Radiotracer Innovations in Breast Cancer Imaging: A Review of Recent Progress
Abstract
:1. Introduction
2. Sources and Selection Criteria
3. Types of Breast Cancer
3.1. Ductal Carcinoma In Situ
3.2. Invasive Ductal Carcinoma
3.3. Invasive Lobular Carcinoma
3.4. Triple-Negative Breast Cancer
3.5. HER2-Positive Breast Cancer
3.6. Hormone Receptor-Positive Breast Cancer (Luminal Subtypes)
4. Current Radiotracers in Breast Cancer Imaging
4.1. 18F-Fluorodeoxyglucose (18F-FDG)
4.1.1. 18F-FDG PET/CT
Ductal Carcinoma In Situ
Invasive Ductal Carcinoma
Invasive Lobular Carcinoma
Triple-Negative Breast Cancer
4.1.2. 18F-FDG Positron Emission Mammography (PEM)
4.1.3. 18F-FDG PET/MRI
4.2. Fibroblast Activation Protein Inhibitor (FAPI)
4.3. 16α-[18F]fluoroestradiol (FES)
4.4. 4-Fluoro-11β-Methoxy-16α-18F-Fluoroestradiol (18F-4FMFES)
4.5. 21-18F-Fluoro-16α,17α-[(R)-(1′-α-Furylmethylidene)dioxy]-19-Norpregn-4-ene-3,20-Dione (FFNP)
4.6. 89Zr-Trastuzumab
4.7. 64Cu-DOTA-Trastuzumab
4.8. 89Zr-Pertuzumab
5. Investigational Radiotracers in Breast Cancer Imaging
5.1. [18F]PSMA-1007
5.2. 68Ga-ABY-025
5.3. 68Ga-NOTA-Fab-Trastuzumab
5.4. 89Zr∙Df-HER2-Fab-PAS200
5.5. 68Ga-HER2-Nanobody
5.6. 68Ga-NOTA-MAL-Cys-MZHER2:342
5.7. 18F-Labeled 1-Amino-3-Fluorocyclobutane-1-Carboxylic Acid (18F-Fluciclovine)
5.8. 3′-Deoxy-3′-[18F]-Fluorothymidine (18F-FLT) and 18F-DPA-714
5.9. Others
6. Future Directions
7. Conclusions
Author Contributions
Funding
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Wilkinson, L.; Gathani, T. Understanding breast cancer as a global health concern. Br. J. Radiol. 2022, 95, 20211033. [Google Scholar] [CrossRef]
- Katsura, C.; Ogunmwonyi, I.; Kankam, H.K.; Saha, S. Breast cancer: Presentation, investigation and management. Br. J. Hosp. Med. 2022, 83, 1–7. [Google Scholar] [CrossRef]
- Tollens, F.; Baltzer, P.A.T.; Dietzel, M.; Schnitzer, M.L.; Schwarze, V.; Kunz, W.G.; Rink, J.; Rübenthaler, J.; Froelich, M.F.; Schönberg, S.O.; et al. Economic potential of abbreviated breast MRI for screening women with dense breast tissue for breast cancer. Eur. Radiol. 2022, 32, 7409–7419. [Google Scholar] [CrossRef] [PubMed]
- Lebron, L.; Greenspan, D.; Pandit-Taskar, N. PET imaging of breast cancer: Role in patient management. PET Clin. 2015, 10, 159–195. [Google Scholar] [CrossRef] [PubMed]
- Fowler, A.M.; Cho, S.Y. PET imaging for breast cancer. Radiol. Clin. N. Am. 2021, 59, 725–735. [Google Scholar] [CrossRef]
- Wang, J.; Li, B.; Luo, M.; Huang, J.; Zhang, K.; Zheng, S.; Zhang, S.; Zhou, J. Progression from ductal carcinoma in situ to invasive breast cancer: Molecular features and clinical significance. Signal Transduct. Target. Ther. 2024, 9, 83. [Google Scholar] [CrossRef] [PubMed]
- van Seijen, M.; Lips, E.H.; Thompson, A.M.; Nik-Zainal, S.; Futreal, A.; Hwang, E.S.; Verschuur, E.; Lane, J.; Jonkers, J.; Rea, D.W.; et al. Ductal carcinoma in situ: To treat or not to treat, that is the question. Br. J. Cancer 2019, 121, 285–292. [Google Scholar] [CrossRef]
- Siegel, R.L.; Giaquinto, A.N.; Jemal, A. Cancer statistics, 2024. CA Cancer J. Clin. 2024, 74, 12–49. [Google Scholar] [CrossRef]
- Narod, S.A.; Iqbal, J.; Giannakeas, V.; Sopik, V.; Sun, P. Breast cancer mortality after a diagnosis of ductal carcinoma in situ. JAMA Oncol. 2015, 1, 888–896. [Google Scholar] [CrossRef]
- Wu, S.G.; Zhang, W.-W.; Sun, J.-Y.; He, Z.-Y. Prognostic value of ductal carcinoma in situ component in invasive ductal carcinoma of the breast: A Surveillance, Epidemiology, and End Results database analysis. Cancer Manag. Res. 2018, 10, 527–534. [Google Scholar] [CrossRef]
- Chamalidou, C.; Fohlin, H.; Albertsson, P.; Arnesson, L.-G.; Einbeigi, Z.; Holmberg, E.; Nordenskjöld, A.; Nordenskjöld, B.; Karlsson, P.; Linderholm, B. Survival patterns of invasive lobular and invasive ductal breast cancer in a large population-based cohort with two decades of follow up. Breast 2021, 59, 294–300. [Google Scholar] [CrossRef]
- Kole, A.J.; Park, H.S.; Johnson, S.B.; Kelly, J.R.; Moran, M.S.; Patel, A.A. Overall survival is improved when DCIS accompanies invasive breast cancer. Sci. Rep. 2019, 9, 9934. [Google Scholar] [CrossRef]
- Grabenstetter, A.; Mohanty, A.S.; Rana, S.; Zehir, A.; Brannon, A.R.; D’Alfonso, T.M.; DeLair, D.F.; Tan, L.K.; Ross, D.S. E-cadherin immunohistochemical expression in invasive lobular carcinoma of the breast: Correlation with morphology and CDH1 somatic alterations. Hum. Pathol. 2020, 102, 44–53. [Google Scholar] [CrossRef]
