Clinical application value and progress of PET/CT in nasopharyngeal carcinoma
Fengwei Zeng, Muhua Cheng
Department of Nuclear Medicine, The Third Hospital Affiliated Sun Yat-sen University, Guangdong, Guangzhou 510630, China
Corresponding author: Cheng Muhua, Professor, M.D.; E-mail: email@example.com
Citation: Zeng FW, Cheng MH. Clinical application value and progress of PET/CT in nasopharyngeal carcinoma. J Nasopharyng Carcinoma, 2014, 1(2): e2. doi:10.15383/jnpc.2.
Competing interests: The authors have declared that no competing interests exist.
Conflict of interest: None.
Copyright: 2014 By the Editorial Department of Journal of Nasopharyngeal Carcinoma. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Abstract: Nasopharyngeal carcinoma (NPC) is one of common head and neck cancers which mainly threaten people in Southeast Asia. PET/CT plays an important role in radiotherapy for NPC. This article reviews the PET/CT in the diagnosis, staging, guiding treatment, monitoring of therapy efficacy, focal residual and recurrence, prognosis and progress of NPC.
Keywords: Nasopharyngeal carcinoma; Clinical application; PET/CT
Nasopharyngeal carcinoma (NPC) is one of the common head and neck malignant tumors among southern China and Southeast Asian countries, which often occur in the pharyngeal recess. There is a close association between Epstein-Barr virus (EBV) and NPC pathogenesis. The annual incidence per 100,000 persons ranged from 10 to 30[2-3]. At present, the main method of treatment for NPC is radiotherapy, which treatment effect is very satisfactory for early NPC, local recurrence and distant metastasis. The 5-year overall survival rate is about 50%-70%[4-7]. Therefore, early diagnosis and staging of NPC patients is very important to improve the survival rate. Positron Emission Tomography/Computed Tomography (PET/CT) images could have a significant impact on diagnosing and staging malignant disease, monitoring of efficacy, prognostic and so on. A lot of researches indicated that fluor-18-fluorodeoxyglucose positron emission tomography with computed tomography (18F-FDG PET/CT) is superior to separate PET and conventional imaging (CT, MRI, etc.) in the diagnosis, staging, guiding treatment, prognosis and so on[8-13]. In recent years, the 11C-choline PET/CT imaging in the diagnosis and staging of NPC patients have obtained satisfactory results, especially in the T staging of NPC.
This review is focused on the the value of PET/CT in the diagnosis, staging, therapeutic evaluation, guiding radiotherapy and prognosis of NPC, the diagnostic value of PET/CT in residual and recurrence of NPC and complications after NPC radiotherapy.
1 The value of PET/CT in the diagnosis of NPC
The diagnostic performance of PET/CT is better than conventional imaging examination such as PET, CT, MRI. Eighty-six cases of NPC were analyzed retrospectively by Chen et al., their result showed that 18F-FDG PET/CT, PET and CT accuracy in the diagnosis of NPC were 95.4%, 82.6%, 73.3%, respectively. Furthermore, the differences between 18F-FDG PET/CT and either PET alone or CT alone were statistically significant (P<0.05). The sensitivity, specificity, accuracy, positive predictive value and negative predictive value of PET/CT studies for diagnosis NPC were 96%, 94.4%, 96% and 94.4%, respectively. Gordian et al. reported that 18F-FDG PET/CT had sensitivity, specificity, positive predictive value, negative predictive value and accuracy of 92%, 90%, 90%, 90%, and 91%, respectively, as compared with 92%, 65%, 76%, 86%, and 80% for PET, and 92%, 15%, 60%, 60%, and 60% for conventional imaging (CT and MRI). The reports of whole body 18F-FDG PET/CT scans, performed 43 NPC patients were analyzed retrospectively (Wang et al.), their results demonstrated that the overall accuracy, specificity, sensitivity, positive predictive value, negative predictive value of 18F-FDG PET/CT were 95.3%, 100.0%, 85.7%, 93.8%, and 100.0%, respectively, and those of conventional imaging (CT and MRI) were 65.5%, 79.4%, 64.7%, 81.8%, and 57.9%, respectively.
