Comparison of 68Ga-FAPI PET CT/MRI and 18F-FDG PET/CT in metastatic lesions of gynecological cancers: a systematic review and head-to-head meta-analysis

Abstract

Background

68Ga-labled fibroblast activating protein inhibitor (68Ga-FAPI) represents a new and exciting positron emission tomography-computed tomography/magnetic resonance (PET-CT/MR) radiotracer.

Purpose

To compare the diagnostic efficacy of 68Ga-FAPI PET CT/MR and 18F-fluorodeoxyglucose (18F-FDG) PET/CT in metastatic lesions of gynecological cancers (GCs).

Material and Methods

The PubMed, Embase, and Web of Science databases were thoroughly investigated from inception until 22 December 2023. A head-to-head contrast between 18F-FDG PET/CT as well as 68Ga-FAPI PET CT/MR for the assessment of GCs was presented by the included studies. A random variable model was employed to examine the sensitivity in detection of lymph node (LN) and peritoneal metastases (PM).

Results

The pooled sensitivity for 68Ga-FAPI PET CT/MR and 18F-FDG PET/CT in lymph node metastases (LNM) of GC were 0.98 (95% confidence interval [CI] = 0.86–1) and 0.85 (95% CI = 0.65–0.98), respectively, while the results about peritoneal metastases in ovarian cancer were 0.98 (95% CI = 0.93–1) and 0.71 (95% CI = 0.55–0.86). Compared with 18F-FDG PET/CT, 68Ga-FAPI PET CT/MR exhibited a better sensitivity in peritoneal involvement of ovarian cancer with a relative risk of 0.24 (95% CI = 0.09–0.40) and P = 0.002.

Conclusion

68Ga-FAPI PET CT/MR displayed a superior sensitivity over 18F-FDG PET/CT in detecting metastatic lesions of ovarian cancer. However, there was insufficient evidence to favor the superiority of 68Ga-FAPI PET CT/MR in LNM of CC. Further studies are needed for evaluating primary and metastatic lesions of 68Ga-FAPI PET CT/MR in different GC.

Keywords

68Ga-FAPI 18F-FDG gynecological cancer positron emission tomography computed tomography

Introduction

Gynecological cancer (GC) encompasses a range of cancers originating in the female reproductive system. The most prevalent types are cervical cancer (CC), uterine corpus cancer, and ovarian cancer (OC), which represent 3.1%, 2.2%, and 1.6% of new cases, respectively, and 3.4%, 1.0%, and 2.1% of new deaths of all cancer sites globally in 2020. Notably, cervical cancer has the second-highest mortality rate behind breast cancer, which continues to be the main trigger of cancer-related fatalities for women (1). The outlook for individuals with metastatic cancers remains impoverished, underscoring the need for a reliable staging tool for effective treatment planning (2,3).

18F-FDG positron emission tomography/computed tomography (PET/CT) is pivotal in diagnosing, tracking, as well as following up on GC. It may be an effective method for evaluating a possible extraperitoneal or extra-pelvic metastases and suspicion of recurrence and is considered to be a valuable diagnostic imaging method (4 –6). However, it has limitations, including false-positive uptake of 18F-FDG in endometriosis cysts, uterine fibroids, and the uterine endometrium during menstrual, ovulatory, and premenopausal periods, as well as in lesions with intense inflammation (7). Moreover, false-negative results have been observed in urinary tract tumors, scirrhous stomach cancer, and hepatocellular cancer (8). The fibroblast activation protein inhibitor (FAPI) variants have emerged as promising tracers for future PET imaging applications (9 –11). 68Ga-FAPI PET/CT has displayed high diagnostic efficiency and detection rates in various tumors, particularly gastric cancers, lung cancers, and other malignant tumors, and has proven effective even in cases challenging for 18F-FDG PET/CT (12 –15).

68Ga-FAPI PET-CT/magnetic resonance (MR) might surpass 18F-FDG PET/CT in detecting gynecological tumors (16). However, a comprehensive comparison of these two tests in assessing metastatic gynecological malignancies has still not been conducted. The goal of the research is to determine and compare the efficacy of 18F-FDG PET and 68Ga-FAPI PET for individuals with gynecological tumors.

