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Surgical Oncology xxx (2011) 1e10

Contents lists available at ScienceDirect

Surgical Oncology
journal homepage: www.elsevier.com/locate/suronc

Review

Mandibular conservation in oral cancer


Latha P. Rao a, Mridula Shukla c, Vinay Sharma b, Manoj Pandey b, *
a
Department of Oral & Maxillofacial Surgery and Cleft & Craniofacial Surgery, Amrita School of Dentistry, Amrita Institute of Medical Sciences, Kochi, India
b
Department of Surgical Oncology, Institute of Medical Sciences, BHU, Varanasi 221005, India
c
Department of Pathology, Institute of Medical Sciences, Banaras Hindu University, Varanasi, India

a r t i c l e i n f o a b s t r a c t

Article history: Surgery is one of the established modes of initial definitive treatment for a majority of oral cancers.
Accepted 21 June 2011 Invasion of bony or cartilaginous structures by advanced upper aero-digestive tract cancer has been
considered an indication for primary surgery on the basis of historic experience of poor responsiveness
Keywords: to radiation therapy [1]. The mandible is a key structure both in the pathology of intra-oral tumours and
Mandibular conservation their surgical management. It bars easy surgical access to the oral cavity, yet maintaining its integrity is
Mandibular preservation
vital for function and cosmesis. Management of tumours that involve or abut the mandible requires
Mandibular invasion
specific understanding of the pattern of spread and routes of tumour invasion into the mandible. This
Marginal mandibulectomy
Segmental mandibulectomy
facilitates the employment of mandibular sparing approaches like marginal mandibulectomy and
Oral squamous cell carcinoma mandibulotomy, as opposed to segmental or hemimandibulectomy which causes severe functional
Oral carcinoma problems, as the mandibular continuity is lost. Accurate preoperative assessment that combines clinical
examination and imaging along with the understanding of the pattern of spread and routes of invasion is
essential in deciding the appropriate level and extent of mandibular resection in oral squamous cell
carcinoma. Studies have shown that local control rates achieved with marginal mandibulectomy are
comparable with that of segmental mandibulectomy. In carefully selected patients, marginal man-
dibulectomy is an oncologically safe procedure to achieve good local control and provides a better quality
of life. This article aims to review the mechanism of spread, evaluation and prognosis of mandibular
invasion, various techniques and role of mandibular conservation in oral squamous cell carcinoma.
Ó 2011 Elsevier Ltd. All rights reserved.

Contents

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
Materials and methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
Mechanism of mandibular invasion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
Prediction of mandibular invasion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
Clinical evaluation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
Radiological evaluation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
Intraoperative evaluation of mandibular invasion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
Histopathological examination . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
Segmental vs. marginal mandibulectomy/mandibular preservation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
Prognosis in cases with mandibular invasion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
Conflict of interest statement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
Uncited references . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
Authorship statement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00

* Corresponding author. Tel.: þ91 542 2309511; fax: þ91 542 2361014.
E-mail address: manojpandey@vsnl.com (M. Pandey).

0960-7404/$ e see front matter Ó 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.suronc.2011.06.003

Please cite this article in press as: Rao LP, et al., Mandibular conservation in oral cancer, Surgical Oncology (2011), doi:10.1016/
j.suronc.2011.06.003
2 L.P. Rao et al. / Surgical Oncology xxx (2011) 1e10

