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Published in: Journal of Translational Medicine 1/2022

Open Access 01-12-2022 | Computed Tomography | Review

Advances in nuclear medicine-based molecular imaging in head and neck squamous cell carcinoma

Authors: Danni Li, Xuran Li, Jun Zhao, Fei Tan

Published in: Journal of Translational Medicine | Issue 1/2022

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Abstract

Head and neck squamous cell carcinomas (HNSCCs) are often aggressive, making advanced disease very difficult to treat using contemporary modalities, such as surgery, radiation therapy, and chemotherapy. However, targeted therapy, e.g., cetuximab, an epidermal growth factor receptor inhibitor, has demonstrated survival benefit in HNSCC patients with locoregional failure or distant metastasis. Molecular imaging aims at various biomarkers used in targeted therapy, and nuclear medicine-based molecular imaging is a real-time and non-invasive modality with the potential to identify tumor in an earlier and more treatable stage, before anatomic-based imaging reveals diseases. The objective of this comprehensive review is to summarize recent advances in nuclear medicine-based molecular imaging for HNSCC focusing on several commonly radiolabeled biomarkers. The preclinical and clinical applications of these candidate imaging strategies are divided into three categories: those targeting tumor cells, tumor microenvironment, and tumor angiogenesis. This review endeavors to expand the knowledge of molecular biology of HNSCC and help realizing diagnostic potential of molecular imaging in clinical nuclear medicine.
Literature
1.
go back to reference Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68:394–424.PubMedCrossRef Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68:394–424.PubMedCrossRef
2.
go back to reference Xu H, Stabile LP, Gubish CT, Gooding WE, Grandis JR, Siegfried JM. Dual blockade of EGFR and c-Met abrogates redundant signaling and proliferation in head and neck carcinoma cells. Clin Cancer Res. 2011;17:4425–38.PubMedPubMedCentralCrossRef Xu H, Stabile LP, Gubish CT, Gooding WE, Grandis JR, Siegfried JM. Dual blockade of EGFR and c-Met abrogates redundant signaling and proliferation in head and neck carcinoma cells. Clin Cancer Res. 2011;17:4425–38.PubMedPubMedCentralCrossRef
4.
go back to reference Adkins D, Ley J, Neupane P, Worden F, Sacco AG, Palka K, et al. Palbociclib and cetuximab in platinum-resistant and in cetuximab-resistant human papillomavirus-unrelated head and neck cancer: a multicentre, multigroup, phase 2 trial. Lancet Oncol. 2019;20:1295–305.PubMedCrossRef Adkins D, Ley J, Neupane P, Worden F, Sacco AG, Palka K, et al. Palbociclib and cetuximab in platinum-resistant and in cetuximab-resistant human papillomavirus-unrelated head and neck cancer: a multicentre, multigroup, phase 2 trial. Lancet Oncol. 2019;20:1295–305.PubMedCrossRef
5.
go back to reference Leblanc O, Vacher S, Lecerf C, Jeannot E, Klijanienko J, Berger F, et al. Biomarkers of cetuximab resistance in patients with head and neck squamous cell carcinoma. Cancer Biol Med. 2020;17:208–17.PubMedPubMedCentralCrossRef Leblanc O, Vacher S, Lecerf C, Jeannot E, Klijanienko J, Berger F, et al. Biomarkers of cetuximab resistance in patients with head and neck squamous cell carcinoma. Cancer Biol Med. 2020;17:208–17.PubMedPubMedCentralCrossRef
7.
go back to reference Langer CJ. Targeted therapy in head and neck cancer: state of the art 2007 and review of clinical applications. Cancer. 2008;112:2635–45.PubMedCrossRef Langer CJ. Targeted therapy in head and neck cancer: state of the art 2007 and review of clinical applications. Cancer. 2008;112:2635–45.PubMedCrossRef
8.
go back to reference Vermorken JB, Trigo J, Hitt R, Koralewski P, Diaz-Rubio E, Rolland F, et al. Open-label, uncontrolled, multicenter phase II study to evaluate the efficacy and toxicity of cetuximab as a single agent in patients with recurrent and/or metastatic squamous cell carcinoma of the head and neck who failed to respond to platinum-based therapy. J Clin Oncol. 2007;25:2171–7.PubMedCrossRef Vermorken JB, Trigo J, Hitt R, Koralewski P, Diaz-Rubio E, Rolland F, et al. Open-label, uncontrolled, multicenter phase II study to evaluate the efficacy and toxicity of cetuximab as a single agent in patients with recurrent and/or metastatic squamous cell carcinoma of the head and neck who failed to respond to platinum-based therapy. J Clin Oncol. 2007;25:2171–7.PubMedCrossRef
9.
go back to reference Ehlerding EB, England CG, McNeel DG, Cai W. Molecular imaging of immunotherapy targets in cancer. J Nucl Med Offl Publ Soc Nucl Med. 2016;57:1487–92. Ehlerding EB, England CG, McNeel DG, Cai W. Molecular imaging of immunotherapy targets in cancer. J Nucl Med Offl Publ Soc Nucl Med. 2016;57:1487–92.
11.
go back to reference Castaldi P, Leccisotti L, Bussu F, Miccichè F, Rufini V. Role of (18)F-FDG PET-CT in head and neck squamous cell carcinoma. Acta Otorhinolaryngol Ital. 2013;33:1–8.PubMedPubMedCentral Castaldi P, Leccisotti L, Bussu F, Miccichè F, Rufini V. Role of (18)F-FDG PET-CT in head and neck squamous cell carcinoma. Acta Otorhinolaryngol Ital. 2013;33:1–8.PubMedPubMedCentral
12.
go back to reference Kalyankrishna S, Grandis JR. Epidermal growth factor receptor biology in head and neck cancer. J Clin Oncol. 2006;24:2666–72.PubMedCrossRef Kalyankrishna S, Grandis JR. Epidermal growth factor receptor biology in head and neck cancer. J Clin Oncol. 2006;24:2666–72.PubMedCrossRef
13.