Material and Methods

The Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines were followed within this meta-analysis (17).

Literature search

Electronic literature databases, including PubMed, Embase, and Web of Science, were looked over on 22 December 2023. The search algorithm incorporated terms such as: (i) “women's” OR “gynecological” OR “cervical” OR “uterine” OR “uterus” OR “endometrial” OR “ovarian” OR “ovary” OR “tubal” AND (ii) “cancer” OR “neoplasm” OR “tumor” OR “tumour” AND (iii) “FAPI-04” OR “68Ga-FAPI-04” OR “FAPI” AND (iv) “fluorodeoxyglucose” OR “FDG” AND (v) “Positron Emission Tomography” OR “PET” OR “PET/CT” OR “PET/MRI.” The search did not impose any starting date or language restrictions.

Inclusion and exclusion criteria

The studies that made up this evaluation satisfied these requirements: (i) the primary focus was a head-to-head contrast of the diagnostic accuracy of 18F-FDG PET/CT and 68Ga-FAPI PET CT/MR for individuals with GC; (ii) the reference standard was based on histopathological outcomes as well as combination of histopathological and follow-up outcomes; and (iii) enough information to reevaluate sensitivity.

The exclusion criteria were as follows: (i) articles no relevant to our field of research; (ii) case reports, conference, meeting abstract, and review articles; (iii) non-comparative trials; and (iv) articles not in English.

Two researchers examined each manuscript to determine if they qualify for inclusion. The examination was needed to repeat twice.

Extracting data and evaluating quality

The first author's name, publication date, country, research structure, individual's features, along with technical information were gathered as basic information. We utilized the Quality Assessment of Diagnostic Accuracy Studies 2 (QUADAS-2) tool to assess the studies’ quality (18). All the publications were independently evaluated by two researchers, and any disagreements were settled in a consensus meeting.

Statistical analysis

A random variable model was employed to evaluate the two imaging modalities’ sensitivity. Pooled data and risk variance, along with 95% confidence intervals (CIs), were derived at a lesion-based level. Forest plots were used to visually represent the statistical pooling of data. I² index (I²) statistics were employed to gauge between-study statistical heterogeneity. Funnel plots were utilized to test the publication bias. An additional sub-analysis compared the sensitivity of the two examinations for ovarian cancer and cervical cancer. The Stata program version 15.1 and Review Manager 5.4 were used to conduct statistical evaluations. If a value's two-sided P value was <0.05, it was deemed statistically significant.

Results

Literature search

The flow diagram of eligible studies is displayed in Fig. 1. A total of 147 papers were found using our search approach; of these, 28 were via PubMed, 83 were via Embase, and 36 were via Web of Science. Of these, 136 studies that did not fit the inclusion criteria were eliminated. After a thorough reading of the remain 11 full-text publications, eight trials were eventually included in this meta-analysis (19 –26).

Fig. 1.

Flow chart of eligible literature.

Characteristics of the included research

Tables 1 and 2 lists the patient and study characteristics as well as specific technical details. All eight studies were analyzed based on a lesion level. Among the eight studies, five focused on ovarian cancers, while the remaining three consisted of cervical cancer patients. Of the eight included studies, six had a prospective design and two were retrospective. There were two studies utilizing 68Ga-FAPI PET/MR as the imaging modality and one study performing PET/CT using 68Ga-FAPI-46 as the radiotracer.

Table 1.

Characteristics of included studies.

Author	Year	Country	Study design	No. of patients	Age* (years)	Type of tumor	Reference standard
Chen et al.	2023	China	Prospective	49	57 (51–66)	Ovarian cancer	Histology/follow-up imaging
Liu et al.	2023	China	Prospective	29	56.90 ± 8.38 (39–75)	Ovarian cancer	Histology
Liu et al.	2023	China	Prospective	52	58.19 ± 11.03 (35–78)	Ovarian cancer	Histology/follow-up imaging
Lyu et al.	2023	China	Prospective	25	53 (28–73)	Cervical cancer	Histology/follow-up imaging
Shu et al.	2023	China	Prospective	35	53 ± 11 (30–76)	Cervical cancer	Histology/follow-up imaging
Wegen et al.	2023	Germany	Retrospective	7	34–37	Cervical cancer	Histology
Xi et al.	2023	China	Prospective	30	56.60 ± 13.81	Ovarian cancer	Histology
Zheng et al.	2023	China	Retrospective	27	56 ± 12 (35–84)	Ovarian cancer	Histology/follow-up imaging

*Values are given as mean ± SD (range) or median (IQR).

