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 Table of Contents  
REVIEW ARTICLE
Year : 2016  |  Volume : 28  |  Issue : 4  |  Page : 409-415

Multimodal imaging techniques in the diagnosis of metastatic lesions


Department of Oral Medicine and Radiology, College of Dental Sciences, Davangere, Karnataka, India

Date of Submission18-Feb-2016
Date of Acceptance03-Dec-2016
Date of Web Publication21-Feb-2017

Correspondence Address:
Dr. Abha Rani
Department of Oral Medicine and Radiology, College of Dental Sciences, Davangere - 577 004, Karnataka
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0972-1363.200629

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   Abstract 

Imaging has a crucial role in the treatment of head and neck cancers as it discloses hidden foci of metastases, especially when it is located outside of the planned treatment field. Metastasis to oral cavity is a rare chance and may involve either soft tissue or jaw bones. Their early and accurate detection is critical and also a real challenge for the clinician. Therefore, pre-, per- and post-treatment imaging in diagnosis is critical. Radiography, computerized tomography, magnetic resonance imaging, followed by positron emission tomography, advancements in ultrasonography, and nuclear medicine along with sentinel node lymphoscintigraphy has greatly added to the diagnostic accuracy of metastases.

Keywords: Computed tomography, magnetic resonance imaging, metastasis, positron emission tomography scan


How to cite this article:
Rani A, Panchaksharappa MG, Mellekatte NC, Annigeri RG. Multimodal imaging techniques in the diagnosis of metastatic lesions. J Indian Acad Oral Med Radiol 2016;28:409-15

How to cite this URL:
Rani A, Panchaksharappa MG, Mellekatte NC, Annigeri RG. Multimodal imaging techniques in the diagnosis of metastatic lesions. J Indian Acad Oral Med Radiol [serial online] 2016 [cited 2021 Jan 18];28:409-15. Available from: https://www.jiaomr.in/text.asp?2016/28/4/409/200629


   Introduction Top


According to Willis, metastases are growths which are separated from the primary growth and have arisen from disseminated transported fragments from it. It is difficult to detect early metastasis because there are no obvious or specific symptoms. Due to aggressive tumor behavior and lack of an effective way to stop malignancy progression, distant metastasis is highly lethal, rapidly leading to patient's death within 3–6 months. Accurate staging of head and neck squamous cell carcinoma (HNSCC) is essential for determining the treatment plan. Treatment plan depends on delineation of the primary tumor, assessment of the presence and extent of lymph node metastases and screening for distant metastases.


   Incidence and Prevalence Top


Metastases from other body parts constitute approximately 1%–3% of the total oral tumor lesions. These metastases usually affect bone and are less likely to affect the oral soft tissues.[1] The mandible is the most frequent location, particularly the molar region.[1],[2] Metastases are more common in males.[3] Breast and lung are the most common sites from where primary carcinomas metastasize to the jaw bones or oral soft tissue, respectively.[4],[5] Oral metastases are manifested as the first sign of the disease in one-third cases of malignancy.[6] Distant metastasis was reported in 5%–25% of oral SCC patients.[7] In SCC, pulmonary metastases are alone accounting for 66% of distant metastases. Some other metastatic sites include bone (22%), liver (10%), skin, and bone marrow.[8]


   Different Imaging Modalities to Detect Metastasis Top


Radiography

Intra- and extra-oral radiography many times helps to determine jaw bone involvement. Radiographic findings of metastases to the jaw do not show pathognomonic radiographic appearance and ranges from minimum manifestation to a lytic or opaque lesion with ill-defined margins. Usually, the osteoblastic and osteoclastic activity determines the characteristic of metastatic bone lesions. Metastases from prostate cancer are usually of osteoblastic nature. On the other hand, bone metastases from kidney, lung, or breast cancers are mostly osteolytic-moth eaten in appearance. Other multiplanar imaging techniques may be needed to determine the degree of spread of some tumors especially, to exclude bone invasion and lymph node involvement such as ultrasound (US), computed tomography (CT), magnetic resonance imaging (MRI), as these are more capable of greater spatial and soft tissue resolution than conventional radiography.[9]