go back to reference Gupta AK, McKenna WG, Weber CN, Feldman MD, Goldsmith JD, Mick R, et al. Local recurrence in head and neck cancer: relationship to radiation resistance and signal transduction. Clin Cancer Res. 2002;8:885–92.PubMed Gupta AK, McKenna WG, Weber CN, Feldman MD, Goldsmith JD, Mick R, et al. Local recurrence in head and neck cancer: relationship to radiation resistance and signal transduction. Clin Cancer Res. 2002;8:885–92.PubMed
14.
go back to reference Rubin Grandis J, Melhem MF, Gooding WE, Day R, Holst VA, Wagener MM, et al. Levels of TGF-alpha and EGFR protein in head and neck squamous cell carcinoma and patient survival. J Natl Cancer Inst. 1998;90:824–32.PubMedCrossRef Rubin Grandis J, Melhem MF, Gooding WE, Day R, Holst VA, Wagener MM, et al. Levels of TGF-alpha and EGFR protein in head and neck squamous cell carcinoma and patient survival. J Natl Cancer Inst. 1998;90:824–32.PubMedCrossRef
16.
go back to reference Hoeben BAW, Molkenboer-Kuenen JDM, Oyen WJG, Peeters WJM, Kaanders JHAM, Bussink J, et al. Radiolabeled cetuximab: dose optimization for epidermal growth factor receptor imaging in a head-and-neck squamous cell carcinoma model. Int J Cancer. 2011;129:870–8.PubMedCrossRef Hoeben BAW, Molkenboer-Kuenen JDM, Oyen WJG, Peeters WJM, Kaanders JHAM, Bussink J, et al. Radiolabeled cetuximab: dose optimization for epidermal growth factor receptor imaging in a head-and-neck squamous cell carcinoma model. Int J Cancer. 2011;129:870–8.PubMedCrossRef
17.
go back to reference van Dijk LK, Hoeben BAW, Stegeman H, Kaanders JHAM, Franssen GM, Boerman OC, et al. 111In-cetuximab-F(ab’)2 SPECT imaging for quantification of accessible epidermal growth factor receptors (EGFR) in HNSCC xenografts. Radiother Oncol J Eur Soc Ther Radiol Oncol. 2013;108:484–8.CrossRef van Dijk LK, Hoeben BAW, Stegeman H, Kaanders JHAM, Franssen GM, Boerman OC, et al. 111In-cetuximab-F(ab’)2 SPECT imaging for quantification of accessible epidermal growth factor receptors (EGFR) in HNSCC xenografts. Radiother Oncol J Eur Soc Ther Radiol Oncol. 2013;108:484–8.CrossRef
18.
go back to reference van Dijk LK, Boerman OC, Franssen GM, Lok J, Kaanders JHAM, Bussink J. Early response monitoring with 18F-FDG PET and cetuximab-F(ab’)2-SPECT after radiotherapy of human head and neck squamous cell carcinomas in a mouse model. J Nucl Med Offl Publ Soc Nucl Med. 2014;55:1665–70. van Dijk LK, Boerman OC, Franssen GM, Lok J, Kaanders JHAM, Bussink J. Early response monitoring with 18F-FDG PET and cetuximab-F(ab’)2-SPECT after radiotherapy of human head and neck squamous cell carcinomas in a mouse model. J Nucl Med Offl Publ Soc Nucl Med. 2014;55:1665–70.
19.
go back to reference van Dijk LK, Hoeben BAW, Kaanders JHAM, Franssen GM, Boerman OC, Bussink J. Imaging of epidermal growth factor receptor expression in head and neck cancer with SPECT/CT and 111In-labeled cetuximab-F(ab’)2. J Nucl Med Offl Publ Soc Nucl Med. 2013;54:2118–24. van Dijk LK, Hoeben BAW, Kaanders JHAM, Franssen GM, Boerman OC, Bussink J. Imaging of epidermal growth factor receptor expression in head and neck cancer with SPECT/CT and 111In-labeled cetuximab-F(ab’)2. J Nucl Med Offl Publ Soc Nucl Med. 2013;54:2118–24.
20.
go back to reference van Dijk LK, Yim C-B, Franssen GM, Kaanders JHAM, Rajander J, Solin O, et al. PET of EGFR with (64) Cu-cetuximab-F(ab’)2 in mice with head and neck squamous cell carcinoma xenografts. Contrast Media Mol Imaging. 2016;11:65–70.PubMedCrossRef van Dijk LK, Yim C-B, Franssen GM, Kaanders JHAM, Rajander J, Solin O, et al. PET of EGFR with (64) Cu-cetuximab-F(ab’)2 in mice with head and neck squamous cell carcinoma xenografts. Contrast Media Mol Imaging. 2016;11:65–70.PubMedCrossRef
21.
go back to reference van Loon J, Even AJG, Aerts HJWL, Öllers M, Hoebers F, van Elmpt W, et al. PET imaging of zirconium-89 labelled cetuximab: a phase I trial in patients with head and neck and lung cancer. Radiother Oncol J Eur Soc Ther Radiol Oncol. 2017;122:267–73.CrossRef van Loon J, Even AJG, Aerts HJWL, Öllers M, Hoebers F, van Elmpt W, et al. PET imaging of zirconium-89 labelled cetuximab: a phase I trial in patients with head and neck and lung cancer. Radiother Oncol J Eur Soc Ther Radiol Oncol. 2017;122:267–73.CrossRef
22.
go back to reference Even AJG, Hamming-Vrieze O, van Elmpt W, Winnepenninckx VJL, Heukelom J, Tesselaar MET, et al. Quantitative assessment of Zirconium-89 labeled cetuximab using PET/CT imaging in patients with advanced head and neck cancer: a theragnostic approach. Oncotarget. 2017;8:3870–80.PubMedCrossRef Even AJG, Hamming-Vrieze O, van Elmpt W, Winnepenninckx VJL, Heukelom J, Tesselaar MET, et al. Quantitative assessment of Zirconium-89 labeled cetuximab using PET/CT imaging in patients with advanced head and neck cancer: a theragnostic approach. Oncotarget. 2017;8:3870–80.PubMedCrossRef
23.
