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Open Access 04.05.2024 | Original Article

Maximum standardized uptake value in ¹¹C-methionine positron emission tomography may predict the prognosis of patients with oral squamous cell carcinoma

verfasst von: Takeshi Kuroshima, Yoshimasa Kitagawa, Jun Sato, Shiro Watanabe, Takuya Asaka, Takahiro Abe, Hiroyuki Harada, Kenji Hirata, Yuji Kuge

Erschienen in: Odontology

Abstract

The present study aimed to elucidate the correlation between the uptake of ¹¹C-methionine (MET) by a primary tumor and the survival of patients with oral squamous cell carcinoma (OSCC). This study enrolled 31 patients who underwent radical surgery for OSCC. The patients underwent pretreatment MET-positron emission tomography (PET) scanning. We analyzed correlations between the maximum standardized uptake value (SUV_max) of MET-PET in a primary tumor and the clinicopathological features. Further, we compared overall survival (OS), disease-specific survival (DSS), and loco-regional recurrence (LRR) rates between the two groups according to SUV_max of MET-PET. SUV_max of MET-PET in a primary tumor was higher in patients with advanced T-classification and advanced clinical stage, with significant differences (P = 0.001 and P = 0.016, respectively). The patients with SUV_max of MET-PET ≥ 4.4 showed significantly lower DSS rates and higher LRR rates than those with SUV_max of < 4.4 (P = 0.015 and P = 0.016, respectively). SUV_max of MET-PET and OS rates showed no significant correlation (P = 0.073). The present study revealed that SUV_max of MET-PET may predict clinical outcomes and prognosis in patients with OSCC who underwent radical surgery.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Introduction

Oral cancer is a prevalent malignancy globally, with an estimated 354,864 new cases and 177,384 deaths in 2018 [1]. Oral squamous cell carcinoma (OSCC), accounting for > 90% of oral malignancies, is mainly treated by surgery, radiotherapy, and adjuvant chemotherapy. The early-stage OSCC can be successfully controlled by curative treatment, with good treatment outcomes and high survival rates. In contrast, the prognosis of patients with advanced OSCC has not significantly improved during the past four decades [2]. Crucial factors remain unknown even at present despite many efforts to identify the prognostic factors of patients with OSCC. Improving the prognosis of patients with OSCC requires a treatment strategy following reliable prognostic factors.

Positron emission tomography (PET) imaging allows clinicians to view and assess the metabolic activities of tumor cells, not the anatomical or structural changes in affected sites, by the uptake of radioactive tracers [3]. ¹⁸F-fluorodeoxyglucose (FDG)-PET is widely used clinically for tumor imaging due to increased glucose metabolism in many tumor types, including OSCC [3, 4]. In theory, cancer with a high uptake of FDG indicates more aggressive behavior, resulting in poor prognosis of patients [5]. However, whether or not FDG-uptake parameters, including the maximum standardized uptakes value (SUV_max), can predict the prognosis of OSCC patients remains controversial [4]. FDG uptake in oral malignancy is likely to overlap with FDG accumulation in dental inflammation or physiological uptake [3, 6]. These artifacts frequently make the evaluation of true FDG uptake by the primary OSCC tumor difficult. Therefore, another metabolic imaging, which can correctly assess tumor malignancy without these artifacts and predict the prognosis of patients with OSCC, is required.

An amino acid PET tracer, ¹¹C-methionine (MET), is used to evaluate several tumor types [6‐16]. MET-uptake reflects increased amino acid transport and protein synthesis [10, 17, 18]. MET-PET is mostly used for brain tumors, and its usefulness has been reported in terms of tumor detection, tumor grading, biopsy and radiotherapy planning, tumor extent and therapeutic response assessment, differentiation between tumor recurrence and radiation necrosis, and patient prognosis [10]. Some studies are conducted on MET-PET for head and neck malignancies [11‐14]. MET-PET imaging has been reported to be useful in detecting lesions [11‐14] and assessing response to radiotherapy in head and neck cancer [12, 14]. To the best of our knowledge, only one study evaluated MET uptake as a prognostic factor in patients with head and neck cancer. Lindholm et al. have revealed no association in the amount of MET uptake by the tumor with clinical outcomes in patients with head and neck cancer [13]. However, some limitations may have influenced this result. First, the study included patients who underwent various types of curative treatment: surgery and definitive radiotherapy with or without chemotherapy. Second, they used SUV_mean as a parameter. The reproducibility of measurement of SUV_mean may be insufficient compared with that of SUV_max because the regions of interest were placed manually on the tumor areas. Additionally, they included a limited number of patients with OSCC. Taken together, whether or not MET uptake by the tumor is predictive for the prognosis of patients with OSCC remains unclear.