Bone scintigraphy

A bone scan is acquired by injecting, 550 MBq technetium-99m (99-mTc)-labeled methylene disphosphonate (range 505–820 MBq); approximately 3–4 h later, whole-body scintigraphy/scan with continuous scanning in multiple views is performed using a double-head gamma-camera with a speed of 15 cm/min, low-energy high-resolution collimators, and a 15% energy window over the 140-keV photopeak of 99-mTc. Although bone scan appearances are non-specific, recognizable pattern of bone scan abnormalities suggest a specific diagnosis. Normally liver scanning is not indicated because two-third findings are false negative. Approximately 6% of patients who were diagnosed with cancer of head and neck cancer showed abnormal features in radionuclide scanning of liver.[10]

Advantages of bone scintigraphy are: Detects skeletal physiology, helps in determining the extent of some benign lesions. It is more sensitive as compared to plain radiography. Predicts graft failure in advance before clinical and radiographic changes become evident.

Disadvantages of bone scintigraphy are: Radiation dose is very high, inability to determine exact dimensions of tumor, acts an adjunct to other detecting and determining modalities, and has low specificity.

Computed tomography and magnetic resonance imaging scan

CT is used to evaluate the extent of the primary tumor and metastatic lymph nodes at diagnosis and to detect tumor recurrences and post-treatment complications. It not only helps in metastases characterization but also in tumor staging, tissue sampling and treatment planning. MRI produces excellent quality images with superb contrast, good spatial resolution, and direct multiplanar formats without using ionizing radiation. CT has an advantage of demonstrating bone erosion over the MRI, whereas MRI has an advantage of demonstrating the primary cancer boundaries and its relationship with the surrounding normal anatomical structures over CT.[11] MRI is not preferable in neck region due to artifacts caused by movement made during swallowing, breathing, and coughing.

In short, the major advantages of CT are:

  • Rapid acquisition time (2–3 s per se ction)
  • Better patient tolerance
  • Relatively low cost
  • Superior osseous detail compared with MRI
  • Superimposition of images of structures outside the area of interest is eliminated
  • Tissues differing in density by even <1% can be distinguished.


Disadvantages of CT scan are:

  • Soft-tissue contrast resolution is poor
  • Risk of allergic reaction due to administration of intravenous contrast material to differentiate vessels from other structures like lymph nodes
  • Degraded by scattered artifacts because of metallic dental appliances.


Advantages of MRI are:

  • The superior soft tissue resolution of MRI allows high-contrast differentiation between neoplasm and adjacent muscle
  • MRI is obtained in multiple planes (sagittal, axial, coronal, and oblique), which is very helpful in assessing tumor mass volumes during and after therapy
  • Need for intravascular contrast administration is not required as the patent vessels appear as “signal void,” because of absent signal within their lumen, which helps to easily distinguishes them from surrounding soft tissue structures.


Disadvantages of MRI:

  • As MRI sequence are obtained simultaneously rather than sequentially, patient movement during an MRI leads to greater number of artifacts as compared to CT
  • Fine-bone detail is inferior to that obtained with CT
  • CT has a specificity of 85% and a sensitivity of 82%, whereas MRI has a specificity of 79% and sensitivity of 80%. Curtin et al. (1998) have stated CT is slightly better than MRI, particularly when internal abnormalities were considered in addition to nodal size.


Cone beam computed tomography

From the past few years, cone beam CT (CBCT) has become a popular clinical practice in the three-dimensional (3D) imaging of the oro-maxillofacial region which has made the complex anatomy of maxilla and mandible very simple.[9] It is not only used to rule out the extension of tumors three-dimensionally and related anatomical structures but also helps in postoperative assessment. In comparison to conventional CT it has many advantages such as CBCT has a lower radiation dose, a higher spatial resolution, and same number of or fewer metal-induced artifacts. However, on the contrary, CBCT is not suitable for assessing soft tissue structures.[12],[13] On a CBCT image, infiltration of the jaws can be identified as an irregular osteolysis with loss of cortical structures.