- Yang, C.; Lei, C.; Zhang, Y.; Zhang, J.; Ji, F.; Pan, W.; Zhang, L.; Gao, H.; Yang, M.; Li, J.; et al. Comparison of overall survival between invasive lobular breast carcinoma and invasive ductal breast carcinoma: A propensity score matching study based on SEER database. Front. Oncol. 2020, 10, 590643. [Google Scholar] [CrossRef] [PubMed]
- Derakhshan, F.; Reis-Filho, J.S. Pathogenesis of triple-negative breast cancer. Annu. Rev. Pathol. Mech. Dis. 2022, 17, 181–204. [Google Scholar] [CrossRef] [PubMed]
- Borri, F.; Granaglia, A. Pathology of triple negative breast cancer. Semin. Cancer Biol. 2021, 72, 136–145. [Google Scholar] [CrossRef]
- Liedtke, C.; Mazouni, C.; Hess, K.R.; André, F.; Tordai, A.; Mejia, J.A.; Symmans, W.F.; Gonzalez-Angulo, A.M.; Hennessy, B.; Green, M.; et al. Response to neoadjuvant therapy and long-term survival in patients with triple-negative breast cancer. J. Clin. Oncol. 2008, 26, 1275–1281. [Google Scholar] [CrossRef] [PubMed]
- Slamon, D.J.; Godolphin, W.; Jones, L.A.; Holt, J.A.; Wong, S.G.; Keith, D.E.; Levin, W.J.; Stuart, S.G.; Udove, J.; Ullrich, A.; et al. Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer. Science 1989, 244, 707–712. [Google Scholar] [CrossRef] [PubMed]
- Slamon, D.J.; Clark, G.M.; Wong, S.G.; Levin, W.J.; Ullrich, A.; McGuire, W.L. Human breast cancer: Correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 1987, 235, 177–182. [Google Scholar] [CrossRef]
- Konecny, G.; Pauletti, G.; Pegram, M.; Untch, M.; Dandekar, S.; Aguilar, Z.; Wilson, C.; Rong, H.-M.; Bauerfeind, I.; Felber, M.; et al. Quantitative association between HER-2/neu and steroid hormone receptors in hormone receptor-positive primary breast cancer. J. Natl. Cancer Inst. 2003, 95, 142–153. [Google Scholar] [CrossRef]
- Cancer Stat Facts: Female Breast Cancer Subtypes. Available online: https://seer.cancer.gov/statfacts/html/breast-subtypes.html (accessed on 15 July 2024).
- Gupta, R.; Gupta, S.; Antonios, B.; Ghimire, B.; Jindal, V.; Deol, J.; Gaikazian, S.; Huben, M.; Anderson, J.; Stender, M.; et al. Therapeutic landscape of advanced HER2-positive breast cancer in 2022. Med. Oncol. 2022, 39, 258. [Google Scholar] [CrossRef] [PubMed]
- Mayrovitz, H.N. (Ed.) Breast Cancer; Exon Publications: Brisbane, Australia, 2022. [Google Scholar]
- Sørlie, T.; Perou, C.M.; Tibshirani, R.; Aas, T.; Geisler, S.; Johnsen, H.; Hastie, T.; Eisen, M.B.; van de Rijn, M.; Jeffrey, S.S.; et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc. Natl. Acad. Sci. USA 2001, 98, 10869–10874. [Google Scholar] [CrossRef] [PubMed]
- Hadebe, B.; Harry, L.; Ebrahim, T.; Pillay, V.; Vorster, M. The role of PET/CT in breast cancer. Diagnostics 2023, 13, 597. [Google Scholar] [CrossRef] [PubMed]
- Paydary, K.; Seraj, S.M.; Zadeh, M.Z.; Emamzadehfard, S.; Shamchi, S.P.; Gholami, S.; Werner, T.J.; Alavi, A. The evolving role of FDG-PET/CT in the diagnosis, staging, and treatment of breast cancer. Mol. Imaging Biol. 2019, 21, 1–10. [Google Scholar] [CrossRef] [PubMed]
- Gradishar, W.J.; Moran, M.S.; Abraham, J.; Aft, R.; Agnese, D.; Allison, K.H.; Anderson, B.; Burstein, H.J.; Chew, H.; Dang, C.; et al. Breast Cancer, Version 3.2022, NCCN Clinical Practice Guidelines in Oncology. J. Natl. Compr. Cancer Netw. 2022, 20, 691–722. [Google Scholar] [CrossRef]
- Jung, N.Y.; Kang, B.J.; Kim, S.H.; Yoo, I.R.; Lim, Y.S.; Yoo, W. Role of FDG-PET/CT in identification of histological upgrade of ductal carcinoma in situ (DCIS) in needle biopsy. Iran. J. Radiol. 2021, 18, e113862. [Google Scholar] [CrossRef]
- Ulaner, G.A. PET/CT for patients with breast cancer: Where is the clinical impact? AJR Am. J. Roentgenol. 2019, 213, 254–265. [Google Scholar] [CrossRef]
- Dashevsky, B.Z.; Goldman, D.A.; Parsons, M.; Gönen, M.; Corben, A.D.; Jochelson, M.S.; Hudis, C.A.; Morrow, M.; Ulaner, G.A. Appearance of untreated bone metastases from breast cancer on FDG PET/CT: Importance of histologic subtype. Eur. J. Nucl. Med. Mol. Imaging 2015, 42, 1666–1673. [Google Scholar] [CrossRef]
- Groheux, D.; Hindié, E.; Giacchetti, S.; Hamy, A.-S.; Berger, F.; Merlet, P.; de Roquancourt, A.; de Cremoux, P.; Marty, M.; Hatt, M.; et al. Early assessment with 18F-fluorodeoxyglucose positron emission tomography/computed tomography can help predict the outcome of neoadjuvant chemotherapy in triple negative breast cancer. Eur. J. Cancer 2014, 50, 1864–1871. [Google Scholar] [CrossRef]
