Evaluation of the Effect of Pet/ct Fdg Inclusion on Mortality and Survival in Operated Thymoma Patients

doi:10.21203/rs.3.rs-3395353/v1

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Evaluation of the Effect of Pet/ct Fdg Inclusion on Mortality and Survival in Operated Thymoma Patients

https://doi.org/10.21203/rs.3.rs-3395353/v1

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Purpose: Thymic epithelial tumors (TET) constitute 50% of anterior mediastinal masses and are divided into three groups as thymoma, thymic carcinoma and neuroendocrine tumors. The most common TET is thymoma. In recent years, the use of Fuorodeoxyglucose Positron Emission Computed Tomography (PET-CT) has become widespread to evaluate the diagnosis, metabolism, stage and distant metastases of thymoma. In this study, it was aimed to investigate the connection of malignancy potential, survival and maximum standardized uptake value (SUVmax) measured by PET-CT before surgery according to the histological classification of the World Health Organization (WHO) in patients operated for thymoma. In addition, the predictive value of the Glasgow prognostic score (GPS) generated by C-Reactive Protein (CRP) and albumin values on recurrence and survival was investigated and its potential as a prognostic biomarker was evaluated.

Materials & Methods: Forty-five patients who underwent surgical resection for thymoma and were examined with PET-CT in the preoperative period between January 2010 and January 2022 were included in the study. The relationship between WHO histological classification, tumor size and SUVmax values on PET-CT according to TNM classification of retrospectively analyzed patients’records were evaluated. Preoperative albumin and CRP values were used to determine GPS.

Results: The cut-off value for SUVmax was found to be 5.65 in the patients and the overall survival rate of low-risk (<5.65) and high-risk (>5.65) patients was compared according to the SUVmax threshold value (5.65) and found to be statistically significant. In addition, the power of PET/CT SUVmax value to predict mortality (according to ROC analysis) was statistically significant (p=0.048). Survival expectancy was 127.6 months in patients with mild GPS (O points), 96.7 months in patients with moderate GPS (1 point), and 25.9 months in patients with severe GPS (2 points).

Conclusions: PET/CT SUVmax values can be used to predict histological subtype in thymoma patients, and pre-operative SUVmax and GPS are parameters that can provide information about survival times and mortality in thymoma patients.

Thymoma

PET – CT

SUVmax

Survival

Glasgow Prognostic Score

In adults, tumors originating from the thymus are the most common tumors in the anterior mediastinum and are divided into four groups: thymic epithelial cell-derived, neuroendocrine cell-derived, thymolipomas, and other rare thymic tumors.

Originating from thymic epithelial cell; Thymoma and thymic carcinoma are the most common primary tumors of the thymus and constitute 50% of anterior mediastinal masses (1).

According to the histological criteria of World Health Organization (WHO) 2004 classification, thymic masses are classified as A, AB, B1, B2, B3 thymoma and thymic carcinomas (2).

As a result of studies investigating the relationship between survival and histology, those with A, AB, B1 histology were grouped as low-risk, and those with B2, B3 and carcinoma histology were grouped as high-risk thymoma (3).

In addition, some studies in the literature suggest that thymic carcinomas with worse prognosis should be included in a separate group as 'type C' (4).

While Thorax Computed Tomography (CT) is the most commonly used imaging method in the diagnosis, staging, surgical or medical treatment decision, Thorax Magnetic Resonance Imaging (MRI) is preferred to determine the borders of the lesion and its relationship with the surrounding tissues (5–6).

The use of PET-CT has increased in the differential diagnosis, preoperative staging, treatment response and restaging of mediastinal masses (7). PET-CT can provide information in the analysis of the prognostic capacity of the mass, both as a qualitative (visual) method and a semi-quantitative method by using the maximum standardized uptake value (SUVmax) (8–9). It is accepted that a high SUVmax value reflects a high degree of tumor invasion and a poor prognosis (10–11). The most commonly used staging system to evaluate the tumor's relationship with surrounding tissues and invasion is the staging by Masaoka et al. (12).

Surgery is preferred for treatment of resectable tumors. While thymectomy is sufficient in low-risk thymomas, chemotherapy or radiotherapy may be required before surgery and chemoradiotherapy may be required after surgery in high-risk thymoma and thymic carcinomas (13).

Since knowing the histological subtype before surgery may affect treatment strategies, it is important to distinguish between early and advanced stage tumor histologically and radiologically (14–15).