go back to reference Benedetto R, Massicano AVF, Crenshaw BK, Oliveira R, Reis RM, Araújo EB, et al. 89Zr-DFO-cetuximab as a molecular imaging agent to identify cetuximab resistance in head and neck squamous cell carcinoma. Cancer Biother Radiopharm. 2019;34:288–96.PubMedPubMedCentralCrossRef Benedetto R, Massicano AVF, Crenshaw BK, Oliveira R, Reis RM, Araújo EB, et al. 89Zr-DFO-cetuximab as a molecular imaging agent to identify cetuximab resistance in head and neck squamous cell carcinoma. Cancer Biother Radiopharm. 2019;34:288–96.PubMedPubMedCentralCrossRef
24.
go back to reference Li W, Niu G, Lang L, Guo N, Ma Y, Kiesewetter DO, et al. PET imaging of EGF receptors using [18F]FBEM-EGF in a head and neck squamous cell carcinoma model. Eur J Nucl Med Mol Imaging. 2012;39:300–8.PubMedCrossRef Li W, Niu G, Lang L, Guo N, Ma Y, Kiesewetter DO, et al. PET imaging of EGF receptors using [18F]FBEM-EGF in a head and neck squamous cell carcinoma model. Eur J Nucl Med Mol Imaging. 2012;39:300–8.PubMedCrossRef
25.
go back to reference Burley TA, Da Pieve C, Martins CD, Ciobota DM, Allott L, Oyen WJG, et al. Affibody-based PET imaging to guide EGFR-targeted cancer therapy in head and neck squamous cell cancer models. J Nucl Med Offl Publ Soc Nucl Med. 2019;60:353–61. Burley TA, Da Pieve C, Martins CD, Ciobota DM, Allott L, Oyen WJG, et al. Affibody-based PET imaging to guide EGFR-targeted cancer therapy in head and neck squamous cell cancer models. J Nucl Med Offl Publ Soc Nucl Med. 2019;60:353–61.
26.
go back to reference Niu G, Li Z, Xie J, Le Q-T, Chen X. PET of EGFR antibody distribution in head and neck squamous cell carcinoma models. J Nucl Med Offl Publ Soc Nucl Med. 2009;50:1116–23. Niu G, Li Z, Xie J, Le Q-T, Chen X. PET of EGFR antibody distribution in head and neck squamous cell carcinoma models. J Nucl Med Offl Publ Soc Nucl Med. 2009;50:1116–23.
27.
go back to reference Song IH, Noh Y, Kwon J, Jung JH, Lee BC, Kim KI, et al. Immuno-PET imaging based radioimmunotherapy in head and neck squamous cell carcinoma model. Oncotarget. 2017;8:92090–105.PubMedPubMedCentralCrossRef Song IH, Noh Y, Kwon J, Jung JH, Lee BC, Kim KI, et al. Immuno-PET imaging based radioimmunotherapy in head and neck squamous cell carcinoma model. Oncotarget. 2017;8:92090–105.PubMedPubMedCentralCrossRef
28.
go back to reference Ku A, Kondo M, Cai Z, Meens J, Li MR, Ailles L, et al. Dose predictions for [177Lu]Lu-DOTA-panitumumab F(ab’)2 in NRG mice with HNSCC patient-derived tumour xenografts based on [64Cu]Cu-DOTA-panitumumab F(ab’)2 - implications for a PET theranostic strategy. EJNMMI Radiopharm Chem. 2021;6:25.PubMedPubMedCentralCrossRef Ku A, Kondo M, Cai Z, Meens J, Li MR, Ailles L, et al. Dose predictions for [177Lu]Lu-DOTA-panitumumab F(ab’)2 in NRG mice with HNSCC patient-derived tumour xenografts based on [64Cu]Cu-DOTA-panitumumab F(ab’)2 - implications for a PET theranostic strategy. EJNMMI Radiopharm Chem. 2021;6:25.PubMedPubMedCentralCrossRef
29.
go back to reference Dhar D, Antonucci L, Nakagawa H, Kim JY, Glitzner E, Caruso S, et al. Liver cancer initiation requires p53 inhibition by CD44-enhanced growth factor signaling. Cancer Cell. 2018;33:1061-77.e6.PubMedPubMedCentralCrossRef Dhar D, Antonucci L, Nakagawa H, Kim JY, Glitzner E, Caruso S, et al. Liver cancer initiation requires p53 inhibition by CD44-enhanced growth factor signaling. Cancer Cell. 2018;33:1061-77.e6.PubMedPubMedCentralCrossRef
30.
go back to reference Orian-Rousseau V. CD44, a therapeutic target for metastasising tumours. Eur J Cancer (Oxford, England: 1990). 2010;46:1271–7.CrossRef Orian-Rousseau V. CD44, a therapeutic target for metastasising tumours. Eur J Cancer (Oxford, England: 1990). 2010;46:1271–7.CrossRef
31.
go back to reference Spiegelberg D, Nilvebrant J. CD44v6-targeted imaging of head and neck squamous cell carcinoma: antibody-based approaches. Contrast Media Mol Imaging. 2017;2017:2709547.PubMedPubMedCentralCrossRef Spiegelberg D, Nilvebrant J. CD44v6-targeted imaging of head and neck squamous cell carcinoma: antibody-based approaches. Contrast Media Mol Imaging. 2017;2017:2709547.PubMedPubMedCentralCrossRef
32.
go back to reference Börjesson PKE, Jauw YWS, Boellaard R, de Bree R, Comans EFI, Roos JC, et al. Performance of immuno-positron emission tomography with zirconium-89-labeled chimeric monoclonal antibody U36 in the detection of lymph node metastases in head and neck cancer patients. Clin Cancer Res Offl J Am Assoc Cancer Res. 2006;12:2133–40.CrossRef Börjesson PKE, Jauw YWS, Boellaard R, de Bree R, Comans EFI, Roos JC, et al. Performance of immuno-positron emission tomography with zirconium-89-labeled chimeric monoclonal antibody U36 in the detection of lymph node metastases in head and neck cancer patients. Clin Cancer Res Offl J Am Assoc Cancer Res. 2006;12:2133–40.CrossRef
33.
go back to reference Colnot DR, Quak JJ, Roos JC, van Lingen A, Wilhelm AJ, van Kamp GJ, et al. Phase I therapy study of 186Re-labeled chimeric monoclonal antibody U36 in patients with squamous cell carcinoma of the head and neck. J Nucl Med Offl Publ Soc Nucl Med. 2000;41:1999–2010. Colnot DR, Quak JJ, Roos JC, van Lingen A, Wilhelm AJ, van Kamp GJ, et al. Phase I therapy study of 186Re-labeled chimeric monoclonal antibody U36 in patients with squamous cell carcinoma of the head and neck. J Nucl Med Offl Publ Soc Nucl Med. 2000;41:1999–2010.
