skin incision is repaired with a simple running suture of 5-0 polypropylene. A drain is not employed. Primary approximation of the inferior forehead wound is rarely a problem because the pedicle width is 2 cm or less. However, superior portions of the donor site may not close completely. Any remaining open wound is filled with an antibacterial ointment. The patient is instructed to keep the wound moist with petroleum ointment until healing is complete. Healing by secondary intention takes 4 to 6 weeks.

The forehead donor site wound is repaired before the flap is sutured in place. The thickness of the flap is tailored by thinning the distal portion. This usually requires removal of the muscle and most of the subcutaneous fat to match the thickness of the nasal defect (Fig. 13-16; see also Fig. 13-11). When necessary, all but the subcutaneous fat immediately attached to the dermis may be removed. If the vertical height of the nasal defect is less than 2 cm, the portion of the flap covering the entire defect may be thinned at the time of initial transfer. For larger defects, the proximal flap covering the more cephalic portion of the defect is left with all of its muscle and subcutaneous fat intact and is thinned at the time of pedicle division. If necessary, the muscle and galea may be removed from the entire length of the flap beginning 1 cm superior to the point at which the supratrochlear artery pierces the frontalis muscle. Any hair follicles transferred with the flap should be individually cauterized with a fine-pointed electric cautery or removed manually. The distal flap, appropriately thinned, will be sufficiently supple and thin to conform to the nasal framework and manifest its contour.

The practice of removing the frontalis muscle and the majority of subcutaneous fat from a paramedian forehead flap used to cover the nose begs the question of why the frontalis muscle is transferred with the flap. Including the muscle in the flap inferiorly near the eyebrow protects the supratrochlear artery as it ascends from the eyebrow between the muscle and skin. The superior aspect of a paramedian forehead flap may be dissected in the deep subcutaneous tissue plane, leaving the frontalis muscle in place. However, elevation in the subcutaneous tissue plane causes more bleeding than elevation beneath the muscle and places the axial blood supply to the distal flap at some risk for injury. Unfortunately, leaving the frontalis muscle in situ when a paramedian forehead flap is transferred to the nose does not preserve the supratrochlear nerve, which must be sacrificed when the pedicle of the flap is divided. Transferring the muscle as part of the flap does not impair the motor function of the more lateral aspect of the frontalis muscle. In addition, removal of the muscle beneath the flap facilitates subgaleal dissection of the remaining forehead skin during closure of the flap donor site. Because most donor wounds of paramedian forehead flaps are closed primarily, any muscle preserved in the depths of the donor wound would require excision to prevent bunching and redundancy of the muscle during advancement of the remaining forehead skin. For all of these reasons, the frontalis muscle immediately beneath the flap is included in the flap during dissection.

After thinning, the flap is pivoted either clockwise or counterclockwise in an arc toward the midline and reflected downward toward the nasal defect. The distal flap is sutured in position with interrupted 5-0 polypropylene vertical mattress cutaneous sutures. Deep dermal or subcuticular sutures are not used. After placement of vertical mattress sutures, a single running 5-0 fast-absorbing plain gut suture on a fine-tipped needle is used to precisely approximate the epidermis by placing the suture in the superficial plane of the skin. It is not possible to approximate the extreme cephalic border of the nasal defect to the flap until pedicle detachment.

On completion of flap transfer, the entire forehead is infiltrated with a solution of 0.25% bupivacaine injected in the subcutaneous plane, with particular attention given to the vertical corridors of the supraorbital and remaining supratrochlear nerves. This helps control postoperative pain and nausea for up to 8 hours. The raw borders of the proximal portion of the flap are cauterized along their entire length to control postoperative bleeding, a common occurrence during the first 12 hours after surgery. The raw ventral aspect of the pedicle is covered with a full-thickness skin graft that is harvested from the supraclavicular fossa. The skin graft is sutured to the exposed borders of the pedicle and covers the entire length of the pedicle. Using a skin graft in this fashion reduces postoperative bleeding and vertical contraction of the pedicle. Restricting the degree of pedicle contraction lessens the tendency for nostril elevation during the early phases of healing.