Ultrasonography

It has been widely accepted that ultrasonography (USG) is superior to palpation in detecting lymph nodes and its metastases.[14] In comparison to other imaging modalities, USG has many advantages such as its low price, low patient burden, and possibilities for follow-up.[15] USG is the method of choice for detecting metastases foci at glandular organs such as the thyroid and salivary glands and in guided biopsy for glandular structures.[11] Compared to CT, USG has comparable spatial resolution and better contrast resolution. Although USG may give a limited field of view, it provides a multiplanar image as in CT and MRI. However, instead of these advantages, many studies have found that borderline lymph nodes cannot be diagnosed with reliability using USG. Hence, USG should not be considered as the diagnostic imaging modality. Furthermore in USG assisted fine needle aspiration cytology (FNAC), there is high chances of aspiration of metastases in the lymph nodes.[16] It has a sensitivity of 72% and specificity of 75% to detect metastases in head and neck.


   Functional Imaging Techniques Top


These techniques facilitate the assessment of the complex interrelated processes occurring in the cancer tissue microenvironment, such as hypoxia, angiogenesis, metabolism, and pH. These techniques have the potential to (1) predict the cancerous tissue behavior and its response to treatment; (2) to evaluate the effectiveness of anti-cancerous drugs such as the anti-vascular agents; (3) to detect cancerous cells response during treatment; and (4) to identify residual/recurrent cancers.[11]

Positron emission tomography

It is a nuclear medicine imaging technique which uses both different isotopes and different camera system to image the distribution of radioisotopes within the body, but as with conventional nuclear medicine techniques, it is functional imaging method. PET isotopes are radioactive isotopes of atoms normally present in many physiological compounds such as carbon, nitrogen, and oxygen.18F-fluoro-2-deoxy-D-glucose (18FDG) is a radioactively labeled glucose analog with fluorine for hydroxy substitution on a D-glucose substrate. It has a half-life of 110 min that is sufficient to perform a complex process of radiolabelling and reconstruction, and also to keep the radiation dose level low for the patient.

18FDG is utilized due to its unique character to emit positrons, and it can be accurately localized in the scanning process. As tumor cells are very active cells, having an increased uptake of glucose (glycolytic rates), FDG accumulates within tumor cells, producing a “hot spot” on the PET image. These hot spots can easily be distinguished from surrounding normal tissue.[17],[18] PET showed an outstanding performance in detection of unknown primary tumors of head and neck region.[19],[20],[21],[22],[23],[24],[25],[26],[27],[28],[29] However, along with multiple advantages FDG-PET scan has certain disadvantages also, like high cost, limitation in detecting an occult primary tumor in cervical lymph node metastasis, automatic segmentation of tumor volume is not possible because of increased background signal caused by radiation-induced inflammation. False negatives result in low-grade tumors such as lymphoma and sarcoma. On the other hand, false positive results are seen in inflammatory and infection (abscesses, tuberculosis).

FDG-PET scan has a sensitivity of 90% and specificity of 94%. Thus, PET scan is superior to CT and MRI scan in detecting metastasis (Kitawaga et al., 2003). Nowadays PET scans are used along with CT or MRI scans. This “co-registration or fusion” of PET with CT/MRI gives an advantage to determine both anatomic and metabolic information. It facilitates the exact localization of abnormal minute areas of increased radiotracer activity that would have been a difficult job or rather impossible to localize on PET images alone. PET-CT is also capable to distinguish structures that normally show high metabolic activity from those tissues with abnormally increased activity. Disadvantages of PET-CT are: Patient motion and attenuation (transmission) of artifacts because of metallic objects in the pathway of the CT beam, such as pacemakers, hip prostheses, and dental prostheses. In comparison with PET scan, the fusion scan PET/CT has greater diagnostic accuracy in the patients of head and neck cancer and metastases.[30]

