18F-fluorodeoxyglucose positron emission computed tomography for monitoring tumor response in esophageal carcinoma treated with concurrent chemoradiotherapy

  • Authors:
    • Peiliang Zhang
    • Zengyun Li
    • Dongqing Wang
    • Fuling Ma
    • Ran Zhang
    • Wanhua Liang
    • Mingping Sun
    • Zheng Fu
    • Xiaorong Sun
  • View Affiliations

  • Published online on: December 5, 2017     https://doi.org/10.3892/ol.2017.7528
  • Pages:1845-1852
Metrics: HTML 0 views | PDF 0 views     Cited By (CrossRef): 0 citations

Abstract

The aim of the present study was to explore the value of 18F-fluorodeoxyglucose positron emission tomography (18F‑FDG PET) in monitoring the early tumor response of esophageal squamous cell carcinoma (ESCC) treated with concurrent chemoradiotherapy (CRT). A total of 48 patients with pathologically proven ESCC were retrospectively analyzed. All patients underwent two serial 18F‑FDG PET scans at baseline (pre‑CRT) and 40 Gy/4 weeks of starting radiation therapy (inter‑CRT). All patients received intensity‑modulated radiotherapy (with a total radiation dose of 59.6 Gy) concurrently with cisplatin‑based chemotherapy. The maximum standardized uptake value (SUVmax) and metabolic tumor volume (MTV) were measured using 18F‑FDG PET. The percentage changes (Δ) in SUVmax and MTV between two serial scans were calculated and were revealed to be associated with the objective tumor response (oTR), according to the Response Evaluation Criteria in Solid Tumors 1.1. Among the 48 patients, 20.8% achieved a complete response, 68.8% exhibited a partial response and the oTR rate was 89.6%. On the pre‑CRT PET scans, the mean SUVmax and MTV were 14.1±5.8 and 58.2±25.4 cm3, respectively. Following 40 Gy irradiation over 4 weeks, the mean SUVmax and MTV significantly decreased to 4.3±3.5 and 19.0±12.1 cm3, respectively (P<0.001). A significantly higher ΔSUVmax and ΔMTV was observed in the responders compared with that in the non‑responders [0.71±0.16 vs. 0.51±0.26 (P=0.015); and 0.64±0.13 vs. 0.42±0.09 (P=0.001), respectively]. Univa­riate analysis revealed that ΔSUVmax and ΔMTV were significantly associated with oTR (P=0.010 and P=0.001, respectively). ΔMTV was used as a predictor and a cut‑off value of 54% discriminated responders from non‑responders with a sensitivity of 69.8% and a specificity of 100% (P=0.001). The area under the receiver operating characteristic curve was 0.837 (95% confidence interval, 0.702‑0.928). The results of the present study indicated that interim 18F‑FDG PET scans may provide early prognostic value for determining oTR in patients with ESCC undergoing treatment with CRT.

Introduction

Esophageal squamous cell carcinoma (ESCC) is the 4th most common cause of cancer-associated mortality and the fifth most frequently diagnosed cancer type in China (1). ESCC is a highly aggressive malignancy with a poor prognosis due to the fact that the majority of tumors are asymptomatic until they have reached advanced stages (1). At present, concurrent chemoradiotherapy (CRT) has been established as an important approach for patients with locally advanced carcinoma of the esophagus (2). This treatment schedule is also appropriate for patients who are either medically unfit for surgery or unwilling to undergo surgery (3). The ability to predict which patients respond to CRT or develop resistance would be invaluable for individualizing therapeutic approaches, as early modifications in therapy regimens for non-responders may improve treatment outcomes.

Conventional anatomic imaging modalities, such as computed tomography, evaluate tumor response as changes in tumor size only after weeks or months following therapy, and are not ideally suitable for early prediction for treatment response. 18F-fluorodeoxyglucose positron emission computed tomography (18F-FDG PET) as a functional imaging technique has demonstrated potential value for monitoring early response to neoadjuvant CRT in esophageal cancer (48), as metabolic variation of the tumor occurs prior to any anatomical structure changes. However, there is no study to date has examined interim treatment 18F-FDG PET for monitoring response to definitive CRT.

The present study aimed to investigate the prognostic value of interim 18F-FDG PET in order to determine the objective tumor response (oTR) in patients with ESCC who received only definitive CRT.