Patients may be discharged home the day of surgery or admitted for overnight observation and wound care. Prescriptions provided to the patient on discharge from the hospital usually include an antistaphylococcal oral antibiotic (when cartilage or bone grafts have been performed), mild pain reliever (acetaminophen with codeine), antiemetic suppositories (promethazine or trimethobenzamide), and topical antibacterial ointment (bacitracin).

Postoperative wound care consists of cleaning the suture lines with hydrogen peroxide and application of the antibacterial ointment twice daily for 3 days, after which the ointment is exchanged for petroleum ointment. The patient is allowed to shampoo and shower on the first postoperative day. After the shower, ointment is reapplied to the suture line and exposed raw edges of the proximal flap. On the sixth to seventh postoperative day, sutures are removed. The wound is carefully checked for flap viability and signs of infection. If all appears well and healing is occurring as expected, the patient is scheduled for pedicle detachment approximately 3 weeks after the date of initial flap transfer. Although the pedicle may be safely divided 2 weeks postoperatively, the shorter interval may limit the ability to thin the more proximal flap remaining at the recipient site when the flap is inset. Patients are allowed to wear their eyeglasses if necessary; however, proper positioning of the eyeglasses may be a problem. Eyeglasses may require temporary readjustment by an optometrist. Devices are also available for suspending eyeglasses from the forehead, circumventing the need to rest them on the nose.

Pedicle separation is accomplished under local anesthesia. Lidocaine 1% containing epinephrine is injected into the base of the pedicle and circumferentially around the flap where it attaches to the nose, followed by the usual sterile preparation and draping. The pedicle is separated with a scalpel at the superior margin of the defect or higher if additional nasal skin is to be removed from the superior aspect of the aesthetic unit (Figs. 13-17 and 13-18). An incision is made in the cephalic portion of the old scars between the flap and adjacent nasal skin on either side of the pedicle. The extent of this incision should be such that it releases the cephalic quarter of the flap from the nose. This is necessary to provide sufficient exposure for thinning and proper trimming and inset of the flap. The skin margins surrounding the skin defect created by the flap release are undermined 1 cm. Thinning is performed of any portion of the flap left attached to the recipient site that was not adequately thinned at the time of the initial flap transfer. In the case of reconstructing skin-only nasal defects that involve the rhinion, it may be necessary to remove all subcutaneous fat to more accurately replicate the naturally thin skin of the rhinion. It is often necessary to remove early scar tissue under the flap to facilitate proper tailoring. Deep-layer closure is unnecessary because there is no wound closure tension. The flap is inset with interrupted vertical mattress and simple 5-0 fast-absorbing plain gut cutaneous sutures. On occasion, a cotton bolster dressing with percutaneous sutures to secure the bolster is used to ensure that the flap conforms to the skeletal framework of the nose. An overnight compression dressing is applied if a bolster dressing is not employed.