2 The value of PET/CT in the staging of NPC
2.1 The T staging of NPC
18F-FDG PET/CT is benefited in the T staging of NPC. Chen et al. compared 18F-FDG PET/CT, PET and CT in the detect of primary site of NPC, the T stage was accurately determined in 18 cases out of 20 cases with 18F-FDG PET/CT. Both PET alone and CT alone correctly assessed the T stage 15 cases out of 20 cases. Lin et al. in the diagnosis of 68 cases of NPC patients indicated that coincidence rate of 18F-FDG PET/CT with MR was 95.5% (65 cases) on lesion. Three cases were clearly displayed by PET/CT, but not by MRI. However, many studies showed 18F-FDG PET/CT in the diagnosis NPC with local invasion such as skull base, intracranial area, orbital apex, parapharyngeal space was not so well compared with MRI. Because the high physiological metabolism of brain and eye muscle affected skull base, intracranial area, orbital apex show. In addition, soft tissue resolution and parapharyngeal space invasion of MRI was better than that of PET/CT. Wu et al. used 11C-choline as a imaging agent in the PET/CT and compared with 18F-FDG PET/CT. Ten patients with newly diagnosed and 5 patients recurrent NPC were enrolled in the study. All of the patients with 11C-choline PET/CT were positive, but 13 cases were showed positive and 2 cases of skull base and intracranial recurrence of NPC patients were showed negative. The sensitivity of 18F-FDG PET/CT in detecting NPC was 86.6%, compared with a 100% sensitivity for 11C-choline PET/CT (t=2.143, P=0.483). The SUVmax of lesions detected was higher using 18F-FDG than using 11C-choline (SUVmax: 6.84±2.76 vs. 12.81±5.00, t=6.416, P<0.001), but the T/B ratio was much higher for 11C-choline than for 18F-FDG (18.62±7.95 vs. 1.38±0.59, t=8.801, P<0.001). Because 11C-choline uptake in normal brain was lower than 18F-FDG (0.38±0.09 vs. 10.01±1.90, t=19.68, P<0.001). Compared with18F-FDG PET/CT, 11C-choline PET/CT improved the delineation of intracranial invasion in 6 of 12 patients, skull base invasion in 4 of 14 patients, and orbital invasion in 3 of 3 patients.
2.2 The N staging of NPC
Neck lymph node metastases was the common clinical symptoms in patients with NPC. Lee et al. did a retrospective analysis of 4768 patients, 75.8% of patients were discovered neck lymph node metastases at initial diagnosis. Chen et al. had compared of 18F-FDG PET/CT, PET and CT on detecting neck lymph node metastases of the NPC patients, PET/CT was found to be accurate in 100% (20/20), where PET alone and CT alone accurately determined lymph node involvement in 20 out of 20 patients (100%) and 18 out of 20 patients. Hu et al. conducted a study which was to compare the diagnostic value of 18F-FDG PET/CT with that of MRI in detecting nodal metastasis of NPC. Among the 105 patients, nodal metastasis patterns shown on PET/CT and MRI were diverse in 35 patients. Thirty cervical nodes were positive on PET/CT, but negative on MRI. Twenty-five of them were later confirmed positive by follow-up. Thirty-seven cervical nodes were negative on PET/CT, but positive on MRI. Twenty-one of them were confirmed negative by follow-up. Lin et al. analyzed 68 cases of NPC patients with lymph node metastases and found that 39 out of 138 positive lymph nodes whose diameters were <1 cm and identified by 18F-FDG PET/CT, which were not assured of positive lymph nodes by MRI, accounting for 28.0% (39/138). Ten patients underwent biopsy on their neck lymph nodes. Fourteen out of 16 positive lymph nodes detected by PET/CT were confirmed by pathological examination, while MRI was not certain about eight lymph nodes and found the other eight lymph nodes negative. Two cases detected by PET/CT changed its N staging because of the lock lymph node metastasis. The results of follow-up a total of 614 lymph nodes in 116 patients were analyzed by Zhang et al. showed that the sensitivity, specificity and accuracy of 18F-FDG PET/CT in diagnosing node metastasis were 93.2%, 98.2% and 95.4%, while those of MRI were 88.8%, 91.2% and 89.9%, respectively. Based on above studies, 18F-FDG PET/CT was superior to MRI in diagnosing lymph node metastasis. We should be alert to the false-positive and false-negative assessment based on 18F-FDG PET/CT scan findings that may be caused by retropharyngeal nodes, inflammatory hyperplastic, large area lymph nodes of necrosis and node in diameter less than spatial resolution limitation of PET[17, 22-23].
