Received: 16 August 2017 | Accepted: 20 December 2017

DOI: 10.1002/jso.24991

RESEARCH ARTICLE

Classification of tongue cancer resection and treatment

algorithm

Giuditta Mannelli MD1 | Francesco Arcuri MD2 | Tommaso Agostini MD2 |

Marco Innocenti3 | Mirco Raffaini MD2 | Giuseppe Spinelli MD2

1 Unitof Otorhinolaryngology−Head and Neck

Surgery, Department of Surgery and
Translational Medicine, University of Florence,
AOU-Careggi, Florence, Italy
2 Maxillo-Facial Surgery Unit, AOU-Careggi,
Florence, Italy
3 Department of Plastic and Reconstructive
Microsurgery, Careggi University Hospital,
Florence, Italy
Correspondence
Giuditta Mannelli, Otorhinolaryngology−Head
and Neck Surgery Unit, Department of
Surgery and Translational Medicine, University
of Florence, AOU-Careggi, Via Largo Palagi 1,
50134 Florence, Italy.
Email: mannelli.giuditta@gmail.com
Background and Objectives: Reconstruction of tongue cancer defects is challenging
due to the complex anatomy and physiology of the tongue. Here, we classify patterns
of tongue tissue loss and describe a treatment algorithm for achieving good functional
and oncologic outcomes.
Methods: We retrospectively reviewed 50 tongue squamous-cell carcinomas
surgically treated between January 2010-June 2015. Cancer resection and tongue
reconstruction were stratified according to the missing anatomical subunits.
Results: A type 1 defect is a unilateral and marginal defect, not crossing the midline, and
not extending to the posterior-third of the tongue. Type 2 involves the two-anterior-
thirds of the mobile body, not crossing the midline, without posterior-third
evolvement. Type 3 involves the two-anterior-thirds of the mobile body of the
tongue with contralateral extension. Type 4 extends to the tongue base. Type 5 defect
comprises any of the previous defects along with involvement of the floor of the
mouth. Type 2 and 3 defects were the most common. Microvascular reconstruction
was performed in 23 out of 50 patients. Complications included infection, partial
necrosis, dehiscence, and microvascular thrombosis.
Conclusions: Our classification system and treatment algorithm represent a reliable
method of addressing management of tongue defects.

KEYWORDS
functional and aesthetic outcomes, reconstructive options, tongue cancer, tongue defect
classification, tongue reconstruction algorithm

1 | INTRODUCTION and overall-survival depends on tumor stage, as per the guidelines of

Oral cavity malignancies accounts for 14% of all head and neck cancers
(HNCs).1–3 Although the tongue represents a unique anatomic region
where the routine detection of early-stage lesions should be possible,
the incidence of advanced-stage tumors (III-IV TNM stage)4 is still
around 30-35%. Moreover, there has been a significant increase of
60% of oral-tongue cancers in patients younger than 40 years of age,5,6
SM
Presented at: AAO-HNSF 2016 Annual Meeting and OTO EXPO in San Diego, on
Monday the 19th of September.
the American Joint Committee on Cancer (AJCC; 7th edition).4 Other
factors, such as the depth of tumor invasion, can also affect the
prognosis significantly.7
More than in other head and neck sites, primary surgical treatment
represents the main therapeutic option for malignancies in the oral
cavity. In assessing the treatment strategy, surgeons should attempt to
gain the best loco-regional control rate with due consideration to the
potential impact of such procedures on speech, swallowing, and
cosmetic outcomes. Immediate reconstruction should be performed
after primary tumor resection and its extent, together with the tongue

J Surg Oncol. 2018;1–8. wileyonlinelibrary.com/journal/jso © 2018 Wiley Periodicals, Inc. | 1