Introduction preservation,’ or ‘mandibular conservation’, or ‘ segmental man-


dibulectomy’, or ‘marginal mandibulectomy’ and ‘oral cancer’, or
In the past it was standard practice to resect mandible as part of ‘oral squamous cell carcinoma’, or ‘carcinoma of the oral cavity’. The
the excision of many intra-oral cancers. Initially it was thought literature review was carried out till June 2011. The following string
necessary for adequate tumour clearance [2e4]. One of the pioneers was used for literature search:((mandible OR mandibular) AND
to study the involvement of mandible in oral cancers was Pan- involvement) AND ((cancer OR carcinoma OR neoplasm OR tumor
agopoulos (1959), he found mandibular involvement in 12/48 cases OR tumour) AND (oral OR head OR neck))
and proposed that the bone involvement in oro maxillary tumours
occur by extension of the neoplasm through nutrient channels [5]. Results
His observations were based on demonstration of tumour cells in
Volkman’s canal in few cases. Later on, despite the histological proof The search revealed 330 articles. Abstracts of all articles were
that many of the mandibles sacrificed were uninvolved [6,7], reviewed to identify the relevant studies, by this process, 76 full
segmental or hemimandibulectomy remained the mainstay of articles of studies thus identified were then obtained and back
surgical treatment for oral cancers adjacent to mandible because it references were checked. Of these 92 articles, only 6 were listed as
provided excellent exposure and easy closure of the surgical defect. clinical trials, no randomized controlled trials were identified
The functional and cosmetic consequences associated are devastating (chart 1). The inclusion criteria was the study should be on oral
to the patients due to impairment of occlusion, mandibular deviation, squamous carcinoma, should be dealing with either identification
overall decreased range of motion, temporomandibular joint pain, of mandibular invasion preoperatively or dealing with mandibular
poor contour of the symphysis and diet restricted to soft foods. The preservation and their results in humans. The articles which were
mandible is critical with respect to dentition and mastication, speech, not directly dealing with mandibular involvement or conservation
and swallowing and maintaining a patent airway. With improvement or preservation in oral squamous cell carcinoma, were excluded
and advances in the imaging as well as reconstruction techniques the from the review. The articles on mandibular excision for tumours
balance has swung in favor of mandible-sparing surgeries, where the other then oral cancer, benign diseases and non-human studies too
results are cosmetically and functionally superior. were excluded.
Clinical evaluation and preoperative radiological studies have
been used to evaluate bony invasion and to decide on the extent of Mechanism of mandibular invasion
mandibulectomy. Understanding of the mechanism of invasion and
spread within the bone, and changes associated with loss of teeth Carcinoma of the mandibular region is defined as carcinoma
is crucial in the successful management of the tumours in close arising from the mandibular alveolar ridge, lower buccal sulcus,
proximity to mandible. sublingual sulcus or mandibular retromolar trigone [8]. It had long
This literature review was carried out to assess the role of been assumed that oral squamous cell carcinoma had the potential
mandibular preservation in case of carcinomas in close proximity to to spread via the lymphatics within the mandibular lingual peri-
the mandible and the correlation between clinical and radiological osteum [9]. Composite resection of oral cancer with en bloc
findings in such carcinomas. resection of a segment or hemi mandible with neck node dissec-
tion was the main stay of treatment for oral squamous cell carci-
Materials and methods noma to allow complete extirpation of tumour [2,10,11]. It was also
felt that involvement of the inferior dental canal or perineural
A detailed Pubmed (Medline) search was made using key words spread adversely influenced the possibility of a limited surgical
‘mandibular involvement’, or ‘mandibular invasion’, or ‘mandibular approach [12,13].

Chart 1. Showing the result of literature search at a glance.

Please cite this article in press as: Rao LP, et al., Mandibular conservation in oral cancer, Surgical Oncology (2011), doi:10.1016/
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L.P. Rao et al. / Surgical Oncology xxx (2011) 1e10 3

In 1971, Marchetta first challenged the concept of periosteal Clinical evaluation