2.3 The M staging of NPC
18F-FDG PET/CT had a better diagnostic efficiency in M staging of NPC. Lin et al. discovered that 18F-FDG PET/CT showed the distant metastases to lung, bone, and liver occurred in eight patients. The stage of 24 NPC patients was adjusted after PET/CT scan, among which the stage of 12 patients was adjusted higher and that of 12 patients was adjusted lower, with a total adjustment rate of 35.3%, when he analyzed sixty-eight NPC patients. Ng et al.  found that PET/CT correctly modified M staging in eight patients (7.2%) and disclosed a second primary lung malignancy in one patient (0.9%) among the 111 NPC patients. Chua et al. thought 18F-FDG PET/CT was superior to PET alone, CT of the thorax and abdomen, skeletal scintigraphy and conventional imaging examination comprising chest X-ray, abdomen ultrasound and bone scanning. The sensitivities and specificities of PET alone, CT of the thorax and abdomen, bone scanning and conventional imaging examination were 83.3%, 83.3%, 66.7% and 33.3%, respectively. And the specificities of PET alone, CT of the thorax and abdomen, bone scanning and conventional imaging examination were 97.2%, 94.4%, 91.7% and 90.3%, respectively. The corresponding accuracies were 96.2%, 93.6%, 89.7% and 85.9%. Tang et al. discovered that 86 cases of the 583 eligible patients were found to have distant metastases. seventy-one patients (82.6%) by 18F-FDG PET/CT were superior to 31 patients (36.0%) by conventional imaging examination, and 34 cases cases detected by 18F-FDG PET/CT accurately up-regulated its staging. Four cases accurately down-regulated its staging. Recently, some scholars applied the meta-analysis to evaluate the accuracy of 18F-FDG PEC/CT in distant metastases of NPS, the result showed 18F-FDG PET/CT had a better diagnostic efficiency than conventional work-up on detecting distant metastases.
3 The role of PET/CT in guiding treatment of NPC
3.1 Generation of gross tumor volume (GTV)
Gross tumor volume and the determination scope of the tumor invasion was the key to radiotherapy of the NPC patients. PET/CT located biological target volume from metabolism, blood flow, tissue proliferation, hypoxia, tumor specific receptor, angiogenesis, apoptosis and so on. In addition, PET/CT had obvious advantages over CT. It is difficult to generate GTV according to the conventional imaging examination after radiotherapy. Zheng et al. identified that for the remaining 29 patients, GTV based on PET/CT was smaller than GTV based on CT in 24 (82.8%) cases and was greater in 5 (17.2%) cases. The target volume had to be significantly modified in 9 of 29 patients, as GTV based on 18FDG-PET images failed to be enclosed by the treated volume in the salvage treatment plan performed based on GTV based on CT simulation images. But another research result of Zheng et al. showed that 39 patients without distant metastasis proceeded to three-dimensional conformal radiotherapy planning. Inadequate coverage of the GTVPET/CT and PTVPET/CT by the PTVCT occurred in 7 (18%) and 20 (51%) patients, respectively. This resulted in < 95% of the GTVPET/CT and PTVPET/CT receiving ≥ 95% of the prescribed dose in 4 (10%) and 13 (33%) patients, respectively. Xin et al. considered simulate actual treatment in the detachable phantom, including clinical treatment volume (CTV), tumor treatment volume (GTV), high metabolic gross treatment volume (FGTV). Its size 10×7 cm, 4×4 cm, 2×2 cm, respectively. The CTV put 0.3 cm into PTV. The radiation dose of PTV, GTV and FGTV were set to 1.8 Gy, 2.0Gy, and 1.8 Gy, respectively, which would achieve good efficacy. Therefore, 18F-FDG PET/CT image-guided dynamic intensity-modulated radiation therapy (IMRT) is feasible.
3.2 Guiding radiotherapy treatment modality and rescue therapy
Some radiotherapy modality for NPC may be changed after 18F-FDG PET/CT examination. Law et al. found that forty-eight patients underwent a staging PET/CT, in which 4 cases (8%) of NPC changed the primary treatment modality, 12 cases (25%) changed treatment modality or dose and 32 cases (66%) was no change in treatment modality. Zheng et al. discovered that all 33 patients were referred for salvage treatment in the pre-FDG-PET decision, after knowledge of the FDG-PET results, the decision to offer salvage treatment was withdrawn in 4 of 33 patients (12.1%), as no abnormal uptake of FDG was found at nasopharynx. Spontaneous remission was observed in repeat biopsies and no local recurrence was found in these 4 cases. Thirty-three patients with NPC had 45 18F-FDG PET/CT examinations were analyzed retrospectively. In this study, Gordin et al. found that imaging with PET/CT eliminated the need for previously planned diagnostic procedures in 11 patients, induced a change in the planned therapeutic approach in 5 patients, and guided biopsy to a speciﬁcal metabolically active area inside an edematous region in 3 patients.
