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Comparison of the hospitalization period after microvascular reconstruction flap in trismus patients: free anterolateral thigh flap versus free forearm flap

  • Wei-Chin Chang
  • Ching-Fen Chang
  • Chia-Mao Cheng
  • Cheng-Yu Yang
  • Yuan-Wu ChenEmail author
Open Access
Original Article
  • 110 Downloads

Abstract

Objectives

The primary strategy for treating oral squamous cell carcinoma (OSCC) is therapeutic resection, with the trismus resection defect reconstructed via free flap. The most popular free flaps include the radial forearm free flap (RFFF) and anterolateral thigh free flap (ALT). This study investigated the relationships between the hospitalization period and a variety of surgical outcomes, as well as maximum inter-incisor distance (IID), in trismus patients who chewed betel nuts.

Materials and methods

Forty-nine primary OSCC patients who chewed betel nuts and underwent surgical resection and reconstruction between 2010 and 2016 were enrolled in this retrospective study. The data were from a single center in Taiwan. The outcome variable after flap recovery surgery was the duration of postoperative hospitalization. Other factors that were analyzed comprised correlations between hospitalization and a variety of factors, including postoperative inter-incisor distances (IIDs), operative time, gender, and WBC count, upon stratification into two reconstruction groups.

Results

The mean postoperative hospitalization duration in the ALT group was 22.9 ± 7.2 days, which was significantly shorter than that in the RFFF group (27.8 ± 7.0 days; p = 0.019). Two-week postoperative IID (ALT group: 16.1 ± 0.8 mm; RFFF group: 7.0 ± 0.6 mm) was inversely related to the duration of hospitalization (p = 0.022, r = − 0.372).

Conclusions

The ALT flap is more effective than the RFFF flap to reduce the length of hospitalization in trismus patients.

Clinical relevance

The ALT flap should be considered as a first-line technique in OSCC reconstruction in trismus patient reconstruction.

Keywords

Free radial forearm flap Free anterolateral thigh flap Trismus Oral squamous cell carcinoma 

Introduction

Oral squamous cell carcinoma (OSCC) is the sixth most prevalent malignancy worldwide, and the most frequent malignant tumor of the oral cavity [1]. In Taiwan, OSCC ranks as the fourth most prevalent cancer in the male population and the sixth most prevalent cancer in both sexes [2]. Nearly 2.5 million individuals with OSCC have trismus, which results from betel nut chewing, and higher rates of mortality and recurrence exist in Taiwan [2]. However, research regarding the prognosis of patients with trismus is limited, and surgical challenges in OSCC need to be explored for a more comprehensive understanding of the problem.

Many considerations are necessary in planning surgical treatment strategies, including therapeutic resection, defect reconstruction, and functional restoration. Therapeutic resection usually adheres to the most recent guidelines [3], and surgery with adjuvant concurrent chemo- and/or radiotherapy remains the primary treatment for OSCC [4, 5, 6]. Defect reconstruction is a critical challenge because the oral cavity consists of complex three-dimensional anatomy [7]. The goal of reconstruction is the restoration of integrity and function. Ideally, postoperative radiation therapy should begin 6 weeks after surgical treatment. The delay between the operation and the start of adjuvant radiation therapy reduces its therapeutic effect [8]. Free flap reconstructions are increasingly being used to correct OSCC defects in recent decades [9], with survival rates rising to > 90% [10]. In contrast, functional restoration is also an important challenge and includes articulation, mastication, and swallowing function. Therefore, reduction of the duration of postoperative hospitalization is important and may influence the outcome of adjuvant therapy.

The most frequently used free flap in OSCC is the radial forearm free flap (RFFF) and the thinned anterolateral thigh cutaneous (ALT) flap [11]. The RFFF is a fasciocutaneous flap originating from the volar region of the forearm and is supplied by the radial artery and comitant venous pedicle. More specifically, the RFFF has high feasibility and a success rate, and donor site morbidity is low. In contrast, the ALT flap is the septocutaneous flap, which is based on musculocutaneous perforators from the descending branch of the lateral circumflex femoral artery [12]. Due to the musculocutaneous flap, the ALT flap maintains sufficient volume in soft tissue to reconstruct the defect and has been a benefit in large-defect reconstruction(s) with respect to the RFFF [13]. However, trismus, which results from oral submucosa fibrosis in OSCC reconstruction, increases surgical difficulty, including lesion resection, adequate surgical reconstructive volume, and healing time of the postoperative flap [14].