Diffusion-weighted imaging

Diffusion-weighted imaging (DWI) is an easy, simple, quick, and functional MR technique, that produces MR images of biological tissues within the body sensitized with the common but specific characteristics based on the difference of the mobility of water in different tissues which lead to generation of DWIs and apparent diffusion coefficient (ADC) maps. ADC acts as a marker of cell density.[31] The ADC value is highest for benign lymphadenopathy and lowest for metastatic nodes. However, the presence of necrosis in metastatic cancers increases the ADC value. DWIs are being used to identify a range of cancers, and the ADC value elucidates the characterization of head and neck tumors and also to monitor the treatment as well as recurrent tumors.[32],[33],[34] During treatment, an increase in the ADC value of cancer can result as a result of an increase in cell permeability and swelling, cell destruction, diffusion of water into extracellular space, and necrosis. These changes may also occur in early phases of treatment, preceding volume changes.[11]

Dynamic contrast-enhanced magnetic resonance imaging

Dynamic contrast-enhanced (DCE)-MRI is the acquisition of MRI images before, after and during administration of low-molecular-weight contrast media (1000 Da) intravenously that rapidly diffuse in the extracellular fluid space.[35] The contrast agents used for DCE-MRI are often gadolinium-based. Gadolinium injection lead to decrease in the relaxation time and therefore, images made after contrast media injection have higher signal. First a T1-weighted MRI scan is done without contrast media, then gadolinium is injected (0.05–0.1 mmol/kg) and another T1-weighted scan is made. Then both scans are compared to rule out the difference in blood flow in the tissues. New vascularization or angiogenesis is a signature of neoplasm and is one of the potent principle targets for quantitative imaging.[36],[37],[38] It is widely accepted that all solid tumors are dependent upon neovascularization for survival and growth,[39] and many anti-angiogenic drugs are currently in clinical trials.[40] Thus, methods for imaging and quantitatively assessing this angiogenesis will be useful in clinical oncology.[41] In damaged tissues with a lower cell density, the gadolinium stays in the extracellular space longer. In comparison to blood vessel formed by normal physiologic processes, the vessels produced during tumor progression angiogenesis are characteristically ill-integrated, fragile, and incompletely formed.[36],[37] DCE-MRI is an imaging technique that can evaluate the density, integrity, and leakiness of tissue vasculature. However, on the contrary, it has some limitations also like overlapping between malignant and benign inflammatory tissue, failure to reveal micrometastases, and the low predictive value with regard to clinical outcome.

Magnetic resonance spectroscopy

Magnetic resonance spectroscopy (MRS) helps in characterization of tissue, forming their anatomic images by interrogating the concentration of certain metabolites during usual cell metabolism with the help of same conventional MRI machine. The most commonly used nuclei in MRS are 1H (proton), 23Na (sodium), 31P (phosphorus). Because of better results due to high signal-to-noise ratio, proton spectroscopy is more preferred as compared to other nuclei.[42],[43] Spectroscopy is a test series that measures the chemical metabolism taking place in different tumor types. There are many metabolites/products of metabolism that can be used to differentiate between tumor types. While MRI identifies the anatomical location of a tumor, MR spectroscopy compares the internal biological reactions in cases of stroke, epilepsy, metabolic disorders, infections, and neurodegenerative diseases and differentiates with that of normal surrounding tissue. The biochemicals which can be detected in MRS include choline-containing compounds (cell membranes), creatine (energy metabolism), inositol and glucose (sugars), N-acetylaspartate, alanine and lactate which are elevated in some tumors.[42] By comparing the frequencies of metabolites in normal and tumor tissue, the type of tissue can be identified and distinguished.[43] Lactate is also been found as a potential biomarker in detection of metastatic nodes from HNSCC.[44]

Blood oxygen level-dependent magnetic resonance imaging

Blood oxygen level-dependent (BOLD) is a non-invasive functional MRI modality that can identify hypoxic cancers (deoxy-hemoglobin) which are likely to respond to radiotherapy and chemotherapy. The BOLD technique takes advantage of the fact that the change from diamagnetic oxyhemoglobin to paramagnetic deoxyhemoglobin, that takes place with tumor mass activation, results in decreased signal intensity on MRI. Abnormal tissue mass are detected on the basis of their differential magnetic susceptibility. There are several limitations for BOLD technique: Signals produced by BOLD may not be result of oxygenation only, short-lived effect of hypoxic tissue which lead to nonreproducibilty of results, and several times changes in signal are minute to detect. But, in spite of certain limitations, BOLD has been proved to be successful to detect decrease in blood deoxyhemoglobin in human cancers [11],[30],[45] and thus joins a helping hand in treatment for hypoxic cancers.


