Significance of radiologically determined prognostic factors for head … · Radiology and head and neck cancer Diagnostic imaging can be used to determine the primary and regional

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Significance of radiologically determined prognostic factors for head and neck cancer

Lodder, W.L.

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Citation for published version (APA):Lodder, W. L. (2013). Significance of radiologically determined prognostic factors for head and neck cancer.

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C h a p t e r1General introduction

and outline of the thesis.

Wouter L. Lodder

25558 Lodder, Wouter OK.indd 11 24-06-13 09:50

Chapter 1

12

GENERAL INTRODUCTION

Epidemiology and prevalence

Head and neck cancer comprises 5% of all newly diagnosed cancers in the Western

World. It is the sixth most diagnosed cancer worldwide.1 Approximately 2700

new cases of head and neck squamous cell cancer (SCC) were diagnosed in the

Netherlands in 2005.2 SCC is most diagnosed in the oral cavity with an estimated

270,000 cases worldwide each year. Oropharyngeal SCC account for approximately

50,000 incident cases per year, hypopharyngeal carcinomas account for

130,000 cases and laryngeal SCC for 160,000 cases.1,3 Several western countries

(Scandinavia, USA, Canada, the Netherlands, Scotland) report an increasing

incidence of oropharyngeal SCC over the last 25 years, while the overall head and

neck SCC incidence has remained stable or has even shown a declining trend in

the same period.3 The main risk factors for cancers of the upper aero-digestive

tract are individual predisposition, a combination of excessive use of alcohol and

tobacco and HPV exposition.4,5 Recent data suggests that Human Papilloma Virus

(HPV) exposure may (in part) explain the rise in oropharyngeal SCC in western

countries. HPV is a small epitheliotropic DNA virus that primarily infects transitional

epithelium present in the upper aerodigestive tract and is sexually transmitted.3

Treatment

Surgery, radiotherapy and concomitant chemoradiation (CCRT) are the

mainstays of treatment of head and neck squamous cell carcinomas.6-11 The

decision of exact treatment management depends on the tumor site and

stage, radiological and histological characteristics as well as on patient’s co-

morbidity.12-15 Molecular genetic tumor characteristics (for example: MTA-112,

MRB-216, RB16) are also expected to play an important role in the decision-making

in the nearby future.

In addition to the number, level and side of lymph node metastases,

extranodal spread (ENS) is used as one of the most important prognosticators in

patients with neck node metastases from squamous cell carcinomas.17-27 ENS is

found to be a significant prognostic factor for local control, distant metastases–

free survival, and overall survival.28-32 ENS is widely accepted to be a criterion for

postoperative radiotherapy. However, several studies have shown ENS lost its

significance in predicting regional failure, when the area of ENS is treated with

an extra boost.23,33,34


Chapter

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INTRODUCTION AND OUTLINE

13

Two large prospective clinical trials from 2004 showed a subgroup

of high-risk patients to benefit in overall survival from postoperative CCRT.8,9

Independently, these trials showed several methodological limitations;

selection criteria varied, follow-up was limited, the reported overall survival

was low compared to many other studies, and in 1 of the 2 trials no survival

benefit could be demonstrated. However, in a combined analysis of the 2 trials,

patients with positive margins and ENS benefited most from CCRT.35 Until now

no prospective clinical trials comparing CCRT + salvage surgery versus primary

surgery and post-operative CCRT have been published. However, most of the

reports in literature have shown post-operative CCRT to be equally effective

as primary surgery.36 Thus, when CCRT seems equally effective it could be in

theory of use as primary treatment in locally and/or regionally advanced head

and neck tumors.

Despite the reported positive results from the 2 prospective trials8,9, it still

remains unclear whether postoperative CCRT is indicated in all patients with

ENS. Langendijk et al. demonstrated that CCRT only has positive significant

effect on tumor control in those cases with N3 disease, multiple nodes with

ENS, or positive resection margins in T3 tumors.37

CCRT is often added to current treatment regimes of all patients in whom ENS

has been proven.27 This implies an enormous increase in treatment burden and

morbidity, especially in combination with major surgery. It is, therefore, crucial

to be critical on the indications of CCRT and search for the subgroup of patients

that might benefit from this treatment.

The main goal of this thesis is to investigate the significance of several

radiological determined prognostic factors that could contribute valuable

information for the determination of an individualized treatment for patients

with head and neck cancer.

TNM-staging

Different methods are used to evaluate the extent of disease. The TNM-staging

system that characterizes tumors by the size of the primary tumor, nodal

involvement and distant metastases is generally used.38 TNM-staging provides a

rough estimation for tumor related criteria for prognosis of patients and plays an

important role in the prognostic stage grouping of head and neck cancer patients.