lymphatics for mandibular invasion and attempted the first
mandibular conservation procedure [4,6]. It was thought that the A detailed clinical examination is important in evaluating the
oral cavity carcinoma travels along the surface mucosa and the tumour invasion (Fig. 1). Clinical assessment of mandibular invasion
submucosal soft tissues until it approaches the attached gingiva is performed by bimanually assessing the mobility of the tumour
where tumour cells may come in contact with the periosteum of mass in relation to the mandible or fixity of the tumour to mandible.
the mandible. In the dentate patient, tumour cells were thought to Inspection and palpation of the tumour and adjacent structures
migrate through the periodontal ligament spaces into the mandible usually pick up additional signs of mandibular invasion namely,
[14,15]. In the edentulous patient, the tumour cells migrate onto the cortical thickening, symptoms of inferior alveolar nerve paraes-
occlusal surface of the alveolus and enter into the mandible via thesia, and bony irregularities and pathological fractures if any
dental pits [7,16e19]. McGregor and MacDonald [10] reported that [29,30]. According to reported literature, clinical evaluation carries
the inferior alveolar nerve could also be invaded and therefore a sensitivity ranging from 32%e96% [6,13,20,25,27,29,31e34].
should be resected along with the mandibular canal during Several studies had shown preoperative clinical assessment as
a marginal mandibulectomy. the primary method for determining mandibular invasion [29,35].
With increasing understanding of disease spread and biological But the clinical assessment of large oral cancers especially in the
behaviour of oral cancer it is now clear that majority of the spread presence of trismus due to submucous fibrosis related to tobacco
to mandible occurs by direct infiltration of the tumour through and betel nut chewing [36,37] or due to pterygoid or masseter
alveolar ridge or lingual cortical plate [11,17,18]. It has also been muscle involvement that precludes bimanual palpation of the
noted that tumours enter at the point of abutment. Histological mandible, can sometimes be inaccurate and therefore unreliable.
studies of the tumourebone interface have revealed that the site Similarly it is not possible to detect subtle cortical invasion with
of tumour entry into the mandible entirely depends on the loca- clinical examination alone [38,39]. A careful clinical and radiological
tion of the tumour in relation to the jaw; the alveolar crest in case correlation is required to achieve the ultimate goal of not sacrificing
of carcinomas of the alveolar mucosa or the lingual cortical bone any more bone than needed to remove the entire tumour.
in the event of tumours lying lingual to the mandible and peri-
neural spread occurred only in case of advanced tumours [13]. Radiological evaluation
Brown [17] and Brown et al. [18], stated that inclusion of the
neurovascular bundle in the marginal resection is not necessary. Controversy still exists about the best way to image the mandible
Other less common routes of entry into the mandible have been in the management of oral cancer when there is a chance that
described such as via the mental and mandibular canals or the a resection of the mandible will be required as part of the treatment.
lower border of the mandible which can be invaded by direct The literature review showed that there is no single investigation
spread from cervical lymph nodes. Brown [19] studied the that can predict whether tumour has invaded the mandible with
mechanisms of cancer invasion of the mandible, and concluded 100% reliability (Table 1).
that there is no preferred pathway of tumour entry into the Radiologically, plain films, orthopantomograms (OPG), computed
mandible. He reported that tumours enter the mandible at the tomography (CT) scans, magnetic resonance imaging (MRI) and bone
point of abutment which is related to the site of the primary scans have been used with varying degrees of accuracy [40].
tumour. It has always been believed that mandible could be Panorex radiographs play an important role in the detection of
preserved if there is normal tissue intervening between tumour bone invasion by oral carcinoma especially in determining the
and the bone [6,20,21]. superioreinferior extent of the tumour in the bone, which is one of
Earlier studies on bone destruction by squamous cell carci- the most important factors influencing the selection between rim
nomas on or adjacent to the lower jaw have generally dealt with and segmental resection of the mandible (Fig. 2) [29,32,41e44].
large tumours and preoperatively irradiated specimens [22,23]. As They also represent the mandible in a way that is easy to extrap-
the early stage of bony involvement can be considered to be olate to the clinical situation and is therefore useful for planning the
amenable to mandible-sparing surgery, detailed knowledge of the surgical procedure [45]. Nakayama et al., (1999) advocated the use
growth patterns in tumours that have not yet completely destroyed of panoramic radiography combined with intra-oral radiography as
the mandibular bone is mandatory [13]. the initial imaging modality to determine the extent of supero-
inferior invasion of the mandible in gingival carcinoma [43].
According to Hong et al. (2001) when deciding the required
Prediction of mandibular invasion anterioreposterior limits of resection, among the different kinds of
imaging modalities, intra-oral periapical films with the paralleling
There is no single imaging technique that can accurately predict technique seem to provide the most valuable information, due to
mandibular invasion in oral squamous cell carcinoma. From their fine anatomical detail [46]. But the panorex and intraoral
a treatment perspective, it is crucial to determine the bone radiographs carry the disadvantage of not detecting early invasion
involvement caused by these tumours and, more importantly, the of mandible with less than 30% of mineral loss [47,48]. The inter-
extent of bone involvement, since an underestimation may lead to foraminal area is difficult to assess by panorex radiographs due to
a partial resection, resulting in local recurrence and potential the superimposition of cervical vertebrae.
metastasis [24]. As a consequence, surgeons are often inclined to CT scan has become standard technique for staging malignant
perform segmental resections to avoid ‘undertreatment’, i.e. posi- tumours of the head and neck region. It is a sensitive method of
tive resection margins, which is reflected in high percentages assessing squamous cell carcinoma of mandibular region in terms of
(35e78%) of resected mandibles with no evidence of mandibular its size, location, spread in the bone as well as soft tissue & regional
invasion, resulting in considerable cosmetic and functional defects lymph node involvement [27,34,49,50]. With axial & coronal CT scans
[7,25e28]. even subtle tumour invasions of angle and ramus of the mandible can
So a careful correlation of clinical and imaging findings is war- be detected (Fig. 3). Because of the ‘ partial volume’ effect in the curved
ranted for the assessment of mandibular invasion and setting the bony surfaces as in anterior mandible and alveolar processes, and
bony margins of resection. The mandibular involvement is further metal artifacts, the specificity of CT scan remains low [51]. But with
assessed intraoperatively. latest 128 slice CT scans, the 3D reconstruction and planning of the

Please cite this article in press as: Rao LP, et al., Mandibular conservation in oral cancer, Surgical Oncology (2011), doi:10.1016/
j.suronc.2011.06.003
4 L.P. Rao et al. / Surgical Oncology xxx (2011) 1e10

Fig. 1. Clinical photograph showing the lesions, A) Superficial lesion of the buccal mucosa extending to retromolar trigone, B) Small lesion in the gingivobuccal sulcus, C) Ulcer-
oinfilterative lesion in the gingivobuccal sulcus extending on to the alveolus, D) Extensive lesion on the gingivo buccal sulcus with involvement of alveolus and mandible.