Therefore, the present study aimed to elucidate the correlation between SUV_max of MET of primary tumor and survival of patients with OSCC.

Materials and methods

Patients

This study enrolled 46 patients with OSCC who were treated in the Department of Oral Medicine and Surgery, Hokkaido University Hospital from 2005 to 2008. All patients underwent pretreatment MET-PET scanning. This study excluded 2 patients who received brachytherapy for tongue cancer, 7 patients with recurrent tumors, and six patients who received palliative treatment. Finally, the analysis included 31 patients who underwent curative surgery. This study complied with the Declaration of Helsinki and was approved (approval no. CT2022-0233) by the Ethical Committee of the Hokkaido University Hospital. Each patient signed informed consent for this study.

The present study included 22 males and 9 females (Table 1). The median age was 69.0 years, ranging from 24 to 84 years. The primary sites of OSCC were the tongue (n = 14), upper gingiva (n = 7), lower gingiva (n = 4), floor of the mouth (n = 3), palate (n = 2), and buccal mucosa (n = 1). The clinical T-classification was T1, T2, T3, and T4 in 2, 13, 6, and 10 patients, respectively. The clinical N-classification was N0, N1, and N2 in 19, 7, and 5 patients, respectively. The clinical staging was stages I, II, III, and IV in 2, 10, 7, and 12 patients, respectively. OSCC was staged according to the 7th edition of the American Joint Committee on Cancer TNM staging system [19].

Table 1

Patient and tumor characteristics

No	Age	Sex	Primary site	cT	cN	MET SUV_max	pN	R or CR	Locoregional failure	Distant failure	prognosis
1	31	M	Tongue	3	2	5.7	2	pre-R	+	−	DOD
2	69	F	Tongue	3	2	8.3	0	pre-CR	−	−	NED
3	76	F	Tongue	2	0	3.1			−	−	NED
4	76	F	Floor of the mouth	3	0	3.9	0		−	−	NED
5	69	M	Tongue	2	0	2.0			−	−	DOC
6	79	M	Upper gingiva	4a	0	5.6			−	−	NED
7	65	M	Lower gingiva	4a	1	4.9	1	pre-CR	+	+	DOD
8	75	M	Tongue	3	1	4.1	1		−	−	NED
9	59	M	Tongue	2	0	1.0			−	−	NED
10	73	M	Upper gingiva	2	0	4.4			−	−	NED
11	48	M	Floor of the mouth	4a	1	5.2	0		−	−	NED
12	84	M	Palate	3	1	5.0	2		−	−	NED
13	78	M	Lower gingiva	2	1	2.7	1		−	−	NED
14	63	M	Tongue	1	0	3.5			−	−	DOC
15	69	M	Tongue	2	1	3.2	2	pre-R	−	−	NED
16	62	M	Tongue	3	0	9.0	0	pre-R	−	−	NED
17	60	F	Upper gingiva	4a	0	3.0			−	−	NED
18	77	F	Lower gingiva	2	0	10.2			−	−	NED
19	58	F	Upper gingiva	4a	0	6.6		post-R	+	+	DOD
20	69	F	Upper gingiva	1	0	2.4			−	−	NED
21	53	M	Palate	4a	2	7.1	0	post-R	−	−	NED
22	45	M	Tongue	2	0	3.4			−	−	NED
23	69	M	Tongue	2	0	6.1			−	−	NED
24	72	F	Upper gingiva	4a	0	8.1		pre-CR	−	−	NED
25	74	M	Lower gingiva	2	1	3.7	0		−	−	NED
26	54	M	Tongue	4a	2	6.1	2		−	−	DOC
27	24	M	Tongue	2	0	3.4	1		−	−	NED
28	63	M	Floor of the mouth	4a	2	4.4	2		+	+	DOD
29	74	M	Upper gingiva	2	0	2.7			−	−	NED
30	70	F	Buccal	4a	0	6.8		pre-CR	+	+	DOD
31	79	M	Tongue	2	0	3.7			−	−	NED