The base of the pedicle is returned to its donor site to restore the normal inter-eyebrow distance. Just as with the inset of the flap at the recipient site, it is often necessary to remove early scar deposition in the donor area to enable the pedicle to lie flat between the eyebrows. The medial aspect of both eyebrows is undermined for several centimeters to release all contractions (Fig. 13-18). This maneuver enables the surgeon to position the medial aspect of the eyebrows in proper relationship to each other and to the superior bony orbital rims. Typically, the medial aspect of the eyebrow on the flap side is displaced inferiorly as a result of secondary movement from flap transfer. The brow must be mobilized sufficiently to correct this displacement. This is accomplished by converting the proximal pedicle of the flap into a small triangle-shaped flap incorporating in its base the medial aspect of the eyebrow on the donor side. To accommodate scar contraction and inferior migration of the eyebrow during healing, the flap is mobilized upward until the level of the medial eyebrow is positioned 2 mm above the level of the opposite eyebrow. Tissue should not be returned to the forehead above the level of this point. Excess pedicle tissue above the portion of the triangular flap necessary for securing the medial eyebrow in proper position is resected and discarded. To facilitate superior advancement of the triangular flap and thus the medial eyebrow on the donor side, it is sometimes necessary to excise a small crescent or triangular segment of skin just lateral to the base of the flap along the superior medial border of the eyebrow (see Figs. 13-17 and 13-18). This maneuver removes the standing cutaneous deformity that forms from advancement. This in essence serves as a direct browlift limited to the extreme medial portion of the eyebrow. The muscle on the deep aspect of the triangular flap is preserved to prevent a postoperative depressed contour. In addition, it is often helpful to create a tongue of muscle and subcutaneous tissue extending 0.5 cm beyond the apex of the triangular flap (see Fig 13-18D). This tissue is tunneled under the most inferior portion of the forehead scar where it meets the apex of the flap triangle. The tissue tongue prevents contour depression at this point. The deep layers of the wound are closed with 4-0 absorbable sutures, and the skin is closed with 5-0 fast-absorbing plain gut sutures placed in vertical mattress fashion.

Postoperative care after pedicle detachment consists of cleaning the suture lines with a hydrogen peroxide solution and application of an antibacterial ointment twice daily for 3 days, followed by petroleum ointment for another 3 days. Sutures are removed in 5 to 7 days. Full physical activities may be resumed 1 week after surgery. The patient is advised to avoid excessive sunlight exposure to the forehead and face region for 3 months to prevent postinflammatory hyperpigmentation of the scars. Patients are instructed that extremes of heat or cold may cause temporary color changes in the flap skin at the recipient site for several months. Revision surgery, such as thinning of the flap, is delayed 3 to 4 months to allow complete wound healing, wound contracture, and the beginning of scar maturation. Revision surgery is occasionally necessary to create or to refine an alar groove (see Fig. 13-15) or to remove persistent hair follicles transferred from the scalp. These revisions are accomplished with use of local anesthesia. The author has not found it necessary or advantageous to perform an intermediate stage consisting of more proximal thinning of the flap before pedicle division. Although an intermediate stage may be advisable for a patient addicted to tobacco, in most patients it is not necessary and does not enhance the final aesthetic appearance of the reconstruction. Depending on the circumstance, the majority of the distal portion of a paramedian forehead flap may be thinned to the subdermis at the time of flap transfer. The remainder of the flap left attached to the nose can be contoured at the time of pedicle division. Performing a contouring procedure as an intermediate stage before the pedicle of the flap is divided subjects the patient to another 2 to 3 weeks of deformity as a result of the flap’s crossing from the eyebrow to the nose. This delays the patient from returning to work and resuming social activities.

The Paramedian Forehead Flap as a Lining Flap

Forehead skin is rarely required for lining full-thickness nasal defects. Septal mucoperichondrium and turbinate mucosa are preferred for this purpose and are generally in adequate supply. However, in total or near-total nasal defects that include the nasal septum, the surgeon must look to other sources of lining. A microsurgical flap of skin or temporoparietal fascia or fascia lata29,30 is a source of internal lining for reconstruction of major full-thickness nasal defects. Another alternative is the simultaneous use of two paramedian forehead flaps. One flap provides internal lining, and the other provides external cover (Fig. 13-19).31 Bone from the calvarium and cartilage grafts from rib or auricle are placed between the two flaps to provide a supporting framework. A template is fashioned that will provide ample skin to line the reconstructed nose, including the dorsum, sidewalls, tip, and alae. Unlike the forehead flap used for covering the exterior of the nose, a forehead flap used as a lining flap is incised and hinged downward without pivoting the base of the flap. This enables the raw undersurface of the flap to face outward. The pedicle may be tunneled under the glabellar skin or delivered superficial to the intervening skin between forehead and defect in such a fashion that it will not prevent the plating of bone grafts to the nasal process of the frontal bone (Fig. 13-20). When the nasal bones are intact, the flap may on occasion be transferred to the nasal defect from a lateral approach, which may necessitate a temporary nasal fistula. The sidewall dehiscence allowing the admittance of the lining flap is closed in layers when the flap is inset. The entire lining flap, except for the base of the pedicle, is thinned to the level of the subcutaneous tissue plane.