Patients and methods

Patients

Between August 2011 and January 2015, 48 consecutive patients with biopsy-proven locally advanced ESCC were enrolled in the present study. The study protocol was approved by the Shandong Tumor Hospital Ethics Committee (Shandong, China) and written informed consent was obtained from all patients. Among the 48 patients, there were 40 (83.3%) male and 8 (16.7%) female, with a median age of 61 years (range, 40–75 years). Pretreatment investigations included a complete blood count, measurement of serum electrolytes, a chest radiograph, a computed tomography (CT) scan of the chest and abdomen, barium swallow radiography and an upper gastroesophageal endoscopy.

Patients who had undergone 18F-FDG PET scans prior to CRT (pre-CRT) and 40 Gy/4 weeks of starting radiation therapy (inter-CRT) were included in the present study. Other inclusion criteria were as follows: i) Patient age was <76 years and the Karnofsky score was >70 without any previous treatment; ii) the absence of distant metastasis; iii) no contraindications to radiotherapy or chemotherapy; and iv) no signs of infection or diagnosis of diabetes at the time of the PET scan. The characteristics of the enrolled patients are listed in Table I. Of the 48 patients treated with definitive CRT, 10 were diagnosed with clinical stage II cancer and did not undergo surgery due to patient refusal, poor cardiopulmonary function or advanced age.

Table I.

Patient characteristics.

Table I.

Patient characteristics.

CharacteristicsResponderNon-responderTotal no. (%)P-value
Sex 0.833
  Male36440 (83.3)
  Female718 (16.7)
Age, years 0.645
  Range40–7561–7540–75
  Median606461
Tumor length, cm 0.361
  Range2–156.4–112–15
  Median5.67.86
Tumor location 0.626
  Cervical404 (8.3)
  Upper thoracic17118 (37.5)
  Middle thoracic18321 (43.8)
  Lower thoracic415 (10.4)
TNM stage 0.689
  IIa707 (14.6)
  IIb303 (6.3)
  III20323 (47.9)
  IVa13215 (31.2)
Chemotherapy 0.943
  Cisplatin + 5-FU20222 (45.8)
  Cisplatin + pemetrexed14216 (33.4)
  Cisplatin + capecitabine9110 (20.8)

[i] TNM, tumor-node-metastasis; 5-FU, fluorouracil.

PET scanning

All patients fasted and rested for >6 h prior to consuming 500 ml water and were then administered with 7–11 mCi radioactive tracer. Patient serum glucose levels were confirmed to be <6.6 mmol/l. All patients were examined on a dedicated PET/CT scanner (GE Healthcare Life Sciences, Little Chalfont, UK). Subsequently, the emission scans were acquired from the level of the calvaria to the thigh for 4 min per position. Each patient received a scan lasting 24–28 min in total covering 14.5 cm at an axial sampling thickness of 4.25 mm per slice. The non-contrast spiral CT component was performed with a slice thickness of 4.25 mm and a rotation speed of 0.8 sec per rotation. PET images were reconstructed with CT-derived attenuation correction using the ordered-subset expectation maximization algorithm. The attenuation-corrected PET images, CT images and fused PET/CT images displayed as coronal, sagittal and transaxial slices were viewed on a GE Xeleris 2 workstation (GE Healthcare Life Sciences, Little Chalfont, UK). Pre-CRT scans were performed 1–5 days prior to commencing CRT and inter-CRT scans were acquired following 40 Gy/4 weeks of starting radiation therapy.

Treatment
Radiotherapy

All patients were placed in a supine position with thermoplastic immobilization prior to the CT simulation and each daily radiotherapy (RT). All patients received intensity-modulated radiotherapy (IMRT) with six MV X-rays and a two-phase irradiation protocol. The first phase was administered as conventionally fractionated RT with a total of 40 Gy in 20 fractions (fx) in 4 weeks, which irradiated the gross tumor volume (GTV), including that of the primary tumor (GTVp) and that of the metastatic lymph nodes (GTVn). The planning target volume was defined as GTVp with the addition of 3–5 cm margins superiorly and inferiorly, 1 cm margins laterally, and with the addition of a 1 cm margin for GTVn. The second phase was delivered to the boost volume as an additional dose of 19.6 Gy twice a day in 14 fx over 7 days at 1.4 Gy/fx, with a 6 h minimal interval between fractions. The total dose administered to the clinical tumor was 59.6 Gy and 34 fx over 35 days.

Chemotherapy

All patients were scheduled to receive two cycles of concurrent chemotherapy, which began on the first day of RT. The chemotherapeutic regimens in the present study consisted of intravenous cisplatin 25 mg/m2/day on days 1–3 plus 500–600 mg/m2 fluorouracil (5-FU) every 24 h by continuous infusion for 120 h, plus 1,000 mg capecitabine twice daily with a 12 h interval on days 1–14 or plus 400–500 mg/m2 pemetrexed on day 1 of a 21-day cycle.