Table 2.

Technical features.

Authors	Imaging modality	Radiotracer	Injection dose (MBq/kg*)	Interval time (scans)	Imaging analysis
Chen et al., 2023	PET/CT	68Ga-FAPI-04	1.85	<1 week	SUVmax TLR
Chen et al., 2023	PET/CT	18F-FDG	3.7	<1 week	SUVmax TLR
Liu et al., 2023	PET/CT	68Ga-DOTA-FAPI-04	1.85	<1 week	SUVmax TBR
Liu et al., 2023	PET/CT	18F-FDG	3.7	<1 week	SUVmax TBR
Liu et al., 2023	PET/CT	68Ga-DOTA-FAPI-04	39.64 ± 13.45 MBq	281.38 ± 106.04 min	TBR
Liu et al., 2023	PET/CT	18F-FDG	279.67 ± 37.07 MBq	281.38 ± 106.04 min	TBR
Shu et al., 2023	PET/CT	68Ga-FAPI-04	1.85	<1 week	SUVmax
Shu et al., 2023	PET/CT	18F-FDG	3.7	<1 week	SUVmax
Lyu et al., 2023	PET/MR	68Ga-FAPI-04	0.04∼0.06 mCi/kg	<2 weeks	SUVmax
Lyu et al., 2023	PET/CT	18F-FDG	0.10∼0.12 mCi/kg	<2 weeks	SUVmax
Wegen et al., 2023	PET/CT	68Ga-FAPI-46	152 ± 24 MBq	<6 days	TBR
Wegen et al., 2023	PET/CT	18F-FDG	234 ± 37.8 MBq	<6 days	TBR
Xi et al., 2023	PET/MR	68Ga-FAPI-04	111–148 MBq	<5 days	SUVmax
Xi et al., 2023	PET/CT	18F-FDG	4.44–5.55 MBq/kg	<5 days	SUVmax
Zheng et al., 2023	PET/CT	68Ga-FAPI-04	1.85–3.7 MBq/kg	<1 week	SUVmax TBR
Zheng et al., 2023	PET/CT	18F-FDG	3.7 MBq/kg	<1 week	SUVmax TBR

*Unless otherwise indicated.

SUVmax, maximum standardized uptake value; TBR, tumor-to-background ratio; TLR, tumor-to-liver ratio.

Quality assessment

The findings of the methodological quality analysis are collected in Fig. 2, which included the risk of bias (patient selection, index test, reference standard, and flow timing) and applicability (patient selection, index test, and reference standard).

Fig. 2.

Risk of bias based on QUADAS-2 tool.

Sensitivity of 68Ga-FAPI PET and 18F-FDG PET in metastatic lesions

The pooled sensitivity of 68Ga-FAPI PET CT/MR and 18F-FDG PET/CT for lymph node metastases (LNM) of GC were 0.98 (95% confidence interval [CI] = 0.86–1) as well as 0.85 (95% CI = 0.65–0.98), with I² values of 74.2% and 80.7%, respectively (Fig. 3).

Fig. 3.

Forest map of the pooled sensitivity of (a) 68Ga-FAPI PET CT/MR and (b) 18F-FDG PET/CT in lymph node metastases of gynecological malignances.

Five studies focusing on OC provided data on peritoneal carcinomatosis (PC). The forest plot analysis (Fig. 4) revealed that the sensitivity of 68Ga-FAPI PET CT/MR and 18F-FDG PET/CT for diagnosing peritoneal carcinomatosis were 0.98 (95% CI = 0.93–1) as well as 0.71 (95% CI = 0.55–0.86), with I² values of 12.2% and 67.9%, respectively.

Fig. 4.