No.: number of the patients; cT: clinical T-classification; cN: clinical N-classification; pN: clinical P-classification; pre-R: preoperative radiotherapy; post-R: postoperative radiotherapy; pre-CR: preoperative chemo-radiotherapy; post-CR: postoperative chemo-radiotherapy; DOD: death of disease; DOC: death of other causes; NED: no evidence of disease

Treatment and prognosis

The treatment for 31 patients with OSCC included surgery alone (22 patients), surgery with preoperative radiotherapy (16–50 Gy; 3 patients: cases 1, 15, and 16), surgery with preoperative chemo-radiotherapy (cisplatin of 4 mg/m² and docetaxel of 10 mg/m²; 26–30 Gy; 4 patients: cases 2, 7, 24, and 30), and surgery with postoperative radiotherapy (60 Gy; 2 patients: cases 19 and 21). The patients with clinical stage III or IV with a long waiting time for surgery received preoperative radiotherapy with concurrent chemotherapy. The primary tumor was resected with surgical margins of > 10 mm. Twelve patients with clinically metastatic cervical lymph nodes received neck dissection. Three patients with N0 tumors underwent elective neck dissection along with the reconstruction using a vascularized-free flap. A total of nine patients had pathological positive nodes. The patients who had pathological close margins in the primary tumor, more than three pathological metastatic nodes, or pathological extra-nodal extension received postoperative radiotherapy.

All 31 patients were followed up for over five years postoperative. Five patients experienced loco-regional recurrence in the follow-up periods. Five patients died of loco-regional and/or distant failure and three died of other causes.

PET study

Whole-body emission images were obtained 15–20 min after injecting 395.6 ± 44.4 MBq (mean ± standard deviation, range 334–512 MBq) of MET using the three-dimensional acquisition method. A day before the PET studies, the patients were requested to fast for at least 3 h before the scheduled MET injection. All patients were requested to remain resting and quiet and to void just before scanning. Whole-body PET acquisitions were performed from the skull base to the pelvis with an axial field of view of 15.5 cm (spatial resolution, 4.5 mm full width at half maximum) using a PET scanner (ECAT EXACT HR + ; Siemens/CTI, Knoxville, TN, USA). Attenuation correction was performed using rotating ⁶⁸Ge–⁶⁸Ga rod sources. The attenuation-corrected images were reconstructed with the ordered subsets expectation maximization algorithm. Two experienced nuclear medicine physicians (KH and SW), who were blinded to the clinical data and the results of other imaging studies, evaluated all PET scans. MET uptake was evaluated by visual analysis and using the maximum standardized uptake value (SUV_max), as reported earlier [20, 21]. The MET-PET imaging results have not affected the treatment of the patients with OSCC.

Statistical analyses

To analyze an association between SUV_max of MET-PET and clinicopathological features, we used the Mann-Whitney U test for comparison of two groups and the Kruskal-Wallis test for comparison of more than three groups. Overall survival (OS) was measured from the date of surgery to death of any cause. Disease-specific survival (DSS) was measured from the date of surgery to death of uncontrolled OSCC. Loco-regional recurrence (LRR) was measured from the date of surgery to loco-regional relapse. The ability of SUV_max of MET-PET to predict prognosis or loco-regional recurrence were evaluated by a receiver operating characteristic curve analysis. Based on maximizing Youden index, the optimal cut-off value of SUV_max was determined as follows: 4.4 (sensitivity: 0.75; AUC 0.58) for OS, 4.4 (sensitivity: 1.0; AUC 0.71) for DSS, and 4.4 (sensitivity: 1.0; AUC 0.71) for LRR. Therefore, we divided the patients into two groups according to SUV_max of primary tumor: SUV_max of ≥ 4.4 and < 4.4. Survival and recurrence rates were analyzed using the Kaplan–Meier method and compared between two groups using the log-rank test. All statistical analyses were performed using JMP14 and JMP17 (SAS Institute Inc., Cary, NC, USA). P-values of < 0.05 indicated statistical significance in all analyses.

