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ORIGINAL ARTICLE
Year : 2019  |  Volume : 15  |  Issue : 3  |  Page : 596-603

Prognostic value of response assessment fluorodeoxyglucose positron emission tomography-computed tomography scan in radically treated squamous cell carcinoma of head and neck: Long-term results of a prospective study


1 Department of Radiation Oncology, Tata Memorial Hospital, Mumbai, Maharashtra, India
2 Department of Bio-Imaging, Tata Memorial Hospital, Mumbai, Maharashtra, India

Date of Web Publication29-May-2019

Correspondence Address:
Dr. Sarbani Ghosh-Laskar
Department of Radiation Oncology, Tata Memorial Hospital, Dr. E Borges Road, Parel, Mumbai, Maharashtra
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jcrt.JCRT_542_17

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 > Abstract 


Objective: The objective of this study is to evaluate the diagnostic and prognostic ability of fluorodeoxyglucose positron emission tomography-computed tomography (FDG PET-CT) scan in patients with squamous cell carcinoma of the head and neck treated with chemoradiotherapy or radiotherapy only.
Materials and Methods: Fifty-nine patients with HNSCC planned for radical nonsurgical treatment were randomized to receive either three-dimensional conformal radiotherapy or intensity-modulated radiation therapy. In addition to routine clinical examination and staging investigations, patients had a FDG PET-CT scan at baseline and on the first follow-up for response assessment. No evidence of clinicopathological disease for at least 6 months after the completion of treatment was considered confirmation of complete response. The presence or absence of disease during the follow-up period was used to calculate the sensitivity, specificity, positive predictive value (PPV), and negative predictive value (NPV) of PET-CT for the primary site and node.
Results: At a median follow-up of 52.5 months, 55.6% of patients were alive and disease free. Response assessment PET-CT was done at a median of 9 weeks (range: 5–18 weeks). PET-CT assessment of the primary had sensitivity, specificity, PPV, and NPV of 81.8%, 93%, 75%, and 95.2%, respectively; the corresponding figures at the node were 44.4%, 95.6%, 66.7%, and 89.6%. The median baseline maximum standardized uptake value (SUVmax) at primary and node was 14.9 and 8.1, respectively. When PET-CT was done after 10 weeks, no false-positive or false-negative findings were seen. Patients with negative PET at the first follow-up had a significantly better progression-free and overall survival.
Conclusions: Disease evaluation using PET-CT has an overall accuracy of 80%. High baseline SUVmax correlates with worse clinical outcomes. Negative PET-CT at the first follow-up is a predictor for survival.

Keywords: Fluorodeoxyglucose positron emission tomography-computed tomography, head and neck cancer, squamous cell carcinoma, treatment response


How to cite this article:
Ghosh-Laskar S, Mummudi N, Rangarajan V, Purandare N, Gupta T, Budrukkar A, Murthy V, Agarwal JP. Prognostic value of response assessment fluorodeoxyglucose positron emission tomography-computed tomography scan in radically treated squamous cell carcinoma of head and neck: Long-term results of a prospective study. J Can Res Ther 2019;15:596-603

How to cite this URL:
Ghosh-Laskar S, Mummudi N, Rangarajan V, Purandare N, Gupta T, Budrukkar A, Murthy V, Agarwal JP. Prognostic value of response assessment fluorodeoxyglucose positron emission tomography-computed tomography scan in radically treated squamous cell carcinoma of head and neck: Long-term results of a prospective study. J Can Res Ther [serial online] 2019 [cited 2019 Aug 22];15:596-603. Available from: http://www.cancerjournal.net/text.asp?2019/15/3/596/244466




 > Introduction Top


Squamous cell carcinoma of the Head and neck (HNSCC) is the sixth most common malignancy worldwide, accounting for nearly 600,000 new patients annually.[1] Patients with HNSCC have been treated traditionally with a combination of surgery, radiation, and chemotherapy. Radiation therapy has been the mainstay of treatment in patients with locally advanced head and neck cancer and as a stand-alone modality is known to result in local control rates of 50%–70%.[2],[3] The addition of chemotherapy to radiation therapy and altered fractionation schedules has improved the outlook in nonmetastatic HNSCC conferring a survival benefit of 4%–7%.[1],[2]