Forest map of sensitivity in assessment peritoneal carcinomatosis of (a) 68Ga-FAPI PET CT/MR and (b) 18F-FDG PET/CT.

Sensitivity of 68Ga-FAPI CT/MR imaging versus 18F-FDG PET/CT

The risk difference for LNM of GCs using 68Ga-FAPI PET CT/MR versus 18F-FDG PET/CT was in the range of 0–0.50, giving a pooled statistic of 0.11 (95% CI = −0.03–0.25) (Fig. 5). The Z value was 1.52 with a P value of 0.13. Subgroup analysis of LNM by different type of GC revealed the risk difference of 0.15 (95% CI = 0.04–0.25) for ovarian tumor with Z value of 2.78 as well as P value of 0.005, respectively. The risk difference was 0.12 (95% CI = −0.22–0.46) for cervical cancer with Z value of 0.69 as well as a P value of 0.49.

Fig. 5.

Comparison forest map of sensitivity in lymph node metastases of 68Ga-FAPI PET CT/MR and 18F-FDG PET/CT.

The risk difference for peritoneal carcinomatosis of GCs using 68Ga-FAPI PET versus 18F-FDG PET was in the range of 0–0.48, giving a pooled statistic of 0.24 (95% CI = 0.09–0.40) (Fig. 6). The Z value was 3.08 with a P value of 0.002.

Fig. 6.

Comparison forest map of sensitivity in assessment peritoneal carcinomatosis of 68Ga-FAPI PET CT/MR and 18F-FDG PET/CT.

Publication bias

The funnel plots and egger tests regarding 68Ga-FAPI PET CT/MR versus 18F-FDG PET/CT in LNM and peritoneal carcinomatosis were shown in Fig. 7. The P values of the egger test were 0.61 and 0.54, correspondingly, indicating no publication bias. In addition, funnel plots did not display obvious asymmetry.

Fig. 7.

(a, b) Egger tests and (c, d) funnel plots of lymph node metastases and peritoneal involvement.

Discussion

Accurate diagnosis, staging and restaging in GC, are crucial for patient clinical management. In addition, it may improve survival rates. For patients with cervical cancer, lymphatic spreads are closely related to prognosis. In other words, nodal staging plays a decisive role in management selection. Once pelvic lymphatic metastasis was demonstrated by 18F-FDG PET/CT or CT/MR, patients would be recommended to receive concurrent chemoradiotherapy (CCRT), which has a deep influence on fertility (27). Apart from LNM, peritoneal involvement is another major metastatic and recurrent mechanism in OC. Thus, detecting metastatic lymph nodes and peritoneal lesions was essential for staging and restaging. 18F-FDG PET/CT has been recommended as a radiological biomarker and routine examination for pre- and postoperative assessment (28). However, there were several diagnostic pitfalls of 18F-FDG PET/CT hampering its application, such as physiological 18F-FDG uptake in intestines, difficult identification in inflammation and malignancies as well as false-negative 18F-FDG uptake in tiny, mucinous, and necrotic lesions (29). Recently, 68Ga-FAPI PET CT/MR has been gradually utilized to evaluate various tumors and non-tumor lesions owing to its advantages of increased tracer uptake in metastatic lesions and decreased background activity (16,30 –34).

To our knowledge, this is the first meta-analysis comparing the diagnostic efficacy of 68Ga-FAPI PET CT/MR and 18F-FDG PET/CT for metastatic lesions of GCs. It included information for 254 participants across eight independent comparative studies who underwent both tests. The meta-analysis revealed 68Ga-FAPI PET CT/MR is usually superior to 18F-FDG PET/CT in terms of diagnostic efficacy for LNM and peritoneal carcinomatosis of OC, with higher pooled sensitivity (0.88 vs. 0.69 and 0.97 vs. 0.74). However, the detection rate of 68Ga-FAPI PET CT/MR and 18F-FDG PET/CT were comparable in LNM of cervical cancer.