34.
go back to reference Verel I, Heider KH, Siegmund M, Ostermann E, Patzelt E, Sproll M, et al. Tumor targeting properties of monoclonal antibodies with different affinity for target antigen CD44V6 in nude mice bearing head-and-neck cancer xenografts. Int J Cancer. 2002;99:396–402.PubMedCrossRef Verel I, Heider KH, Siegmund M, Ostermann E, Patzelt E, Sproll M, et al. Tumor targeting properties of monoclonal antibodies with different affinity for target antigen CD44V6 in nude mice bearing head-and-neck cancer xenografts. Int J Cancer. 2002;99:396–402.PubMedCrossRef
35.
go back to reference Stroomer JW, Roos JC, Sproll M, Quak JJ, Heider KH, Wilhelm BJ, et al. Safety and biodistribution of 99mTechnetium-labeled anti-CD44v6 monoclonal antibody BIWA 1 in head and neck cancer patients. Clin Cancer Res Offl J Am Assoc Cancer Res. 2000;6:3046–55. Stroomer JW, Roos JC, Sproll M, Quak JJ, Heider KH, Wilhelm BJ, et al. Safety and biodistribution of 99mTechnetium-labeled anti-CD44v6 monoclonal antibody BIWA 1 in head and neck cancer patients. Clin Cancer Res Offl J Am Assoc Cancer Res. 2000;6:3046–55.
36.
go back to reference Colnot DR, Roos JC, de Bree R, Wilhelm AJ, Kummer JA, Hanft G, et al. Safety, biodistribution, pharmacokinetics, and immunogenicity of 99m Tc-labeled humanized monoclonal antibody BIWA 4 (bivatuzumab) in patients with squamous cell carcinoma of the head and neck. Cancer Immunol Immunother. 2003;52:576–82.PubMedCrossRef Colnot DR, Roos JC, de Bree R, Wilhelm AJ, Kummer JA, Hanft G, et al. Safety, biodistribution, pharmacokinetics, and immunogenicity of 99m Tc-labeled humanized monoclonal antibody BIWA 4 (bivatuzumab) in patients with squamous cell carcinoma of the head and neck. Cancer Immunol Immunother. 2003;52:576–82.PubMedCrossRef
37.
go back to reference Odenthal J, Rijpkema M, Bos D, Wagena E, Croes H, Grenman R, et al. Targeting CD44v6 for fluorescence-guided surgery in head and neck squamous cell carcinoma. Sci Rep. 2018;8:10467.PubMedPubMedCentralCrossRef Odenthal J, Rijpkema M, Bos D, Wagena E, Croes H, Grenman R, et al. Targeting CD44v6 for fluorescence-guided surgery in head and neck squamous cell carcinoma. Sci Rep. 2018;8:10467.PubMedPubMedCentralCrossRef
39.
go back to reference Haylock A-K, Spiegelberg D, Nilvebrant J, Sandström K, Nestor M. In vivo characterization of the novel CD44v6-targeting Fab fragment AbD15179 for molecular imaging of squamous cell carcinoma: a dual-isotope study. EJNMMI Res. 2014;4:11.PubMedPubMedCentralCrossRef Haylock A-K, Spiegelberg D, Nilvebrant J, Sandström K, Nestor M. In vivo characterization of the novel CD44v6-targeting Fab fragment AbD15179 for molecular imaging of squamous cell carcinoma: a dual-isotope study. EJNMMI Res. 2014;4:11.PubMedPubMedCentralCrossRef
40.
go back to reference Haylock A-K, Spiegelberg D, Mortensen AC, Selvaraju RK, Nilvebrant J, Eriksson O, et al. Evaluation of a novel type of imaging probe based on a recombinant bivalent mini-antibody construct for detection of CD44v6-expressing squamous cell carcinoma. Int J Oncol. 2016;48:461–70.PubMedCrossRef Haylock A-K, Spiegelberg D, Mortensen AC, Selvaraju RK, Nilvebrant J, Eriksson O, et al. Evaluation of a novel type of imaging probe based on a recombinant bivalent mini-antibody construct for detection of CD44v6-expressing squamous cell carcinoma. Int J Oncol. 2016;48:461–70.PubMedCrossRef
41.
go back to reference Theodoropoulou M, Stalla GK. Somatostatin receptors: from signaling to clinical practice. Front Neuroendocrinol. 2013;34:228–52.PubMedCrossRef Theodoropoulou M, Stalla GK. Somatostatin receptors: from signaling to clinical practice. Front Neuroendocrinol. 2013;34:228–52.PubMedCrossRef
42.
go back to reference Hu Y, Ye Z, Wang F, Qin Y, Xu X, Yu X, et al. Role of somatostatin receptor in pancreatic neuroendocrine tumor development, diagnosis, and therapy. Front Endocrinol. 2021;12:679000.CrossRef Hu Y, Ye Z, Wang F, Qin Y, Xu X, Yu X, et al. Role of somatostatin receptor in pancreatic neuroendocrine tumor development, diagnosis, and therapy. Front Endocrinol. 2021;12:679000.CrossRef
43.