The lining flap may be transferred to the nose before or after construction of the nasal framework, depending on the circumstance. It is usually preferable to transfer the lining flap to the nose before attaching the framework. An incision is made at the mucocutaneous junction around the perimeter of the nasal defect. Adjacent skin is reflected sufficiently to expose the bone of the frontal processes of the maxillae. This provides access to attach bone grafts for skeletal support of the upper and middle nasal vaults. The mucosa along the perimeter is reflected sufficiently to provide a flap of tissue. The mucosal margins are approximated to the margins of the forehead lining flap with 3-0 running polyglactin suture. Bone or costal cartilage grafts are shaped and contoured to provide a framework for the dorsum and sidewalls. In cases in which the nasal bones are absent, a dorsal bone graft can be plated to the frontal bone at the level of the planned nasal-frontal junction. This creates strong stable skeletal support for the upper and middle nasal vaults. Additional cranial bone is fashioned into two rectangular grafts. The length of the grafts is sufficient to extend from the maxilla to the level of the lower nasal vault. The grafts are plated to the dorsal bone graft and to the adjacent maxillae and serve as the framework for the nasal sidewalls. Several holes are drilled through the bone grafts, and horizontal mattress polyglactin sutures are placed through the holes and the lining flap to appose the exposed raw surface of the lining flap against the undersurface of the bone grafts. Cartilage grafts are then used to create the framework for the lower nasal vault. The grafts may be stabilized to the caudal end of the bony sidewall grafts with sutures passed through holes drilled in the bone. Once the framework for the lower vault has been constructed, mattress sutures are used to approximate the forehead lining flap against the undersurface of the cartilage grafts. It is important that the lining flap completely cover the undersurface of the bone and cartilage grafts so they are not exposed to the nasal passage.

When the framework has been constructed and secured to the maxillae and the lining flap has been apposed to the framework, a template is fashioned to design a covering flap using a second paramedian forehead flap. The second flap is usually based on the ipsilateral supratrochlear artery (Fig. 13-21). The second flap is pivoted toward the midline, and the distal two-thirds of the flap is thinned and used to cover the entire framework. The caudal border of this flap is sutured to the caudal border of the lining flap, completely enveloping the cartilage grafts used for the lower nasal vault framework. The lateral borders of the covering flap are sutured to the surrounding skin edges of the nasal defect. A few bolster sutures passing through both the covering and lining flaps may be used to coapt the undersurfaces of the two flaps, eliminating dead space between the flaps. The forehead donor site is large when bilateral paramedian forehead flaps are used and can only partially be closed. The remaining forehead wound is allowed to heal by secondary intention.

When dual paramedian forehead flaps are used to provide lining and cover to the nose, pedicle detachment is delayed for 2 months as both flaps depend on vascularization across a circumferential scar at the perimeter of the reconstructed nose. The pedicle of the lining flap is detached first, and the nasal fistula is closed. It is important to remove all of the skin of the portion of the pedicle that is beneath the covering flap and not exposed to the reconstructed nasal passage. This is to prevent development of skin line cysts and subsequent infection and drainage. The covering flap is inset 2 months after inset of the lining flap. At the time of pedicle division, the proximal pedicles of the two forehead flaps are returned to the forehead in their entirety and without trimming. Returning all of the skin and soft tissue composing the proximal pedicles of the flaps restores all of the forehead skin between the eyebrows as well as most of the skin of the central forehead. This will provide the inferior central forehead with a natural appearance (Fig. 13-22).