In terms of the diagnostic efficiency of an LNM diagnosis of OC, 68Ga-FAPI-04 PET outperformed 18F-FDG PET/CT, with an extremely short axis size of less than 1 cm (19). The superior detection rate of 68Ga-FAPI PET might be attributed to the higher tracer uptake in OCs as well as lower tumor-to-background ratio (TBR) (35,36). However, tiny LNs, with an axis size smaller than 0.4 cm, were missed easily in both modalities. This might be because of the limited FAP expression in tiny LNs and confusable distinguishment from peritoneal involvement (37). Of note, lymphatic inflammation might also lead to false-positive LNs on 68Ga-FAPI-04 PET. Regarding LNM of cervical cancer, the sensitivity of the two examinations was not satisfactory. However, only three studies reported related data. The results should be interpreted with caution, and further research is needed to investigate the diagnostic efficiency of 68Ga-FAPI-04 PET and 18F-FDG PET/CT.

Peritoneal implant is a main metastatic mode of OC and considered to be a terminal stage of the disease (38,39). Kim et al. revealed that 18F-FDG PET/CT exhibited an excellent diagnostic efficiency in detection of PC in different cancers with a pooled sensitivity of 0.87 and specificity of 0.92 (40). Tsili et al. reported that compared to MRI and MDCT, FDG PET/CT has a higher combined sensitivity (93.7% vs. 82.7% vs. 79.7%), and the diagnostic accuracy of FDG PET/CT and MRI were comparable in detection of PCs in OC (41). Those findings seemed to indicate a high detection rate of PC for 18F-FDG PET/CT. Nevertheless, a recent meta-analysis showed a contrasting view. The diagnosis of FDG PET/CT in PC was poor with sensitivity of 59.9%, while 68Ga-FAPI PET/CT exhibited excellent sensitivity (98.2%) (42). This finding was in accordance with our research (sensitivity of 0.98 vs. 0.71). 68Ga-FAPI PET CT/MR showed an obviously higher tracer uptake ratio than FDG PET/CT in detecting PCs. Xi et al. (25) speculated this may depend on high density NAFs in the mesentery and omentum, which can cause increased FAP expression indirectly when presenting metastasis. Moreover, 68Ga-FAPI PET CT/MR always has advantages of higher volumetric parameters, and lower background activity (43). In addition, surgery-induced fibrous tissue hyperplasia should not be overlooked, which was the major reason for false-positive findings. The drawback of both modalities was the influence of abdomen movement and small lesions.

The present study has some limitations. First, there are insufficient data to evaluate the specificity for ovarian and cervical cancer, respectively, since limited articles reported the true-negative findings. Moreover, the diagnostic value of 68Ga-FAPI PET CT/MR and FDG PET/CT for LNMs of cervical cancer needs more exploration. Second, not all the studies focused on newly diagnosed cancer; two focused on tumor recurrence and metastasis (20,21). Finally, imaging examinations and radiotracers are not unified. One study performed PET/CT using 68Ga-FAPI-46 and two trials utilized PET/MR instead of PET/CT to detect primary and metastatic lesions.

In conclusion, when evaluating metastatic GC, 68Ga-FAPI PET MR/CT displayed superior sensitivity to 18F-FDG PET/CT in detecting LNM and PC of ovarian cancer. There was no significant difference between the two tests in evaluating the LNM of cervical cancer. Nevertheless, as the findings are based on limited sample sizes, further investigation is needed to confirm the conclusion and explore the diagnostic ability of 68Ga-FAPI PET MRI/CT for different types and stages of GC.

Footnotes

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

ORCID iDs

Lixin Sun

Ruchen Peng

References

Sung

Ferlay

Siegel

, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2021;71:209–249.

Fennell

Scholber

Grosu

, et al. MRI and FDG-PET/CT imaging in gynecological malignancies: the radiation oncology perspective. Q J Nucl Med Mol Imaging 2016;60:117–123.

Cheng

. Advances in diagnosis and treatment of metastatic cervical cancer. J Gynecol Oncol 2016;27:e43.

Luczynska

Zbigniew

. Diagnostic imaging in gynecology. Ginekol Pol 2022;93:63–69.

Nogami

Iida

Banno

, et al. Application of FDG-PET in cervical cancer and endometrial cancer: utility and future prospects. Anticancer Res 2014;34:585–592.