go back to reference Reubi JC. Peptide receptors as molecular targets for cancer diagnosis and therapy. Endocr Rev. 2003;24:389–427.PubMedCrossRef Reubi JC. Peptide receptors as molecular targets for cancer diagnosis and therapy. Endocr Rev. 2003;24:389–427.PubMedCrossRef
44.
go back to reference Werner RA, Weich A, Kircher M, Solnes LB, Javadi MS, Higuchi T, et al. The theranostic promise for Neuroendocrine Tumors in the late 2010s - Where do we stand, where do we go? Theranostics. 2018;8:6088–100.PubMedPubMedCentralCrossRef Werner RA, Weich A, Kircher M, Solnes LB, Javadi MS, Higuchi T, et al. The theranostic promise for Neuroendocrine Tumors in the late 2010s - Where do we stand, where do we go? Theranostics. 2018;8:6088–100.PubMedPubMedCentralCrossRef
45.
go back to reference Stafford ND, Condon LT, Rogers MJC, MacDonald AW, Atkin SL. The expression of somatostatin receptors 1 and 2 in benign, pre-malignant and malignant laryngeal lesions. Clin Otolaryngol Allied Sci. 2003;28:314–9.PubMedCrossRef Stafford ND, Condon LT, Rogers MJC, MacDonald AW, Atkin SL. The expression of somatostatin receptors 1 and 2 in benign, pre-malignant and malignant laryngeal lesions. Clin Otolaryngol Allied Sci. 2003;28:314–9.PubMedCrossRef
46.
go back to reference Loh KS, Waser B, Tan LKS, Ruan RS, Stauffer E, Reubi JC. Somatostatin receptors in nasopharyngeal carcinoma. Virchows Arch. 2002;441:444–8.PubMedCrossRef Loh KS, Waser B, Tan LKS, Ruan RS, Stauffer E, Reubi JC. Somatostatin receptors in nasopharyngeal carcinoma. Virchows Arch. 2002;441:444–8.PubMedCrossRef
47.
go back to reference Schartinger VH, Falkeis C, Laimer K, Sprinzl GM, Riechelmann H, Rasse M, et al. Neuroendocrine differentiation in head and neck squamous cell carcinoma. J Laryngol Otol. 2012;126:1261–70.PubMedCrossRef Schartinger VH, Falkeis C, Laimer K, Sprinzl GM, Riechelmann H, Rasse M, et al. Neuroendocrine differentiation in head and neck squamous cell carcinoma. J Laryngol Otol. 2012;126:1261–70.PubMedCrossRef
48.
go back to reference Bennink RJ, van der Meulen FW, Freling NJ, Booij J. Somatostatin receptor scintigraphy in nasopharyngeal carcinoma. Clin Nucl Med. 2008;33:558–61.PubMedCrossRef Bennink RJ, van der Meulen FW, Freling NJ, Booij J. Somatostatin receptor scintigraphy in nasopharyngeal carcinoma. Clin Nucl Med. 2008;33:558–61.PubMedCrossRef
49.
go back to reference Doan JT, Arnold CD. An unusual case of positive somatostatin receptor scintigraphy in squamous cell carcinoma of head and neck. Clin Nucl Med. 2011;36:380–1.PubMedCrossRef Doan JT, Arnold CD. An unusual case of positive somatostatin receptor scintigraphy in squamous cell carcinoma of head and neck. Clin Nucl Med. 2011;36:380–1.PubMedCrossRef
50.
go back to reference Viswanathan K, Sadow PM. Somatostatin receptor 2 is highly sensitive and specific for Epstein-Barr virus-associated nasopharyngeal carcinoma. Hum Pathol. 2021;117:88–100.PubMedCrossRef Viswanathan K, Sadow PM. Somatostatin receptor 2 is highly sensitive and specific for Epstein-Barr virus-associated nasopharyngeal carcinoma. Hum Pathol. 2021;117:88–100.PubMedCrossRef
51.
go back to reference Lechner M, Schartinger VH, Steele CD, Nei WL, Ooft ML, Schreiber L-M, et al. Somatostatin receptor 2 expression in nasopharyngeal cancer is induced by Epstein Barr virus infection: impact on prognosis, imaging and therapy. Nat Commun. 2021;12:117.PubMedPubMedCentralCrossRef Lechner M, Schartinger VH, Steele CD, Nei WL, Ooft ML, Schreiber L-M, et al. Somatostatin receptor 2 expression in nasopharyngeal cancer is induced by Epstein Barr virus infection: impact on prognosis, imaging and therapy. Nat Commun. 2021;12:117.PubMedPubMedCentralCrossRef
52.
go back to reference Zhao L, Pang Y, Wang Y, Chen J, Zhuang Y, Zhang J, et al. Somatostatin receptor imaging with [68Ga]Ga-DOTATATE positron emission tomography/computed tomography (PET/CT) in patients with nasopharyngeal carcinoma. Eur J Nucl Med Mol Imaging. 2021;49(4):1360–73.PubMedCrossRef Zhao L, Pang Y, Wang Y, Chen J, Zhuang Y, Zhang J, et al. Somatostatin receptor imaging with [68Ga]Ga-DOTATATE positron emission tomography/computed tomography (PET/CT) in patients with nasopharyngeal carcinoma. Eur J Nucl Med Mol Imaging. 2021;49(4):1360–73.PubMedCrossRef
53.
go back to reference Unterrainer M, Maihoefer C, Cyran CC, Bartenstein P, Niyazi M, Albert NL. 68Ga-DOTATATE PET/CT Reveals epstein-barr virus-associated nasopharyngeal carcinoma in a case of suspected sphenoid wing meningioma. Clin Nucl Med. 2018;43:287–8.PubMedCrossRef Unterrainer M, Maihoefer C, Cyran CC, Bartenstein P, Niyazi M, Albert NL. 68Ga-DOTATATE PET/CT Reveals epstein-barr virus-associated nasopharyngeal carcinoma in a case of suspected sphenoid wing meningioma. Clin Nucl Med. 2018;43:287–8.PubMedCrossRef
54.