- Park, H.L.; Lee, S.-W.; Hong, J.H.; Lee, J.; Lee, A.; Kwon, S.J.; Park, S.Y.; Yoo, I.R. Prognostic impact of 18F-FDG PET/CT in pathologic stage II invasive ductal carcinoma of the breast: Re-illuminating the value of PET/CT in intermediate-risk breast cancer. Cancer Imaging 2023, 23, 2. [Google Scholar] [CrossRef]
- Kitajima, K.; Miyoshi, Y. Present and future role of FDG-PET/CT imaging in the management of breast cancer. Jpn. J. Radiol. 2016, 34, 167–180. [Google Scholar] [CrossRef]
- Vag, T.; Steiger, K.; Rossmann, A.; Keller, U.; Noske, A.; Herhaus, P.; Ettl, J.; Niemeyer, M.; Wester, H.-J.; Schwaiger, M. PET imaging of chemokine receptor CXCR4 in patients with primary and recurrent breast carcinoma. EJNMMI Res. 2018, 8, 90. [Google Scholar] [CrossRef] [PubMed]
- Song, B.I.; Hong, C.M.; Lee, H.J.; Kang, S.; Jeong, S.Y.; Kim, H.W.; Chae, Y.S.; Park, J.Y.; Lee, S.-W.; Ahn, B.-C.; et al. Prognostic value of primary tumor uptake on F-18 FDG PET/CT in patients with invasive ductal breast cancer. Nucl. Med. Mol. Imaging 2011, 45, 117–124. [Google Scholar] [CrossRef] [PubMed]
- Hildebrandt, M.G.; Gerke, O.; Baun, C.; Falch, K.; Hansen, J.A.; Farahani, Z.A.; Petersen, H.; Larsen, L.B.; Duvnjak, S.; Buskevica, I.; et al. [18F]fluorodeoxyglucose (FDG)-positron emission tomography (PET)/computed tomography (CT) in suspected recurrent breast cancer: A prospective comparative study of dual-time-point FDG-PET/CT, contrast-enhanced CT, and bone scintigraphy. J. Clin. Oncol. 2016, 34, 1889–1897. [Google Scholar] [CrossRef]
- Loh, C.Y.; Chai, J.Y.; Tang, T.F.; Wong, W.F.; Sethi, G.; Shanmugam, M.K.; Chong, P.P.; Looi, C.Y. The E-cadherin and N-cadherin switch in epithelial-to-mesenchymal transition: Signaling, therapeutic implications, and challenges. Cells 2019, 8, 1118. [Google Scholar] [CrossRef] [PubMed]
- Sahin, E.; Kus, T.; Aytekin, A.; Uzun, E.; Elboga, U.; Yilmaz, L.; Cayirli, Y.B.; Okuyan, M.; Cimen, V.; Cimen, U. 68Ga-FAPI PET/CT as an alternative to 18F-FDG PET/CT in the imaging of invasive lobular breast carcinoma. J. Nucl. Med. 2024, 65, 512–519. [Google Scholar] [CrossRef]
- Gilardi, L.; Farulla, L.S.A.; Curigliano, G.; Corso, G.; Leonardi, M.C.; Ceci, F. FDG and Non-FDG radiopharmaceuticals for PET imaging in invasive lobular breast carcinoma. Biomedicines 2023, 11, 1350. [Google Scholar] [CrossRef]
- Bonnin, D.; Ladoire, S.; Briot, N.; Bertaut, A.; Drouet, C.; Cochet, A.; Alberini, J.-L. Performance of [18F]FDG-PET/CT imaging in first recurrence of invasive lobular carcinoma. J. Clin. Med. 2023, 12, 2916. [Google Scholar] [CrossRef] [PubMed]
- Park, H.L.; Yoo, I.R.; O, J.H.; Kim, H.; Kim, S.H.; Kang, B.J. Clinical utility of 18F-FDG PET/CT in low 18F-FDG-avidity breast cancer subtypes: Comparison with breast US and MRI. Nucl. Med. Commun. 2018, 39, 35–43. [Google Scholar] [CrossRef]
- Ulaner, G.A.; Castillo, R.; Goldman, D.A.; Wills, J.; Riedl, C.C.; Pinker-Domenig, K.; Jochelson, M.S.; Gönen, M. (18)F-FDG-PET/CT for systemic staging of newly diagnosed triple-negative breast cancer. Eur. J. Nucl. Med. Mol. Imaging 2016, 43, 1937–1944. [Google Scholar] [CrossRef]
- Lee, H.J.; Lim, H.S.; Ki, S.Y.; Park, H.M.; Lee, J.E.; Jeong, W.G.; Shin, S.S.; Kwon, S.Y.; Park, M.H.; Lee, J.S. 18F-fluorodeoxyglucose uptake on PET/computed tomography in association with androgen receptor expression and other clinicopathologic factors in surgically resected triple-negative breast cancer. Nucl. Med. Commun. 2021, 42, 101–106. [Google Scholar] [CrossRef] [PubMed]
- Patel, M.M.; Adrada, B.E.; Fowler, A.M.; Rauch, G.M. Molecular breast imaging and positron emission mammography. PET Clin. 2023, 18, 487–501. [Google Scholar] [CrossRef]
- Keshavarz, K.; Jafari, M.; Lotfi, F.; Bastani, P.; Salesi, M.; Gheisari, F.; Hemami, M.R. Positron Emission Mammography (PEM) in the diagnosis of breast cancer: A systematic review and economic evaluation. Med. J. Islam. Repub. Iran 2020, 34, 100. [Google Scholar] [CrossRef] [PubMed]
- Berg, W.A.; Weinberg, I.N.; Narayanan, D.; Lobrano, M.E.; Ross, E.; Amodei, L.; Tafra, L.; Adler, L.P.; Uddo, J.; Stein, W.; et al. High-resolution fluorodeoxyglucose positron emission tomography with compression (“positron emission mammography”) is highly accurate in depicting primary breast cancer. Breast J. 2006, 12, 309–323. [Google Scholar] [CrossRef] [PubMed]
- Yamamoto, Y.; Tasaki, Y.; Kuwada, Y.; Ozawa, Y.; Inoue, T. A preliminary report of breast cancer screening by positron emission mammography. Ann. Nucl. Med. 2016, 30, 130–137. [Google Scholar] [CrossRef]