Recent studies in the field of oncology have revealed that inflammation is an important determinant of disease progression in various types of cancer. (16–17). Based on these data, it is now well established that host-tumor interaction in the form of a systemic inflammatory response is closely related to outcomes in cancer patients (18–19). GPS is a predefined inflammation-based scale based on serum levels of two acute phase proteins, C-reactive protein (CRP) and albumin. Studies have shown that GPS can be used as a prognostic biomarker for malignant diseases (20).

Despite the widespread use of PET-CT, the number of studies evaluating the histological classes of mediastinal tumors using SUVmax is limited (21). In our study, the relationship between pre-treatment SUVmax values and thymoma histological classes and the effect of these values on mortality and overall survival were analyzed. In this way, we aimed to find an answer to the question of whether PET-CT can be used to distinguish WHO Thymoma histological classification and predict mortality of these classes, and whether GPS can be used as a biomarker to predict recurrence and survival in thymoma patients.

A total of 45 patients who were operated for thymoma between January 2010 and January 2022 and who were examined with PET-CT in the preoperative period were included in the study. Patients; with no preoperative alb, no CRP values, no PET-CT examination, with thymic carcinoma histology, receiving neoadjuvant chemotherapy or radiotherapy, with primary malignancy in another organ, having advanced stage with metastasis, who died in the operation or during early postoperative period, who were excluded from oncological follow-up, and with unavailable data were excluded from the study. The pathology results of the patients were analyzed and according to the WHO classification, those with histology A and AB were classified as Group 1 and those with histology of B1, B2 and B3 were classified as Group 2. PET-CT, taken for staging purposes before surgery was re-evaluated by the nuclear medicine physician in our hospital and the SUVmax value was recalculated by a single physician. The relationship between the histological type of the tumor and the PET-CT SUV max value was evaluated.

In order to determine GPS; 1 point was given for patients with high CRP (> 0.5 mg/dl) and 1 point was given for the presence of hypoalbuminemia (< 3.5 g/dl). Patients with normal CRP and albumin levels were given 0 points. The effect of the score based on these values on recurrence and survival in thymoma patients was investigated.

All procedures followed were in accordance with the ethical standards of the responsible human experiments committee (institutional and national) and the 1975 Declaration of Helsinki, as renewed in 2008. Ethics committee approval was obtained from our institution with protocol number 2020 – KAEK – 139.

Data were analyzed using the SPSS 22.0 program. The normal distribution of continuous variables was performed using the Shapiro-Wilk and Kolmogorov-Smirnov tests of normality. The Student-T test was used to compare the normally distributed parameters between the groups, and the Mann-Whitney U test was used to compare the non-normally distributed parameters. Chi-square and Fisher's Exact tests were used to compare categorical variables. The results were given as mean ± sd, median (min-max), and n (%).

The predictive power of mortality of SUVmax value and sample size were evaluated by ROC analysis. Cut-off value for SUVmax was determined by using the area under the curve (AUC) and Youden index values.

Survival analyzes were performed with Kaplan-Meier (log rank test) to evaluate the effects of variables affecting mortality on survival times. Results are presented with 95% confidence intervals. P < 0.05 was considered statistically significant in all tests.

A total of 45 patients, 18 (40%) female and 27 (60%) male, aged between 23 and 80 were included in this study. The mean age of the participants was 54.5 (between 23–80 years).

Twenty-eight patients were operated by median sternotomy, 15 patients by video-assisted thoracoscopic surgery (VATS), and 2 patients by right thoracotomy.

Pathological examination revealed type A in 10 patients (22.2%), type AB in 5 patients (11.1%), type B in 10 patients (22.2%), type B2 in 8 patients (17.8%), and type B3 in 12 patients (26.7%). The median tumor size was 57 mm (ranging from 1.3 to 14.2). Eight Stage I, 9 Stage IIA, 18 Stage IIB, 2 Stage III, 8 Stage IV tumors were observed. There were no patients with distant metastases. (Table 1).