2 |
subsite involved, influences the severity of the subsequent functional
8,9
impairment.
Owing to advancements in microsurgical techniques, more
extensive resections are now possible in both young and old
patients.10 The appropriate selection of reconstructive techniques
should facilitate the healing of both donor and recipient regions, with
maximization of patients' capacity for rehabilitation.
Since 1983, the free radial forearm flap (FRFF) has been
considered the first choice for the restoration of soft tissue ablation
11
in the oral cavity, despite several disadvantages concerning the
donor site, including the sacrifice of radial artery. Recently, the
anterolateral thigh flap (ALTF), has challenged the superiority of
FRFF because it does not necessitate a skin graft and does not
involve the sacrifice of an artery or possible damage to the tendons
of the hand.12,13 Moreover, in case of extensive and complex
defects involving multiple anatomical and functional subunits, the
use of double flaps has shown objective benefits in the reconstruc-
tion.14–16
These patients are often left with a complex, large defect that
necessitates restoration of form to achieve successful rehabilitation.
However, recent publications have provided conflicting data regard-
ing functional outcomes after microvascular reconstruction of the
tongue, and there is little guidance in the literature on flap selection
for tongue reconstruction. Although a one-flap approach seems to be
preferred by most authors,17,18 we believe that treatment planning
should involve a more strategic approach with a wider variety of flap
options.
In the present study, we retrospectively analyzed 50 patients
affected by tongue squamous-cell carcinomas (TSCC), including
tongue base cancers. We described the use of a novel classification
system that simplifies the patterns of tongue tissue loss during
composite cancer resection and provide a decision algorithm for
immediate reconstruction.
The main aim was to elucidate the indications for the use of
different reconstructive techniques and flaps, in both early and
advanced tongue cancers, based on our personal experience and the
latest literature updating.
2 | M E TH O D S
2.1 | Study population
Between January 2010 and June 2015, a total of 62 patients affected by
TSCC were surgically treated at the Maxillo-Facial Unit of Florence. All
the participants signed an informed consent agreement before
undergoing surgery. The indications for treatment included the
presence of a tongue mass, either of the tongue body or of the tongue
base, with a pre-operative biopsy report indicative for squamous-cell
carcinoma with or without clinical evidence of cervical lymph node
metastasis. The study was approved by the local institutional review
board (IRB). All patients were reviewed and retrospectively restaged in
accordance with the AJCC4 and World Health Organization (WHO;
2005)19 guidelines.
MANNELLI ET AL.
The exclusion criteria were as follows: previously treated for
head and neck cancer; previously undergone any head and neck
surgical procedures; previously received radiotherapy and/or
chemotherapy; did not consent to be enrolled in the study; or
incomplete charts.
Patient, tumor, and treatment characteristics were extracted the
patients' records. During the follow-up, speech, swallowing, and
cosmetic evaluations were performed at 1, 3, 6, and 12 months after
the operation. Speech evaluation was performed using a numeric scale
as follows: normal = 4, intelligible = 3, and slurred speech = 2, trache-
ostomy required = 1. Swallowing function was classified using the
following scale: normal = 4, soft = 3, liquid = 2, and requiring nasogas-
tric or gastric feeding tube (NGFT or GFT) = 1. Patients rated their own
appearance using the following scale: excellent = 4, good = 3, fair = 2,
and poor = 1.
2.2 | Surgical classification
The mobile body of the tongue can be dived into three segments.
The anterior and middle segments are divided by the median
raphe, which represents a physiological barrier o tumor spread.
Meanwhile, the tongue base represents the posterior third of the
tongue, including the circumvallate papillae and its lymphatic tissue
(Figure 1a).
Our novel classification system for tongue defects focuses on the
functional subunits that require reconstruction. It is based on intra-
operative findings of tongue defects, which we classified into five
groups in ascending order of reconstructive complexity:
1. Type 1 defect: a unilateral and marginal defect, rarely involving the
tip of the tongue without crossing the midline, not extending to
more than one third of the mobile tongue body and not extending to
the posterior third of the tongue (Figure 1b);
2. Type 2 defect: a unilateral defect not crossing the midline without
posterior third involvement, extending to more than one third of the
tongue (Figure 1c);
3. Type 3 defect: a defect that involves the two anterior thirds of the
mobile body of the tongue with contralateral extension
(Figure 1d);
4. Type 4 defect: extends to the tongue base, and is further divided
into variant 4A, involving less than 50% of the tongue base, and
variant 4B, involving more than 50% of the tongue base (Figure 1e);
5. Type 5 defect: any type of defect along with involvement of the
floor of the mouth without (5A)/with bone resection (5B)
(Figure 1f).
Subsequently, the choice of reconstruction technique in our
algorithm was determined by the estimated volume of tongue to be
replaced, with the aim of restoring the tongue's natural form and
volume, and preserving its remaining mobility in order to ensure a good
functional outcome.
Under this system, type 1 and 2 defects mainly require restoration
of the tongue form, considering that more than 50% of the mobile body
MANNELLI ET AL.
| 3