18F-fluorodeoxyglucose positron emission tomography-computed tomography (18F-FDG PET-CT) is an important diagnostic tool for evaluation in HNSCC and finds application in clinical settings, ranging from pretreatment staging to radiotherapy planning, treatment response assessment, and posttherapy follow-up.[3],[4],[5] Using a response assessment tool, 18F-FDG PET-CT identifies viable tumor within residual disease, overcoming the known limitations of clinical examination and conventional CT imaging.[6] The functional imaging information provided by PET-CT can be combined with the structural imaging of contrast-enhanced CT and physical examination in evaluating patients for posttreatment salvage.

Many studies have validated the high negative predictive value (NPV) and low positive predictive value (PPV) of 18F-FDG PET-CT. Posttreatment edema and scarring account for the higher false-positive rates and can be reduced by delaying the scan.[7],[8],[9],[10] Parameters such as maximum standardized uptake value (SUVmax), mean standardized uptake value (SUVmean), total lesion glycolysis (TLG), and metabolic tumor volume (MTV) have been explored by investigators to quantify the prognostic value of FDG PET.[5],[11],[12],[13],[14]

The main objective of this study was to evaluate the diagnostic and prognostic ability of the response assessment 18F-FDG PET-CT scan in patients with HNSCC treated with radical radiotherapy or chemoradiotherapy.


 > Materials and Methods Top


Study design and patient population

Between August 2005 and October 2007, 59 newly diagnosed patients with HNSCC were enrolled in a prospective study. Inclusion criteria comprised a pretreatment FDG PET, squamous histology, and curative-intent treatment; patients with distant metastases, any surgical procedure before radiotherapy other than for tissue diagnosis, and recurrent HNSCC were excluded from the study. Patients were randomized to receive either LA-based three-dimensional conformal radiotherapy (3DCRT) or intensity-modulated radiation therapy (IMRT). The study design and protocol were reviewed and approved by the institutional review board. Patients were staged according to the American Joint Committee on Cancer staging system (7th Edition).

Treatment and follow-up

In addition to routine clinical examination and staging investigations, patients had an 18F-FDG PET-CT scan performed at baseline. All patients were planned for definitive radiotherapy. 3DCRT was delivered in two phases to a total tumor dose of 70 Gy in 35 fractions over 7 weeks, while IMRT was delivered with simultaneous integrated boost technique to a dose of 66 Gy in 30 fractions over 6 weeks. Concurrent chemotherapy with weekly cisplatin (30 mg/m 2) was given to patients with locally advanced disease. On the first follow-up at 8–12-week posttreatment, clinical examination and 18F-FDG PET-CT scan were performed for response assessment. Patients with residual disease (suspected clinically or on the basis of imaging) were considered for biopsy of the primary tumor site or fine-needle aspiration of an enlarged node. In the presence of viable tumor, patients who were operable underwent appropriate salvage surgery. Patients with equivocal findings were re-evaluated clinicoradiologically after 12 weeks. No evidence of disease for at least 6 months after the completion of treatment was considered confirmation of complete clinical response.

18F-fluorodeoxyglucose positron emission tomography-computed tomography

After ensuring euglycemic state and minimum 6 h fasting, patients were injected with 370 MBq of FDG and whole-body PET images were acquired using a hybrid PET/CT scanner (GE Discovery ST, GE Medical Systems, Milwaukee, WI, USA). Furthermore, a low-dose noncontrast CT was acquired from vertex to mid-thigh region. Using an inbuilt software, the PET and CT images were fused. SUVs were calculated on the axial images in the regions of increased FDG uptake, and SUVmax was documented as the maximum SUV within the volume contoured. MTV, defined as the volume of FDG activity in the tumor assessed by automated volume of interest delineation, and TLG, defined as MTV multiplied with SUVmean, were calculated. PET images and the fused PET-CT images were interpreted by an experienced nuclear medicine physician and a diagnostic radiologist. PET-CT images were interpreted through visual analysis and SUVs by an experienced nuclear medicine physician and radiologist. Focal and asymmetric FDG uptake with intensity greater than that of the surrounding normal tissues was considered as suggestive of residual disease (PET positive). The absence of or insignificant FDG uptake at the previously diseased site was considered as PET negative; diffuse uptake in the irradiated field was considered as post-treatment inflammation and disregarded.

