Bilobed PMMC in Females: Our Challenging yet Meritorious Experience

Abstract

The gold standard reconstructive options for full-thickness defect of the oral cavity after resection of malignant lesions are the free flaps. But in developing nations due to resource constraints, it cannot be offered to all. Hence, pectoralis major myocutaneous (PMMC) flap as bilobed flaps is most commonly used. Bilobed flaps are technically demanding, and in females, it is more challenging due to higher complication rates especially in large breasts. There has been no major reported data evaluating outcomes of bilobed PMMC in females. This is a retrospective evaluation of outcomes of patients who underwent the bilobed PMMC flap reconstruction for full-thickness defect of the oral cavity after resection of malignant lesions from June 2018 to December 2019. Out of 80 patients, all patients ultimately had adequate tissue coverage for the defect with acceptable facial aesthetics. Functional outcomes with regards to oral continence, speech and swallowing were encouraging. Our study had 33.75% flap-related complications. Fifteen percent of patients developed varying degrees of flap loss, of which only 3.75% had total flap loss and 11.25% had partial flap loss which was managed accordingly. Our study concludes that with careful planning, raising of flap based on sound anatomic concepts and applying oncoplastic techniques, shortcomings of bilobed female PMMC can be addressed and still used as suitable alternatives for free flap for full-thickness oral cavity defects in limited resource settings.

Reconstruction of full-thickness defects of the oral cavity after extensive resection for malignant lesions is technically cumbersome. Any adverse events after reconstruction affect wound healing, which delays the adjuvant treatment thus hampering the oncological outcomes and it also affects functions like speech and swallowing.

The gold standard in reconstructive option for oral cavity defects is the free flap. Unfortunately, in most developing nations due to resource constraints pedicled flaps, especially the pectoralis major myocutaneous (PMMC) flaps are used [1]. Full-thickness defects in the oral cavity mandate the need for technically challenging bilobed PMMC flaps. In females, it is even more challenging because of substantial breast tissue between the skin-paddle and the muscle, hence increasing the chances of skin-paddle loss [2]. To reduce the same, we try to limit the entire skin paddle over the muscle, which can cause significant disfigurement of the breast. Traction of the flap superiorly during harvest may cause mal-position of the cutaneous portion of the flap jeopardising its vascularity and can lead to flap loss. Complications frequently occur in large-sized breasts and when more substantial defects are reconstructed.

Previously published significant data assessing outcomes of bipaddled PMMC included only male patients [3–5]. There have not been any major reported data appraising outcomes of bilobed PMMC in females. In this article, we outline the technical considerations we adopted to reduce flap complications and our outcomes of bilobed PMMC in females.

Materials and Methods

We evaluated females who underwent the bilobed/folded PMMC flap reconstruction for oral cavity malignancy from June 2018 to December 2019 at our institute. During this period, 80 patients underwent composite resection, which included a full-thickness excision of the primary tumour with 1–2 cm margin, mandibulectomy with or without upper alveolectomy and neck dissection for clinical T4 SCC of the oral cavity. Through-and-through defects of the oral cavity underwent reconstruction with bilobed PMMC flaps. Retrospective analysis of data was done with regards to types of flaps, method of harvest, site of tumour, neoadjuvant treatments, operating time, complications and time to adjuvant treatment. Results were evaluated separately for transverse and paramedian flaps. Incidence of flap-related complications graded as per Clavien-Dindo morbidity grading and requirement of second surgical interventions were noted. Functional outcomes in terms of oral continence, speech and swallowing were assessed. We outlined flap success as those who eventually had satisfactory tissue coverage for the defect with minimal complications. Breast aesthetics assessment was not feasible due to insufficient peri-operative data. Statistical analysis was done by IBM SPSS software.

Techniques of Flap Harvest

The flap is raised based on the thoracoacromial artery and blood supply for skin paddle is from musculocutaneous branches. Before flap harvest, the size of the outer skin and inner mucosal defect is measured with a scale or roughly based on the surgeon’s finger breadth after resection.

Skin Paddle Marking

Marking of skin paddle was done after considering the following

1. Breast size

2. The size of the defect, measured after resection of the primary lesion (Fig. 1b).

3. Distance between the pivot point of the flap (the midclavicular point) and the recipient site (Fig. 1c)

4. Surface marking of the vascular pedicle was made by drawing a line from the ipsilateral acromion to the xiphisternum and another line vertically from the midpoint of the clavicle to intersect the first line.