Engbersen

Van Driel

Lambregts

, et al. The role of CT, PET-CT, and MRI in ovarian cancer. Br J Radiol 2021;94:20210117.

Liu

. Benign ovarian and endometrial uptake on FDG PET-CT: patterns and pitfalls. Ann Nucl Med 2009;23:107–112.

Shida

Murakami

Tsukada

, et al. F-18 fluorodeoxyglucose uptake in leiomyomatous uterus. Int J Gynecol Cancer 2007;17:285–290.

Loktev

Lindner

Mier

, et al. A tumor-imaging method targeting cancer-associated fibroblasts. J Nucl Med 2018;59:1423–1429.

10.

Lindner

Loktev

Altmann

, et al. Development of quinoline-based theranostic ligands for the targeting of fibroblast activation protein. J Nucl Med 2018;59:1415–1422.

11.

Mori

Dendl

Cardinale

, et al. FAPI PET: fibroblast activation protein inhibitor use in oncologic and nononcologic disease. Radiology 2023;306:e220749.

12.

Çermik

Ergü

Yilmaz

, et al. Tumor imaging with 68Ga-DOTA-FAPI-04 PET/CT: comparison with 18F-FDG PET/CT in 22 different cancer types. Clin Nucl Med 2022;47:E333–E339.

13.

Wang

Luo

. [(68)Ga]Ga-FAPI-04 PET MRI/CT in the evaluation of gastric carcinomas compared with [(18)F]-FDG PET MRI/CT: a meta-analysis. Eur J Med Res 2023;28:34.

14.

Ouyang

Ding

Zhang

, et al. Head-to-head comparison of (68)Ga-FAPI-04 PET/CT and (18)F-FDG PET/CT in the evaluation of primary digestive system cancer: a systematic review and meta-analysis. Front Oncol 2023;13:1202505.

15.

Kömek

Can

Güzel

, et al. (68)Ga-FAPI-04 PET/CT, a new step in breast cancer imaging: a comparative pilot study with the (18)F-FDG PET/CT. Ann Nucl Med 2021;35:744–752.

16.

Dendl

Koerber

Finck

, et al. (68)Ga-FAPI-PET/CT in patients with various gynecological malignancies. Eur J Nucl Med Mol Imaging 2021;48:4089–4100.

17.

Liberati

Altman

Tetzlaff

, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. PLoS Med 2009;6:e1000100.

18.

Whiting

Rutjes

Westwood

, et al. QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med 2011;155:529–536.

19.

Chen

, et al. [68ga]Ga-FAPI-04 PET/CT in the evaluation of epithelial ovarian cancer: comparison with [18F]F-FDG PET/CT. Eur J Nucl Med Mol Imaging 2023;50:4064–4076.

20.

Liu

Feng

, et al. Head-to-head comparison of [18F]-FDG and [68 Ga]-DOTA-FAPI-04 PET/CT for radiological evaluation of platinum-sensitive recurrent ovarian cancer. Eur J Nucl Med Mol Imaging 2023;50:1521–1531.

21.

Liu

Chen

Jing

, et al. Feasibility of one-day PET/CT scanning protocol with 68Ga-DOTA-FAPI-04 and 18F-FDG for the detection of ovarian cancer recurrence and metastasis. Cancer Biother Radiopharm 2024;39:55–63.

22.

Lyu

Chen

Liu

, et al. Comparison of the diagnostic value of [68 Ga]Ga-FAPI-04 PET/MR and [18F]FDG PET/CT in patients with T stage ≤ 2a2 uterine cervical cancer: a prospective study. Eur J Nucl Med Mol Imaging 2024;51:1163–1172.

23.

Shu

Chen

, et al. Head-to-head comparison of 18F-FDG and 68Ga-FAPI-04 PET/CT for radiological evaluation of cervical cancer. Clin Nucl Med 2023;48:928–932.

24.

Wegen

Roth

Weindler

, et al. First clinical experience with [68Ga]Ga-FAPI-46-PET/CT versus [18F]F-FDG PET/CT for nodal staging in cervical cancer. Clin Nucl Med 2023;48:150–155.

25.