   Strategic Planning in Detection of Metastasis Top


Strategic planning for lymph node metastases detection

Cervical lymph node metastasis is one of the most important prognostic factors in treatment of HNSCC. A meta-analysis concluded that, for the detection of lymph node metastases, US and especially US-guided FNAC, CT, MRI are the techniques with better diagnostic value than that of conventional imaging.[46] FDG-PET has also an excellent diagnostic role in the overall evaluation of the presence of lymph node metastases in HNSCC patients.[47] The most important indicator in HNSSC prognosis is detection of occult lymph node, particularly micrometastases (>0.2 mm but <2.0 mm). A meta-analysis by Kyzas et. al.,[47] inferred that, only 50% of the occult lymph node metastases can be detected by FDG-PET. This led to the use of sentinel lymph node scintigraphy, which proved to be a valid alternative to elective stage dissection. FDG-PET with CT/MRI has been found to be more accurate than FDG-PET alone in detection of subclinical lymph node (N0) metastases.[48] Thus, PET and PET-CT have the highest accuracy for detecting occult micrometastases in cervical lymph nodes.[49]

New high-resolution MRI like DW-MRI is also considered complimentary to standard MRI. Further implementation of DW-MRI into routine imaging will mostly depend on the standardization of imaging technique and interpretation.[49]

Strategic planning for detection of distant metastases

The incidence of distant metastasis in HNSCC is directly related to the stage of disease. Till date, no comparisons between the accuracy of CT, PET, PET-CT were not made. Chest CT is a gold standard for detection of lung metastasis (most common) from HNSCC.[50] Introduction of multi-receiver channel MR has brought a miraculous change in imaging world, now whole-body MRI has become possible, which has potential to detect metastases of primary head and neck tumors.[51]

Most studies that used FDG-PET for screening of distant metastases are deficient in valid comparison between PET and CT. With high spatial resolution, multi-detector row CT may act as an imaging tool comparable to FDG-PET in evaluation of distant metastases in HNSCC patients and help to rule out FDG abnormalities.[51] Combination of PET and CT in PET-CT provides the most attractive, most accurate and onestop option. Besides advancements, in clinical practice the detection of distant metastases during follow-up is of minimal concern since currently no treatment options with complete cure is available.


   Conclusion Top


The diagnosis of metastatic lesions is a real challenge, to both the clinician and the radiologist. Tumor thickness is more critical than the size of the tumor in terms of prognosis, and it is closely related to metastasis. The tumor primary site, tumor thickness and degree of differentiation are the most important determinants for metastasis. Early detection of metastasis is the most efficient way to reduce the high mortality and morbidity resulting from it. Pretherapeutic imaging has predictive value for patient outcome. Based on per-therapeutic imaging, personalized replanning during radiotherapy may help to increase control rates and reduce toxic effects to normal tissues. Post-therapeutic imaging is of utmost importance in detection of recurrent tumors. Hence, it is an urgent need to devise efficient diagnostic tools for early detection of oral dysplasia, malignancy and metastasis that are diagnostic, noninvasive and can be easily performed in an outpatient set-up.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
   References Top

1.
Kumar G, Manjunatha B. Metastatic tumors to the jaws and oral cavity. J Oral Maxillofac Pathol 2013;17:71-5.  Back to cited text no. 1
[PUBMED]  Medknow Journal  
2.
Bodner L, Sion-Vardy N, Geffen DB, Nash M. Metastatic tumors to the jaws: A report of eight new cases. Med Oral Patol Oral Cir Bucal 2006;11:E132-5.  Back to cited text no. 2
    
3.
van der Waal RI, Buter J, van der Waal I. Oral metastases: Report of 24 cases. Br J Oral Maxillofac Surg 2003;41:3-6.  Back to cited text no. 3
    