Statistical analysis

The presence or absence of residual or recurrent disease during the follow-up period was used to calculate the sensitivity, specificity, PPV, and NPV, and overall accuracy of PET-CT for the primary site and neck. All statistical analyses were performed using SPSS version 20.0 (SPSS, Chicago, IL, USA). Kaplan–Meier survival analysis was used to calculate locoregional control and overall survival (OS) from the date of randomization. The cutoff date for time-to-event analysis was January 31, 2017.


 > Results Top


Patient and treatment characteristics

We enrolled 59 patients for the study, 30 patients in the IMRT arm and 29 in the 3DCRT arm. Five patients were excluded from this analysis; four patients did not have a response assessment PET-CT imaging and one patient died after seven fractions of RT due to treatment complications. Although one patient was treated using conventional technique (protocol violation), his PET-CT data were included in this analysis. The characteristics of the patient population are presented in [Table 1].
Table 1: Demographics

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Treatment outcomes

Majority of the patients had locally advanced disease (Stage III/IV – 63%); 78% of the patients had received concurrent chemotherapy. All patients included in this analysis completed their planned course of radiotherapy. Median duration to complete treatment was 47.5 days (range: 40–68 days). Thirty-one patients (57.4%) were alive with no evidence of disease; the median follow-up period of the surviving fraction was 101 months (range: 9–125 months).

18F-fluorodeoxyglucose positron emission tomography-computed tomography

All patients had 18F-FDG uptake at the primary on the baseline PET-CT. The average pre-RT SUVmax of the primary disease was 14.9 (median: 13.3; interquartile range [IQR]: 9.3–18.7). For the nodal disease, the average pre-RT SUVmax was 8.1 (median: 5.3; IQR: 3.7–11.5). The mean MTV for primary and nodal disease was 11.5 and 6.5 cc, respectively; the average primary and nodal TLG was 133 and 36.5 g, respectively. After completion of RT, patients underwent 18F-FDG PET-CT scan at a median of 9 weeks (range: 5–18 weeks; IQR: 8–9 weeks). Of the 54 patients, 42 (77.8%) patients had a complete metabolic response (CMR) at the primary; out of the 27 patients with nodal disease at presentation, 21 (73%) patients had CMR at the node.

The sensitivity, specificity, and overall accuracy for the primary disease, nodal disease, and overall disease are shown in [Table 2] and [Table 3]. 18F-FDG PET-CT had a PPV of 75% (95% confidence interval [CI]: 42.8%–94.2%) at the primary, 66.7% (95% CI: 22.7%–94.7%) at the node, and 73.3% (95% CI: 44.9%–92.1%) overall and NPV of 95.2% (95% CI: 83.8%–99.3%) at primary, 89.6% (95% CI: 77.3%–96.5%) at node, and 82.1% (95% CI: 66.5%–92.4%) overall.
Table 2: Overall results of positron emission tomography-computed tomography

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Table 3: Positron emission tomography-computed tomography scan performance characteristics

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At first follow-up, 13 patients (24%) had clinicoradiological evidence of residual disease [Figure 1] and [Figure 2], of which 6 patients (11%) had disease at the primary and 10 patients (18%) at the node (3 patients had disease at both primary and node). In the six patients, who had residual disease at the primary, PET-CT was positive in five patients. Histopathological (HP) confirmation was available in three of these patients, and all of these were positive. In the one patient in whom there was no FDG uptake at the primary, subsequent follow-up showed the primary to be controlled (true negative). Out of the ten patients with clinicoradiological residual disease at the node at the first follow-up, four patients had increased FDG uptake, and there was HP confirmation of disease in three patients (true positive) and the other patients remain disease free (false positive). In the remaining six patients with no uptake in the neck, four patients had HP-proven disease (false negative), one patient was found to have disease on subsequent follow-up (false negative), and one patient remains disease free (true negative).
Figure 1: Diagnostic performance of positron emission tomography-computed tomography on primary disease

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Figure 2: Diagnostic performance of positron emission tomography-computed tomography on nodal disease