FIGURE 1 A, Schematic representation of the three segments of the tongue body, each in turn divided along the median tongue raphe.
The tongue base belongs to the oropharynx, while the mobile body of the tongue belongs to the oral cavity; B, Example of type 1 defect;
C, Example of type 2 defect; D, Example of type 3 defect; E, Example of type 4 defect; F, Example of type 5 defect

can be preserved with good following functional expectations. In Kruskal-Wallis test was used for statistical comparisons with the
contrast, type 3 and 4 defects require wide tongue resection, causing software program STATA version 12.1 (StataCorp. 2011. Stata
complex tissue loss. In such cases, more than 50% of the whole tongue Statistical Software: Release 12, College Station, TX, StataCorp LP),
body needs to be replaced, with a significant reduction in swallowing and a value of P < 0.05 was considered statistically significant.
and speech function in cases of wide tongue base resection (type 4B).
Type 5 defects, the main reconstructive issue is to keep saliva
3 | RESULTS
secretions from entering the neck space, together with the other
functional and aesthetic goals. Here, tumor involvement could could
Twelve out of sixty-two patients were excluded from our study: seven
include the mandible bone, and any reconstruction should attempt to
had already undergone a head and neck surgical procedure, or were
restore its profile and function as well.
affected by cancer relapse or second primary head and neck tumor
All head and neck surgical procedures were performed by a senior
(11%); two had already received chemo-radiotherapy for other
surgeon (G.S.), and tongue cancer resection included neck dissection in
malignancies (one for breast cancer and one for leukemia) (3%); one
accordance with AJCC stage.4
did not give his consent to be enrolled in the study (2%); and two had
We did not perform any type of dynamic tongue reanimation, nor
incomplete charter notes (3%). Thus, a final number of 50 patients
did we make use of gastro-omental free flap along with free gracilis
were included in our study.
muscle flap, although these have been reported to be suitable for
Type 2 defects were predominant (n = 17), followed by type 3
achieving functional dynamic tongue reconstruction.20,21
(n = 15), type 1 (n = 10), and type 4 (n = 5), while type 5 defects were the
most uncommon (n = 3). Patients received either pedicle flap or free flap,
while 11 patients (22%) did not undergo any flap reconstruction; four
2.3 | Statistical analysis
patients (8%) underwent double flap reconstruction.
Categorical variables were calculated in terms of frequencies and Type 1 defects (n = 10; 20%) were reconstructed by primary
percentages for all of the patients included in the study. The closure. Type 2 defects (n = 17; 34%) were reconstructed using the
4 | MANNELLI ET AL.

following techniques: eight suprafascial-ALTF (47%), six RFFF (35%),
one facial artery musculo-mucosal flap (FAMM; 6%), and one
pectoralis major myocutaneous flap (PMMCF; 6%); one patient did
not receive any reconstruction because of severe co-morbidities (6%).
Type 3 defects (n = 15; 30%) were reconstructed using the following
methods: nine received ALTF flaps (53%), five RFFF (40%), and one
PMMCF (7%). Of the five patients with type 4 defects (10%), two
received rectus abdominis muscle free flaps (RAMFF) (40%) and three
received double flaps: myocutaneous-ALTF flap plus RFFF (60%). Of
the three patients with type 5 defects (6%), one received a RAMFF
(33%), one with severe co-morbidities underwent a pedicle flap
reconstruction (PMMCF) (33%), and one received double flaps,
PMMCF plus RFFF (33%).
There were two complete and one partial flap failures out of 43
flaps harvested, giving a success rate of 93%. The overall rate of post-
operative complications was 16%. The mean number of reoperations
per patient was 0.06. Specifically, both cases of complete flap necrosis
required surgical revision, and one PMMCF and one ALTF were
harvested; in addition, one out of the three wound complications
needed a surgical revision. These details together with those of the
complications are listed in Table 1.
The mean follow-up duration was 27.24 ± 14.71 months (95%
confident interval [CI] 23.02-31.47, range 0-60, median 25), four
patients (8%) experienced loco-regional recurrence, while two patients
died from disease (4%) and one from immediate post-operative
complication (2%). The overall survival (OS) rate was 94% and the
disease-free survival (DFS) rate was 80%.
Forty-nine patients were evaluated at at 1, 3, 6, and 12
months after surgery regarding functional outcomes. At one year
post-operative follow-up, thirty-two patients (65%) achieved normal
speech, 13 patients (26%) achieved intelligible speech, and 4 (9%) had
slurred speech. None of the patients required permanent tracheos-
tomy. Compared to type 4 and 5 patients, type 1 and 2 patients had
significantly better speech recovery (P < 0.05), where none of them
underwent adjuvant radiotherapy. In the swallowing assessment, 29
patients (59%) were able to eat normally, 14 patients (29%) managed a
soft diet, and six patients (12%) were dependent on a liquid diet. There
was no significant difference concerning swallowing function among
the five groups (P = 0.39). The aesthetic results were rated excellent in
28 patients (58%), good in 13 patients (28%), and fair in eight patients
(14%). There was no statistical significant difference among the groups
(P = 0.76).
4 | DISCUSSION
The ideal tissue for tongue reconstruction should be versatile in
design, adequate in tissue stock, provide consistent texture with
minimal donor site morbidity, and ensure large and long pedicle
feeding of different tissue types; further, its harvesting should be
easy, fast and safe. Because of these numerous requirements, the
surgical management of tongue cancer is challenging, as it is
influenced by not only the particular anatomy and physiology of the
tongue, but also by specific donor site characteristics and the
patient's expectations. In fact, the tongue represents one of the most
difficult structures of both oral cavity and oropharynx to reconstruct,
because of its central role in speech, swallowing, and airway
protection.22 Each tongue subunits (see Figure 1a) plays a role in