4.
Hirshberg A, Leibovich P, Buchner A. Metastases to the oral mucosa: Analysis of 157 cases. J Oral Pathol Med 1993;22:385-90.  Back to cited text no. 4
    
5.
Yoshii T, Muraoka S, Sano N, Furudoi S, Komori T. Large cell carcinoma of the lung metastatic to the mandibular gingiva. J Periodontol 2002;73:571-4.  Back to cited text no. 5
    
6.
Hirshberg A, Shnaiderman-Shapiro A, Kaplan I, Berger R. Metastatic tumours to the oral cavity – Pathogenesis and analysis of 673 cases. Oral Oncol 2008;44:743-52.  Back to cited text no. 6
    
7.
Calhoun KH, Fulmer P, Weiss R, Hokanson JA. Distant metastases from head and neck squamous cell carcinomas. Laryngoscope 1994;104:1199-205.  Back to cited text no. 7
    
8.
Genden EM, Ferlito A, Bradley PJ, Rinaldo A, Scully C. Neck disease and distant metastases. Oral Oncol 2003;39:207-12.  Back to cited text no. 8
    
9.
Omar EA. The outline of prognosis and new advances in diagnosis of oral squamous cell carcinoma (OSCC): Review of the literature. J Oral Oncol 2013;2013:519312.  Back to cited text no. 9
    
10.
Scully C, Bagan J. Oral squamous cell carcinoma overview. Oral Oncol 2009;45:301-8.  Back to cited text no. 10
    
11.
King AD. Multimodality imaging of head and neck cancer. Cancer Imaging 2007;7:S37-46.  Back to cited text no. 11
    
12.
Boeddinghaus R, Whyte A. Current concepts in maxillofacial imaging. Eur J Radiol 2008;66:396-418.  Back to cited text no. 12
    
13.
Schulze R, Heil U, Gross D, Bruellmann DD, Dranischnikow E, Schwanecke U, et al. Artefacts in CBCT: A review. Dentomaxillofac Radiol 2011;40:265-73.  Back to cited text no. 13
    
14.
Ying M, Pang BS. Three-dimensional ultrasound measurement of cervical lymph node volume. Br J Radiol 2009;82:617-25.  Back to cited text no. 14
    
15.
Ganguly A, Burnside G, Nixon P. A systematic review of ultrasound-guided FNA of lesions in the head and neck – Focusing on operator, sample inadequacy and presence of on-spot cytology service. Br J Radiol 2014;87:20130571.  Back to cited text no. 15
    
16.
van den Brekel MW. Lymph node metastases: CT and MRI. Eur J Radiol 2000;33:230-8.  Back to cited text no. 16
    
17.
Rusthoven KE, Koshy M, Paulino AC. The role of fluorodeoxyglucose positron emission tomography in cervical lymph node metastases from an unknown primary tumor. Cancer 2004;101:2641-9.  Back to cited text no. 17
    
18.
Mahoney EJ, Spiegel JH. Evaluation and management of malignant cervical lymphadenopathy with an unknown primary tumor. Otolaryngol Clin North Am 2005;38:87-97, viii-ix.  Back to cited text no. 18
    
19.
Hanasono MM, Kunda LD, Segall GM, Ku GH, Terris DJ. Uses and limitations of FDG positron emission tomography in patients with head and neck cancer. Laryngoscope 1999;109:880-5.  Back to cited text no. 19
    
20.
Joshi U, van der Hoeven JJ, Comans EF, Herder GJ, Teule GJ, Hoekstra OS. In search of an unknown primary tumour presenting with extracervical metastases: The diagnostic performance of FDG-PET. Br J Radiol 2004;77:1000-6.  Back to cited text no. 20
    
21.
Queiroz MA, Huellner MW. PET/MR in cancers of the head and neck. Semin Nucl Med 2015;45:248-65.  Back to cited text no. 21
    
22.
Chen AY, Myers JN. Cancer of the oral cavity. Dis Mon 2001;47:275-361.  Back to cited text no. 22
    
23.
Canjau S, Sinescu C, Negrutiu M, Rusu L, Todea C.18 FDG-PET and PET/CT for minimal invasive diagnosis of head and neck cancer. Fiziol Physiol 2014;24:20-5.  Back to cited text no. 23
    