Table 1

*Demographic and clinical characteristics of patients*
Age years	54.5±11.8 (23.0-73.0)
Gender Male Female	27 (60.0) 18 (40.0)
Stage Stage 1 Stage 2A Stage 2B Stage 3 Stage 4A	8 (17,8) 9 (20,0) 18 (40,0) 2 (4,4) 8 (17,8)
Sample size	5,7±3,0 (1,3-14,2)
Thymoma subtype A AB B1 B2 B3	10 (22.2) 5 (11.1) 10 (22.2) 8 (17.8) 12 (26.7)
Group Thymoma A+AB (group 1) Thymoma B1+B2+B3 (group 2)	15 (33.3) 30 (66.7)
PET Suv_max	5.7±3.4 (1.2-15.7)
Albumin mg/dl	4.0±0.6 (2.4-4.8)
CRP mg/l	6.85±9.60 (0.06-42.40)
mGPS Good prognosis Moderate prognosis Poor prognosis	33 (73.3) 5 (11.1) 7 (15.6)
Mortality	10 (22.2)
Follow-up time months	51.8±33.6 (0.6-147.8)

Patients were divided into two groups according to histological classification as Group 1 (type A and AB, n = 15) and Group 2 (type B1, B2, B3, n = 30). The median SUVmax value of the patients on PET-CT was 5.7 (1.2–15.7). The SUVmax value showed a statistically significant difference between Group 1 (median 3.3 (1.9–12.2) and Group 2 (median 5.7 (1.2–15.7) (p = 0.013) (Table 2).

Table 2

*Comparison of demographic and clinical characteristics of patients according to groups*
	Group 1 n = 15	Group 2 n = 30	P value
Age (years)	54.6 ± 10.9	54.5 ± 12.3	0.978
Gender Male Female	9 (60.0) 6 (40.0)	18 (60.0) 12 (40.0)	1.000
Stage Stage 1 Stage 2A Stage 2B Stage 3 Stage 4A	5 (33.3) 5 (33.3) 5 (33.3) 0 (0.0) 0 (0.0)	3 (10.0) 4 (13.3) 13 (43.3) 2 (6.7) 8 (26.7)	0.035
Sample Size	6.0 (2.5–14.2)	5.1 (1.3–10.6)	0.145
PET SUV_max	3.3 (1.9–12.2)	5.7 (1.2–15.7)	0.013
Albumin mg/dl	4.3 ± 0.6	3.9 ± 0.6	0.096
CRP mg/l	1.55 (0.06–19.40)	1.40 (0.14–42.40)	0.354
mGPS Good Moderate Bad	13 (86.7) 2 (13.3) 0 (0.0)	20 (66.7) 3 (10.0) 7 (23.3)	0.160
Mortality	2 (13.3	8 (26.7)	0.456

When the SUVmax median values were examined according to the stages, it was determined as 5.3 for Stage I (n = 8), 5.7 for Stage IIA-IIB (n = 27) and 6.2 for Stage III-IV (n = 10). And no statistically significant difference was found (p: 0.842) (Table 3).

Table 3

*Comparison of sample size and PET* *Suv_max* *value according to stages*
	Stage 1 N = 8	Stage 2A-2B N = 27	Stage 3–4 N = 10	P value
Sample size	6,6 ± 3,7	5,5 ± 3,0	5,6 ± 2,7	0,707
PET Suv_max	5,3 ± 4,1	5,7 ± 3,0	6,2 ± 3,9	0,842

Mortality was not observed in the first year postoperatively in either groups. The follow-up period of the patients was median 51.8 (0.6-147.8) months. Mortality was observed in 2 (13.3%) patients in Group 1 and in 8 (26.8%) patients in Group 2 (p: 0.456). When the survival results among the patient groups were examined, the meadian survival was 89.2 months in Group 1 and 102.4 months in Group 2. No statistical significance was found in the survival results between groups (p: 0.519) (Fig. 1).

The SUV max cut-off value was calculated as 5.65 (1.2–15.7) in the patients. Patients with SUV max below the cut-off value were considered low risk, and patients with SUV max value above the cut-off value were considered high risk. The overall survival rate of low-risk patients was 98 months, and high-risk patients were 87 months (p:0.023). (Fig. 3)

The predictive power of PET-CT SUVmax for mortality (based on ROC analysis) was statistically significant (p = 0.048) (Table 4).

Table 4

*The power of PET* *Suv_max* *to predict mortality (ROC analysis)*
	AUC	95% CI	P value	Cut-off	Sensitivity	Specificity
Suv_max	0.707	0.555–0.859	0.048	5.65	80.0%	68.6%

PET-CT SUVmax value in thymoma patients was found to be statistically significant in histological classification of patients and predicting mortality (p:0.023) (Table: 5).