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In addition to the above patients, there were nine instances of increased FDG uptake where the clinicoradiological impression was negative; seven instances were at the primary and 2 instances were at the neck. In patients with increased FDG uptake at the primary, four patients had HP which also did not show disease; however, on further follow-up, three of these patients were found to have disease (true positive), while one remained disease free (false positive). Of the remaining three in whom HP confirmation was not available, two patients remained controlled (false positive) while one patient had a recurrence (true positive). Of the two patients with FDG uptake at the node, one was negative on HP and remained controlled (false positive), the other had no HP confirmation but failed at the node subsequently (true positive).

When PET-CT was done after 10-week posttreatment, no false-positive or false-negative findings were seen. A pre-RT primary site SUVmax cutoff of 10 or 15 was not found to significantly influence any of the survival measures. However, a pre-RT primary site SUVmax cutoff of 20 or more was strongly associated with residual disease (P = 0.006) and recurrence (P = 0.057). These patients also had a worse median disease-free survival (DFS, 10 vs. 48 months) and OS (48 vs. 66 months) than those with a lesser value.

The median OS and DFS were 58.5 and 39 months, respectively. The 5-year OS and DFS for the entire cohort was 55.3% and 54.6%, respectively. On univariate and multivariate analysis, none of the pre- and post-RT PET-CT parameters (SUVmean, SUVmax, TLG, and MTV), treatment arm, or disease characteristics were found to influence OS or DFS. However, a negative response assessment PET-CT was found to be associated with better survival; 5-year OS and DFS were found to be significantly inferior in patients with a positive uptake on response assessment PET-CT scan (35.3% vs. 68.2%; P = 0.014 and 17.6% vs. 79.2%; P < 0.001, respectively). Furthermore, as expected, patients with a true negative PET-CT scan (complete metabolic, clinical, and radiological response) had a significantly better 5-year survival (OS: 72.9% vs. 36.4%; P = 0.006; DFS: 91.7% vs. 13.6%; P < 0.001) [Figure 3].
Figure 3: Five-year overall survival and disease-free survival: (a and b) Response assessment positron emission tomography-computed tomography positive versus negative; (c and d) response assessment positron emission tomography-computed tomography true negatives versus rest

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 > Discussion Top


In this prospective study, we have analyzed the diagnostic and prognostic capability of posttreatment response assessment 18F-FDG PET-CT scans in the management of HNSCC. A number of prospective and retrospective studies have shown the superiority of PET or PET-CT over conventional imaging in the evaluation of response to the treatment of HNSCC after definitive nonsurgical treatments.[15],[16],[17] Unlike conventional imaging modalities, PET-CT scans have the ability to provide information about potential regions of tumor metabolic activity, tumor biology including hypoxia, and proliferation in addition to conventional anatomic localization. 18F-FDG is the most widely used radiopharmaceutical, due to its easy availability, and high signal-to-background ratio. Although PET-CT scans are not used in the routine diagnostic workup of HNSCC, they are being increasingly used to identify unknown primaries, to improve nodal or distant disease staging of HNSCC, and to detect recurrences in addition to conventional imaging modalities.[18],[19],[20] A recently published meta-analysis [21] has assessed the role of PET-CT for detecting distant metastases in patients with recurrent HNSCC planned for definitive salvage treatment.

The practice of performing a planned neck dissection in patients with higher nodal burden at presentation or for patients with persistent palpable lymph nodes was considered prudent as clinical examination and conventional imaging modalities do not reliably rule out residual viable tumor. Complete response rates in the neck after radiotherapy or chemoradiation vary from 59% to 83%, with higher rates observed in patients with N1 disease. However, up to a third of patients with higher nodal burden (N2 and N3 disease) might still harbor residual disease, in the absence of demonstrable clinical disease.[22] Hence, one of the important functions of posttreatment imaging is the early differentiation of treatment responders and nonresponders, thereby preventing unnecessary interventions.[23] In particular, 18F-FDG PET-CT has a high NPV, whereby patients can be spared unnecessary invasive diagnostic procedures and neck dissection, with a significant impact on patient outcome and morbidity. Studies have demonstrated that in patients with a CMR, neck dissection can be avoided, even if conventional imaging shows residual nodal disease.[6],[23]