surgical margins have become more accurate (Fig. 3). The cone-beam ‘hot spots’ on bone scan thus detecting even periosteal involve-
CT and dentascan have shown promising results in identification of ment. But as the osteoblast activity can be high in osteomyelitis,
mandibular invasion by oral carcinoma [52e57]. children, fractures, or even periodontal diseases, the specificity of
MRI scan is superior to CT scans as it detects early soft tissue and bone scintigraphy is rather low. Several studies have reported on
medullary involvement and not as effected by metal artifacts high sensitivity & low specificity of bone scans [17,25,27,32,63].
[58,59]. However it is less reliable in evaluation of cortical bone Schimming et al.(2000) reported 100% sensitivity and 91.6% speci-
involvement because of lack of signal from cortex secondary to its ficity for computer-aided 3-D 99mTc-DPD-SPECT(Technetium-
low number of mobile hydrogen ions [60,61]. Imaizumi et al.(2006) Dicarboxy propan-single photon emission CT) and conventional
reported on low specificity of MRI scan to detect mandibular 99m Tc-DPD-SPECT in their comparison of these imaging modali-
cortical invasion and inferior alveolar canal involvement [62]. The ties with clinical examination, panoramic radiography, and CT scan
large number of false positive results obtained with MR imaging in in the assessment of mandibular bone invasion by squamous cell
contrast to CT scan seemed to be attributed to chemical shift arti- carcinoma in 50 cases [64].
facts induced by bone marrow fat. Namely, it was considered that The various studies comparing the effectiveness of various
the black line of the cortex adjacent to the tumour mass was investigative modalities in detecting mandibular invasion in oral
obscured by spatial misplacement of fat, or severe periodontal squamous cell carcinoma have failed to demonstrate 100% accuracy
disease or secondary changes from tooth extraction. MR imaging with any one technique [34,50,65,66]. Results of these studies show
often showed the tumour and the surrounding inflammation in the superior results when the data from different imaging techniques is
bone marrow with similar signal intensity, resulting in over- correlated with the clinical findings [67].
estimation of the tumour extent. Brown and Lewis eJones (2001) in their review of different
Bone scintigraphy is generally considered as the most reliable investigative modalities commented that the decision to resect the
method of detecting bone invasion & distant metastases (Fig. 4). mandible as part of the management of oral cancer should be taken
Increased bone turnover in squamous cell carcinoma gives rise to on the evidence of clinical examination, intra-operative periosteal

Please cite this article in press as: Rao LP, et al., Mandibular conservation in oral cancer, Surgical Oncology (2011), doi:10.1016/
j.suronc.2011.06.003
L.P. Rao et al. / Surgical Oncology xxx (2011) 1e10 5

Table 1
showing sensitivity and specificity of various radiological techniques in detecting bony invasion in various series.

OPG CT MRI Scintigraphy

Sensitivity (%) Specificity (%) Sensitivity (%) Specificity (%) Sensitivity (%) Specificity (%) Sensitivity (%) Specificity (%)
78 88 89 79 Weisman & Kimmelman (1982) [25]
57 92 O’Brien et al., (1986) [31]
100 88 96 54 Imaizumi et al., (2006) [62]
69.6 66.7 91.3 96.3 39.1 96.3 100 66.7 Zupi et al., (1996) [33]
92 88 Rao et al., (2004) [29]
97 70 Muller & Slootweg (1990) [42]
80 72 Acton et al., (2000) [50]
64 97 100 97 Close et al., (1986) [49]
89 57 100 SPECT 29 Curran et al., (1996) [39]
91 96.3 39 96 100 67 Zupi et al., (1996) [33]
64 89 94 73 94 73 Van den Brekel et al., (1998) [65]
85 89.5 93.8 100 SPECT 91.6 Schimming et al., (2000) [64]
86.6 80 53 92.5 Ord et al., (1997) [34]
93 93 Bolzoni et al., (2004) [59]
76 93 53 90 100 92 95 72 Brown et al., (1994) [73]
91 66 Totsuka et al., (1991) [77]
71 64 71 71 Leipzig (1985) [108]
80 94 100 88 Bahadur (1990) [27]
50 86 100 50 Tsue et al., (1994) [20]
78 80 98 47 Kalavrezos et al., (1996) [24]
61 88 Lane et al., (2000) [66]

stripping and at least two imaging techniques that complement Histopathological examination
each other in terms of specificity and sensitivity [68].
Babin et al. (2008) reported on fusing of positron emission Both macroscopically and histologically, distinct patterns of
tomography with CT scan images to maximise data information mandibular bone invasion by the carcinoma have been identified
[69]. Positron emission tomography/CT fusion showed a sensitivity
of 100% with specificity of 85%. Van Cann et al., (2008) reported on
combinations of CT and bone SPECT, or MRI and bone SPECT to
predict mandibular invasion without yielding false negative results
[70]. If CT or MRI showed mandibular invasion, bone SPECT was
not performed avoiding unnecessary costs. Gu et al., (2010)
reported improved sensitivity in detection of mandibular invasion
by squamous cell carcinoma of the oral cavity with combined
analysis of CT, MR, and PET/CT than when they were assessed
independently [71].