Table 5: Comparison of overall survival times in Suv_max risk groups (based on ROC analysis) (Kaplan Meier analysis)

Suv_max groups	Estimated OS (months)	95% CI	P value
< 5.65 (low risk)	98.0	88.4-107.6	0.023
> 5.65 (high risk)	87.0	58.0-115.9	0.023
OS; Overall survival

When the sample size and PET SUVmax values were compared in the stage groups, no statistically significant difference was found. There was no correlation between sample size and PET-CT SUV max value (r = 0.045, p = 0.767). The effects of age, gender and stage on overall survival were not statistically significant.

In addition, it was evaluated whether there was a statistical difference in survival times between the GPS severity groups. Survival time was calculated as 127.6 months in patients with mild GPS, 96.7 months in moderate GPS, and 25.9 months in severe GPS. There was a statistically significant difference between survival times (p < 0.001) (Table 6) (Fig. 2).

Table 6

*Comparison of overall survival times in GPS severity groups (Kaplan Meier analysis)*
mGPS score	Estimated OS (months)	95% CI	P value
Mild	127.6	109.8-145.3	< 0.001	p = 0.824 p = 0.015 **p < 0.001
Moderate	96.7	96.6–96.6
Severe	25.9	6.9–44.8
mild vs moderate, * moderate vs severe, ***mild vs severe .mGPS; modified Glasgow’s prognostic score, OS; Overall survival

Although thymoma and thymic carcinoma, which are the most common primary tumors of the thymus, are common tumors in thoracic surgery practice, their rate among adult cancers is below 1% (22).

The WHO thymoma classification constitutes a heterogeneous group of tumors ranging from thymomas with a low risk of invasion to carcinomas with an aggressive course (23).

Although thorax CT and MRI are the most commonly used imaging modalities in the diagnosis of thymoma, there are studies showing that CT and MRI are insufficient in differentiating early stage thymoma, thymic cancer and carcinoma (24).

Despite the increasing use of PET-CT in the planning of staging and treatment strategies (25), there are not enough studies for definition of its role in histological classification of thymoma and predicting mortality (26). Yanarates et al. showed that although PET-CT could not distinguish the histological subtypes of TET, it was useful in the differentiation of benign and malignant anterior mediastinal masses (27). In a similar study by Travaini et al., it was emphasized that PET-CT is useful in the differential diagnosis of benign and malignant lesions with thymic location (28). Again in a multicenter study, Lococo et al. emphasized that PET CT may be useful in predicting thymoma histology (29).

The high SUVmax value in PET-CT reflects the invasiveness of the tumor and poor prognosis (30). In the study of Igai et al., it was noted that the SUV max value of thymic carcinomas was higher than that of thymomas in PET-CT, and the SUV max value increased in correlation with both WHO and Masaoka classifications (31). In a similar study by Sung et al., thymic epithelial tumors were classified into three groups as low-risk, high-risk and thymic carcinoma; it was shown that the SUV max value of low-risk thymomas was lower than that of high-risk thymomas and thymic carcinoma (32).

In another study on TET, although there was no significant difference in SUVmax between low and high risk thymomas, SUV max values were found to be significantly higher in thymic carcinomas. In the same study, an interesting finding was that while a more heterogeneous uptake of FDG is generally observed in low-risk thymomas, homogeneous uptake is more likely in high-risk thymomas and particularly thymic carcinomas, which is attributed to the positive correlation between FDG uptake and tumor growth rate or cell density (33–34).

Masaoka staging, which is based on the relationship of the mass with the surrounding tissues, is most commonly used in staging of thymomas. Although Luzzi et al. showed that there is a direct and significant relationship between tumor stage and SUV max, it was thought that the inclusion of both thymoma and thymic carcinoma in the study group may lead to an incorrect assessment. In the same study, since the possibility of local invasion is high in lesions with a high SUVmax value, it is recommended to prefer open surgery instead of needle biopsy (35). Researching the use of PET-CT in thymoma, Rini et al. argued that in general, PET-CT is an important imaging technique in the evaluation of a patient presenting with an anterior mediastinal mass, but it is not very reliable in determining the stage of thymoma and thymic carcinoma (36).

When prognostic factors were investigated in thymoma; some authors have stated that histological classification alone is a prognostic factor in TET patients (37). Li et al. reported that age and Masaoka stage are prognostic factors, while Yanagiya et al. has shown that thymoma histological type rather than stage is a significant prognostic factor (38). In another study, Weis et al. showed that stage and histological subtype are strong factors affecting prognosis (39).