The meta-analysis by Gupta et al.[24] reviewed a large data of 2335 patients from 51 studies; the mean pooled estimates of sensitivity and specificity for the primary and nodes were 79.9%, 87.5% and 72.7%, 87.6%, respectively. PPV for both primary and nodes was low because of high false positivity rates, while NPV was significantly high. In their meta-analysis, Pasamontes Pingarrón et al.[8] included 18 studies conducted between 1994 and 2007 and concluded that 18F-FDG PET presented an intermediate-high specificity (80%; 95% CI: 76%–84%) and a high sensitivity (94%; 95% CI: 91%–96%), which shows that there were very little false negatives. A similar systemic review [6] of 27 studies showed a global sensitivity and specificity of 94% (95% CI: 87%–97%) and 82% (95% CI: 76%–86%) respectively for the primary; 74% (95% CI: 50%–89%) and 88% (95% CI: 74%–95%), respectively for nodal disease. In another recent meta-analysis of 23 studies published till 2014, Sheikhbahaei et al.[25] reported a pooled estimates of sensitivity of 0.92% (95% CI: 0.90%–0.94%) and specificity of 0.87% (95% CI: 0.82%–0.90%) for follow-up FDG PET-CT. The pooled mean PPV and NPV of our study for the detection of residual disease at the primary site were similar to those observed in the meta-analysis [Table 4].
Table 4: Comparison with published meta-analyses

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The blurring of distinction between active tumor and necrotic/reactive tissue, brought about by treatment-induced anatomical and morphological distortion, leads to the observation of high number of false-positive results. This results in low PPV of FDG-PET scans. However, by allowing inflammation to settle with time, it has been observed that PPV indeed improves. Hence, the timing of the response PET-CT is of paramount importance and is best performed after 8–12 weeks of radiation.[27] Isles et al.[7] calculated that the sensitivity would be significantly higher for scans performed >10 weeks after treatment (P = 0.002) although there were insufficient data to provide an accurate assessment of the size of this difference. In the present study, in patients who underwent imaging 10 weeks after treatment completion, there was no instance of false-positive or false-negative results. 18F-FDG PET-CT should be probably done before 8 weeks only in those patients with residual nodal disease when there is a dilemma between whether to observe or to do early neck dissection and those with clinically progressive nodal disease in the presence of a favorable response at the primary.[10],[23]

As established clinical and pathological prognostic factors in HNSCC are not entirely reliable, identification of new biological prognostic factors for HNSCC may allow tailored therapy. Various cutoff values of SUVmax have been studied as prognostic indices to correlate with outcomes; while a few of the trials found a positive correlation,[28],[29],[30] some did not.[13] Querellou et al.[31] showed that a SUVmax cutoff value of 7 remained a statistically significant independent prognostic value for DFS and OS. In our study, the median pretreatment primary SUVmax was 14.9. We observed that patients with pre-RT SUVmax of >20 were more frequently found to have residual disease at first follow-up (P = 0.001) and recurrent disease (P = 0.05). We also observed that patients who demonstrate CMR at the end of therapy have a significantly longer DFS and numerically better OS rates.

Various other indices including MTV, integrated SUV and SUVmax of the primary tumor, SUVmean, and TLG have been studied as candidates for better prognostic markers and need further exploration.[5],[12],[14],[26]

Our study is one of the few prospective clinical trials which have evaluated the prognostic and diagnostic role of PET-CT. The study population consisted of nonnasopharyngeal head and neck cancer, which is the most common problem in this part of the world. Availability of patient data on longer follow-up is the other strength of this study.


 > Conclusions Top


18F-FDG PET-CT has an overall PPV of 73% and NPV of 82% for detecting recurrent or residual disease both at the primary and neck node following chemoradiotherapy. False-positive rates can be effectively reduced by timing the posttreatment study over 10-week posttreatment. Owing to its superior ability to differentiate disease from post-RT changes, 18F-FDG PET-CT can obviate the requirement for morbid interventions. Identifying the role of various PET-CT markers to predict, prognosticate, and thereby aid in tailoring treatment is of dormant potential and prime importance.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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