Thus far, no study has evaluated the utility of free flap reconstruction in a surgical healing time analysis of trismus patients with OSCC who regularly chew betel nuts. The purpose of this study was to compare the length of the hospitalization period between the two commonly used free flap reconstruction methods for OSCC patients. The investigators hypothesized that the ALT would be more beneficial than the RFFF. The specific aims of the study were to measure and compare the surgical healing period in the two flap reconstruction methods, and to assess relationships between other surgical wound recovery parameters, including inter-incisor distances (IIDs), operative time, gender, and WBC count.

Materials and methods

Patients and methods

To address the research purpose, the investigators evaluated surgical outcome in a group of OSCC patients who underwent surgical resection and reconstruction with free flap. The study population comprised all patients presenting for evaluation and management of flap recovery during the period between the date of operation with the two flaps and the date of full flap healing.

Patients with treated primary OSCC underwent surgical resection between 2010 and 2016 in the same medical center hospital. For inclusion in the study sample, the study inclusion criteria were as follows: (1) previously untreated oral cancer, (2) histologically proven squamous cell carcinoma, (3) reconstruction with the ALT or RFFF flap, (4) therapeutic resection and selective neck lymphatic dissection with or without adjuvant postoperative therapy, and (5) a history of betel nut exposure with the trismus problem of maximum inter-incisor distances (IIDs) < 5 mm. The exclusion criteria were as follows: (1) unavailable data regarding IIDs at initial recording and postoperative recording, (2) final pathological diagnosis of T3 or T4 lesion due to the inability to use RFFF, (3) history of treatment for other cancers, (4) contraindication for curative surgery, (5) distant metastasis, and (6) history of oral submucosa fibrosis and treatment via free flap.

Finally, we included 49 trismus patients, and IID was measured as the maximal distance between the edges of the incisors of the mandible and the maxilla at three points in time: before operation (initial IID), post operation 2 weeks, and post operation 6 months. The IID was expressed in millimeter, similar to the report by Dijsktra et al. [15]. Due to the trismus problem, tumor excisions were performed using mandibulectomy or the pull-through technique with the lymphatic nodal specimen. All patients were followed and registered in an institutional database corrected and updated with the patients’ most recent treatment condition. The follow-up duration was at least 2 years or until death by the endpoint of December 2017. The Ethics Committee of the Tri-Service General Hospital (Taipei, Taiwan) approved the study (Institutional Review Board protocol no: 2-107-05-021). Given the retrospective nature of the study and the use of anonymized patient data, requirements for informed consent were waived.

Surgical reconstruction was performed by the same group of experienced plastic surgeons; patients were transferred to the intensive care unit for flap monitoring after reconstruction, and then sent to the general ward for wound healing. After appropriate healing and restoration of basic function, the patients were discharged. These patients were candidates for reconstruction with RFFF or ALT flap independent of surgeon and patients’ preference. The reason for selection of the ALT flap was concern regarding the fine motor activity of the hand; the reason for selection of the RFFF flap was concern regarding the operative time. The donor site evaluation was performed before surgery using Doppler ultrasonography. Specifically, the radial forearm flap was surveyed using Doppler ultrasonography, and the Allen test was performed and the radial side was pressed to guarantee re-perfusion from the ulnar side to a healthy color within 15 s. The RFFF was dissected and reconstructed on the same operative day, and the skin graft from the anterolateral thigh region was used to cover the RFFF site. This study did not detect any complication or prolonged healing period in the skin graft. In contrast, the ALT flap was checked using Doppler ultrasonography with or without computed tomography angiography. After mapping and draping the perforators to penetrate the fascia in the medial or proximal one-third of the anterolateral thigh region, the ALT was dissected at the time of the therapeutic operation. After reconstruction, these patients were transferred to the flap care intensive critical unit, and the flaps were monitored according to physical appearance and handheld Doppler ultrasound probe monitoring. Surgical parameters were registered as multiple factors, such as flap reconstructive time, postoperative recovery days, patient survival, complications of flap healing, and data on serum white blood cell (WBC) count, were collected and analyzed to assess flap healing.

Flap recovery analyses

The important surgical parameters are primarily based on the flap recovery healing period and the incidence of postoperative complications. The primary comparison of recovery between the two flaps was the measurement of flap healing from the date of the operation to the date of discharge. Postoperative complications were also compared between the two flaps; fortunately, these patients experienced no major complications, such as flap crisis, thrombosis, or failure, similar to the success rate in general flap operation. However, minor complications at the surgical site were observed.