In our study, no relationship was found between tumor size and SUV max value. In addition, when the SUVmax median values according to the stages were examined, no statistically significant difference was observed (p: 0.842), while the mortality predictive power of the PET-CT SUVmax value (based on the ROC analysis) was statistically significant (p = 0.048).

When we analyzed the survival according to the stages; Stage I was 102.1 months, Stage IIA-IIB was 96.7 months, Stage III-IV was 54.3 and it was not statistically significant. (p: 0.226). No early postoperative mortality was observed in either group. Mortality was observed in 2 (13.3%) patients in Group 1 and in 8 (26.8%) patients in Group 2 (p: 0.456).

Thymoma treatment varies depending on whether the tumor is low or high risk. Therefore, it is important to distinguish low-risk and high-risk tumors histologically and radiologically. In a prospective study, 23 patients were evaluated and it was emphasized that, anterior mediastinal tumors with a mean SUVmax of < 5 are most likely to be low-risk thymic tumors and can usually be treated with direct surgery unless there are other clinical indications, whereas lesions with an SUVmax of > 5 are more likely to be thymic carcinoma or lymphoma and biopsy is a necessity (40). In our study, the cut-off value was found to be 5.65, and the survival of low-risk (< 5.65) patients was 98 months, and the overall survival of high-risk (> 5.65) patients was 87 months, which was significant compared to the SUV max value (5.65) (p: 0.023).

Our study showed that PET-CT is useful in predicting the histological type and mortality of thymic epithelial tumors, that tumors in thymoma A, AB, and B1 histology have low SUVmax, while tumors in B2 and B3 histology have high SUVmax. However, the rarity of anterior mediastinal tumors caused the number of patients to be limited. We think that it would be useful to evaluate the same criteria in a larger study group.

In a recent analysis of 125 thymoma patients, height of preoperative GPS was independently associated with lower overall and recurrence-free survival (NSC) after thymectomy. Therefore, it was stated that GPS could be a valuable biomarker for the postoperative prognosis of TET (41). In this study, it was determined that the survival expectancy was calculated as 127.6 months in patients with mild GPS, 96.7 months in patients with moderate GPS, and 25.9 months in severe patients. The relationship between GPS and survival was statistically significant (< 0.001).

The comparison of SUVmax values in different subtypes of thymoma on PET/CT showed that patients with histological class A and AB thymomas had lower SUVmax values. Therefore, pre-treatment PET/CT appears to be a suitable imaging modality to better characterize thymomas and reduce unnecessary invasive procedures in patients with low SUVmax values. Additionally, it was found that both SUVmax values and GPS prognostic groups have an impact on survival durations. In patients with thymoma, PET/CT should be the preferred imaging method in the preoperative period. The SUVmax value on PET/CT can provide valuable information about the histological subtype of the tumor. Both preoperative SUVmax and GPS can serve as predictive parameters for disease mortality and survival durations.

CAR : C-Reactive protein-to-albumin ratio

CT : Computerized tomography

F – 18 FDG : Fluorodeoxyglucose F – 18

MG : Myasthenia Gravis

MRI : Magnetic resonance imaging

OS : Overall survival

PET : Positron emission tomography

PET/CT : Positron emission tomography – computerized tomography

RFS : Recurrence free survival

ROC : Receiver Operating Characteristics

SPSS : Statistics Package for the Social Sciences

SUV_max : Maximum standardized uptake value

TEN : Thymic epithelial neoplasms

WHO : World Health Organization

Ethics approval and consent to participate: The study has been approved by the ethics committee at 2020 - KAEK with protocol number 139.

Informed consent

All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, as revised in 2008. Ethics committee approval has been granted from our institution and informed consent has been obtained from all participants.

Consent for publication: Not applicable

Availability of data and material: All data generated or analysed during this study are included in this published article [and its supplementary information files]

Competing interests: The authors declare that they have no competing interests.

Funding There is no specific funding related to this research.

Authors' contributions:

B.A.S and S.Y made substantial contributions to the design of the work;

B.G and B.A.S made the analysis of data;

E.D and SY made the creation of new software used in the work;

N.A and B.A.S have drafted the work

A.U and K.C.C revised it

Acknowledgements: Not applicable

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No competing interests reported.

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Evaluation of the Effect of Pet/ct Fdg Inclusion on Mortality and Survival in Operated Thymoma Patients

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