Sun

Che

, et al. A comparative study of [68Ga]Ga-FAPI-04 PET/MR and [18F]FDG PET/CT in the diagnostic accuracy and resectability prediction of ovarian cancer. Eur J Nucl Med Mol Imaging 2023;50:2885–2898.

26.

Zheng

Liu

Feng

, et al. Comparison of 68Ga-FAPI-04 and fluorine-18-fluorodeoxyglucose PET/computed tomography in the detection of ovarian malignancies. Nucl Med Commun 2023;44:194–203.

27.

Abu-Rustum

Yashar

Arend

, et al. NCCN Guidelines(R) insights: cervical cancer, version 1.2024. J Natl Compr Canc Netw 2023;21:1224–1233.

28.

Armstrong

Alvarez

Bakkum-Gamez

, et al. Ovarian cancer, version 2.2020, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw 2021;19:191–226.

29.

Zhang

, et al. The added value of (68)Ga-FAPI PET/CT in patients with head and neck cancer of unknown primary with (18)F-FDG-negative findings. J Nucl Med 2022;63:875–881.

30.

Kratochwil

Flechsig

Lindner

, et al. (68)Ga-FAPI PET/CT: tracer uptake in 28 different kinds of cancer. J Nucl Med 2019;60:801–805.

31.

Chen

Pang

, et al. Comparison of [(68)Ga]Ga-DOTA-FAPI-04 and [(18)F] FDG PET/CT for the diagnosis of primary and metastatic lesions in patients with various types of cancer. Eur J Nucl Med Mol Imaging 2020;47:1820–1832.

32.

Rosenkrans

Massey

Bernau

, et al. [(68) Ga]Ga-FAPI-46 PET for non-invasive detection of pulmonary fibrosis disease activity. Eur J Nucl Med Mol Imaging 2022;49:3705–3716.

33.

Luo

Pan

Zhou

, et al. (68)Ga-FAPI PET/CT for rheumatoid arthritis: a prospective study. Radiology 2023;307:e222052.

34.

Meyer

Dahlbom

Lindner

, et al. Radiation dosimetry and biodistribution of (68)Ga-FAPI-46 PET imaging in cancer patients. J Nucl Med 2020;61:1171–1177.

35.

Wang

Yang

Tang

, et al. (68)Ga-DOTA-FAPI-04 PET/CT as a promising tool for differentiating ovarian physiological uptake: preliminary experience of comparative analysis with (18)F-FDG. Front Med (Lausanne) 2021;8:748683.

36.

Pang

Zhao

Luo

, et al. Comparison of (68)Ga-FAPI and (18)F-FDG uptake in gastric, duodenal, and colorectal cancers. Radiology 2021;298:393–402.

37.

Hassler

. Hemodynamic aspects of cerebral angiomas. Acta Neurochir Suppl (Wien) 1986;37:1–136.

38.

Coakley

Choi

Gougoutas

, et al. Peritoneal metastases: detection with spiral CT in patients with ovarian cancer. Radiology 2002;223:495–499.

39.

Nougaret

Addley

Colombo

, et al. Ovarian carcinomatosis: how the radiologist can help plan the surgical approach. Radiographics 2012;32:1775–1800; discussion 1800–1803.

40.

Kim

Lee

. Diagnostic accuracy of (18)F-FDG PET/CT for detection of peritoneal carcinomatosis; a systematic review and meta-analysis. Br J Radiol 2018;91:20170519.

41.

Tsili

Alexiou

Tzoumpa

, et al. Imaging of peritoneal metastases in ovarian cancer using MDCT, MRI, and FDG PET/CT: a systematic review and meta-analysis. Cancers (Basel) 2024;16:1467.

42.

Gege

Xueju

Bin

. Head-to-head comparison of (68)Ga-FAPI PET/CT and FDG PET/CT for the detection of peritoneal metastases: systematic review and meta-analysis. AJR Am J Roentgenol 2023;220:490–498.

43.

Tian

Chen

, et al. Usefulness of [(68)Ga]FAPI-04 and [(18)F]FDG PET/CT for the detection of primary tumour and metastatic lesions in gastrointestinal carcinoma: a comparative study. Eur Radiol 2023;33:2779–2791.