Metabolic parameters

The pre- and inter-CRT PET images were analyzed by two experienced and independent nuclear medicine physicians. Semi-quantitative analysis of the SUV was corrected by the injected dose and body weight (g) and was calculated as follows: Tissue activity concentration (Bq/ml)/[administered activity (Bq)/weight (g)]. Metabolic and volumetric parameters were measured using PET-Volume Computer-Assisted Reading software (AW4.5 Platform; GE Healthcare, Chicago, IL, USA), which provides an automatically delineated volume of interest using an isocontour threshold method based upon the SUV. SUVmax was defined as the SUV on the highest pixel image in the tumor region. MTV was defined as the volume of interest of tumor segmented by a threshold of 2.5 (Fig. 1) (9,10). The percentage changes (Δ) of metabolic parameters (P) between pre- and inter-CRT were calculated and expressed as a ratio, and were marked for ΔP, which was calculated as follows: ΔP = [(Ppre-CRT - Pinter-CRT)/Ppre-CRT] × 100%.

Response evaluation

The oTR evaluation was performed ≥4 weeks after the end of therapy based upon the Response Evaluation Criteria in Solid Tumors 1.1 (RECIST 1.1) (11), outlined as follows: Complete response (CR), disappearance of all target lesions; partial response (PR), ≥30% decrease from baseline; progressive disease (PD), ≥20% increase over smallest sum observed or appearance of new lesions; and stable disease (SD), neither PR nor PD criteria met. The assessment of oTR included repeated endoscopy, barium swallow and contrast-enhanced CT scan. Response was assessed by two experienced radiologists who were blinded to the outcomes of the PET scans. Patients with an outcome of CR or PR were defined as responders and those with an outcome of SD, or PD were classed as non-responders.

Statistical analysis

Descriptive analyses are expressed as the mean ± standard deviation. Statistical comparisons between responders and non-responders were performed using independent Student's t-tests. Parameter comparisons between pre- and inter-CRT were calculated using paired Student's t-tests. Associations between parameters and the oTR were analyzed using univariate analysis. Receiver-operating characteristic (ROC) curve analysis was used to evaluate the predictive ability of parameters. All statistical analysis was performed using SPSS version 20.0 (IBM Corp., Armonk, NY, USA) and MedCalc version 15.2 (MedCalc Software bvba, Ostend, Belgium). All tests were two-tailed and P<0.05 was considered to indicate a statistically significant difference.

Results

Treatment response

There were 10 (20.9%) patients with stage II disease, 23 (47.9%) with stage III disease and 15 (31.2%) with stage IVa disease, according to the American Joint Committee on Cancer 7th staging system (12). The median tumor length was 6.0 cm (range, 2.0–15.0 cm). Following the completion of treatment, 10 patients (20.8%) attained a CR, 33 (68.8%) exhibited a PR and 5 (10.4%) had SD, with no cases of PD. The overall oTR rate was 89.6% (43/48). No significant differences in patient characteristics between responders and non-responders were observed (Table I; all P>0.05). Figs. 2 and 3 show two representative cases of clinical CR and PR, respectively.

FDG uptake by tumors

All 48 patients had abnormal FDG uptake in their primary tumors or lymph nodes on pre-CRT PET scans, with a mean SUVmax of 14.1±5.8 and a mean MTV of 58.2±25.4 cm3. However, following 40 Gy irradiation over 4 weeks and 1–2 cycles of concurrent chemotherapy, FDG uptake by tumors in the interim PET scans was significantly decreased, with a mean SUVmax of 4.3±3.5 and a mean MTV of 19.0±12.1 cm3 (Table II; P<0.001). Fig. 4 demonstrates the changes in MTV and SUVmax in 5 non-responders between pre- and inter-CRT PET scans compared with the changes in responders. The metabolic and volumetric parameters of FDG PET were all decreased steadily from baseline to interim treatment in responders, and non-responders. However, the reduction rate of MTV between pre- and inter-CRT in responders was 0.64±0.13 vs. 0.42±0.09 in non-responders, a difference that was statistically significant (P=0.001). A similar difference was observed for ΔSUVmax, (0.71±0.16 in responders vs. 0.51±0.26 in non-responders; P=0.015; Table III).

Table II.

Comparisons of fluorodeoxyglucose positron emission tomography parameters between the baseline (pre-CRT) and 4 weeks after starting concurrent chemoradiotherapy (inter-CRT).