TABLE 1 Reconstructive details and complication of the 50 enrolled patients

Defect type 1 Defect type 2 Defect type 3 Defect type 4 Defect type 5 Total (%)
No. of cases (%) 10 (20) 17 (34) 15 (30) 5 (10) 3 (6) 50 (100)
Primary closure (%) 10 (100) 1 (6) None None None 11 (22)
Pedicle flap (%) None 2 (12) 1 (7) None 1 (33) 4 (8)
Free flap (%) None 14 (82) 14 (93) 2 (40) 1 (33) 31 62)
Double flaps (%) None None None 3 (60) 1 (33) 4 (8)
Partial flap loss (%) None 1 (6) None None None 1 (2)
Complete flap loss (%) None None 1 (7) 1 (20) None 2 (4)
Hemorrhage (%) None 1 (6) None None None 1 (2)
Wound infection (%) None None None 1 (20) None 1 (2)
Wound dehiscence (%) None None 1 (7) 1 (20) None 2 (4)
Other complications (%) None None None None 1 IMA* (33) 1 (2)
Total complications (%) None 2 (12) 2 (13) 3 (60) 1 (33) 8 (16)
NGFT removal (days) Mean 1 ± 0.67 Mean 4.41 Mean 5.87 Mean 10.40 Mean 13.00 Mean 5.28
SD ± 1.18 SD ± 1.30 SD ± 2.88 SD ± 2.65 SD ± 3.52 SD
Tracheostomy tube Mean 0.5 Mean 3.53 Mean 3.93 Mean 8.20 Mean 9.67 Mean 3.88
removal (days) ± 0.71 SD ± 1.37 SD ± 1.03 SD ± 3.96 SD ± 2.08 SD ± 2.97 SD
Hospital stay (days) Mean 2.50 Mean 6.59 Mean 7.73 Mean 12.20 Mean 15.67 Mean 7.22
± 0.53 SD ± 1.18 SD ± 1.58 SD ± 3.56 SD ± 2.08 SD ± 3.75 SD
MANNELLI ET AL.
determining tongue form, volume, and action. Speech and swallow-
ing recovery requires large volumes of reconstructed tissues for
minimal scarring, and residual bulk is needed to compensate for long-
term shrinkage.9,23,24
Therefore, reconstructive options should attempt to maintain
23–31 32–35
mobility or to provide bulk. Since 1979, when Ariyan
developed the pectoralis major myocutaneous flap (PMMCF),36 the
major contribution to head and neck reconstruction has been
microvascular free tissue transfer. Concerning reconstruction choice,
most authors focused mainly on single flap or on a comparison
between two different flaps for the reconstruct a limited range of
tongue defects18,24,30,37–39; here, through a retrospective review of a
single-center case series in accordance with the latest literature
updated findings, we propose an algorithm for both tongue resection
options and reconstructive selections based on tumor extent and
tissue loss (Figures 2 and 3).
For type 1 defect patients, primary closure was the best choice to
achieve restoration of the primary tongue form after a “wedge-shaped
tongue resection,” considering that the mobility and volume were not
affected. These patients experienced a complete recovery of
functions, with a normal speech and swallowing in the early follow-
up period. None complained of any cosmetic dissatisfaction. Similar
functional results were recorded in type 2 defect patients. In these
patients, surgeons had to manage a wider tongue resection, “hemi-
glossectomy,” involving the mobile portion of the organ, but without a
FIGURE 2 Proposal of guidelines for tongue cancer resection design based on our surgical classification
| 5
consistent tissue lost. This allowed the use of thin free flaps (eight
suprafascial-ALT and six RFF; 82% of cases), which have good pliability
and versatility; they restore almost half of the tongue volume loss
while preserving its complex mobility.24,39,40 In case of contra-
indications for microsurgery, accordingly to literature, pedicle flaps
such as PMMC and FAMM, or submental artery island flap (SAIF) might
be considered as good reconstructive options for this type of
defect.41–44
In comparison to type 2 defects, patients with type 3 defects
require more extensive and complex resection, involving more than
50% of tongue volume (“Extended hemiglossectomy”). In other words,
multiple tongue subunits are removed, sometimes requiring man-
dibulotomy or lip split for access, thus affecting form and mobile
function considerably. Here, the surgeons' aim was first to provide bulk
in order to ensure a good swallowing recovery; maintaining tongue
articulation ability was secondary. ALT flap with its muscular