- Freitas, V.; Li, X.; Scaranelo, A.; Au, F.; Kulkarni, S.; Ghai, S.; Taeb, S.; Bubon, O.; Baldassi, B.; Komarov, B.; et al. Breast cancer detection using a low-dose positron emission digital mammography system. Radiol. Imaging Cancer 2024, 6, e230020. [Google Scholar] [CrossRef]
- Schilling, K.; Narayanan, D.; Kalinyak, J.E.; The, J.; Velasquez, M.V.; Kahn, S.; Saady, M.; Mahal, R.; Chrystal, L. Positron emission mammography in breast cancer presurgical planning: Comparisons with magnetic resonance imaging. Eur. J. Nucl. Med. Mol. Imaging 2011, 38, 23–36. [Google Scholar] [CrossRef]
- Berg, W.A.; Madsen, K.S.; Schilling, K.; Tartar, M.; Pisano, E.D.; Larsen, L.H.; Narayanan, D.; Ozonoff, A.; Miller, J.P.; Kalinyak, J.E. Breast cancer: Comparative effectiveness of positron emission mammography and MR imaging in presurgical planning for the ipsilateral breast. Radiology 2011, 258, 59–72. [Google Scholar] [CrossRef]
- Koyasu, H.; Goshima, S.; Noda, Y.; Nishibori, H.; Takeuchi, M.; Matsunaga, K.; Yamada, T.; Matsuo, M. The feasibility of dedicated breast PET for the assessment of residual tumor after neoadjuvant chemotherapy. Jpn. J. Radiol. 2019, 37, 81–87. [Google Scholar] [CrossRef]
- Sasada, S.; Masumoto, N.; Goda, N.; Kajitani, K.; Emi, A.; Kadoya, T.; Okada, M. Dedicated breast PET for detecting residual disease after neoadjuvant chemotherapy in operable breast cancer: A prospective cohort study. Eur. J. Surg. Oncol. 2018, 44, 444–448. [Google Scholar] [CrossRef]
- Argus, A.; Mahoney, M.C. Positron emission mammography: Diagnostic imaging and biopsy on the same day. AJR Am. J. Roentgenol. 2014, 202, 216–222. [Google Scholar] [CrossRef]
- Hendrick, R.E. Radiation doses and cancer risks from breast imaging studies. Radiology 2010, 257, 246–253. [Google Scholar] [CrossRef]
- Moy, L.; Noz, M.E.; Maguire, G.Q., Jr.; Melsaether, A.; Deans, A.E.; Murphy-Walcott, A.D.; Ponzo, F. Role of fusion of prone FDG-PET and magnetic resonance imaging of the breasts in the evaluation of breast cancer. Breast J. 2010, 16, 369–376. [Google Scholar] [CrossRef] [PubMed]
- Botsikas, D.; Bagetakos, I.; Picarra, M.; Barisits, A.C.D.C.A.; Boudabbous, S.; Montet, X.; Lam, G.T.; Mainta, I.; Kalovidouri, A.; Becker, M. What is the diagnostic performance of 18-FDG-PET/MR compared to PET/CT for the N- and M- staging of breast cancer? Eur. Radiol. 2019, 29, 1787–1798. [Google Scholar] [CrossRef]
- Zhang, C.; Liang, Z.; Liu, W.; Zeng, X.; Mo, Y. Comparison of whole-body 18F-FDG PET/CT and PET/MRI for distant metastases in patients with malignant tumors: A meta-analysis. BMC Cancer 2023, 23, 37. [Google Scholar] [CrossRef] [PubMed]
- Fowler, A.M.; Strigel, R.M. Clinical advances in PET-MRI for breast cancer. Lancet Oncol. 2022, 23, e32–e43. [Google Scholar] [CrossRef] [PubMed]
- Lindner, T.; Loktev, A.; Altmann, A.; Giesel, F.; Kratochwil, C.; Debus, J.; Jäger, D.; Mier, W.; Haberkorn, U. Development of quinoline-based theranostic ligands for the targeting of fibroblast activation protein. J. Nucl. Med. 2018, 59, 1415–1422. [Google Scholar] [CrossRef]
- Pang, Y.; Zhao, L.; Chen, H. 68Ga-FAPI outperforms 18F-FDG PET/CT in identifying bone metastasis and peritoneal carcinomatosis in a patient with metastatic breast cancer. Clin. Nucl. Med. 2020, 45, 913–915. [Google Scholar] [CrossRef]
- Li, T.; Jiang, X.; Zhang, Z.; Chen, X.; Wang, J.; Zhao, X.; Zhang, J. Case Report: (68)Ga-FAPI PET/CT, a more advantageous detection mean of gastric, peritoneal, and ovarian metastases from breast cancer. Front. Oncol. 2022, 12, 1013066. [Google Scholar] [CrossRef]
- Elboga, U.; Sahin, E.; Kus, T.; Cayirli, Y.B.; Aktas, G.; Uzun, E.; Cinkir, H.Y.; Teker, F.; Sever, O.N.; Aytekin, A.; et al. Superiority of 68Ga-FAPI PET/CT scan in detecting additional lesions compared to 18FDG PET/CT scan in breast cancer. Ann. Nucl. Med. 2021, 35, 1321–1331. [Google Scholar] [CrossRef]
- Chen, H.; Pang, Y.; Wu, J.; Zhao, L.; Hao, B.; Wu, J.; Wei, J.; Wu, S.; Zhao, L.; Luo, Z.; 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. [Google Scholar] [CrossRef]
- Giesel, F.L.; Kratochwil, C.; Schlittenhardt, J.; Dendl, K.; Eiber, M.; Staudinger, F.; Kessler, L.; Fendler, W.P.; Lindner, T.; Koerber, S.A.; et al. Head-to-head intra-individual comparison of biodistribution and tumor uptake of (68)Ga-FAPI and (18)F-FDG PET/CT in cancer patients. Eur. J. Nucl. Med. Mol. Imaging 2021, 48, 4377–4385. [Google Scholar] [CrossRef] [PubMed]
- Eshet, Y.; Tau, N.; Apter, S.; Nissan, N.; Levanon, K.; Bernstein-Molho, R.; Globus, O.; Itay, A.; Shapira, T.; Oedegaard, C.; et al. The role of 68 Ga-FAPI PET/CT in detection of metastatic lobular breast cancer. Clin. Nucl. Med. 2023, 48, 228–232. [Google Scholar] [CrossRef]