go back to reference Schartinger VH, Dudás J, Decristoforo C, Url C, Schnabl J, Göbel G, et al. 68Ga-DOTA0-Tyr3-octreotide positron emission tomography in head and neck squamous cell carcinoma. Eur J Nucl Med Mol Imaging. 2013;40:1365–72.PubMedCrossRef Schartinger VH, Dudás J, Decristoforo C, Url C, Schnabl J, Göbel G, et al. 68Ga-DOTA0-Tyr3-octreotide positron emission tomography in head and neck squamous cell carcinoma. Eur J Nucl Med Mol Imaging. 2013;40:1365–72.PubMedCrossRef
55.
go back to reference Schartinger VH, Dudás J, Url C, Reinold S, Virgolini IJ, Kroiss A, et al. 68Ga-DOTA0-Tyr3-octreotide positron emission tomography in nasopharyngeal carcinoma. Eur J Nucl Med Mol Imaging. 2015;42:20–4.PubMedCrossRef Schartinger VH, Dudás J, Url C, Reinold S, Virgolini IJ, Kroiss A, et al. 68Ga-DOTA0-Tyr3-octreotide positron emission tomography in nasopharyngeal carcinoma. Eur J Nucl Med Mol Imaging. 2015;42:20–4.PubMedCrossRef
56.
go back to reference Wild D, Schmitt JS, Ginj M, Mäcke HR, Bernard BF, Krenning E, et al. DOTA-NOC, a high-affinity ligand of somatostatin receptor subtypes 2, 3 and 5 for labelling with various radiometals. Eur J Nucl Med Mol Imaging. 2003;30:1338–47.PubMedCrossRef Wild D, Schmitt JS, Ginj M, Mäcke HR, Bernard BF, Krenning E, et al. DOTA-NOC, a high-affinity ligand of somatostatin receptor subtypes 2, 3 and 5 for labelling with various radiometals. Eur J Nucl Med Mol Imaging. 2003;30:1338–47.PubMedCrossRef
57.
go back to reference Wild D, Mäcke HR, Waser B, Reubi JC, Ginj M, Rasch H, et al. 68Ga-DOTANOC: a first compound for PET imaging with high affinity for somatostatin receptor subtypes 2 and 5. Eur J Nucl Med Mol Imaging. 2005;32:724.PubMedCrossRef Wild D, Mäcke HR, Waser B, Reubi JC, Ginj M, Rasch H, et al. 68Ga-DOTANOC: a first compound for PET imaging with high affinity for somatostatin receptor subtypes 2 and 5. Eur J Nucl Med Mol Imaging. 2005;32:724.PubMedCrossRef
58.
go back to reference Khor LK, Loi HY, Sinha AK, Tong KT, Goh BC, Loh KS, et al. Correlation between (68)Ga-DOTA-NOC PET/CT and (18)F-FDG PET/CT in EBV-positive undifferentiated nasopharyngeal carcinoma. Eur J Nucl Med Mol Imaging. 2015;42:1162–3.PubMedCrossRef Khor LK, Loi HY, Sinha AK, Tong KT, Goh BC, Loh KS, et al. Correlation between (68)Ga-DOTA-NOC PET/CT and (18)F-FDG PET/CT in EBV-positive undifferentiated nasopharyngeal carcinoma. Eur J Nucl Med Mol Imaging. 2015;42:1162–3.PubMedCrossRef
59.
go back to reference Khor LK, Loi HY, Sinha AK, Tong KT, Goh BC, Loh KS, et al. 68Ga-DOTA-peptide: a novel molecular biomarker for nasopharyngeal carcinoma: 68Ga-DOTA-peptide in NPC. Head Neck. 2016;38:E76–80.PubMedCrossRef Khor LK, Loi HY, Sinha AK, Tong KT, Goh BC, Loh KS, et al. 68Ga-DOTA-peptide: a novel molecular biomarker for nasopharyngeal carcinoma: 68Ga-DOTA-peptide in NPC. Head Neck. 2016;38:E76–80.PubMedCrossRef
60.
go back to reference Zhu W, Zhang J, Singh A, Kulkarni HR, Baum RP. Metastatic nasopharyngeal carcinoma treated with intraarterial combined with intravenous peptide receptor radionuclide therapy. Clin Nucl Med. 2019;44:989–90.PubMedCrossRef Zhu W, Zhang J, Singh A, Kulkarni HR, Baum RP. Metastatic nasopharyngeal carcinoma treated with intraarterial combined with intravenous peptide receptor radionuclide therapy. Clin Nucl Med. 2019;44:989–90.PubMedCrossRef
61.
go back to reference Junttila MR, de Sauvage FJ. Influence of tumour micro-environment heterogeneity on therapeutic response. Nature. 2013;501:346–54.PubMedCrossRef Junttila MR, de Sauvage FJ. Influence of tumour micro-environment heterogeneity on therapeutic response. Nature. 2013;501:346–54.PubMedCrossRef
63.
go back to reference Curry JM, Sprandio J, Cognetti D, Luginbuhl A, Bar-ad V, Pribitkin E, et al. Tumor microenvironment in head and neck squamous cell carcinoma. Semin Oncol. 2014;41:217–34.PubMedCrossRef Curry JM, Sprandio J, Cognetti D, Luginbuhl A, Bar-ad V, Pribitkin E, et al. Tumor microenvironment in head and neck squamous cell carcinoma. Semin Oncol. 2014;41:217–34.PubMedCrossRef
64.
go back to reference Kim J, Bae J-S. Tumor-associated macrophages and neutrophils in tumor microenvironment. Mediators Inflamm. 2016;2016:6058147.PubMedPubMedCentral Kim J, Bae J-S. Tumor-associated macrophages and neutrophils in tumor microenvironment. Mediators Inflamm. 2016;2016:6058147.PubMedPubMedCentral
65.
go back to reference Peltanova B, Raudenska M, Masarik M. Effect of tumor microenvironment on pathogenesis of the head and neck squamous cell carcinoma: a systematic review. Mol Cancer. 2019;18:63.PubMedPubMedCentralCrossRef Peltanova B, Raudenska M, Masarik M. Effect of tumor microenvironment on pathogenesis of the head and neck squamous cell carcinoma: a systematic review. Mol Cancer. 2019;18:63.PubMedPubMedCentralCrossRef
66.