The other factors related to the flap recovery healing time were inter-incisor distances, flap operative time, WBC count, and the onset of leukocytosis; these were analyzed as indicators of flap recovery. The flap operative time is measured from the initiation of the plastic specialist’s procedure until full flap reconstruction. The WBC count referred to the number of white blood cells via blood exam. Normal WBC count in peripheral blood is within the reference range of 4300 to 10,800 WBC/mm3 [16]. Leukocytosis was defined as WBC count above the normal range in the blood. The chi-squared test was used to compare categorical variables of patient demographic profiles between the ALT and RFFF groups. The Kaplan-Meier method was used to calculate overall survival (OS), measured from the day of therapeutic surgery to the date of death or the last follow-up; this was used to evaluate survival rate stratified according to different flap reconstructions. Statistical analysis was performed by using commercially available statistical software (SPSS version 20.0, IBM Corporation, Armonk, NY, USA); p < 0.05 was considered statistically significant.

Results

Patient demographics

Demographic information of the entire patient cohort, including age, sex, population, histopathology T stage, N stage, treatment modality, and anatomical site, are presented in Table 1. Final histopathological results revealed 22 (44.9%) patients with pT1 status and 27 (55.1%) with pT2 status. RFFF reconstructions were performed in approximately 23 cases and ALT reconstructions were performed in 26. The reconstructed flap was divided into two sub-groups for comparative analyses with characteristic features (Table 2). Accordingly, no significant relationships were found between the reconstructed free flaps and sex, age, tumor stage, pathological T or N status, smoking habits, and initial inter-incisor distances via chi-square analysis. The follow-up period indicated no significant differences via independent t test. The mean (± standard deviation [SD]) follow-up period for all patients was 36.6 ± 19.6 months. The mean OS period was 57.8 ± 4.0 months among the 49 patients. According to Kaplan-Meier analysis, OS at 1, 3, and 5 years was 89.4%, 71.5%, and 67.7%, respectively. There was no statistically significant difference in OS between the two reconstruction groups.
Table 1

Patient demographic information

Characteristic

n (%)

Sex

 Male

42 (86)

 Female

7 (14.0)

Mean age, years, 53.96 (range, 31–76)

49 (100)

Tobacco exposure

 No

8 (16.3)

 Yes

41 (83.7)

Alcohol exposure

 No

17 (34.7)

 Yes

32 (65.3)

Preoperative inter-incisor distance 3.08 (range, 2–4)

49 (100)

Overall TNM stage

 I

20 (40.8)

 II

17 (34.7)

 III

5 (10.2)

 IV

7 (14.3)

T classification

 1

22 (44.9)

 2

27 (55.1)

N classification

 N0

37 (75.5)

 N1

5 (10.2)

 N2a

0 (0)

 N2b

7 (14.3)

Treatment

 Surgery only

19 (38.8)

 Surgery + radiotherapy

3 (6.1)

 Surgery + chemotherapy

12 (24.5)

 Surgery + concurrent chemoradiotherapy

15 (30.6)

Anatomical site

 Lip

2 (4.1)

 Retromolar trigone

4 (8.2)

 Gingiva

3 (6.1)

 Tongue 2

13 (26.5)

 Palate

3 (6.1)

 Buccal mucosa

22 (44.9)

 Mouth floor

4 (4.1)

Follow-up duration for all patients

 Mean 36.6 ± 19.6

49 (100)

 Median 34

 

 Range: 0–75

 

TNM, tumor, node, metastasis

Table 2

Characteristics of the patient sample, and sub-groups stratified according to reconstruction flap type

Characteristic

Flap

p

ALT

RFF

Age, years (mean ± SD)

51.5 ± 10.1

56.8 ± 8.4

0.081

Sex, male:female, n:n

22:4

20:3

0.815

Tumor stage

 T1

10

12

0.336

 T2

16

11

Nodal stage

 N0

21

16

0.371

 N1

3

2

 N2

2

5

Stage

 I

9

11

0.221

 II

12

5

 III

3

2

 IV

2

5

Cigarette

 Yes

22

19

0.850

 No

4

4

Alcohol

 Yes

17

15

 

 No

9

8

0.990

Follow-up period (months)

35.9 ± 19.8

37.2 ± 19.7

0.814

Initial IIDs (mm)

3.2 ± 10.4

3.0 ± 10.5

0.235

Data presented as mean ± SD or n, unless otherwise indicated. ALT, anterolateral thigh cutaneous; RFF, radial forearm free; IIDs, inter-incisor distances; TNM, tumor, node, metastasis