5. The major part of the skin paddle was positioned over pectoralis major (PM) muscle (Fig. 2).

6. Incision should not extend over cutaneous area of deltopectoral (DP) flap (Fig. 2 a and b).

Fig. 1.

Marking the primary tumour and defect assessment after resection

Fig. 2.

Types of flap incisions and postoperative picture after paramedian submammary incision

Marking is done after assessing the distance between the pivot point of the flap (the midclavicular point) and the cranial aspect of the defect in the recipient site (which is the farthest point) with a long surgical gauze or scale (Fig. 1c). The lowest level of skin paddle is made based on that.

The flap is marked after considering combined inner and outer defect size (Fig. 2 a and c) and making sure that the significant part of the skin paddle is positioned over the PM muscle. Skin paddle should not extend beyond seventh rib/intercostal space as, beyond this, it is mainly supplied by the superior epigastric artery. So, possible options are

• (i)Transversely/horizontally oriented flap sparing DP area (Fig. 2a)
• (ii)Paramedian flaps (vertically oriented) sparing DP area (Fig. 2b)
• (iii)Paramedian flaps raised by submammary approach (Fig. 2c)

Smaller breasts: If a small paddle is needed, infra-mammary skin paddle or paramedian paddle can be used. If a large skin paddle is needed in a small-sized breast, we design the skin paddle transversely, including the nipple-areola complex (NAC), causing significant disfigurement of the breast (Fig. 2a).

In medium and larger breasts, paramedian paddles (Fig. 2c) are preferred so that the breast tissue between the skin and the muscle is less and causes limited disfigurement of the breast. If a very large paddle is needed, transverse flaps were harvested.

Paramedian flaps raised by submammary approach had better breast aesthetic outcomes (Fig. 2 c and d).

Usually, in transversely oriented flaps, the lateral part of the skin paddle is used for intraoral mucosal defect and medial part for cutaneous defect (Fig. 2a) while in paramedian flaps, the cranial part is for mucosal and caudal part for cutaneous defects (Fig. 2c).

Flap Raising

Skin incision is made using a knife and deepened till the muscle using monopolar cautery in cut mode. The skin paddle was bevelled to avoid undercutting and to include more myocutaneous perforators.

To avoid shearing injury to perforators while handling the skin paddle, the dermis of the paddle is sutured to the underlying muscle with 3–0 vicryl (Fig. 3a) and it is covered with warm saline gauze.

Fig. 3.

Key steps of flap elevation and tunnelling

The upper skin flap is raised till the clavicle; medially, the skin flap is elevated safeguarding vessels of the DP flap and laterally till the lateral border of PM muscle.

The inter-pectoral plane is delineated (Fig. 2b), and the flap is elevated from ribs in this plane, keeping in view and safeguarding the vascular pedicle at all times and dividing the muscle medial and lateral to the pedicle till clavicle (Fig. 3c).

The lateral thoracic artery is usually sacrificed to maximise the reach of the flap. Flap reach is enhanced by dividing the clavicular portion of the muscle above the pedicle and very rarely by removing the middle one-third of the clavicle.

Lateral pectoral nerve should be divided as its lie is parallel or oblique to the vascular pedicle. When a 180-degree rotation is made, the nerve becomes taut and can cause compression of the pedicle.

The flap is passed into the neck under the subcutaneous tunnel over the clavicle. The tunnel should be sufficiently (3–4 fingers) wide to avoid the compression over the pedicle. While tunnelling the flap, the skin and muscle of the flap should be held together (Fig. 3d). In females, usually the donor site can be closed primarily.

Flap Insert

Insert of the flap is done once adequate reach without tension is ensured. If the reach of the flap is limited, extension placed during procedure is taken off and the neck is kept flexed.

Mucosal Defect Closure

Initially, the mucosal aspect of the defect is closed. In transversely oriented flaps, usually the lateral aspect of the flap is used to close the mucosal defect, whereas in paramedian flaps, the cranial aspect is used.

Usually, an absorbable material (3–0, 2–0 vicryl or monocryl sutures with round body or tapper cutting needles) is used. Intermittent stitches, as half or full mattress sutures are made use of, depending on the surgeon’s preference. Usually, suturing starts from the posterior-most aspect of defect followed by superior and inferior aspects.