- Ballal, S.; Yadav, M.P.; Roesch, F.; Wakade, N.; Raju, S.; Sheokand, P.; Mishra, P.; Moon, E.S.; Tripathi, M.; Martin, M.; et al. Head-to-head comparison between [(68)Ga]Ga-DOTA.SA.FAPi and [(18)F]F-FDG PET/CT imaging in patients with breast cancer. Pharmaceuticals 2023, 16, 521. [Google Scholar] [CrossRef]
- Katzenellenbogen, J.A. The quest for improving the management of breast cancer by functional imaging: The discovery and development of 16α-[18F]fluoroestradiol (FES), a PET radiotracer for the estrogen receptor, a historical review. Nucl. Med. Biol. 2021, 92, 24–37. [Google Scholar] [CrossRef] [PubMed]
- Katal, S.; McKay, M.J.; Taubman, K. PET molecular imaging in breast cancer: Current applications and future perspectives. J. Clin. Med. 2024, 13, 3459. [Google Scholar] [CrossRef] [PubMed]
- Mortimer, J.E.; Dehdashti, F.; Siegel, B.A.; Trinkaus, K.; Katzenellenbogen, J.A.; Welch, M.J. Metabolic flare: Indicator of hormone responsiveness in advanced breast cancer. J. Clin. Oncol. 2001, 19, 2797–2803. [Google Scholar] [CrossRef]
- Peterson, L.M.; Kurland, B.F.; Schubert, E.K.; Link, J.M.; Gadi, V.; Specht, J.M.; Eary, J.F.; Porter, P.; Shankar, L.K.; Mankoff, D.A.; et al. A phase 2 study of 16α-[18F]-fluoro-17β-estradiol positron emission tomography (FES-PET) as a marker of hormone sensitivity in metastatic breast cancer (MBC). Mol. Imaging Biol. 2014, 16, 431–440. [Google Scholar] [CrossRef]
- Dehdashti, F.; Flanagan, F.L.; Mortimer, J.E.; Katzenellenbogen, J.A.; Welch, M.J.; Siegel, B.A. Positron emission tomographic assessment of “metabolic flare” to predict response of metastatic breast cancer to antiestrogen therapy. Eur. J. Nucl. Med. 1999, 26, 51–56. [Google Scholar] [CrossRef]
- van Kruchten, M.; Glaudemans, A.W.J.M.; Schröder, C.P.; de Vries, E.G.E.; Hospers, G.A.P. Positron emission tomography of tumour [18F]fluoroestradiol uptake in patients with acquired hormone-resistant metastatic breast cancer prior to oestradiol therapy. Eur. J. Nucl. Med. Mol. Imaging 2015, 42, 1674–1681. [Google Scholar] [CrossRef]
- Kurland, B.F.; Peterson, L.M.; Lee, J.H.; Schubert, E.K.; Currin, E.R.; Link, J.M.; Krohn, K.A.; Mankoff, D.A.; Linden, H.M. Estrogen receptor binding (18F-FES PET) and glycolytic activity (18F-FDG PET) predict progression-free survival on endocrine therapy in patients with ER+ breast cancer. Clin. Cancer Res. 2017, 23, 407–415. [Google Scholar] [CrossRef] [PubMed]
- Hao, W.; Li, Y.; Du, B.; Li, X. Heterogeneity of estrogen receptor based on 18F-FES PET imaging in breast cancer patients. Clin. Transl. Imaging 2021, 9, 599–607. [Google Scholar] [CrossRef]
- Gennari, A.; Brain, E.; De Censi, A.; Nanni, O.; Wuerstlein, R.; Frassoldati, A.; Cortes, J.; Rossi, V.; Palleschi, M.; Alberini, J.; et al. Early prediction of endocrine responsiveness in ER+/HER2-negative metastatic breast cancer (MBC): Pilot study with 18F-fluoroestradiol (18F-FES) CT/PET. Ann. Oncol. 2024, 35, 549–558. [Google Scholar] [CrossRef] [PubMed]
- Gupta, M.; Datta, A.; Choudhury, P.S.; Dsouza, M.; Batra, U.; Mishra, A. Can 18F-fluoroestradiol positron emission tomography become a new imaging standard in the estrogen receptor-positive breast cancer patient: A prospective comparative study with 18F-fluorodeoxyglucose positron emission tomography? World J. Nucl. Med. 2017, 16, 133–139. [Google Scholar] [CrossRef] [PubMed]
- Mankoff, D.A.; Tewson, T.J.; Eary, J.F. Analysis of blood clearance and labeled metabolites for the estrogen receptor tracer [F-18]-16α-Fluorestradiol (FES). Nucl. Med. Biol. 1997, 24, 341–348. [Google Scholar] [CrossRef]
- Bénard, F.; Ahmed, N.; Beauregard, J.-M.; Rousseau, J.; Aliaga, A.; Dubuc, C.; Croteau, E.; van Lier, J.E. [18F]Fluorinated estradiol derivatives for oestrogen receptor imaging: Impact of substituents, formulation and specific activity on the biodistribution in breast tumour-bearing mice. Eur. J. Nucl. Med. Mol. Imaging 2008, 35, 1473–1479. [Google Scholar] [CrossRef]
- Beauregard, J.M.; Croteau, E.; Ahmed, N.; van Lier, J.E.; Bénard, F. Assessment of human biodistribution and dosimetry of 4-fluoro-11beta-methoxy-16alpha-18F-fluoroestradiol using serial whole-body PET/CT. J. Nucl. Med. 2009, 50, 100–107. [Google Scholar] [CrossRef]
- Paquette, M.; Phoenix, S.; Lavallée, É.; Rousseau, J.A.; Guérin, B.; Turcotte, É.E.; Lecomte, R. Cross-species physiological assessment of brain estrogen receptor expression using (18)F-FES and (18)F-4FMFES PET imaging. Mol. Imaging Biol. 2020, 22, 1403–1413. [Google Scholar] [CrossRef]