Flap recovery analysis

Reconstructed flaps were divided into two sub-groups for comparative analyses (Table 3) and the flap indicators were subsequently divided for recovery analysis. The mean number of hospitalization days for recovery from the flap surgery day to the day flap stability that was sufficient for discharge was 22.9 ± 7.2 in the ALT group and 27.8 ± 7.0 in the RFFF group, a difference that was statistically significant (p = 0.012). The mean WBC counts in the ALT and RFFF groups were 7428.9 ± 2454.9 WBC/mm3 and 9438.7 ± 3151.3 WBC/mm3, respectively, a difference that was statistically significant (p = 0.016). Two-week maximum IIDs were measured: 16.1 ± 0.8 mm in the ALT group and 7.0 ± 0.6 mm in the RFFF group. The ALT group had significantly wider mouth opening ability than the RFFF group. After 6 months of rehabilitation, these two groups exhibited similar IIDs. In flap operative time, the ALT operation was approximately 619.9 ± 250.1 min, while the RFFF was approximately 390.5 ± 108.9 min.
Table 3

Comparison of indicators in the recovery period according to reconstruction flap type

Indicator

Flap

p

ALT (n = 26)

RFF (n = 23)

IID at 6 months (mm)

12.5 ± 0.6

12.4 ± 0.06

0.675

IID at 2 weeks (mm)

16.1 ± 0.8

7.0 ± 0.6

0.000*

Hospitalization (days)

22.9 ± 7.2

27.8 ± 7.0

0.012*

WBC count (WBC/mm3)

7428.9 ± 2454.9

9438.7 ± 3151.3

0.016*

Flap operative time (min)

618.9 ± 250.1

390.5 ± 108.9

0.000*

Complication (rate)

3/26

3/23

0.873

Survival (dead/alive)

9/17

6/17

0.518

Mean survival (days)

52.6 ± 5.4

57.8 ± 5.8

0.554 (Log rank)

Data presented as mean ± standard deviation or n/n, unless otherwise indicated. *Statistically significant difference. ALT, anterolateral thigh cutaneous; RFF, radial forearm free; IID, inter-incisor distance; WBC, white blood cell

In analysis of the relationship with the hospitalization period (Table 4), we found that the 2-week postoperative IIDs in the ALT group were much larger than those of the RFFF group, and there was minimal correlation with the number of hospitalization days (r = − 0.327; p = 0.022). Additionally, there was no relation of other factors with the hospitalization period, including WBC count, initial IID, postoperative 6 months IID, patient sex, and flap operative time.
Table 4

Pearson correlation coefficients of hospitalization period

Variable

r

p

White blood cell count

0.131

0.368

Preoperative initial inter-incisor distance

− 0.018

0.905

Postoperative inter-incisor distance (2 weeks)

− 0.327

0.022*

Postoperative inter-incisor distance (6 months)

− 0.050

0.734

Sex

0.084

0.568

Flap operative time

0.211

0.146

*Statistically significant, but with inverse correlation

There were some minor complications in the two groups, while the success rate for the two groups was 100% without major complications (Table 5). There was no significant difference in the minor complication distribution between two groups using chi-square test (p = 0.050). The minor complication in ALT group was hematoma, and the complications in RFFF group were infection and dehiscence.
Table 5

Complications in the entire cohort, and sub-groups stratified according to reconstruction flap type

Complication

Flap

p

ALT

RFF

Minor complication

  

0.05

 Infection

0

1

 

 Dehiscence

0

2

 

 Hematoma

3

0

 

Data presented as n unless otherwise indicated. ALT, anterolateral thigh cutaneous; RFF, radial forearm free

Discussion

In this study, the utility of free flap reconstruction was evaluated in an analysis of surgery-related parameters of trismus patients with OSCC who regularly chew betel nuts. The major goal of this study was the comparison of surgery-related parameters between the two commonly used free flaps for reconstruction surgery in OSCC patients. The ALT method was hypothesized to be more beneficial than the RFFF method for reduction of the hospitalization period; moreover, it compared other surgical parameters between the two flap reconstruction methods. The results showed that the ALT group required a 1-week shorter hospital stay.

Additionally, we compared other factors related to the surgical healing period, and found that the 2-week postoperative IIDs in the ALT group were significantly larger than those in the RFFF group; this parameter moderately correlated with the number of days of hospitalization. In summary, the ALT flap provided elasticity and mouth opening ability in trismus patients and reduced wound recovery time.

Trismus related to oral submucosa fibrosis decreases the ability to open the mouth [15]; however, its exact pathogenesis remains unclear. The popular hypothesis is that fibrosis and hyalinization of the sub-epithelial tissues are believed to increase collagen synthesis or decrease collagen degradation [17]. Pathogenesis is triggered by a chemical irritant; the most well-known are the chemical constituents of the betel nut [18]. Trismus increases the challenge in the surgical release and approach, flap monitoring, and postoperative follow-up [19]. In this study, we performed sufficient release in thee submucosa fibrosis layer, and the defect was reconstructed via two different free flaps. Our results suggest that the ALT flap can resolve trismus immediately after operation; however, postoperative, long-term rehabilitation requires more intensive treatment and training [20, 21, 22].