Table II.

Comparisons of fluorodeoxyglucose positron emission tomography parameters between the baseline (pre-CRT) and 4 weeks after starting concurrent chemoradiotherapy (inter-CRT).

ParameterPre-CRTInter-CRTP-value
MTV, cm358.2±25.419.0±12.1<0.001
SUVmax14.1±5.84.3±3.5<0.001

[i] Data are presented as the mean ± standard deviation. CRT, chemoradiotherapy; SUVmax, maximum standardized uptake value; MTV, metabolic tumor volume.

Table III.

Differences in fluorodeoxyglucose positron emission tomography parameters between responders and non-responders.

Table III.

Differences in fluorodeoxyglucose positron emission tomography parameters between responders and non-responders.

ParameterResponderNon-responderP-value
ΔMTV0.64±0.130.42±0.090.001
ΔSUVmax0.71±0.160.51±0.260.015

[i] Data are presented as the mean ± standard deviation. SUVmax, maximum standardized uptake value; MTV, metabolic tumor volume.

Associations between clinical characteristics and tumor response

Univariate analysis revealed that ΔSUVmax and ΔMTV were significantly associated with oTR (P=0.010 and P=0.001, respectively). An association between interim MTV (MTVinter) and oTR was also observed (P=0.041), while no significant association was observed between interim SUVmax and oTR (P=0.056). Age, sex, tumor location, tumor diameter, chemotherapy and clinical tumor-node-metastasis (TNM) stage were not significantly associated with oTR (Table IV; all P>0.05). ROC curve analysis (Table V and Fig. 5) revealed that ΔSUVmax (cut-off, 57%) displayed an area under the ROC curve (AUC) of 0.744 [95% confidence interval (CI), 0.544–0.890], with a sensitivity of 0.761 and a specificity of 0.800 (P=0.057). However, a threshold of 54% ΔMTV divided the responders from the non-responders with a sensitivity of 0.698, a specificity of 1.000 and an AUC of 0.837 (95% CI, 0.702–0.928; P=0.001).

Table IV.

Associations between parameters and objective tumor response.

Table IV.

Associations between parameters and objective tumor response.

ParameterThreshold valueaχ2P-value
MTVpre, cm350.60.810.367
MTVinter, cm320.44.160.041
ΔMTV0.5411.00.001
SUVpre12.50.590.442
SUVinter3.43.650.056
ΔSUVmax0.579.320.010
Age (years)1.260.461
Sex0.080.778
Tumor location3.200.361
Tumor diameter2.250.086
TNM stage2.870.412
Chemotherapy0.210.712

a Threshold value was determined by receiver operating characteristic curve analysis. SUVmax, maximum standardized uptake value; MTV, metabolic tumor volume; TNM, Tumor-Node-Metastasis.

Table V.

ROC curve analysis of metabolic parameters for treatment response prediction.

Table V.

ROC curve analysis of metabolic parameters for treatment response prediction.

ParameterAUC95% CI of AUCSensitivitySpecificityP-value
ΔMTV0.8370.702–0.9280.6981.0000.001
ΔSUVmax0.7440.544–0.8900.7610.8000.057

[i] ROC, receiver operating characteristic; AUC, area under the ROC curve; CI, confidence interval; SUVmax, maximum standardized uptake value; MTV, metabolic tumor volume.

Discussion

ESCC is a highly heterogeneous type of cancer where patients at the same TNM stage and undergoing the same treatment regimens, exhibit different treatment responses and survival rates. Therefore, it is necessary to obtain a reliable tool to identify the treatment-resistant patients and to develop individualized treatment strategies, which may be an effective way to improve the survival of patients.

A previous study reported that clinical parameters (age, sex, TNM stage, tumor location and pathology) were unable to predict response to CRT (13). Certain studies have focused on biological markers to estimate possible treatment responses to CRT; however, these promising biomarkers require further validation with larger high-quality clinical trials (14,15). Previous studies have suggested that 18F-FDG PET is a non-invasive method for monitoring pathological response and prognosis for carcinomas of the esophagus during or following neoadjuvant CRT (48). Monjazeb et al (16) reviewed 163 patients with esophageal cancer receiving neoadjuvant CRT with or without resection. 18F-FDG PET scans were performed and analyzed pre- and post-CRT. In a study undertaken by Monjazeb et al (16), for patients treated with definitive CRT, the median survival time and the 2-year overall survival (OS) rate for the patients achieving complete response was 38 months, and 71% vs. 11 months and 11% for those patients who had not achieved a complete response. Multivariate analysis indicated that PET complete response is the strongest independent prognostic factor for esophageal cancer [survival hazard ratio (HR), 9.82; P<0.01; local failure HR, 14.13; P<0.01].