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FIGURE 13-22 Same patient as shown in Figure 13-21. A-F, Preoperative and 1.5-year postoperative views. No revision surgery performed.

Forehead Expansion

Tissue expansion of the forehead in anticipation of using a paramedian forehead flap is not recommended because of the additional morbidity of the expansion process. In addition, forehead donor wounds that cannot be closed primarily heal by secondary intention and result in an acceptable-appearing scar. However, tissue expansion may have a role in patients who require dual paramedian forehead flaps, which will require removal of the majority of the central forehead skin.32 The patient must be informed that expansion of the forehead will be an additional surgical procedure and will cause an increasingly noticeable deformity of the forehead for several weeks before nasal reconstruction can be initiated.

Tissue expanders are Silastic balloons with self-sealing valves or reservoirs that are inserted beneath the skin. They are available in many different sizes and shapes, such as round, rectangular, and elliptical, and in volumes ranging from a few cubic milliliters to several thousand cubic milliliters. Tissue expanders are implanted by performing a ring block with lidocaine 1% and epinephrine (1:100,000 concentration). An access incision for insertion of the expander is oriented vertically 3 cm behind the hairline in the paramedian position. The length of the incision should be limited to approximately half the length of the width of the expander. A recipient pocket is created by blunt dissection between the periosteum and the deep fascia of the frontalis muscle. The pocket should be large and extend inferiorly to the level of the superior bony orbital rims. An endoscope may be inserted through a separate scalp incision to assist in visualizing the dissection. The pocket is irrigated with a solution containing an antibiotic. A 250-mL rectangular tissue expander is folded on itself and inserted into the pocket through the access incision. The expander is unfolded within the pocket and manipulated until the base lies flat against the frontal bone without kinking. The injection port is tunneled posteriorly beneath the parietal scalp. Anchoring sutures to prevent migration of the expander are not necessary. The expander is partially expanded (approximately 25 mL for a 250-mL expander) with saline before wound closure to obliterate dead space and to assist with hemostasis concomitantly. The incision is closed in layers with permanent sutures to approximate both the galea and the skin.

Inflation begins 2 weeks after implantation of the expander. After the injection site is prepared with an alcohol swab, saline is infused by percutaneous puncture of the injection port with a 23-gauge scalp needle attached to a 50-mL syringe. The volume of injection depends on the tensile strength and tension of the skin overlying the expander and the amount of the patient’s discomfort. If it is not precluded by the patient’s discomfort, the forehead is expanded until slight blanching is observed in the skin overlying the expander. Saline is then withdrawn until the blanching disappears. However, tightness or pain is usually the limiting factor. Usually 25 to 30 mL of saline may be injected into a 250-mL volume expander on a weekly interval. The discomfort from inflation resolves within 24 to 48 hours, and the patient remains comfortable until the next inflation. Inflation is conducted once a week; more frequent expansion is associated with a greater risk of expander extrusion.

The volume of injected saline is recorded with each inflation. If weekly visits to the office for inflation are not possible, the patient or a family member may be taught the inflation technique. In-home expansion is facilitated by a written list of instructions. A small amount of methylene blue dye may initially be injected into the expander at the time the expander is implanted. Before inflation, the person performing the inflation may aspirate a small quantity of saline through the injection port. Proper placement of the needle has been achieved if blue solution is returned.

As expansion proceeds, the dermis becomes thinner, and a capsule forms around the expander. This often results in a reversible blue or red hue of the expanded skin. Dilated subcutaneous veins are frequently observed. The presence of the veins is not an indication of cyanosis or infection. Expansion continues until the circumference of the dome of the expanded skin measures two or three times the width of the anticipated defect. For nasal reconstruction, 6 to 8 weeks of expansion are required to achieve this goal.