67.
go back to reference Bussard KM, Mutkus L, Stumpf K, Gomez-Manzano C, Marini FC. Tumor-associated stromal cells as key contributors to the tumor microenvironment. Breast Cancer Res. 2016;18:84.PubMedPubMedCentralCrossRef Bussard KM, Mutkus L, Stumpf K, Gomez-Manzano C, Marini FC. Tumor-associated stromal cells as key contributors to the tumor microenvironment. Breast Cancer Res. 2016;18:84.PubMedPubMedCentralCrossRef
68.
go back to reference Hamson EJ, Keane FM, Tholen S, Schilling O, Gorrell MD. Understanding fibroblast activation protein (FAP): substrates, activities, expression and targeting for cancer therapy. Proteomics Clin Appl. 2014;8:454–63.PubMedCrossRef Hamson EJ, Keane FM, Tholen S, Schilling O, Gorrell MD. Understanding fibroblast activation protein (FAP): substrates, activities, expression and targeting for cancer therapy. Proteomics Clin Appl. 2014;8:454–63.PubMedCrossRef
69.
go back to reference Zi F, He J, He D, Li Y, Yang L, Cai Z. Fibroblast activation protein α in tumor microenvironment: recent progression and implications (review). Mol Med Rep. 2015;11:3203–11.PubMedPubMedCentralCrossRef Zi F, He J, He D, Li Y, Yang L, Cai Z. Fibroblast activation protein α in tumor microenvironment: recent progression and implications (review). Mol Med Rep. 2015;11:3203–11.PubMedPubMedCentralCrossRef
70.
go back to reference Jansen K, Heirbaut L, Verkerk R, Cheng JD, Joossens J, Cos P, et al. Extended structure-activity relationship and pharmacokinetic investigation of (4-quinolinoyl)glycyl-2-cyanopyrrolidine inhibitors of fibroblast activation protein (FAP). J Med Chem. 2014;57:3053–74.PubMedCrossRef Jansen K, Heirbaut L, Verkerk R, Cheng JD, Joossens J, Cos P, et al. Extended structure-activity relationship and pharmacokinetic investigation of (4-quinolinoyl)glycyl-2-cyanopyrrolidine inhibitors of fibroblast activation protein (FAP). J Med Chem. 2014;57:3053–74.PubMedCrossRef
71.
go back to reference Kratochwil C, Flechsig P, Lindner T, Abderrahim L, Altmann A, Mier W, et al. 68Ga-FAPI PET/CT: tracer uptake in 28 different kinds of cancer. J Nucl Med Offl Publ Soc Nucl Med. 2019;60:801–5. Kratochwil C, Flechsig P, Lindner T, Abderrahim L, Altmann A, Mier W, et al. 68Ga-FAPI PET/CT: tracer uptake in 28 different kinds of cancer. J Nucl Med Offl Publ Soc Nucl Med. 2019;60:801–5.
72.
go back to reference Lindner T, Loktev A, Altmann A, Giesel F, Kratochwil C, Debus J, et al. Development of quinoline-based theranostic ligands for the targeting of fibroblast activation protein. J Nucl Med Offl Publ Soc Nucl Med. 2018;59:1415–22. Lindner T, Loktev A, Altmann A, Giesel F, Kratochwil C, Debus J, et al. Development of quinoline-based theranostic ligands for the targeting of fibroblast activation protein. J Nucl Med Offl Publ Soc Nucl Med. 2018;59:1415–22.
73.
go back to reference Giesel FL, Kratochwil C, Lindner T, Marschalek MM, Loktev A, Lehnert W, et al. 68Ga-FAPI PET/CT: biodistribution and preliminary dosimetry estimate of 2 DOTA-containing FAP-targeting agents in patients with various cancers. J Nucl Med. 2019;60:386–92.PubMedPubMedCentralCrossRef Giesel FL, Kratochwil C, Lindner T, Marschalek MM, Loktev A, Lehnert W, et al. 68Ga-FAPI PET/CT: biodistribution and preliminary dosimetry estimate of 2 DOTA-containing FAP-targeting agents in patients with various cancers. J Nucl Med. 2019;60:386–92.PubMedPubMedCentralCrossRef
74.
go back to reference Serfling S, Zhi Y, Schirbel A, Lindner T, Meyer T, Gerhard-Hartmann E, et al. Improved cancer detection in Waldeyer’s tonsillar ring by 68Ga-FAPI PET/CT imaging. Eur J Nucl Med Mol Imaging. 2021;48:1178–87.PubMedCrossRef Serfling S, Zhi Y, Schirbel A, Lindner T, Meyer T, Gerhard-Hartmann E, et al. Improved cancer detection in Waldeyer’s tonsillar ring by 68Ga-FAPI PET/CT imaging. Eur J Nucl Med Mol Imaging. 2021;48:1178–87.PubMedCrossRef
75.
go back to reference Ballal S, Yadav MP, Moon ES, Kramer VS, Roesch F, Kumari S, et al. Biodistribution, pharmacokinetics, dosimetry of [68Ga]Ga-DOTA.SA.FAPi, and the head-to-head comparison with [18F]F-FDG PET/CT in patients with various cancers. Eur J Nucl Med Mol Imaging. 2021;48:1915–31.PubMedCrossRef Ballal S, Yadav MP, Moon ES, Kramer VS, Roesch F, Kumari S, et al. Biodistribution, pharmacokinetics, dosimetry of [68Ga]Ga-DOTA.SA.FAPi, and the head-to-head comparison with [18F]F-FDG PET/CT in patients with various cancers. Eur J Nucl Med Mol Imaging. 2021;48:1915–31.PubMedCrossRef
76.