As a semi-quantitative parameter of 18F-FDG PET, SUV, which may reflect the intensity of metabolic activity of the tumor, has been suggested as a prognostic marker for the histopathological response of esophageal carcinoma (48,1720). For example, Wieder et al (7) reported that, for histopathological responders, the decrease in SUV between baseline and 2 weeks after initiation of therapy was 44%, but was only 21% in the non-responders (P=0.0055). At the preoperative scan (3–4 weeks after CRT), tumor metabolic activity had decreased by 70% in histopathological responders and by 51% in histopathological non-responders. Lordick et al (5) reported that the median event-free survival time was 29.7 months (95% CI, 23.6–35.7 months) in metabolic responders vs. 14.1 months (95% CI, 7.5–20.6 months) in non-responders (HR, 2.18; P=0.002). Chhabra et al (18) observed that with a cut-off value of a 35% decrease in SUVmax between baseline and post-CRT, the 3-year OS rate for responders (ΔSUV ≥35%) was 64%, while that for non-responders (ΔSUV <35%) was only 15% (P=0.004). Another study undertaken by Huang et al (19) revealed that ΔSUV was significantly associated with OS and disease-free survival rates. The 3-year OS rate of the ΔSUV >60% group was 71% and that of the ΔSUV ≤60% group was 40.7% (P=0.045). In the present study, the SUVmax of tumor(s) decreased steadily from baseline to interim treatment in responders and non-responders, and the reduction rates of SUVmax (ΔSUVmax) were significantly different between the responders and the non-responders. However, a threshold of 57% ΔSUVmax was unable to divide the responders from the non-responders successfully, with an AUC of 0.744 (95% CI, 0.544–0.934; P=0.057).

The ability of SUVmax to predict oTR remains controversial and is influenced by a variety of factors, including the total dose of FDG injected, the time between the injection and scanning, noise and image reconstruction. Furthermore, a number of biological and technological factors influence the measurement of SUVmax (21). Therefore, the exploration of other metabolic parameters is required. MTV and total lesion glycolysis (TLG) are volume-based parameters that represent metabolic tumor burden. A number of previous studies have reported the effectiveness of MTV and/or TLG as prognostic factors in esophageal carcinoma (6,2224). Roedl et al (24) reported that a decrease in MTV between pre- and post-treatment PET scans was a better predictor of histopathological response, and survival in comparison with a decrease in the SUV or the clinical response evaluation based on the RECIST 1.1 in adenocarcinomas of the esophagus. Kim et al (6) revealed that a threshold of 25.5% ΔMTV divided the responders from the non-responders with a sensitivity of 80%, a specificity of 76.3% and an AUC of 0.731 (95% CI, 0.591–0.843; P=0.0027). The present study observed that MTV decreased steadily from baseline to interim treatment in responders and non-responders. Furthermore, the reduction rate of MTV was significantly higher in responders compared with that in non-responders. Univariate analysis demonstrated that ΔMTV was significantly associated with oTR. A threshold of 54% ΔMTV divided the responders from the non-responders with an AUC of 0.837 (95% CI 0.702–0.928), a sensitivity of 0.698 and a specificity reaching 1.000 (P=0.001). One retrospective multi-center study demonstrated that the MTV defined by a physician significantly decreased from PET1 (pre-CRT) to PET2 (3 weeks from the start of CRT), whereas the MTV defined as 40% of the SUVmax did not decrease significantly (25). The MTV from PET1 or PET2 was significantly lower in patients with CR at 3 months, while the SUVmax was not.