Chapter 1

14

TNM staging of a tumor is generally performed twice: First, the

pretreatment clinical classification (cTNM) is determined. This is based on

physical examination, conventional imaging, endoscopy, biopsy, and other

relevant examinations. Primary therapy is selected and evaluated based on

the cTNM. The second classification is the pathological classification (pTNM).

This is the postsurgical histopathological classification that is used to evaluate

the pre-surgical treatment effect, guide adjuvant therapy and provides also

additional data to estimate prognosis and calculate end result.

The latest additions to this classification system involve the identification

of micrometastases. The classification describes the increasing involvement of

regional lymph nodes histologically. Distinction is made in direct extension of

the primary tumor into lymph nodes, tumor deposits (satellites, i.e. macro- or

microscopic nests or nodules, in the lymph drainage area of a primary carcinoma

without histological evidence of residual lymph node in the nodule or totally

replaced lymph nodes), distant metastases or micrometastases (metastases

smaller than 0.2 cm). Although the anatomical extent of disease, as categorized

by TNM, is a very powerful prognostic indicator in cancer, many factors have

a significant impact on predicting outcomes. Some have been incorporated

into stage grouping, as has grade in soft tissue sarcoma and age in thyroid

cancer.38 Some factors are not yet available in the TNM staging system. For

example, tumor thickness has shown to be of prognostic significance in oral

cancer39-41 and also encasement of the internal carotid artery is of prognostic

significance.42,43

Radiology and head and neck cancer

Diagnostic imaging can be used to determine the primary and regional anatomy

and extent of disease, detect occult disease, assess response to treatment

and assist in treatment of patients, e.g. by neuro-navigation.44 Imaging could

also be used for prognostication of head and neck tumors. Primary tumor

volume emerged as a significant prognostic factor for hypopharyngeal and

laryngeal cancers and could be of added value next to the TNM-staging.45,46

Ultrasonography, CT and MR imaging and PET-CT are regularly used imaging

modalities for staging of head and neck cancer, Sentinel node biopsies47,48,

SPECT-CT49 and DWI-MRI50 are newly developed technologies for tumor staging

and are beyond the scope of this thesis.


Chapter

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15

Imaging Techniques

Each anatomic region of interest in the head and neck area needs a specific

imaging modality to optimize the detection or characterization of anatomical

structures or lesions.

Ultrasound

High-resolution ultrasound sonography is very accurate in detecting lymph

nodes in the neck and can even depict anatomical details inside these lymph

nodes. The spatial resolution of a 7.5 MHz or 10 MHz transducer is about 0.3

mm. It is relatively inexpensive compared to CT or MRI. Limitations include

the field of view with a lack of easily identifiable anatomic landmarks on the

images, and interpretation of images is more operator dependent. High-

resolution ultrasound evaluation of the salivary glands and neck is also limited

to the soft tissue structures because of the impediment to sound transmission

caused by the highly reflective facial bones, mandible, mastoid tip, and air

within the oral cavity and pharynx. Nevertheless, superficial lesions in the oral

cavity and oropharynx can accurately be staged by endo-ultrasonography,

with measurements of the tumor thickness (depth of invasion). Figure 1 shows

an example of an ultrasound image of the normal tongue with an intra-oral

ultrasound probe. Particularly in the oral cavity tumor thickness has proven to

be an important prognostic factor for loco-regional survival.44 New techniques

in ultrasound and new small probes increased the sensitivity for depiction of

lesions. For example, contrast-enhanced ultrasonography allows continuous

imaging at low acoustic power, providing an easier and more accurate depiction

of tumor vascularization, especially when considering microcirculation, not

assessable by means of color Doppler techniques.51


Chapter 1

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Figure 1. The Ultrasound probe has been placed under the tongue (looking up). The internal tongue musculature is well seen as a radiating pattern of alternating hyperechoic (white) and hypoechoic (dark lines). The tongue lies against the palate. The mucosal surface of the tongue stands out as a hyperechoic line (arrows) against the more hypoechoic palatal structures.

Computed Tomography (CT)

CT imaging is still one of the most important staging tools for primary tumors

in the head and neck area next to MRI. Multichannel CT scanner revolutionized

head and neck imaging, since the entire neck can be scanned in less than a

minute at a slice thickness of less than 1 mm.52 This high speed imaging makes

CT scanning suitable for assessing vocal cord immobility, an important staging

characteristic of larynx and hypopharynx carcinoma, and for imaging of

larynx and pharynx during breathing and swallowing movements. Discussion

remains whether the tumor extent towards the cartilage bone structures and

prevertebral space can be better appreciated on CT44,53 compared with MRI.54

However, MRI provides a superior display of cranial soft tissue structures, as it

has better tissue contrast resolution than CT. CT and MRI play a complementary

role in three-dimensional image display of many head and neck tumors.