The exposed bone (mandible/palatal) should be covered by the flap, by using inter-dental needle passes and hitching to the tooth or passing sutures through a drill hole made in the bone.

Tri-pointer between flap and two mucosal surfaces should be adequately secured to obtain a watertight closure.

Skin Defect Closure

Once the mucosal defect is closed, the rest of the paddle is used for cutaneous defects; the following can be done

• (i)Incising bridging area of the paddles till the subcutaneous fat/muscle depth (Fig. 4b).
• (ii)De-epithelialising the bridge (Fig. 4a).
• (iii)Dumbbell-shaped flaps (Fig. 4c)—simply folding the flap and suturing lips on to flap.

Fig. 4.

Splitting/folding (dumbbell) of the skin paddle and long-term follow-ups

Dumbbell flaps are used when a significant part of the lip is also removed and primary closure of lips would result in microstomia. However, the disadvantage is the continuous drooling of saliva, which may mandate a second procedure like commissuroplasty.

Outer aspect of the flap is sutured to the skin by non-absorbable sutures (3–0, 4–0 Nylon) with intermittent half-buried mattress sutures (Army navy suture) or simple sutures. Limit the skin sutures to minimum to avoid tension on the flap (Fig. 1d).

Results

Descriptive Analysis

Out of 80 cases, 52 were operated upfront, 24 operated after neoadjuvant chemotherapy and 4 were operated after radiotherapy. The most common site is buccal mucosa. The average age was 48 years (29–76). Size of paddle used for mucosal defect ranged from 5 × 3 to 10 × 8 cm and skin cover ranged from 4 × 3 to 10 × 7 cm. Total size ranged from 9 × 3 to 18 × 8 cm. The mean operating time was 120 min (80–200 min) and the mean hospital stay was 12 days (5–50) (Table 1).

Table 1.

Our results

	Transverse (45)		Paramedian (35)
Age (years)
20–40 years	12		18
40–60 years	26		12
60–80 years	7		5
Site
Buccal mucosa	30		21
Lower alveolus	7		5
Retromolar trigone	6		5
Central arch	2		4
Preoperative haemoglobin (gm%)
< 10	2		1
> 10	43		34
Serum albumin (gm/dl)
< 3.5	4		3
3.5–4.0	33		26
> 4	8		6
Upfront operated	34		18
Neoadjuvant chemotherapy	10		14
Post-chemoradiotherapy	1		3
Operating time (harvest + insert)
80–120 min	28		20
120–160 min	12		9
160–200 min	5		6
Defect
Buccal mucosa	39		30
Buccal mucosa with lip	6		5
Defect size
Mucosal lining
5 × 3 to 7 × 5 cm	26		26
7 × 5 to 10 × 8 cm	19		9
Outer skin
4 × 3 to 7 × 5 cm	32		28
7 × 5 to 10 × 7 cm	13		7
Total
9 × 3 to 12 × 4 cm	13		7
12 × 4 to 15 × 6 cm	22		25
15 × 6 to 18 × 8 cm	7		4
Donor site closure
Primary	45		35
Others	0		0
Hospital stay (days)
< 10	27		25
10–20	10		6
> 20	8		4
Outcomes
Oral continence
Normal	37		29
Occasional drooling	7		5
Continuous drooling	1		1
Speech
Perceptible speech	44		35
Permanent tracheostomy	1		0
Swallowing
Full diet tolerated	32		26
Soft diet tolerated	12		8
Tube feeding	1		1
Adjuvant treatment needed
Yes	43		34
No	2		1
Time to adjuvant radiotherapy
< 42 days	41		33
42–50 days	2		1
Radiotherapy denied by patients	3		2
Delay in adjuvant treatment(> 6 weeks)	2		1
Complications
Breast size	Small (30)	Medium (34)	Large (16)	Total (80)
Flap harvest orientation
Transverse	20	20	5	45
Paramedian	10	14	11	35
Total flap loss				3 (3.75%)
Transverse	0	1	1	2
Paramedian	0	1	0	1
Partial flap loss				9 (11.25%)
Transverse	2	3	1	6
Paramedian	1	1	1	3
Minor complications				15 (18.75%)
Transverse	3	4	2	9
Paramedian	2	2	3	7
Morbidity (Clavien-Dindo grading)	8	12	7	27(33.75%)
Grade 2	5	3	2	10(12.5%)
Grade 3a (under LA/SA)	3	6	4	13(16.25%)
Grade 3b (under GA)	0	3	1	4 (5%)
Reinterventions				17(21.25%)
Major interventions	0	3	1	4 (5%)
Minor procedures	3	6	4	13 (16.25%)