Results

SUV_max of MET-PET and clinical factors of patients with OSCC

Of all 31 patients, MET uptake by the primary tumor was detected in 30 patients (96.8%). Figure 1 illustrates the representative case. The median SUV_max of MET-PET in the primary tumor was 4.4 (range: 1.0–10.2). MET uptake was not detected in the patient with a tongue tumor classified as T2N0 (Table 1, case 9). In this case, SUV_max of MET-PET was arbitrarily assigned to 1.0. The highest SUV_max as an outlier of 10.2 was detected in a patient with a lower gingival tumor classified as T2N0 (Table 1, case 18).

We analyzed correlations between SUV_max of MET-PET in the primary tumor and clinicopathological features (Table 2). SUV_max of MET-PET in the primary tumor was higher in patients with advanced T-classification (T3 + T4) and clinical stage (III + IV) with significant differences (P = 0.001 and P = 0.016, respectively; Table 2). SUV_max according to age, sex, primary site, and clinical N-classification showed no significant difference (Table 2).

Table 2

Correlation between SUV_max of MET-PET in the primary tumor and clinicopathological features in patients with OSCC

Clinicopathological features	Number of patients	Median SUV_max of MET (range)	P-value
Age (median age 69)
≥69 years	18	4.0 (2.0–10.2)	0.689*
< 69 years	13	4.9 (1.0–9.0)	0.689*
Sex
Male	22	4.2 (1.0–9.0)	0.277*
Female	9	6.6 (2.4–10.2)	0.277*
Primary Site
Tongue	14	3.6 (1.0–9.0)	0.819**
Upper gingiva	7	4.4 (2.4–8.1)
Lower gingiva	4	4.3 (2.7–10.2)
Floor of the mouth	3	4.4 (3.9–5.2)
Palate	2	6.1 (5.0–7.1)
Buccal mucosa	1	6.8
Clinical T-classification
T1 + T2	15	3.4 (1.0–10.2)	0.001*
T3 + T4	16	5.7 (3.0–9.0)	0.001*
Clinical N-classification
N0	19	3.7 (1.0–10.2)	0.372*
N1 + N2	12	4.9 (2.7–8.3)	0.372*
Clinical stage
I + II	12	3.4 (1.0–10.2)	0.016*
III + IV	19	5.2 (2.7–9.0)	0.016*

*Mann-Whitney U test

**Kruskal-Wallis test

P < 0.05 was considered statistically significant in all analyses

SUV_max of MET-PET and the prognosis of patients with OSCC

The patients with SUV_max of ≥ 4.4 had significantly lower DSS rates and higher LRR rates than those with SUV_max of < 4.4 (P = 0.015 and P = 0.016, respectively; Fig. 2a and b). Meanwhile, there was no significant correlation between SUV_max of MET-PET and OS rate (P = 0.073) (Fig. 2c).

Discussion

This is the first study to reveal the prognostic impact of MET uptake by the primary tumor in patients with OSCC. The present study demonstrated significantly higher LRR rate and poor DSS rate in the patients with SUV_max of MET-PET of ≥ 4.4 than those with SUV_max of MET-PET of < 4.4. Notably, advanced primary tumors exhibited higher uptake of MET in comparison to early tumors. These results indicate that the SUV_max of MET-PET may correctly reflect the malignancy of the tumor and be predictive for the prognosis of patients with OSCC.