- Paquette, M.; Lavallée, É.; Phoenix, S.; Ouellet, R.; Senta, H.; van Lier, J.E.; Guérin, B.; Lecomte, R.; Turcotte, E.E. Improved estrogen receptor assessment by PET using the novel radiotracer (18)F-4FMFES in estrogen receptor-positive breast cancer patients: An ongoing phase II clinical trial. J. Nucl. Med. 2018, 59, 197–203. [Google Scholar] [CrossRef]
- Lee, J.H.; Zhou, H.-B.; Dence, C.S.; Carlson, K.E.; Welch, M.J.; Katzenellenbogen, J.A. Development of [F-18]fluorine-substituted Tanaproget as a progesterone receptor imaging agent for positron emission tomography. Bioconjugate Chem. 2010, 21, 1096–1104. [Google Scholar] [CrossRef]
- Kochanny, M.J.; VanBrocklin, H.F.; Kym, P.R.; Carlson, K.E.; O’Neil, J.P.; Bonasera, T.A.; Welch, M.J.; Katzenellenbogen, J.A. Fluorine-18-labeled progestin ketals: Synthesis and target tissue uptake selectivity of potential imaging agents for receptor-positive breast tumors. J. Med. Chem. 1993, 36, 1120–1127. [Google Scholar] [CrossRef]
- Buckman, B.O.; Bonasera, T.A.; Kirschbaum, K.S.; Welch, M.J.; Katzenellenbogen, J.A. Fluorine-18-labeled progestin 16 alpha, 17 alpha-dioxolanes: Development of high-affinity ligands for the progesterone receptor with high in vivo target site selectivity. J. Med. Chem. 1995, 38, 328–337. [Google Scholar] [CrossRef] [PubMed]
- Kym, P.R.; Carlson, K.E.; Katzenellenbogen, J.A. Progestin 16 alpha, 17 alpha-dioxolane ketals as molecular probes for the progesterone receptor: Synthesis, binding affinity, and photochemical evaluation. J. Med. Chem. 1993, 36, 1111–1119. [Google Scholar] [CrossRef] [PubMed]
- Vijaykumar, D.; Mao, W.; Kirschbaum, K.S.; Katzenellenbogen, J.A. An efficient route for the preparation of a 21-fluoro progestin-16 alpha,17 alpha-dioxolane, a high-affinity ligand for PET imaging of the progesterone receptor. J. Org. Chem. 2002, 67, 4904–4910. [Google Scholar] [CrossRef] [PubMed]
- Jeselsohn, R.; Yelensky, R.; Buchwalter, G.; Frampton, G.; Meric-Bernstam, F.; Gonzalez-Angulo, A.M.; Ferrer-Lozano, J.; Perez-Fidalgo, J.A.; Cristofanilli, M.; Gómez, H.; et al. Emergence of constitutively active estrogen receptor-α mutations in pretreated advanced estrogen receptor-positive breast cancer. Clin. Cancer Res. 2014, 20, 1757–1767. [Google Scholar] [CrossRef]
- Dehdashti, F.; Laforest, R.; Gao, F.; Aft, R.L.; Dence, C.S.; Zhou, D.; Shoghi, K.I.; Siegel, B.A.; Katzenellenbogen, J.A.; Welch, M.J. Assessment of progesterone receptors in breast carcinoma by PET with 21-18F-fluoro-16α,17α-[(R)-(1′-α-furylmethylidene)dioxy]-19-norpregn-4-ene-3,20-dione. J. Nucl. Med. 2012, 53, 363–370. [Google Scholar] [CrossRef]
- Dehdashti, F.; Wu, N.; Ma, C.X.; Naughton, M.J.; Katzenellenbogen, J.A.; Siegel, B.A. Association of PET-based estradiol-challenge test for breast cancer progesterone receptors with response to endocrine therapy. Nat. Commun. 2021, 12, 733. [Google Scholar] [CrossRef]
- Dijkers, E.C.; Oude Munnink, T.H.; Kosterink, J.G.; Brouwers, A.H.; Jager, P.L.; De Jong, J.R.; Van Dongen, G.A.; Schroder, C.P.; Lub-de Hooge, M.N.; de Vries, E.G. Biodistribution of 89Zr-trastuzumab and PET imaging of HER2-positive lesions in patients with metastatic breast cancer. Clin. Pharmacol. Ther. 2010, 87, 586–592. [Google Scholar] [CrossRef]
- Ulaner, G.A.; Hyman, D.M.; Lyashchenko, S.K.; Lewis, J.S.; Carrasquillo, J.A. 89Zr-trastuzumab PET/CT for detection of human epidermal growth factor receptor 2-positive metastases in patients with human epidermal growth factor receptor 2-negative primary breast cancer. Clin. Nucl. Med. 2017, 42, 912–917. [Google Scholar] [CrossRef]
- Gebhart, G.; Lamberts, L.E.; Wimana, Z.; Garcia, C.; Emonts, P.; Ameye, L.; Stroobants, S.; Huizing, M.; Aftimos, P.; Tol, J.; et al. Molecular imaging as a tool to investigate heterogeneity of advanced HER2-positive breast cancer and to predict patient outcome under trastuzumab emtansine (T-DM1): The ZEPHIR trial. Ann. Oncol. 2016, 27, 619–624. [Google Scholar] [CrossRef]
- Tamura, K.; Kurihara, H.; Yonemori, K.; Tsuda, H.; Suzuki, J.; Kono, Y.; Honda, N.; Kodaira, M.; Yamamoto, H.; Yunokawa, M.; et al. 64Cu-DOTA-trastuzumab PET imaging in patients with HER2-positive breast cancer. J. Nucl. Med. 2013, 54, 1869–1875. [Google Scholar] [CrossRef]
- Mortimer, J.E.; Bading, J.R.; Colcher, D.M.; Conti, P.S.; Frankel, P.H.; Carroll, M.I.; Tong, S.; Poku, E.; Miles, J.K.; Shively, J.E.; et al. Functional imaging of human epidermal growth factor receptor 2-positive metastatic breast cancer using (64)Cu-DOTA-trastuzumab PET. J. Nucl. Med. 2014, 55, 23–29. [Google Scholar] [CrossRef]