LA local anaesthesia, SA spinal anaesthesia, GA general anaesthesia

Complications

Our study had 33.75% flap-related complications (Table 1). Fifteen percent of patients developed varying degrees of flap loss, of which only 3.75% had total flap loss (TFL),11.25% had partial flap loss (PFL) and 18.75% had minor complications (wound infections, wound dehiscence, seroma). Out of the total flap complications (33.75%), 5% patients needed major re-interventions (procedures under general anaesthesia—second flaps), 16.25% patients needed minor interventions (procedures under local anaesthesia—like debridement, resuturing, split skin grafts, hematoma evacuation and repeated seroma aspiration) and consider changing to and rest of the 12.5% patients were managed by pharmacological interventions (changing antibiotics according to culture and topical antibiotic used dressing for wound infection). Complication rates were less in the small and moderate-sized breasts. Flap-related complications were lesser in paramedian flaps.

Flap success was taken as those who ultimately had satisfactory tissue coverage for the defect with acceptable aesthetics (Fig. 1 a and d). Out of 80 patients, all achieved satisfactory cover with PMMC except three who had complete flap loss. One was reconstructed with forehead flap and two had opposite PMMC and forehead flap. Partial flap losses were managed with debridement followed by re-suturing or skin grafts except one patient, who needed forehead flap reconstruction. All patients eventually had satisfactory tissue cover.

When various factors like age, diabetic mellitus, size of flap, neoadjuvant therapy, the bulk of breast, preoperative haemoglobin and albumin were evaluated causative for flap necrosis, none of these factors were significant on univariate analysis. In three patients with TFL, all had bulky breasts. Meticulous handling of the flap was followed, the lateral thoracic artery was sacrificed as usually we do and tension-free reach without dividing clavicular fibres was easily attained with preserved pedicles. On assessing these patients, two of them were over 65 years with one being diabetic; both had a large defect mandating need of a transverse flap in which NAC was included. The third case was a known cardiac patient, in which paramedian flap was raised but had an intra-operative cardiac event and was on ionotropic support during the initial postoperative period.

Outcomes

On follow-up, all patients were able to take their nutrition orally except two, one was on Ryles tube feeding and one had percutaneous endoscopic gastrostomy. All patients had perceptible speech except one who had permanent tracheostomy (Table 1). All these patients were operated for central arch SCC. All patients were fit to receive radiotherapy within 6 weeks except three patients, which took 7 weeks for complete wound healing, and out of these, five patients denied radiotherapy. Detailed assessment of breast aesthetics was not possible due to insufficient peri-operative data.

Discussion

PMMC flaps are selectively used as a reconstructive option in females as it is associated with higher complication rates. There have been very limited published literatures available per se evaluating the outcomes of PMMC flaps in females. Bilobed PMMC flaps are even more susceptible for complications. Henceforth, bilobed PMMC are selectively relied upon in females. Previously published major series assessing bipaddled PMMC included only male patients [3–5]. There is a lack of notable published data assessing outcomes of bilobed PMMC in females, which are deemed susceptible to higher complications rates.

Reconstruction of complex oral cavity defects after full thickness resection needs to create both an intraoral lining and skin cover. Reconstruction options include bipaddled PMMC, folded forehead flap, dual flaps and free flaps. Currently, free flaps are considered to be the gold standard, but its widespread utility is limited, especially in developing nations due to the resource constraints [1], hence pedicled flaps like PMMC are heavily relied upon. The modification of PMMC as bilobed/bipaddled/bilobular/double-paddled/Gemini flap simplifies the closure of such defects [3]. PMMC flap was first reported in 1979 by Ariyan [6] and later described the division of the skin into two parts [7]. It was suggested that because of the rich collateral supply of the PMMC flap, it could be split axially or folded either axially or contra-axially with a de-epithelialised strip along the fold [8]. Later, it was found that the cutaneous layer can be divided in any direction [9]. The advantages of PMMC are shorter operating time, short learning curve, good vascular framework and adequate coverage of major vessels. Success of this flap is hampered by obesity, long neck, short thorax and female patients with big breasts [4].