Intraoperative evaluation of mandibular invasion

McGregor and MacDonald (1988) advocated the clinical assess-


ment of mandibular invasion by lifting the periosteum at the time of
surgery [72]. Brown et al. (1994) compared several methods for
assessing bone invasion and found that periosteal stripping at the
time of resection represented an accurate predictor of the presence
of mandibular invasion [73]. They reported only one case of false
prediction in 35 cases analyzed. They recommended the assessment
of macroscopic invasion of the mandible after periosteal stripping as
a helpful and worthwhile addition in planning the resection of the
mandible in oral cancer surgery. Pandey et al., (2009) too have
reported on the findings on periosteal stripping namely sub-
periosteal reaction, cortical expansion, and presence of pathologic
fracture as significant predictors of bone invasion [30].
Forrest et al. (1995) advocated frozen- section analysis of
cancellous bone to confirm the adequacy of bony margins [74].
Oxford and Ducic (2006) had presented the frozen- section analysis
of bone margins as a reliable method to evaluate bony margins
intra-operatively [75]. Wysluch et al., (2010) assessed the effec-
tiveness of intra-operative frozen- section analysis of trephine
drilled bone specimens and found 94% consistency between the
frozen- section analysis and routine histopathological examination
of decalcified bone specimen techniques, with a sensitivity of 79% Fig. 2. Orthopantomogram: A) showing loss of teeth and early doubtful invasion B)
and specificity of 98%. This technique promised to be suitable for Showing definite invasion of mandible C) Extensive invasion reaching almost to the lower
intra-operative detection of malignant bone infiltration [76]. border of mandible D) Invasion of the lower border of mandible from a large lymph node.

Please cite this article in press as: Rao LP, et al., Mandibular conservation in oral cancer, Surgical Oncology (2011), doi:10.1016/
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6 L.P. Rao et al. / Surgical Oncology xxx (2011) 1e10

Fig. 3. Computerized tomography scan showing A) tumour of the buccal mucosa and gingivobuccal sulcus abutting the mandible with possible early erosion of outer cortex.
B) Tumour of the upper alveolus with extension in retromolar trigone and involvement of mandibular ramus. C) tumour of the tongue and lateral floor of mouth with extension to
the alveolus and destruction of mandibular bone. D) 3-D reconstruction showing the destruction of outer cortex of mandible. E) 3-D reconstruction of the same patient
demonstrating the destruction of inner cortex.

[13,77] (Fig. 5). The tumour can advance in the bone either as a more aggressive behavior with an increased likelihood of positive
a broad front, referred to as arrosion or in a diffusely infiltrating margins, recurrence, death with disease, and shorter disease-free
pattern [13]. In the arrosive pattern, the tumourebone interface is survival. The 3-year disease-free survival was 30% for the infiltra-
well demarcated one with a continuous layer of new bone and tive pattern and 73% for the arrosive pattern.
connective tissue. The second tumour pattern, infiltrative, is Hong et al. (2001) had reported an underestimation of tumour
a diffuse one with extensive, irregular destruction of bone and invasion width in mandible by 9.2 mm and tumour invasion depth by
spread into cancellous bone. The infiltrative pattern is marked by 3.4 mm, when the radiological findings and the actual defect from
nests and cords of tumour cells along an irregular tumour front, and histopathological findings were compared in 21 patients with
the erosive pattern exhibits a broad, pushing tumour front [5,37]. gingival squamous cell carcinoma of the molar region [46]. Two
Wong et al. (2000) reported a significantly worse prognosis for specimens showed the microscopic tumour extension within the
infiltrative pattern of mandibular invasion when compared with medullary bone, without any perforation of the lingual and buccal
the arrosive pattern [78]. The infiltrative pattern clearly exhibited cortices, into the mandibular body and ramus. These findings
reflected that, especially in infiltrative pattern, it was difficult to
determine the resection margin anteroposteriorly because bone
invasion by tumour cells spreading transmedullarly is not radiologi-
cally identifiable. Moreover, the tumour cells rapidly spread between
cancellous bony trabeculae and there was no definite resistance to
spread. The surgeons, therefore, should be more cautious in planning
the width of resection especially if a bone defect of the gingival
carcinoma is thought to be an infiltrative defect in radiological
studies. In general terms, an excision margin of at least 1e2 cm of
normal bone on either side is recommended [7,17,21,46,79e82]. More
aggressive resection is advised in selected cases when the invasive
bone defect is apparently identified in the radiographs [46].