Next to the TNM classification, tumor volume is a significant prognostic

factor in the treatment of malignant head and neck tumors.45,46,55-60 Several

studies have confirmed the prognostic value of CT determined tumor volume

for outcome after definitive radiation therapy in head and neck cancer, including

tonsillar57, hypopharyngeal58, supraglottic59 and glottic45 cancer. The widespread

use of CT scans, as it is less time consuming and can be easier interpreted, means

that it is still more frequently used for the staging of head and neck cancer.


Chapter

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17

Magnetic Resonance Imaging (MRI)

MRI is an imaging modality that uses the response of biologic tissue to an

applied and changing magnetic field to generate images. MRI derives its

signal from spinning hydrogen protons, which are aligned in the direction of

the magnetic field. Radiofrequency pulses are transmitted into the subject

to excite the spinning protons, changing their orientation with respect to

the magnetic field. As the protons realign with the magnetic field, they lose

energy and give off a signal, which is picked up by coils and reconstructed

into an image. The strong magnetic forces may cause chemical shift artifacts

and susceptibility artifacts (artifacts in the response to an applied magnetic

field) from metallic implants and eyelid mascara, containing metal particles. A

typical imaging sequence may last from 2 to 8 minutes which makes MRI more

sensitive to motion artifacts. As mentioned before, MRI provides a superior

display of cranial soft tissue structures, which makes this modality first choice

for cases with suspected tumor invasion into mandibular bone, perineural

growth or for tumors located above the hyoid bone (because its relation to

the soft tissue structures).44 Especially in case of a carcinoma of the tongue, the

contrast between tumor tissue and the soft tissues of the tongue is displayed

with higher detail than CT imaging can provide. Figure 2 shows a MR image of

a patient with a tumor in the neck at the right site.

Figure 2. Axial MR T2-weighted image at the level of the mandible of a patient with an aggressive lymph node metastasis in level I at the right side (large arrow). There is extracapsular spread around the body of the mandible and invasion of the lateral aspect of the tongue (small arrows). Note: additional lymph node metastasis in level II, posterior to the carotid artery (without sign of extranodal spread).


Chapter 1

18

In case of parotid gland tumors61 and sinonasal carcinomas62 MRI

is believed to be superior compared to CT imaging. Assessment of semi-

automatic volume measurements of the primary tumor has been performed

for prostate cancer and breast cancer63-65 using dynamic contrast-enhanced

magnetic resonance imaging (DCE-MRI).

Positron Emission Tomography (PET)

Fluorodeoxyglucose positron emission tomography (FDG PET/CT) imaging

provides physiologic and biochemical data as well as anatomical images.

A positron emitting radiopharmaceutical is intravenously injected and its

distribution in the body is measured. Depending on the radiopharmaceutical

chosen, PET imaging can provide information regarding blood flow, ischemia,

deoxyribonucleic acid metabolism, glucose metabolism, protein synthesis,

amino-acid metabolism and receptor status. Increased glucose metabolism

in rapidly growing neoplastic cells is targeted with the FDG PET imaging.

Quantitative evaluation of FDG PET images by determination of the SUV

(standard uptake value) is sufficient for most clinical purposes. The detection

rate of an occult primary tumor in the setting of squamous cell carcinoma

with FDG PET is slightly superior to that with MRI and CT.66 FDG PET may

identify a primary tumor that is not detected by other diagnostic modalities

in the setting of cervical nodal metastasis with unknown primary.44 Several

studies examined the additional value of PET/CT in the detection of unknown

primary tumors.67-70 Sensitivity of 88% and specificity of 75% are observed.66

Two major disadvantages of PET are lack of anatomic information and poor

spatial resolution. Also the definition used for unknown primary tumors is non-

uniform. Different inclusion criteria are used, such as inclusion after physical

examination or after diagnostic imaging and after direct biopsies taken under

general examination.70,71 A recent publication revealed PET/CT increased the

detection of a primary site from 25% to 55% compared to traditional staging.72

Integrated PET/CT showed to be superior to PET in the detection of the primary

site of clinically occult tumors in unknown primary tumors.73 Other applications

for PET/CT are response monitoring after CCRT or radiotherapy and lymph

node staging, especially in planning radiotherapy fields and doses.