The reasons for certain discrepancies in the aforementioned studies may be explained by differences in the pathological types of cancer, treatment regimens or criteria used to evaluate the tumor response. In Western countries, the most common pathological type of esophageal cancer is esophageal adenocarcinoma, which may be more suited for neoadjuvant CRT followed by surgery at locally advanced stages. The pathological CR may be used to assess treatment response. However, in China, a substantial proportion of newly diagnosed esophageal carcinomas were squamous cell carcinomas and were not suitable for surgery (26). For these patient, CRT was an important treatment option. Therefore, the patients enrolled in the present study all received definitive CRT. The aim of the present study was to identify a reliable predictor to permit the early identification of patients who may or may not respond to CRT. The RECIST criteria is recommended to evaluate the solid tumor response using the changes in tumor size on CT images. Due to radiation-induced inflammation, edema may remain present in the esophageal wall of certain patients, even >8 weeks after radiotherapy (27). When using metabolic parameters of FDG PET, OTR may be assessed 4 weeks from the start of CRT (after 40 Gy irradiation), as in the present study. However, it must be accounted for that FDG PET may have difficulty in differentiating between complete responses and residual disease or post-treatment inflammation (28), as glucose accumulates in tumor and inflammatory cells, and inflammatory cells are common in irradiated esophageal tissue. Therefore, uptake on an 18F-FDG PET scan may represent either residual tumor or esophagitis. For example, Yue et al (29) recruited 21 patients with inoperable locally advanced ESCC who underwent a serial 3′-deoxy-3′-(18)F-fluorothymidine (18F-FLT) PET scan during radiotherapy. Among the 19 patients, 2 patients who had undergone scans following completion of the entire radiotherapy course exhibited no tumor uptake on the 18F-FLT PET scan, but high uptake on the 18F-FDG PET scan. Pathological examination of these regions revealed inflammatory infiltrates, but no residual tumor (29). The aforementioned study suggests that 18F-FLT PET may discriminate tumor from esophagitis more effectively than 18F-FDG PET, which may have important clinical applications.

The present study has a number of limitations that must be taken into account. To begin with, the study was retrospective in design and comprised a small population. Additionally, 18F-FDG PET scan results were compared with objective therapeutic responses according to the RECIST 1.1 and not with the pathological response to treatment. According to the pathological criteria, pathological T (primary tumor) and N (lymph nodes) were assessed according to the percentage of viable residual tumor cells within the postoperative cancerous tissues. In the present study, it was not possible to acquire the postoperative pathological tissues. Future prospective studies with a larger study population may be able to accurately identify the association between 18F-FDG PET scan results and oTR.

In conclusion, given the aforementioned limitations, the present study provides clinical evidence that interim 18F-FDG PET scans may exhibit early prognostic value for determining oTR in patients with ESCC. The findings of the present study suggest that ΔMTV may be a useful parameter to assess clinical oTR to definitive CRT, which may permit early identification of CRT responders and non-responders.

References

1 

Chen W, He Y, Zheng R, Zhang S, Zeng H, Zou X and He J: Esophageal cancer incidence and mortality in China, 2009. J Thorac Dis. 5:19–26. 2013.PubMed/NCBI

2 

Cooper JS, Guo MD, Herskovic A, Macdonald JS, Martenson JA Jr, Al-Sarraf M, Byhardt R, Russell AH, Beitler JJ, Spencer S, et al: Chemoradiotherapy of locally advanced esophageal cancer: Long-term follow-up of a prospective randomized trial (RTOG 85-01). Radiation therapy oncology group. JAMA. 281:1623–1627. 1999. View Article : Google Scholar : PubMed/NCBI

3 

Ajani J, Bekaii-Saab T, D'Amico TA, Fuchs C, Gibson MK, Goldberg M, Hayman JA, Ilson DH, Javle M, Kelley S, et al: Esophageal cancer clinical practice guidelines. J Natl Compr Canc Netw. 4:328–347. 2006. View Article : Google Scholar : PubMed/NCBI

4 

Wieder HA, Ott K, Lordick F, Becker K, Stahl A, Herrmann K, Fink U, Siewert JR, Schwaiger M and Weber WA: Prediction of tumor response by FDG-PET: Comparison of the accuracy of single and sequential studies in patients with adenocarcinomas of the esophagogastric junction. Eur J Nucl Med Mol Imaging. 34:1925–1932. 2007. View Article : Google Scholar : PubMed/NCBI

5 

Lordick F, Ott K, Krause BJ, Weber WA, Becker K, Stein HJ, Lorenzen S, Schuster T, Wieder H, Herrmann K, et al: PET to assess early metabolic response and to guide treatment of adenocarcinoma of the oesophagogastric junction: The MUNICON phase II trial. Lancet Oncol. 8:797–705. 2007. View Article : Google Scholar : PubMed/NCBI

6 

Kim SJ, Koo PJ and Chang S: Predictive value of repeated F-18 FDG PET/CT parameters changes during preoperative chemoradiotherapy to predict pathologic response and overall survival in locally advanced esophageal adenocarcinoma patients. Cancer Chemother Pharmacol. 77:723–731. 2016. View Article : Google Scholar : PubMed/NCBI