Segmental vs. marginal mandibulectomy/mandibular preservation

Despite significant improvement in functional oromandibular


Fig. 4. Bone scintigraphic scan showing two areas of increased isotope uptake in right reconstruction, segmental mandibular defects remain a source of
mandible and at the arch. functional and cosmetic difficulty for patients with head and neck

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j.suronc.2011.06.003
L.P. Rao et al. / Surgical Oncology xxx (2011) 1e10 7

Fig. 5. Photomicrograph showing A) Tumour invasion in mandible in a broad front (E) characteristic of erosive pattern with no bony remnants within the tumour mass, tumour cells
are separated from the normal bone by a well demarcated fibrous zone (F). B) Tumour invasion in the mandible as irregular cords and islands (I) characteristic of infiltrative pattern,
partially lysed bone spicules (B) are present within the tumour mass with no clear cut demarcating tissue between tumour and bone. C) Tumour invasion (T) into the perineural space
of the inferior alveolar nerve bundles. D) Tumour invasion (T) into the mandible involving the superior portion of the inferior alveolar canal with no invasion of nerve bundles (N). E)
Diffuse irregular tumour infiltrating bone, fibrous marrow (FM) and bony remnants (B). F): Fatty marrow in post radiotherapy patient. (reproduced with permission from Pandey M
et al. Patterns of mandibular invasion in oral squamous cell carcinoma of the mandibular region. World Journal of Surgical Oncology 2007, 5:12 doi:10.1186/1477-7819-5-12).

cancer. Although the application of free-flap allows for single- stage retromolar trigone and advanced tumours of the adjacent tonsillar
composite reconstruction [83], the use of free-flap technology fossa have historically been treated with posterior segmental
requires significantly more health care resources than simpler mandibulectomy [88]. The retromolar trigone is the most posterior
reconstructions [84]. Therefore, preserving the continuity of the aspect of the oral cavity. It is a pyramidal-shaped region of mucosa
mandibular arch, when oncologically feasible, remains the preferred covering the ascending ramus of the mandible and bordered by the
surgical alternative. Preservation of mandibular continuity can be buccal mucosa laterally, the tonsillar fossa medially, the maxillary
achieved either by temporarily dividing the mandible, allowing tuberosity superiorly, and the molar teeth inferiorly. The oral
access to the posterior oral cavity and oropharynx (mandibulotomy), mucosa adheres tightly to this non-tooth-bearing portion of the
or by resection of only a portion of either the vertical height or mandible. Invasion of the mandibular ramus in this region is
sagittal diameter of the mandible (marginal mandibulectomy). difficult to determine preoperatively; however, when involved,
Marginal mandibulectomy was described by Crile in 1923 as an extensive bone infiltration by tumour is common [21,73,89]. The
incision that is “carried down to the underlying bone, and thence lack of a reliable radiographic assessment of the retromolar trigone
into the bone by a sharp chisel or saw, so that a slice of bone can be makes surgical decision making in this region difficult. Studies
split off in one piece, bearing the undisturbed cancer off as on indicate that the incidence of mandibular invasion in retromolar
a bone platter.” [85]. trigone cancers is as high as 75% [20,22,90].
Contemporary marginal mandibulectomy usually refers to In 1983, Wald and Calcaterra reported the result of the treat-
resections of either the inner table or alveolar ridge of the mandible ment of mandibular gingival cancer, and the failure rates for
[86]. In the absence of radiographic evidence of mandibular inva- marginal and segmental groups were similar. The advanced stages
sion, marginal mandibulectomy has been shown to be a sound required a radical operation with segmental mandibulectomy;
oncologic procedure for patients with cancers of floor of the mouth. however, the locoregional recurrence rate was high despite this
Marginal mandibulectomy has been used in cases in which the treatment [89]. Byers et al. (1984) reported local recurrence of 7% in
tumour abuts the mandible, is adherent to the periosteum, or their series of 110 patients undergoing various forms of man-
where resection of the alveolar process is necessary to obtain dibulectomy with or without coronoidectomy for retromolar trig-
a third dimension on the deep surface of the tumour [87]. one cancer [88].
Unlike tumours of the anterior oral cavity that are more Shaha et al. (1984) used marginal mandibulectomy for the
amenable to marginal mandibular resection; carcinomas of the treatment of smaller floor of the mouth malignancy and segmental