ENS can be regarded as a pure anatomical feature, i.e. tumor has grown

beyond the lymph node capsule. However, it can also be regarded as a sign of

an aggressive growth pattern. This suggests a relation with biological processes


Chapter

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19

in tumor tissue, such as metabolic activity. In theory, with a more aggressive

tumor, a higher glucose consumption rate should then be found, possibly

indicating that aggressive growth is associated with ENS.72 Proliferation and

growth in a tumor are positively correlated with SUV determined on PET with

FDG.74 A recent meta-analysis showed that FDG PET/CT could also be used

for risk stratification.66 The pretreatment SUV was prognostic for disease free

survival, overall survival and local control in head and neck cancer. Thus, nodal

characteristics on PET/CT could improve prognostic stratification beyond

standard clinical and pathologic risk factors. Consequently, PET/CT could be

used to identify subgroups of patients with an increased risk for recurrence and

distant metastases before initiation of treatment.

Outline of the thesis

The increased accuracy of tumor imaging by the above described imaging

modalities make it possible to improve the prognostic significance of specific

imaging characteristics in head and neck malignancies. Tumor thickness

appears to be an important prognostic indicator in oral cavities carcinomas.

To measure tumor thickness, different techniques are available. Several studies

have compared intra-oral ultrasound (US) with MRI or CT.37,38 In the literature

the cut-off thickness predicting neck metastasis and survival varied from

1.5 mm to 10 mm.39 Limited oral cancer is treated generally surgically, with

additional postoperative radiotherapy or CCRT in the case of unfavourable

histopathological features. In superficial oral cancer, apart from local excision,

CO2 laser resections and photodynamic therapy (PDT) have also been shown

to yield excellent results.15 PDT results are dependent of tumor thickness;

therefore in Chapter 2 we studied the value and feasibility of tumor thickness

measurements with an intra-operative ultrasound probe as well as the cut-off

value for lymph node metastases.

Apart from the number, level, and side of lymph node metastases, ENS

is used as one of the most important prognosticators in patients with regional

neck node metastases from squamous cell carcinomas. In the literature several

authors studied the value of pre-operative imaging in the determination of

macroscopic ENS. Their results demonstrate a wide range in sensitivity and

specificity for MRI based characteristics. Possibly these differences are caused


Chapter 1

20

by the disagreement between pathologists on determining ENS. In Chapter 3

inter- and intraobserver variability for detection of extranodal spread, amongst

pathologists, is discussed. Because the clinical consequences of ENS these days

often lead to CCRT8,9,27 it would be important to be informed on ENS presurgically

as this can lead to a nonsurgical management strategy. In Chapter 4 different

radiological findings that could potentially be indicative of the presence of ENS

(maximal diameter, capsular contour, infiltration of adjacent planes, central

nodal necrosis and radiologists’ impression of presence of ENS) are studied. In

literature some authors reported an added value in the detection of ENS when

PET is used. Because MRI remains rather insensitive determining the presence

of ENS, Chapter 5 discusses the value of PET for the determination of ENS in

our patient group. ENS can be regarded as a pure anatomical feature, i.e. tumor

has grown beyond the lymph node capsule. However, it is also thought to be

an alteration of the tumor towards a more aggressive growth pattern. This

suggests a relation with biological processes in tumor tissue, such as metabolic

activity. In theory, a higher glucose consumption rate should then be found,

possibly in relation to aggressive growth associated with ENS.75

Primary tumor volume emerged as a significant prognostic factor for

hypopharyngeal and laryngeal cancers and could be of added value next to

the TNM-staging. Nodal involvement of tumor is recognized to be important

for the prognosis of head and neck cancer patients. However, the prognostic

value of nodal volumes next to the TNM staging is not yet extensively studied

in literature. Chapter 6 discusses the prognostic value of nodal volumes with

the help of a systematic review. In daily practice however tumor volume

measurements are not performed routinely probably due to the extra

workload involved. To implement the primary tumor volume and nodal volume

in the TNM staging, we think, firstly consensus should be accomplished on

standardization of volume measurements, preferably automatic. A workstation

previously developed for semi-automated segmentation of breast cancers on

DCE-MRI is employed to segment the head and neck cancers. In Chapter 7 we

determine the accuracy of semi-automated volume measurements with the

help of this workstation.

Encasement of the carotid artery is both a poor prognostic indicator

and a contraindication to surgical treatment. Until now no consensus has been

reached on standardization of imaging parameters for defining encasement of


Chapter

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21

the carotid artery. MR imaging seems the most sensitive imaging modality to

visualize contrasts between soft tissues compartments and therefore should

be optimal for the assessment of carotid encasement. Chapter 8 studies the

value of CT and MR imaging in the preoperative evaluation of carotid artery

encasement.


Chapter 1

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