7 

Wieder HA, Brücher BL, Zimmermann F, Becker K, Lordick F, Beer A, Schwaiger M, Fink U, Siewert JR, Stein HJ and Weber WA: Time course of tumor metabolic activity during chemoradiotherapy of esophageal squamous cell carcinoma and response to treatment. J Clin Oncol. 22:900–908. 2004. View Article : Google Scholar : PubMed/NCBI

8 

Swisher SG, Erasmus J, Maish M, Correa AM, Macapinlac H, Ajani JA, Cox JD, Komaki RR, Hong D, Lee HK, et al: 2-Fluoro-2-deoxy-D-glucose positron emission tomography imaging is predictive of pathologic response and survival after preoperative chemoradiation in patients with esophageal carcinoma. Cancer. 101:1776–1785. 2004. View Article : Google Scholar : PubMed/NCBI

9 

Vali FS, Nagda S, Hall W, Sinacore J, Gao M, Lee SH, Hong R, Shoup M and Emami B: Comparison of standardized uptake value-based positron emission tomography and computed tomography target volumes in esophageal cancer patients undergoing radiotherapy. Int J Radiat Oncol Biol Phys. 78:1057–1063. 2010. View Article : Google Scholar : PubMed/NCBI

10 

Jeganathan R, McGuigan J, Campbell F and Lynch T: Does pre-operative estimation of oesophageal tumour metabolic length using 18F-fluorodeoxyglucose PET/CT images compare with surgical pathology length? Eur J Nucl Med Mol Imaging. 38:656–662. 2011. View Article : Google Scholar : PubMed/NCBI

11 

Wahl RL, Jacene H, Kasamon Y and Lodge MA: From RECIST to PERCIST: Evolving considerations for PET response criteria in solid tumors. J Nucl Med. 50 Suppl 1:122S–150S. 2009. View Article : Google Scholar : PubMed/NCBI

12 

Edge SB, Byrd DR, Compton CC, Fritz AG, Greene FL and Trotti A: From the AJCC cancer staging manualAJCC Cancer Staging Handbook. 7th. Springer; New York, NY: 2010

13 

Elimova E, Wang X, Etchebehere E, Shiozaki H, Shimodaira Y, Wadhwa R, Planjery V, Charalampakis N, Blum MA, Hofstetter W, et al: 18F-FDG PET/CT as predictive of response after chemoradiation in esophageal cancer patients. Eur J Cancer. 51:2545–2552. 2015. View Article : Google Scholar : PubMed/NCBI

14 

Findlay JM, Middleton MR and Tomlinson I: A systematic review and meta-analysis of somatic and germline DNA sequence biomarkers of esophageal cancer survival, therapy response and stage. Ann Oncol. 26:624–644. 2015. View Article : Google Scholar : PubMed/NCBI

15 

Sato Y, Motoyama S, Saito H and Minamiya Y: Novel candidate biomarkers of chemoradiosensitivity in esophageal squamous cell carcinoma: A systematic review. Eur Surg Res. 56:141–153. 2016. View Article : Google Scholar : PubMed/NCBI

16 

Monjazeb AM, Riedlinger G, Aklilu M, Geisinger KR, Mishra G, Isom S, Clark P, Levine EA and Blackstock AW: Outcomes of patients with esophageal cancer staged with [18F]fluorodeoxyglucose positron emission tomography (FDG-PET): Can postchemoradiotherapy FDG-PET predict the utility of resection? J Clin Oncol. 28:4714–4721. 2010. View Article : Google Scholar : PubMed/NCBI

17 

Yuan H, Tong DK, Vardhanabhuti V, Law SY, Chiu KW and Khong PL: PET/CT in the evaluation of treatment response to neoadjuvant chemoradiotherapy and prognostication in patients with locally advanced esophageal squamous cell carcinoma. Nucl Med Commun. 37:947–955. 2016. View Article : Google Scholar : PubMed/NCBI

18 

Chhabra A, Ong LT, Kuk D, Ku G, Ilson D, Janjigian YY, Wu A, Schöder H and Goodman KA: Prognostic significance of PET assessment of metabolic response to therapy in oesophageal squamous cell carcinoma. Br J Cancer. 113:1658–1665. 2015. View Article : Google Scholar : PubMed/NCBI

19 

Huang JW, Yeh HL, Hsu CP, Lu YY, Chuang CY, Lin JC, Lin JF and Chang CF: To evaluate the treatment response of locally advanced esophageal cancer after preoperative chemoradiotherapy by FDG-PET/CT scan. J Chin Med Assoc. 78:229–234. 2015. View Article : Google Scholar : PubMed/NCBI