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8 L.P. Rao et al. / Surgical Oncology xxx (2011) 1e10

mandibulectomy for the larger tumours. This resulted in 21% classification of bone resorption pattern in edentulous jaws given
recurrence at the primary site following marginal mandibulectomy by Cawood and Howell (1988, 1991) was used as the basis on which
[80]. treatment planning was carried out depending on radiographic
Barttlebort et al. (1987) reported 25% local recurrence rate findings [99,100]. They advocated a rim or marginal man-
following marginal mandibulectomy. The local failures had dibulectomy in radiologically negative tumours which are close to
occurred in soft tissues and not in bones [90]. the mandibular region or abut onto mandible, in dentate or
Collins and Saunders (1987) described the intra-oral ramus recently extracted cases. In rounded or knife e edge ridges or flat or
marginal mandibulectomy in 2 of 8 patients treated with conser- depressed ridges, with radiological evidence of mandibular inva-
vative mandibulectomy for oral cavity carcinomas “adjacent to or sion, a segmental resection is always preferred [98].
clinically attached to the mandibular periosteum” without clear
radiographic evidence of bone destruction. The intra-oral defects in Prognosis in cases with mandibular invasion
both of these patients were closed primarily, and both patients had
normal recovery of speech and swallowing [79]. The prognostic impact of mandibular invasion by oral squamous
Randall (1987) recommended marginal mandibulectomy only cell carcinoma (SCC) is controversial. There have been reports of
when there was no radioragphic evidence of bone lesion and less decreased survival rates and increased recurrence with bone
than 50% of the mandibular circumference was involved by the invasion and survival rates independent of bone invasion. There
tumour [91]. The studies of Totsuka et al. (1991a,b) regarding have been conflicting reports by the same authors, who had
mandibular gingival carcinoma showed almost the same survival compared rim and sagittal marginal mandibulectomy in one study
rate at 2-year follow-up after marginal technique (86%) and and marginal mandibulectomy with segmental mandibulectomy
segmental technique (82%) [44,77]. [95e101].
Shaha (1992) reported that whenever the tumour is close to the Ogura et al. (2002) showed that bony invasion identified on
mandible or adherent to the periosteum, consideration should be dental CT images was a significant prognostic factor in cervical
given to marginal mandibulectomy. In 65 patients that the author metastases [101]. Tankere et al. (2002) [102] and Guerra et al.
reported, 22 underwent marginal mandibulectomy. Most of the (2003) found no statistical relationship between the presence of
patients had oblique mandibulectomy including resection of the histological bone invasion and the risk of local recurrence [97,99].
upper rim and medial cortex of the mandible [92]. The size of bone resection >4 cm and tumour invasion of surgical
Barttelbort and Ariyan (1993) compared two types of mandib- margins were found to be associated with increased local recur-
ular preservation procedures namely rim (marginal) man- rence rates [102].
dibulecctomy and lingual sagittal mandibulectomy in fresh cadaver O’Brien et al. (2003) reported a series of 94 patients who
human mandibles in terms of strength [93]. Using strain gauge underwent marginal resections and 33 underwent segmental
techniques, it was noted that the rim mandibulectomy was more resections. Among patients with bone invasion, the local control
resistant to fracturing than was lingual sagittal mandibulectomy rate was higher following segmental resection when compared to
and maintenance of a 1-cm-thick segment of bone inferiorly was marginal resections (87% vs 75%) but this was not statistically
required to reduce the risk of fracture formation. significant. Survival was significantly influenced by positive soft
The posterior marginal mandibulectomy was used by Pinsolle tissue margins but not bone invasion or the type of resection [103].
et al. (1997) in 14 patients with tumours of the oral cavity and Shaw et al. (2004) reported on strong correlation between
oropharynx without preoperative radiographic evidence of bone mandibular invasion and disease- specific survival rates [104]. Patel
erosion. These authors reported no complications associated with et al. (2008) assessed the effect that extent of bone invasion has on
the mandibulectomy and good maintenance of cosmesis [94]. recurrence and survival in 111 patients treated with marginal and
Ord et al.(1997) reported a local control rate of 92.3% [34] and segmental mandible resection [105]. Five-year local control was
Werning et al. (2001) published a local control rate of 87.4% in similar following marginal (83%) and segmental mandibulectomy
a study of 222 patients [35] with marginal mandibulectomy. (86%). There was no correlation with presence or extent of bone
Petruzzelli et al., (2003) reported a local control rate of 93.75% invasion. Survival at 5 years was 71% and this correlated with bone
(15 out of 16 patients) with posterior marginal mandibulectomy for invasion and involved margins, but not with extent of mandible
tumours of the posterior oral cavity &/or oropharynx [95]. invasion or resection.
Guerra et al. (2003) reported equal locoregional recurrence rate Pandey et al. (2009b) reported tumour stage, margin of surgical
and survival rate in 106 patients with oral squamous cell carcinoma excision and nodal stage as predictors of survival in their study of
treated by segmental or marginal mandibulectomy [96]. In 51 patients with squamous cell carcinoma of mandibular region.
marginal resection group 10 cases (20%) showed a local recurrence, They found no significant difference in survival between patients
whereas in the segmental resection group there were 19 (33.9%) with pathologically positive mandible with those not having
recurrences. Analysis of these 2 modalities in their study showed mandibular involvement and concluded that mandibular conser-
“no evidence of disease” at 2 years after surgery for the segmental vation might be carried out, even in presence of involved mandible
and marginal were almost the same, 56% and 61%, respectively. if negative resection margins could be achieved [106].
Tei et al. (2003) reported a recurrence rate of 13.3% and 29.4%
and 5 year survival rate of 78.1% and 72.8% with marginal man- Conclusion
dibulectomy and segmental mandibulectomy respectively [97].
Bone fracture due to insufficient thickness of the remaining Segmental resections cause severe functional and cosmetic
mandible after marginal resection occurred in 4 of the 45 marginal problems due to loss of the continuity of the mandible. Functional
resection cases. morbidity after mandibular resection depends on the maintenance
Brown et al. (2005) stressed on the need to consider the extent of arch continuity. This can be achieved in the case of segmental
of bone resorption after the loss of teeth in the clinical management resections mainly with microvascular transfer of vascularized bone
of the mandible invaded by squamous cell carcinoma [98]. They grafts.
described a guide to help the surgical team in the decision-making Conservative resection of the mandible is safe as long as
process and increase the accuracy of mandibular resection to marginal mandibulectomy does not lead to compromise of soft
maximize the chance of cure without increasing morbidity. The tissue margins, and in cases where there are no radiographic