The second surgical stage requires removal of the expander and proceeding with reconstruction. The expander is deflated and removed through one of the incisions used to create the two paramedian forehead flaps. The capsule surrounding the expander provides an excellent blood supply to the flaps and is not disturbed unless thinning of the flap is necessary to achieve optimal results. A suction drain tube is employed at the donor site, which can usually be closed primarily. Wound closure and postoperative care are similar to those used for standard flap surgery. It is important that the expanded forehead skin be supported by a rigid nasal framework to prevent flap contraction and loss of contour. The flaps should not be oversized but designed to reflect accurately the exact surface area required of the lining and cover for the missing nose.

Complications

Complications arising from the use of paramedian forehead flaps are rare as this is the “golden” flap of nasal reconstruction. The superficial axial blood supply of the flap provides ample nourishment, making distal flap necrosis unlikely. The superb vascularity of the flap also markedly reduces the risk of wound infection. However, this vascularity accounts for the most common complication observed with paramedian forehead flaps: the development of small hematomas under the distal flap. Hematomas develop at the time of initial flap transfer. The rich vascularity of the flap creates a tendency for the undersurface of the portion of the flap thinned of its muscle and subcutaneous fat at the time of transfer to bleed postoperatively. The potential dead space between the flap and the underlying nasal framework will accommodate small hematomas because there are usually no adhesions or sutures that attach the covering flap to the framework. To reduce the development of hematomas, careful hemostasis is achieved over the entire raw undersurface of the thinned portion of the flap. This portion requires special attention because it may ooze blood continually for a few hours after surgery. Compression dressings secured with a few bolster sutures passing full thickness through the flap to the nasal passage and back again may be placed judiciously if bleeding is profuse (see Fig. 13-13). Bolster dressings, however, are not used routinely because they risk impairment of the circulation to the distal flap.

Hematomas that do develop beneath the distal portion of the flap frequently cause a greater amount of swelling than expected and give the flap the appearance of early trap-door deformity. Usually, hematomas are not discovered until the pedicle of the flap is detached and the flap is inset. The exposed hematoma is managed by evacuating the accumulated blood and sharply scraping and débriding the fibrinous tissue deposited under the flap.

Advantages

The advantages of the excellent blood supply of the paramedian forehead flap far exceed the problems of an occasional postoperative hematoma beneath the flap. In a review of the University of Michigan Mohs database from 1993 to 1999, 147 patients underwent forehead flap repair of nasal defects after micrographic (Mohs) surgery.33 Secondary procedures after flap inset were performed in 79 patients (54%), with 1 procedure in 56 patients, 2 procedures in 22 patients, and 3 procedures in 1 patient. These procedures consisted of contouring of the flap in 68 patients, dermabrasion in 40, Z-plasty scar revision in 11, additional cartilage grafting in 2, and suspension suture for opening of the nasal valve in 1. High aesthetic and functional goals were achieved in all patients (Figs. 13-23 and 13-24). No tumor recurrence or significant episodes of local bleeding or infection occurred. Perhaps the most significant finding of this study was that not a single case of significant flap necrosis occurred. Two patients (1%) did develop superficial partial-thickness necrosis. One case was related to a lengthy flap that was markedly thinned for the purpose of destroying hair follicles in an extended portion of the flap used to reconstruct the columella. The other case occurred in an oblique forehead flap that was harvested 3 to 4 cm lateral to the axis of the supratrochlear artery. Epidermolysis and superficial necrosis occurred in the center of the distal flap. Fortunately, the area healed without impairing the appearance of the reconstructed nose.

References

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27. Baker, SR. Oblique forehead flap for total reconstruction of the nasal tip and columella. Arch Otolaryngol Head Neck Surg. 1985; 111:425.

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33. Boyd, CM, Baker, SR, Fader, DJ, et al. The forehead flap for nasal reconstruction. Arch Dermatol. 2000; 136:1365.