component provides large skin territory together with high reliability,
versatility, and bulkiness when combined with the vastus lateralis or
the tensor fasciae latae muscles.24 ALTFF and RFFF can act not only as
spacers, but also allow the remaining tongue a certain degree of
movement, confirmed by a median time of tracheostomy tube and
NGFT removal of 4 and 5 days, respectively, with a median hospital
stay of 7 days. Five patients out of 15 had normal speech (33%) and
only one patients needed to maintain liquid diet (6%). Pedicle flaps
still represent a good alternative reconstructive options when
6 |
FIGURE 3 Flowchart of algorithm for tongue defect classification and surgical reconstructive options
contraindications to free flaps exist, and in case of free flap failure,
PMMCF is a good salvage option.
Type 4 and 5 defects require multiple approaches, because of the
almost complete tongue involvement and the need to avoid
communications between the oral cavity and neck spaces. Here,
mandibulotomy or lip split for access, as well as mandibulectomy in
case of mandible invasion (Figure 3), were always performed. For
instance, type 4 defects or type 5 soft tissue defects required very
bulky flaps; tongue resections were mainly involved subtotal
glossectomy or total glossectomy, which were often reconstructed
by free bulky soft tissue transfer such as myocutaneous-ALTFF or
rectus abdominis muscle free flaps (RAMFF), in accordance with recent
45
publications. However, the complexity of type 5 defects arises from
the presence of through-and-through defects that require composite
resection of the tongue, floor of the mouth, cheek, and/or the
mandible. In these cases, fibula osteocutaneous free (FOSCF) flap has
been commonly proposed as the main choice for reconstruction, but
due to the limitations in harvesting soft tissue and skin along the fibula
bone, combined RFFF, or ALTF is usually performed instead.15,46–48
In summary, we recorded a final complication rate of 16%, median
tracheostomy tube removal time of 4 day, median NGFT removal time
of 5 days, median hospital stay length of 7 days, and an updated DFS
rate of 80% during a median follow-up time of 25 months. These
findings suggest that our novel classification system and treatment
algorithm is a consistent and reliable method of addressing tongue
defects by focusing on both oncologic and functional outcomes.
5 | C ONC LU SI ON
Our study identified a strategic approach for different types of tongue
defects, represented by a classification system and treatment algorithm
MANNELLI ET AL.
based on subunit reconstruction, which has ensured good final
functional outcomes comparable to other studies49,50 (Figures 2 and 3).
This algorithm could be a useful tool for patient counseling and
treatment selection, which might allow a more tailored patient care
protocol together with a high success rates in terms of oncologic,
functional, and aesthetic results.
We have shown that the use of double flaps, whether pedicle and
free or two free flaps, achieved optimal functional outcomes by
allowing wide and complex cancer resection. Such a combination
permitted better three-dimensional multiple subunits reconstruction
and better rehabilitation. However, further research is needed to
elucidate the relation between the incidence of complications and the
specific characteristics of the reconstruction technique.
ORCID
Giuditta Mannelli http://orcid.org/0000-0001-7079-3964
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SYNOPSIS

The main aim of this original article was to elucidate the indications for the use of different reconstructive techniques and flaps, in both early and
advanced tongue cancers. A treatment algorithm for managing tongue cancer with/without oral cavity floor defects and the subsequent
reconstruction was developed. Our classification system and treatment algorithm of tongue defects represent a reliable method of addressing
management of tongue cancer patients, with good oncologic and functional outcomes.