In our study, 15% of patients developed varying degrees of flap loss (3.75% had total flap loss, 11.25% had partial flap loss) and overall complications rate (OCR) of 33.5%. There has not been any primary published data assessing complications of per se bilobed PMMC in females. In previously published series for bilobed PMMC, TFL of 0–2.12% and PFL of 0–8.33% were noted, but these included only male patients [3–5]. Analysing other published data for PMMC (mainly non-bilobed), TFL and PFL rates were in the range of 0–12% and 3–20%, respectively, and OCR was 13–63% [10–12]. Complications were higher in females [11, 12]. Chakrabarti S [11], in a series of 66 cases, reported that TFL was 6.06% and female sex accounted for major complications (55.5%). Kroll [12], in his series of 168 cases, reported an OCR of 63%, TFL of 2.4% and also noted a predilection of flap necrosis in the female sex. McLean [13] in a series of 136 reported OCR of 13%. Zou [14], in his study of 24 cases, reported an OCR of 62.5%, TFL of 8.3% and PFL of 20.8%. Baek [15], in their study of 133 cases, reported TFL of 1.5% and PFL of 7%. Mehrhof [16], in their study of 73 cases, reported TFL and PFL of 12.3% each.

Our flap loss rates are well within acceptable limits when compared with previously published data. Our results can be considered meritorious, because it was entirely bilobed flaps that too in female patients, both being considered as high-risk factor for flap failure. We strictly follow the below mentioned steps while harvesting flaps in females:

1. Skin paddle is marked over PM muscle territory while avoiding incision over DP flap area

2. If skin paddle is planned beyond PM muscle, it should be limited to a maximum 2 cm beyond it and going below the seventh intercostals—space is avoided [17].

3. Use of paramedian flaps [1, 2] with the submammary approach and considering the feasibility of oncoplastic principles whenever possible [2].

4. Suture skin paddle to muscle before elevating flaps from the chest wall and limit handling of the flap to a minimum. If required, cover the paddle with warm saline and keep tractional force to minimum

5. Lateral pectoral nerves should be divided; subcutaneous tunnel over the clavicle should be adequately wide, while tunnelling hold the skin and muscle of flap together and ensures tension-free reach of flap to defect site. If reach is still compromised, clavicular fibres above the pedicle are divided carefully.

6. While bipaddling of flap is done, limit to de-epithelialisation rather than cutting till muscle wherever possible. When suturing the external aspect of the flap, limit sutures to a minimum.

From our institutional experience, bilobed PMMC flaps in females are used mainly for the reconstruction of bucco-alveolar defects. In large breasts, paramedian paddles are preferred over transverse flaps. In small breasts, either paramedian or transverse flaps can be used. When there is a flap loss, we decide re-interventions with the aim that the adjuvant treatment is not delayed. In cases of TPL, re-intervention is performed at the earliest. In cases of PFL, we select patients judiciously for re-interventions depending on patient general conditions, degree of flap loss and whether the floor of the mouth is open causing significant wound infections. When various factors were evaluated as causative for flap loss, none were statistically significant, though we noted a higher complication rate in large breasts. So, careful planning and meticulous surgical techniques followed during harvesting bilobed PMMC in females are the prime prospect in limiting complications, with utmost care to be taken for large breasts. Application of the oncoplastic techniques (volume displacement) while doing PMMC can preserve the aesthetics of the breast to an extent. Hence, we can look beyond simple closure while performing PMMC in females [2].

Conclusion

Free flaps are considered the gold standard for reconstruction of full-thickness defects of the oral cavity. However, bilobed PMMC flaps, with its versatility, are an excellent reconstructive alternative for free flap especially in male patients in resource-constrained settings. In females, it is sparsely used due to higher complications especially in large breasts and causes significant breast deformity after primary closure. Our study concludes that with careful planning, raising of flap based on sound anatomic concepts and applying oncoplastic techniques, shortcomings of bilobed female PMMC can be addressed and still used as suitable alternatives for free flap for full-thickness oral cavity defects in resource-limited settings.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.