20 

Myslivecek M, Neoral C, Vrba R, Vomackova K, Cincibuch J, Formanek R, Koranda P and Zapletalova J: The value of 18F-FDG PET/CT in assessment of metabolic response in esophageal cancer for prediction of histopathological response and survival after preoperative chemoradiotherapy. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub. 156:171–179. 2012. View Article : Google Scholar : PubMed/NCBI

21 

Adams MC, Turkington TG, Wilson JM and Wong TZ: A systematic review of the factors affecting accuracy of SUV measurements. AJR Am J Roentgenol. 195:310–320. 2010. View Article : Google Scholar : PubMed/NCBI

22 

Lemarignier C, Di Fiore F, Marre C, Hapdey S, Modzelewski R, Gouel P, Michel P, Dubray B and Vera P: Pretreatment metabolic tumour volume is predictive of disease-free survival and overall survival in patients with oesophageal squamous cell carcinoma. Eur J Nucl Med Mol Imaging. 41:2008–2016. 2014. View Article : Google Scholar : PubMed/NCBI

23 

Chang S, Koo PJ, Kwak JJ and Kim SJ: Changes in total lesion glycolysis evaluated by repeated F-18 FDG PET/CT as prognostic factor in locally advanced esophageal cancer patients treated with preoperative chemoradiotherapy. Oncology. 90:97–102. 2016. View Article : Google Scholar : PubMed/NCBI

24 

Roedl JB, Colen RR, Holalkere NS, Fischman AJ, Choi NC and Blake MA: Adenocarcinomas of the esophagus: Response to chemoradiotherapy is associated with decrease of metabolic tumor volume as measured on PET-CT. Comparison to histopathologic and clinical response evaluation. Radiother Oncol. 89:278–286. 2008. View Article : Google Scholar : PubMed/NCBI

25 

Palie O, Michel P, Ménard JF, Rousseau C, Rio E, Bridji B, Benyoucef A, Meyer ME, Jalali K, Bardet S, et al: The predictive value of treatment response using FDG PET performed on day 21 of chemoradiotherapy in patients with oesophageal squamous cell carcinoma. A prospective, multicentre study (RTEP3). Eur J Nucl Med Mol Imaging. 40:1345–1355. 2013. View Article : Google Scholar : PubMed/NCBI

26 

Shi XH: Advances on esophageal carcinoma radiotherapy in China. China Oncol. 2001.

27 

Lloyd S and Chang BW: Current strategies in chemoradiation for esophageal cancer. J Gastrointest Oncol. 5:156–165. 2014.PubMed/NCBI

28 

Arslan N, Miller TR, Dehdashti F, Battafarano RJ and Siegel BA: Evaluation of response to neoadjuvant therapy by quantitative 2-deoxy-2-[18F]fluoro-D-glucose with positron emission tomography in patients with esophageal cancer. Mol Imaging Biol. 4:301–310. 2002. View Article : Google Scholar : PubMed/NCBI

29 

Yue J, Chen L, Cabrera AR, Sun X, Zhao S, Zheng F, Han A, Zheng J, Teng X, Ma L, et al: Measuring tumor cell proliferation with 18F-FLT PET during radiotherapy of esophageal squamous cell carcinoma: A pilot clinical study. J Nucl Med. 51:528–534. 2010. View Article : Google Scholar : PubMed/NCBI

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February 2018
Volume 15 Issue 2

Print ISSN: 1792-1074
Online ISSN:1792-1082

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APA
Zhang, P., Li, Z., Wang, D., Ma, F., Zhang, R., Liang, W. ... Sun, X. (2018). 18F-fluorodeoxyglucose positron emission computed tomography for monitoring tumor response in esophageal carcinoma treated with concurrent chemoradiotherapy. Oncology Letters, 15, 1845-1852. https://doi.org/10.3892/ol.2017.7528
MLA
Zhang, P., Li, Z., Wang, D., Ma, F., Zhang, R., Liang, W., Sun, M., Fu, Z., Sun, X."18F-fluorodeoxyglucose positron emission computed tomography for monitoring tumor response in esophageal carcinoma treated with concurrent chemoradiotherapy". Oncology Letters 15.2 (2018): 1845-1852.
Chicago
Zhang, P., Li, Z., Wang, D., Ma, F., Zhang, R., Liang, W., Sun, M., Fu, Z., Sun, X."18F-fluorodeoxyglucose positron emission computed tomography for monitoring tumor response in esophageal carcinoma treated with concurrent chemoradiotherapy". Oncology Letters 15, no. 2 (2018): 1845-1852. https://doi.org/10.3892/ol.2017.7528