24.
Di Martino E, Nowak B, Hassan HA, Hausmann R, Adam G, Buell U, et al. Diagnosis and staging of head and neck cancer: A comparison of modern imaging modalities (positron emission tomography, computed tomography, color-coded duplex sonography) with panendoscopic and histopathologic findings. Arch Otolaryngol Head Neck Surg 2000;126:1457-61.  Back to cited text no. 24
    
25.
Greven KM, Williams DW 3rd, McGuirt WF Sr., Harkness BA, D'Agostino RB Jr., Keyes JW Jr., et al. Serial positron emission tomography scans following radiation therapy of patients with head and neck cancer. Head Neck 2001;23:942-6.  Back to cited text no. 25
    
26.
Jungehülsing M, Scheidhauer K, Damm M, Pietrzyk U, Eckel H, Schicha H, et al. 2[F]-fluoro-2-deoxy-D-glucose positron emission tomography is a sensitive tool for the detection of occult primary cancer (carcinoma of unknown primary syndrome) with head and neck lymph node manifestation. Otolaryngol Head Neck Surg 2000;123:294-301.  Back to cited text no. 26
    
27.
Joo YH, Yoo IR, Cho KJ, Park JO, Nam IC, Kim CS, et al. The value of preoperative 18F-FDG PET/CT for the assessing contralateral neck in head and neck cancer patients with unilateral node metastasis (N1-3). Clin Otolaryngol 2014;39:338-44.  Back to cited text no. 27
    
28.
Rankin SC. PET in face and neck tumours. Cancer Imaging 2006;6:S89-95.  Back to cited text no. 28
    
29.
Schaarschmidt BM, Heusch P, Buchbender C, Ruhlmann M, Bergmann C, Ruhlmann V, et al. Locoregional tumour evaluation of squamous cell carcinoma in the head and neck area: A comparison between MRI, PET/CT and integrated PET/MRI. Eur J Nucl Med Mol Imaging 2016;43:92-102.  Back to cited text no. 29
    
30.
Rijpkema M, Kaanders JH, Joosten FB, van der Kogel AJ, Heerschap A. Effects of breathing a hyperoxic hypercapnic gas mixture on blood oxygenation and vascularity of head-and-neck tumors as measured by magnetic resonance imaging. Int J Radiat Oncol Biol Phys 2002;53:1185-91.  Back to cited text no. 30
    
31.
Schöder H, Yeung HW, Gonen M, Kraus D, Larson SM. Head and neck cancer: Clinical usefulness and accuracy of PET/CT image fusion. Radiology 2004;231:65-72.  Back to cited text no. 31
    
32.
Maeda M, Kato H, Sakuma H, Maier SE, Takeda K. Usefulness of the apparent diffusion coefficient in line scan diffusion-weighted imaging for distinguishing between squamous cell carcinomas and malignant lymphomas of the head and neck. AJNR Am J Neuroradiol 2005;26:1186-92.  Back to cited text no. 32
    
33.
Sumi M, Sakihama N, Sumi T, Morikawa M, Uetani M, Kabasawa H, et al. Discrimination of metastatic cervical lymph nodes with diffusion-weighted MR imaging in patients with head and neck cancer. AJNR Am J Neuroradiol 2003;24:1627-34.  Back to cited text no. 33
    
34.
Habermann CR, Gossrau P, Graessner J, Arndt C, Cramer MC, Reitmeier F, et al. Diffusion-weighted echo-planar MRI: A valuable tool for differentiating primary parotid gland tumors? Rofo 2005;177:940-5.  Back to cited text no. 34
    
35.
Padhani AR. Dynamic contrast-enhanced MRI in clinical oncology: Current status and future directions. J Magn Reson Imaging 2002;16:407-22.  Back to cited text no. 35
    
36.
Ribatti D, Vacca A, Presta M. The discovery of angiogenic factors: A historical review. Gen Pharmacol 2000;35:227-31.  Back to cited text no. 36
    