4 The value of PET/CT in NPC therapeutic evaluation
Assessment of early treatment effect helped to adjust therapy method and reduce the complications. Lesions of metabolic reduced before and after radiotherapy, namely the reduction of 18F-FDG uptake were consistent with the pathological changes of tumor tissue. A study of Lin et al. was to evaluate the treatment response of 18F-FDG PET/CT. The medium SUVmax of primary tumor lesion was 11.1 (range 3.4-26.9) in 61 NPC patients before treatment, then, reduced to 3.5 (range 0-8.1) after radiotherapy with a dose of 50 Gy, and decreased to 3.1 (range 0-8.2) after radiotherapy. The medium SUVmax of primary tumor lesion was 2.5 (range 0-6.9) one month after radiotherapy (P<0.001). The medium SUVmax of regional lymph node lesion was 9.3 (range 2.5-31.5) before treatment, and reduced to 3.1 (range 0-15.8) after radiotherapy with a dose of 50 Gy, then, decreased to 2.4 (range 0-7.2) after radiotherapy. The medium SUVmax of regional lymph node lesions was 1.5 (range 0-5.4) one month after radiotherapy (P<0.01). The efficacy of 41 NPC patients who underwent 18F-FDG PET/CT scan were reported by Xie et al.. The mean SUVmax was 7.3 (range 3.2-20.7) before treatment, and the SUVmax<2.5 of 26 patients with metabolic complete remission after treatment, the remaining 15 patients’ SUVmax≥2.5. Another study of Xie et al. reported that the median SUVmax was 8.55 (range 2.8-24.6) in 62 NPC patients before treatment. Fifty-eight of the 62 patients’ treatment responses were evaluated by 18F-FDG PET/CT scan. The post-treatment PET/CT scan did not show any abnormal FDG uptake (SUVmax<2.5, metabolic complete response, MCR) in 35 patients, and the remaining 23 patients with SUVmax≥2.5. Law et al. found that PET/CT had higher negative predictive value than conventional imaging examination (CT or MRI) that were 93 %, 91%, respectively in 21 NPC patients, and had fewer equivocal results than MRI.
5 The value of PET/CT in diagnosis of residual and recurrence of NPC
Radiotherapy of NPC would cause regional tissue radioactive damaging, mucosal thickening, soft tissue swelling, fibrosis or scar tissue formation and so on, meanwhile, metastases maybe occur in other tissues. Correct evaluation of regional and systemic disease progression was of great significance to prolong survival and improve life quality. The radiotherapy techniques in continuous improvement, but the local residual NPC and recurrence rate were still as high as 10%-30% after radiotherapy[7,9,30], which mainly because NPC tumor cells were resistant to radiation therapy in the GTV region. Chen et al.  indicated that the cases of T stage detected by 18F-FDG PET/CT, PET, CT were 66, 64 and 62, respectively in sixty-six patients with residual and recurrence NPC. The cases were 6, 63 and 58 in N stage and 64, 60 and 60 in M stage, respectively. There are three cases of false-positive lymph nodes, which mainly occurred in jugular vein and submental lymph node hyperplasia. Thirty-eight NPC patients with radiotherapy were reported by Yu et al. . 18F-FDG PET/CT scan was a better tool than CT alone for the detection of recurrence or residue, a litter better than PET alone. The sensitivity and specificity of 18F-FDG PET/CT, CT and PET were 100%, 77.8%, 100%, and 89.5%, 84.2%, 80.0%, respectively. There are also false-negatives and false-positives occurred. The false-negative was mainly muscle uptake, while false-positive was mainly lymph nodes and lung lesions inflammatory intake. However, some scholars believed that the accuracy of MRI over PET/CT in detecting residual or recurrent NPC at the primary site (accuracy rate 92.1% vs. 85.7%).