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j.suronc.2011.06.003
L.P. Rao et al. / Surgical Oncology xxx (2011) 1e10 9

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Conflict of interest statement clinical features in the assessment of mandibular invasion of oral carcinomas.
None declared. Int J Oral Maxillofac Surg 1996;25(6):439e45.
[25] Weisman RA, Kimmelman CXP. Bone scanning in the assessment of mandib-
ular invasion by oral cavity carcinomas. Laryngoscope 1982;92:1e4.
Authorship statement [26] Gilbert S, Tzadik A, Leonard G, Farmington CT. Mandibular involvement by oral
squamous cell carcinoma. Laryngoscope 1986;96:96e101.
[27] Bahadur S. Mandibular involvement in oral cancer. J Laryngol Otol 1990;104:
Guarantor of the integrity of the study: Manoj Pandey 968e71.
Study concepts: Manoj Pandey, Vinay Sharma, Latha P. Rao [28] Smyth DA, O’Dwyer TP, Keane CO, Stack J. Predicting mandibular invasion in
Study design: Manoj Pandey, Latha P. Rao mouth cancer. Clin Otolaryngol Allied Sci 1996;21(3):265e8.
[29] Rao LP, Das SR, Mathews A, Naik BR, Chacko E, Pandey M. Mandibular invasion
Definition of intellectual content: Manoj Pandey, Mridula Shukla in oral squamous cell carcinoma: investigation by clinical examination and
Literature research: Mridula Shukla, Latha P. Rao orthopantomogram. Int J Oral Maxillofac Surg 2004;33:454e7.
Clinical studies: Not applicable [30] Pandey M, Rao LP, Das SR. Predictors of mandibular involvement in cancers of
the oromandibular region. J Oral Maxillofac Surg 2009;67:1069e73.
Experimental studies: Not applicable [31] O’Brien CJ, Carter R, Soo KC, Barr LC, Hamlyn PJ, Shaw HJ. Invasion of the
Data acquisition: Latha P. Rao, Vinay Sharma mandible by squamous carcinomas of the oral cavity and oropharynx. Head
Data analysis: Manoj Pandey, Mridula Shukla Neck Surg 1986;8:247e56.
[32] Shaha AR. Preoperative evaluation of the mandible in patients with carcinoma
Statistical analysis: Not applicable of the floor of the mouth. Head Neck 1991;13:398e402.
Manuscript preparation: Vinay Sharma, Latha P. Rao, Mridula [33] Zupi A, Califano L, Maremonti P, Longo F, Ciccarelli R, Soricelli I. Accuracy in
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Manuscript editing: Manoj Pandey, Mridula Shukla
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Manuscript review: Manoj Pandey, Mridula Shukla bony resection for oral squamous cell carcinoma involving mandible. J Oral
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Please cite this article in press as: Rao LP, et al., Mandibular conservation in oral cancer, Surgical Oncology (2011), doi:10.1016/
j.suronc.2011.06.003

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