37.
Sadick M, Schoenberg SO, Hoermann K, Sadick H. Current oncologic concepts and emerging techniques for imaging of head and neck squamous cell cancer. Laryngorhinootologie 2012;91 Suppl 1:S27-47.  Back to cited text no. 37
    
38.
Atri M. New technologies and directed agents for applications of cancer imaging. J Clin Oncol 2006;24:3299-308.  Back to cited text no. 38
    
39.
Carmeliet P, Jain RK. Angiogenesis in cancer and other diseases. Nature 2000;407:249-57.  Back to cited text no. 39
    
40.
Verhoef C, de Wilt JH, Verheul HM. Angiogenesis inhibitors: Perspectives for medical, surgical and radiation oncology. Curr Pharm Des 2006;12:2623-30.  Back to cited text no. 40
    
41.
Yankeelov TE, Gore JC. Dynamic contrast enhanced magnetic resonance imaging in oncology: Theory, data acquisition, analysis, and examples. Curr Med Imaging Rev 2009;3:91-107.  Back to cited text no. 41
    
42.
Majós C, Aguilera C, Cos M, Camins A, Candiota AP, Delgado-Goñi T, et al. In vivo proton magnetic resonance spectroscopy of intraventricular tumours of the brain. Eur Radiol 2009;19:2049-59.  Back to cited text no. 42
    
43.
Sanghvi DA. Recent advances in imaging of brain tumors. Indian J Cancer 2009;46:82-7.  Back to cited text no. 43
[PUBMED]  Medknow Journal  
44.
Razek AA, Elsorogy LG, Soliman NY, Nada N. Dynamic susceptibility contrast perfusion MR imaging in distinguishing malignant from benign head and neck tumors: A pilot study. Eur J Radiol 2011;77:73-9.  Back to cited text no. 44
    
45.
Christen T, Bolar DS, Zaharchuk G. Imaging brain oxygenation with MRI using blood oxygenation approaches: Methods, validation, and clinical applications. AJNR Am J Neuroradiol 2013;34:1113-23.  Back to cited text no. 45
    
46.
de Bondt RB, Nelemans PJ, Hofman PA, Casselman JW, Kremer B, van Engelshoven JM, et al. Detection of lymph node metastases in head and neck cancer: A meta-analysis comparing US, USGFNAC, CT and MR imaging. Eur J Radiol 2007;64:266-72.  Back to cited text no. 46
    
47.
Kyzas PA, Evangelou E, Denaxa-Kyza D, Ioannidis JP. 18F-fluorodeoxyglucose positron emission tomography to evaluate cervical node metastases in patients with head and neck squamous cell carcinoma: A meta-analysis. J Natl Cancer Inst 2008;100:712-20.  Back to cited text no. 47
    
48.
Ng SH, Yen TC, Chang JT, Chan SC, Ko SF, Wang HM, et al. Prospective study of [18F] fluorodeoxyglucose positron emission tomography and computed tomography and magnetic resonance imaging in oral cavity squamous cell carcinoma with palpably negative neck. J Clin Oncol 2006;24:4371-6.  Back to cited text no. 48
    
49.
de Bree R, Castelijns JA, Hoekstra OS, Leemans CR. Advances in imaging in the work-up of head and neck cancer patients. Oral Oncol 2009;45:930-5.  Back to cited text no. 49
    
50.
Senft A, de Bree R, Hoekstra OS, Kuik DJ, Golding RP, Oyen WJ, et al. Screening for distant metastases in head and neck cancer patients by chest CT or whole body FDG-PET: A prospective multicenter trial. Radiother Oncol 2008;87:221-9.  Back to cited text no. 50
    
51.
Ng SH, Chan SC, Liao CT, Chang JT, Ko SF, Wang HM, et al. Distant metastases and synchronous second primary tumors in patients with newly diagnosed oropharyngeal and hypopharyngeal carcinomas: Evaluation of (18) F-FDG PET and extended-field multi-detector row CT. Neuroradiology 2008;50:969-79.  Back to cited text no. 51
    




 

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