The ALT flap has been the most frequently used flap reconstruction method over the past two decades; the flap provides a large amount of soft tissue and skin [11]. The ALT flap is a fasciocutaneous flap that is harvested from a site around the anterior thigh area overlying the septum between the rectus femoris and the vastus lateralis muscles [23]. Due to sufficient soft tissue, it is easy to manipulate the flap to adapt to the size and shape of the defect. Moreover, this useful free flap exhibits sufficient elasticity to tolerate elastic elongation. Therefore, the intraoral flap can be monitored using a transoral approach. However, one disadvantage of the ALT flap is excessive thickness in obese patients, while another is prolonged operative duration [24]. In our study, we used an adequate thickness of ALT flap that tolerated tissue elongation to provide the initial postoperative IIDs, and enhance the quality of flap care, including flap monitoring and flap suture line irrigation. Therefore, the increased initial postoperative IID facilitates flap care and reduces recovery times. Nevertheless, flap operative time was much longer than in the RFFF group.

Although the RFFF is also a fasciocutaneous flap, it does not contain as much soft tissue as the ALT flap. The flap is harvested from the volar area of the forearm and can provide a large amount of thin and pliable skin soft tissue [25]. Due to the reproducible vascular anatomy, the success rate and shorter operative times are advantages, and the reproducible vascular anatomy is one of the most popular free flap donor sites chosen [26]; however, it cannot provide a flap > 3 cm in thickness. In this study, we used the RFFF to treat OSCC defects and reduce operative duration. However, the thin reconstructive flap was unable to tolerate mouth opening to monitor the flap; this situation aggravated the difficulty of flap care.

OS is based on conventional OSCC nodal staging category and adverse features. Aside from that, survival requires a combination of current staging categories combined with other factors, such as pathological cell differentiation [27] and lymph node density [28, 29]. These factors require more comprehensive analyses. In our survival analysis, the type of flap reconstruction was not significantly related to OS.

This study had some limitations: first, it included a small sample size, which was associated with patient enrollment and poor cooperation during follow-up. In addition, the surgical outcome of functional tests for different flaps, such as quality of life, as well as swallowing and speech function, should be addressed in future studies. Notable study strengths were that we compared the commonly used flaps in OSCC reconstruction and investigated the challenge of trismus. Furthermore, we found co-related factors in the surgical healing period in patients with trismus; the IID was a related factor in reconstruction.

Conclusions

The ALT flap reduced hospitalization and the incidence of leukocytosis, and enhanced maximum 2-week postoperative IIDs in trismus patients, compared with the RFFF. Based on this reduction in the length of the hospitalization period, the ALT flap should be regarded as a first-line technique in OSCC reconstruction for patients with trismus. Future research that considers functional evaluation to compare predictive factors with larger sample sizes is warranted.

Notes

Funding

This study was supported by research grants from Tri-Service General Hospital, Republic of China (Grant Nos. TSGH-C106-004-006-008-S05, TSGH-C107-008-S06, TSGH-C108-007-008-S06, TSGH-C106-144, TSGH-C105-164, TSGH-C108-189), Ministry of National Defense, Republic of China (Grant No. MAB-106-090), and National Science Council, Taiwan, Republic of China (Grant No. MOST 105-2314-B-016-021-MY3).

This research was also supported by the Cancer Registry Group and Medical Records Room of Tri-Service General Hospital.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

The Ethical Committee of the Tri-Service General Hospital (Taipei, Taiwan) approved this retrospective study (institutional review board protocol no: 2-107-05-021).

Informed consent

Informed consent was obtained from all individual participants included in the study.

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Copyright information

© The Author(s) 2019

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  • Wei-Chin Chang
    • 1
    • 2
  • Ching-Fen Chang
    • 3
  • Chia-Mao Cheng
    • 4
  • Cheng-Yu Yang
    • 2
  • Yuan-Wu Chen
    • 1
    • 2
    Email author
  1. 1.Department of Oral and Maxillofacial SurgeryTri-Service General HospitalTaipei CityTaiwan, Republic of China
  2. 2.National Defense Medical CenterTaipei CityTaiwan, Republic of China
  3. 3.Department of Internal MedicineChina Medical University HospitalTaichung CityTaiwan, Republic of China
  4. 4.Department of DentistryTri-Service General HospitalTaipei CityTaiwan, Republic of China

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