6 The evaluation of PET/CT in prognosis of NPC
SUV was used to reflect glycometabolism of carcinoma, which is the most common indicator of PET/CT and the most important indicator of prognosis evaluation of NPC. Some studies indicated the higher the T staging of NPC, the higher SUVmax[35-36]. The worst prognosis was found in patients with the greater SUVmax. The prognosis would become worse, when SUVmax of lymph nodes metastasis (SUVmax-N) was higher than SUVmax of primary lesions(SUVmax-T). Chan et al. believed that patients with SUVmax-T<7.5 and SUVmax-N<6.5 (P=0.042 and P=0.019, respectively) would have significantly better 2 year DFS. The study of Hung et al.  showed that 371 NPC patients with SUVmax-T<9.3 and SUVmax-N<7.4 had a significantly better 5-year distant metastasis-free survival (DMFS) (91.1% vs. 84.0%, and 83.7% vs.78.0%, respectively). The 5-year DMFSs of SUVmax-T≥9.3 and SUVmax-N≥7.4 group lower than other three groups (84.3% vs. 94.6%-97.4%) in stage I-III NPC patients. The 5-year DMFSs of SUVmax-T<9.3 and SUVmax-N<7.4 group higher than other three groups (91.6% vs. 68.5%-82.9%) in stage IVA-B patients.
In recent years, some scholars found tumour volume (TV) were positively correlated with T-stage in primary NPC. Metabolic tumor volume (MTV) and metabolic index (MI, MI=MTV×SUVmean) from PET/CT were the semi-quantitative indicators in the evaluation of the prognosis of NPC[30,39-40]. NPC patients having tumors with an MTV< 30 cm3 had significantly better 5-year overall survival (OS) (84.6% vs. 46.7%, P=0.006) and disease-free survival (DFS) (73.1% vs. 40.0%, P=0.014) than patients with an MTV≥30 cm3 were reported by Xie et al.. And the patients with MI <130 had significantly higher 5-year OS (88.0% vs. 43.8%, P=0.002) and DFS (76.0% vs. 37.5%, P=0.005) than other patients. A study of 196 patients with primary stage III-IV NPC showed that MI values greater than 330 independently predicted OS (P=0.0014) and DFS (P=0.0005) as independent predictors of local failure-free survival. Tang et al. analysed that pretreatment N staging and EBV DNA level were significant risk factors for distant metastases. 18F-FDG PET/CT was not superior to conventional imaging examination for detecting distant metastases in very low-risk patients (N 0-1 and EBV DNA<4 000 copies/mL, P=0.062), but was superior for the low-risk patients (N 0-1 and EBV DNA≥4 000 copies/mL, N 2-3 and EBV DNA<4 000 copies/mL, P=0.039) and intermediate-risk patients (N 2-3 and EBV DNA≥4 000 copies/mL, P<0.001). Fifty-six NPC transferred patients were reported by Chen et al. . The research found that EBV DNA titre>5000 copies/mL (P=0.001), and MTV>110 mL (P=0.013) were independent risk factors for progression-free survival (PFS) and OS.
7 The diagnostic value of PET/CT in complications after NPC radiotherapy
Radiotherapy was the main therapeutic method for NPC. Meanwhile, temporal lobe, brain stem and cerebellum were inevitably exposed to radiation field in the treatment, which would lead to some patients occurred radiation encephalopathy (RE). Wang et al.[41-42] found that 18F-FDG PET/CT demonstrated anteromedial temporal lobes metabolic significantly decreased in 35 of the 53 NPC patients receiving radical radiotherapy (namely 70 lobes). However, CT displayed normal density in the 25 temporal lobes lesions of the 35 delayed RE patients. And metabolism of unilateral temporal lobe obviously reduced in 18 cases (18 lobes). The incidence of brain stem metabolic reductions was 24.5% (13/53) in the investigated patients, including 4 patients with hypometabolic changes shown by PET and negative finding shown by CT. According to the PET/CT imaging finding, the lesions could be classified as oedema type (56 temporal lobes), liquefactive necrosis type (10 temporal lobes) and atrophic calcification type (22 temporal lobe), and the former two types of lesions may progress into the third type .
In summary, PET/CT play an important role in radiotherapy for NPC. Correct diagnosis and accurate staging are a prerequisite for radiotherapy, and target delineation and radiation dose determination are the key to radiation therapy. The efficacy of radiotherapy, recurrence and residue of NPC, prognosis judgment have an important impact on the long-term quality of life and survival of patients. 11C-choline PET/CT in the diagnosis of skull base and intracranial invasion of NPC patients are significantly better than 18F-FDG PET/CT. However, there was no good solution to identify lymph node metastases, inflammatory lymph nodes, lung micrometastases and inflammatory lesions. The application of new imaging agents for PET/CT is to be further researched.
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