FDG is widely used as a PET tracer for tumor imaging. One of the limitations in FDG-PET imaging is most likely caused by increased FDG accumulation in the physiological structures and benign lesions such as infection and inflammation [3, 6]. Almost all patients with OSCC have multiple FDG uptakes in the oral cavity, such as the muscle, salivary gland, tonsil, and dental inflammations, on FDG-PET/CT imaging; therefore, the SUV_max of the primary tumor frequently overlaps with that of these areas [22]. Moreover, FDG uptake in the whole tumor has been reported to be accentuated by the macrophages and granulation tissues, in animal models [23]. Hence, FDG accumulation by oral cancer might not correctly reflect the biological activity and malignancy of its cancer cells. Recent studies have revealed that SUV_max of FDG-PET is not significantly associated with prognosis in most patients with OSCC or nasopharyngeal cancer [24, 25].

Its uptake reflects increased amino acid transport, protein synthesis, and cellular proliferation activity in MET-PET imaging [17, 18, 26]. MET and FDG have been reported to show different distributions in tumor tissue of the animal models [27]. A high MET uptake by the tumor was mostly observed by the viable cancer cells, and its uptake by macrophages and granulation tissues was lower than that of FDG [27]. Clinical studies of lung cancer have demonstrated that MET-PET may reduce the false-positive findings in inflammatory lung diseases when compared with FDG-PET [6, 9, 28]. Hsieh et al. studied 14 cases of solitary lung nodules using MET-PET and FDG-PET to differentiate between malignant and benign diseases [6]. Their results revealed that MET-PET accurately diagnosed 7 cases of inflammatory and infectious nodules with true negative results, despite false positives of FDG-PET [6]. This result indicates that MET uptake by the tumor might be less under the influence of inflammation and be likely to reflect the true activity of cancer cells.

It is unclear whether metabolic assessment of the primary tumor can predict regional lymph node metastasis. Goksel et al. reported that metabolic tumor volume of the primary tumor on FDG-PET/CT was a significant predictor of cervical lymph node metastasis in patients with head and neck cancer [29]. Meanwhile, Yamada et al. demonstrated that SUV_max in OSCC primary tumor was not associated with cervical lymph node metastasis [30]. The results of MET-PET investigation by Lindholm et al. showed that the proportion of patients with cervical lymph node metastasis was not different in the low and high SUV groups in patients with head and neck cancer [13]. In the present study, higher MET uptake of the primary tumor was significantly correlated with advanced T-classification, locoregional recurrence, and prognosis. However, there was no association between N-classification and SUV_max of MET. These results suggest that higher MET uptake by the primary tumor may be a potential predictor of locoregional recurrence, but does not appear to be a predictor of cervical lymph node metastasis in patients with OSCC.

The present study has some limitations. (1) This study included a relatively small number of patients. Therefore, the statistical power to draw firm conclusions was insufficient. (2) Preoperative radiotherapy and chemo-radiotherapy are currently not standard treatments for patients with OSCC; however, seven patients received these treatments in the present study.

In conclusion, the present study revealed that SUV_max of MET-PET may predict clinical outcomes and prognosis in patients with OSCC who underwent curative surgery. Additional prospective studies with a large cohort of patients are necessary to verify and further extend our study results.

Declarations

Ethical approval

This study complied with the Declaration of Helsinki and was approved (Approval No. CT2022-0233) by the Ethical Committee of the Hokkaido University Hospital.

Each patient signed informed consent for this study.

Conflict of interest

No potential conflicts of interest were disclosed.

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Titel: Maximum standardized uptake value in 11C-methionine positron emission tomography may predict the prognosis of patients with oral squamous cell carcinoma
verfasst von: Takeshi Kuroshima
Yoshimasa Kitagawa
Jun Sato
Shiro Watanabe
Takuya Asaka
Takahiro Abe
Hiroyuki Harada
Kenji Hirata
Yuji Kuge
Publikationsdatum: 04.05.2024
Verlag: Springer Nature Singapore
Erschienen in: Odontology
Print ISSN: 1618-1247
Elektronische ISSN: 1618-1255
DOI: https://doi.org/10.1007/s10266-024-00946-w

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Maximum standardized uptake value in ¹¹C-methionine positron emission tomography may predict the prognosis of patients with oral squamous cell carcinoma

Abstract

Publisher's Note

Introduction