- Mortimer, J.E.; Bading, J.R.; Park, J.M.; Frankel, P.H.; Carroll, M.I.; Tran, T.T.; Poku, E.K.; Rockne, R.C.; Raubitschek, A.A.; Shively, J.E.; et al. Tumor uptake of (64)Cu-DOTA-trastuzumab in patients with metastatic breast cancer. J. Nucl. Med. 2018, 59, 38–43. [Google Scholar] [CrossRef] [PubMed]
- Mortimer, J.E.; Bading, J.R.; Frankel, P.H.; Carroll, M.I.; Yuan, Y.; Park, J.M.; Tumyan, L.; Gidwaney, N.; Poku, E.K.; Shively, J.E.; et al. Use of (64)Cu-DOTA-trastuzumab PET to predict response and outcome of patients receiving trastuzumab emtansine for metastatic breast cancer: A pilot study. J. Nucl. Med. 2022, 63, 1145–1148. [Google Scholar] [CrossRef] [PubMed]
- Ulaner, G.A.; Lyashchenko, S.K.; Riedl, C.; Ruan, S.; Zanzonico, P.B.; Lake, D.; Jhaveri, K.; Zeglis, B.; Lewis, J.S.; O’donoghue, J.A. First-in-human human epidermal growth factor receptor 2-targeted imaging using (89)Zr-pertuzumab PET/CT: Dosimetry and clinical application in patients with breast cancer. J. Nucl. Med. 2018, 59, 900–906. [Google Scholar] [CrossRef]
- Ulaner, G.A.; Carrasquillo, J.A.; Riedl, C.C.; Yeh, R.; Hatzoglou, V.; Ross, D.S.; Jhaveri, K.; Chandarlapaty, S.; Hyman, D.M.; Zeglis, B.M.; et al. Identification of HER2-positive metastases in patients with HER2-negative primary breast cancer by using HER2-targeted (89)Zr-pertuzumab PET/CT. Radiology 2020, 296, 370–378. [Google Scholar] [CrossRef]
- Yeh, R.; O’donoghue, J.A.; Jayaprakasam, V.S.; Mauguen, A.; Min, R.; Park, S.; Brockway, J.P.; Bromberg, J.F.; Zhi, W.I.; Robson, M.E.; et al. First-in-human evaluation of site-specifically labeled (89)Zr-pertuzumab in patients with HER2-positive breast cancer. J. Nucl. Med. 2024, 65, 386–393. [Google Scholar] [CrossRef] [PubMed]
- Arslan, E.; Ergül, N.; Beyhan, E.; Erol Fenercioglu, Ö.; Sahin, R.; Cin, M.; Battal Havare, S.; Can Trabulus, F.D.; Mermut, Ö.; Akbas, S.; et al. The roles of 68 Ga-PSMA PET/CT and 18 F-FDG PET/CT imaging in patients with triple-negative breast cancer and the association of tissue PSMA and claudin 1, 4, and 7 levels with PET findings. Nucl. Med. Commun. 2023, 44, 284–290. [Google Scholar] [CrossRef]
- Andryszak, N.; Świniuch, D.; Wójcik, E.; Ramlau, R.; Ruchała, M.; Czepczyński, R. Head-to-head comparison of [(18)F]PSMA-1007 and [(18)F]FDG PET/CT in patients with triple-negative breast cancer. Cancers 2024, 16, 667. [Google Scholar] [CrossRef]
- Sörensen, J.; Velikyan, I.; Sandberg, D.; Wennborg, A.; Feldwisch, J.; Tolmachev, V.; Orlova, A.; Sandström, M.; Lubberink, M.; Olofsson, H.; et al. Measuring HER2-receptor expression in metastatic breast cancer using [68Ga]ABY-025 Affibody PET/CT. Theranostics 2016, 6, 262–271. [Google Scholar] [CrossRef]
- Alhuseinalkhudhur, A.; Lindman, H.; Liss, P.; Sundin, T.; Frejd, F.Y.; Hartman, J.; Iyer, V.; Feldwisch, J.; Lubberink, M.; Rönnlund, C.; et al. Human epidermal growth factor receptor 2-targeting [(68)Ga]Ga-ABY-025 PET/CT predicts early metabolic response in metastatic breast cancer. J. Nucl. Med. 2023, 64, 1364–1370. [Google Scholar] [CrossRef]
- Alhuseinalkhudhur, A.; Lindman, H.; Liss, P.; Frejd, F.Y.; Feldwisch, J.; Brun, N.C.; Lubberink, M.; Velikyan, I.; Sörensen, J. [68Ga]Ga-ABY-025 PET in HER2-positive breast cancer: Benefits and pitfalls in staging of axillary disease. J. Clin. Oncol. 2024, 42 (Suppl. 16), 1035. [Google Scholar] [CrossRef]
- Rathore, Y.; Shukla, J.; Laroiya, I.; Deep, A.; Lakhanpal, T.; Kumar, R.; Singh, H.; Bal, A.; Singh, G.; Thakur, K.G.; et al. Development 68Ga trastuzumab Fab and bioevaluation by PET imaging in HER2/neu expressing breast cancer patients. Nucl. Med. Commun. 2022, 43, 458–467. [Google Scholar] [CrossRef] [PubMed]
- Rathore, Y.; Shukla, J.; Bhusari, P.; Laroiya, I.; Sood, A.; Kumar, R.; Singh, H.; Singh, G.; Mittal, B.; Bal, A. Clinical evaluation of Ga-68 NOTA-Fab in HER2 expressing breast cancer patients. J. Nucl. Med. 2019, 60 (Suppl. S1), 1228. [Google Scholar]
- Yue, T.T.C.; Ge, Y.; Aprile, F.A.; Ma, M.T.; Pham, T.T.; Long, N.J. Site-specific (68)Ga radiolabeling of trastuzumab Fab via methionine for immunoPET imaging. Bioconjugate Chem. 2023, 34, 1802–1810. [Google Scholar] [CrossRef]
- Richter, A.; Knorr, K.; Schlapschy, M.; Robu, S.; Morath, V.; Mendler, C.; Yen, H.-Y.; Steiger, K.; Kiechle, M.; Weber, W.; et al. First in-human medical imaging with a PASylated (89)Zr-labeled anti-HER2 Fab-fragment in a patient with metastatic breast cancer. Nucl. Med. Mol. Imaging 2020, 54, 114–119. [Google Scholar] [CrossRef] [PubMed]
- Keyaerts, M.; Xavier, C.; Heemskerk, J.; Devoogdt, N.; Everaert, H.; Ackaert, C.; Vanhoeij, M.; Duhoux, F.P.; Gevaert, T.; Simon, P.; et al. Phase I study of 68Ga-HER2-Nanobody for PET/CT assessment of HER2 expression in breast carcinoma. J. Nucl. Med. 2016, 57, 27–33. [Google Scholar] [CrossRef]
- Gondry, O.; Caveliers, V.; Xavier, C.; Raes, L.; Vanhoeij, M.; Verfaillie, G.; Fontaine, C.; Glorieus, K.; De Grève, J.; Joris, S.; et al. Phase II trial assessing the repeatability and tumor uptake of [(68)Ga]Ga-HER2 single-domain antibody PET/CT in patients with breast carcinoma. J. Nucl. Med. 2024, 65, 178–184. [Google Scholar] [CrossRef]
- Xu, Y.; Wang, L.; Pan, D.; Yu, C.; Mi, B.; Huang, Q.; Sheng, J.; Yan, J.; Wang, X.; Yang, R.; et al. PET imaging of a (68)Ga labeled modified HER2 affibody in breast cancers: From xenografts to patients. Br. J. Radiol. 2019, 92, 20190425. [Google Scholar] [CrossRef]
- Savir-Baruch, B.; Schuster, D.M. Prostate cancer imaging with 18F-fluciclovine. PET Clin. 2022, 17, 607–620. [Google Scholar] [CrossRef]
- Ulaner, G.A.; Goldman, D.A.; Corben, A.; Lyashchenko, S.K.; Gönen, M.; Lewis, J.S.; Dickler, M. Prospective clinical trial of (18)F-fluciclovine PET/CT for determining the response to neoadjuvant therapy in invasive ductal and invasive lobular breast cancers. J. Nucl. Med. 2017, 58, 1037–1042. [Google Scholar] [CrossRef]
- Ma, G.; Goldman, D.A.; Corben, A.; Lyashchenko, S.K.; Gönen, M.; Lewis, J.S.; Dickler, M. (18)F-FLT PET/CT imaging for early monitoring response to CDK4/6 inhibitor therapy in triple negative breast cancer. Ann. Nucl. Med. 2021, 35, 600–607. [Google Scholar] [CrossRef] [PubMed]
- Rousseau, C.; Metz, R.; Kerdraon, O.; Ouldamer, L.; Boiffard, F.; Renaudeau, K.; Ferrer, L.; Vercouillie, J.; Doutriaux-Dumoulin, I.; Mouton, A.; et al. Pilot feasibility study: 18 F-DPA-714 PET/CT macrophage imaging in triple-negative breast cancers (EITHICS). Clin. Nucl. Med. 2024, 49, 701–708. [Google Scholar] [CrossRef] [PubMed]
- Sathekge, M.; Lengana, T.; Modiselle, M.; Vorster, M.; Zeevaart, J.; Maes, A.; Ebenhan, T.; Van de Wiele, C. (68)Ga-PSMA-HBED-CC PET imaging in breast carcinoma patients. Eur. J. Nucl. Med. Mol. Imaging 2017, 44, 689–694. [Google Scholar] [CrossRef]
- Venema, C.M.; Mammatas, L.H.; Schröder, C.P.; Van Kruchten, M.; Apollonio, G.; Glaudemans, A.W.J.M.; Bongaerts, A.H.; Hoekstra, O.S.; Verheul, H.M.; Boven, E.; et al. Androgen and estrogen receptor imaging in metastatic breast cancer patients as a surrogate for tissue biopsies. J. Nucl. Med. 2017, 58, 1906. [Google Scholar] [CrossRef]
- Stoykow, C.; Erbes, T.; Maecke, H.R.; Bulla, S.; Bartholomä, M.; Mayer, S.; Drendel, V.; Bronsert, P.; Werner, M.; Gitsch, G.; et al. Gastrin-releasing peptide receptor imaging in breast cancer using the receptor antagonist (68)Ga-RM2 and PET. Theranostics 2016, 6, 1641–1650. [Google Scholar] [CrossRef]
- Vorster, M.; Hadebe, B.P.; Sathekge, M.M. Theranostics in breast cancer. Front. Nucl. Med. 2023, 3, 1236565. [Google Scholar] [CrossRef]
- Choi, H.; Kim, K. Theranostics for triple-negative breast cancer. Diagnostics 2023, 13, 272. [Google Scholar] [CrossRef]
- Altena, R.; Tzortzakakis, A.; Burén, S.A.; Tran, T.A.; Frejd, F.Y.; Bergh, J.; Axelsson, R. Current status of contemporary diagnostic radiotracers in the management of breast cancer: First steps toward theranostic applications. EJNMMI Res. 2023, 13, 43. [Google Scholar] [CrossRef]
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Haidar, M.; Rizkallah, J.; El Sardouk, O.; El Ghawi, N.; Omran, N.; Hammoud, Z.; Saliba, N.; Tfayli, A.; Moukadem, H.; Berjawi, G.; et al. Radiotracer Innovations in Breast Cancer Imaging: A Review of Recent Progress. Diagnostics 2024, 14, 1943. https://doi.org/10.3390/diagnostics14171943
Haidar M, Rizkallah J, El Sardouk O, El Ghawi N, Omran N, Hammoud Z, Saliba N, Tfayli A, Moukadem H, Berjawi G, et al. Radiotracer Innovations in Breast Cancer Imaging: A Review of Recent Progress. Diagnostics. 2024; 14(17):1943. https://doi.org/10.3390/diagnostics14171943
Chicago/Turabian StyleHaidar, Mohamad, Joe Rizkallah, Omar El Sardouk, Nour El Ghawi, Nadine Omran, Zeinab Hammoud, Nina Saliba, Arafat Tfayli, Hiba Moukadem, Ghina Berjawi, and et al. 2024. "Radiotracer Innovations in Breast Cancer Imaging: A Review of Recent Progress" Diagnostics 14, no. 17: 1943. https://doi.org/10.3390/diagnostics14171943