go back to reference Chen H, Zhao L, Ruan D, Pang Y, Hao B, Dai Y, et al. Usefulness of [68Ga]Ga-DOTA-FAPI-04 PET/CT in patients presenting with inconclusive [18F]FDG PET/CT findings. Eur J Nucl Med Mol Imaging. 2021;48:73–86.PubMedCrossRef Chen H, Zhao L, Ruan D, Pang Y, Hao B, Dai Y, et al. Usefulness of [68Ga]Ga-DOTA-FAPI-04 PET/CT in patients presenting with inconclusive [18F]FDG PET/CT findings. Eur J Nucl Med Mol Imaging. 2021;48:73–86.PubMedCrossRef
77.
go back to reference Gu B, Xu X, Zhang J, Ou X, Xia Z, Guan Q, et al. The added value of 68Ga-FAPI-04 PET/CT in patients with head and neck cancer of unknown primary with 18 F-FDG negative findings. J Nucl Med. 2022;63:875–81.PubMedCrossRef Gu B, Xu X, Zhang J, Ou X, Xia Z, Guan Q, et al. The added value of 68Ga-FAPI-04 PET/CT in patients with head and neck cancer of unknown primary with 18 F-FDG negative findings. J Nucl Med. 2022;63:875–81.PubMedCrossRef
78.
go back to reference Syed M, Flechsig P, Liermann J, Windisch P, Staudinger F, Akbaba S, et al. Fibroblast activation protein inhibitor (FAPI) PET for diagnostics and advanced targeted radiotherapy in head and neck cancers. Eur J Nucl Med Mol Imaging. 2020;47:2836–45.PubMedPubMedCentralCrossRef Syed M, Flechsig P, Liermann J, Windisch P, Staudinger F, Akbaba S, et al. Fibroblast activation protein inhibitor (FAPI) PET for diagnostics and advanced targeted radiotherapy in head and neck cancers. Eur J Nucl Med Mol Imaging. 2020;47:2836–45.PubMedPubMedCentralCrossRef
79.
go back to reference Zhao L, Pang Y, Zheng H, Han C, Gu J, Sun L, et al. Clinical utility of [68Ga]Ga-labeled fibroblast activation protein inhibitor (FAPI) positron emission tomography/computed tomography for primary staging and recurrence detection in nasopharyngeal carcinoma. Eur J Nucl Med Mol Imaging. 2021;48:3606–17.PubMedCrossRef Zhao L, Pang Y, Zheng H, Han C, Gu J, Sun L, et al. Clinical utility of [68Ga]Ga-labeled fibroblast activation protein inhibitor (FAPI) positron emission tomography/computed tomography for primary staging and recurrence detection in nasopharyngeal carcinoma. Eur J Nucl Med Mol Imaging. 2021;48:3606–17.PubMedCrossRef
80.
go back to reference Linz C, Brands RC, Kertels O, Dierks A, Brumberg J, Gerhard-Hartmann E, et al. Targeting fibroblast activation protein in newly diagnosed squamous cell carcinoma of the oral cavity—initial experience and comparison to [18F]FDG PET/CT and MRI. Eur J Nucl Med Mol Imaging. 2021;48:3951–60.PubMedPubMedCentralCrossRef Linz C, Brands RC, Kertels O, Dierks A, Brumberg J, Gerhard-Hartmann E, et al. Targeting fibroblast activation protein in newly diagnosed squamous cell carcinoma of the oral cavity—initial experience and comparison to [18F]FDG PET/CT and MRI. Eur J Nucl Med Mol Imaging. 2021;48:3951–60.PubMedPubMedCentralCrossRef
82.
go back to reference Chen H, Pang Y, Wu J, Zhao L, Hao B, Wu J, et al. Comparison of [68Ga]Ga-DOTA-FAPI-04 and [18F] 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;47:1820–32.PubMedCrossRef Chen H, Pang Y, Wu J, Zhao L, Hao B, Wu J, et al. Comparison of [68Ga]Ga-DOTA-FAPI-04 and [18F] 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;47:1820–32.PubMedCrossRef
83.
go back to reference Qin C, Liu F, Huang J, Ruan W, Liu Q, Gai Y, et al. A head-to-head comparison of 68Ga-DOTA-FAPI-04 and 18F-FDG PET/MR in patients with nasopharyngeal carcinoma: a prospective study. Eur J Nucl Med Mol Imaging. 2021;48:3228–37.PubMedCrossRef Qin C, Liu F, Huang J, Ruan W, Liu Q, Gai Y, et al. A head-to-head comparison of 68Ga-DOTA-FAPI-04 and 18F-FDG PET/MR in patients with nasopharyngeal carcinoma: a prospective study. Eur J Nucl Med Mol Imaging. 2021;48:3228–37.PubMedCrossRef
84.
go back to reference Whiteside TL. Head and neck carcinoma immunotherapy: facts and hopes. Clin Cancer Res. 2018;24:6–13.PubMedCrossRef Whiteside TL. Head and neck carcinoma immunotherapy: facts and hopes. Clin Cancer Res. 2018;24:6–13.PubMedCrossRef
85.
go back to reference Ferris RL, Blumenschein G, Fayette J, Guigay J, Colevas AD, Licitra L, et al. Nivolumab for recurrent squamous-cell carcinoma of the head and neck. N Engl J Med. 2016;375:1856–67.PubMedPubMedCentralCrossRef Ferris RL, Blumenschein G, Fayette J, Guigay J, Colevas AD, Licitra L, et al. Nivolumab for recurrent squamous-cell carcinoma of the head and neck. N Engl J Med. 2016;375:1856–67.PubMedPubMedCentralCrossRef
86.
go back to reference Cohen EEW, Soulières D, Le Tourneau C, Dinis J, Licitra L, Ahn M-J, et al. Pembrolizumab versus methotrexate, docetaxel, or cetuximab for recurrent or metastatic head-and-neck squamous cell carcinoma (KEYNOTE-040): a randomised, open-label, phase 3 study. Lancet (London, England). 2019;393:156–67.CrossRef Cohen EEW, Soulières D, Le Tourneau C, Dinis J, Licitra L, Ahn M-J, et al. Pembrolizumab versus methotrexate, docetaxel, or cetuximab for recurrent or metastatic head-and-neck squamous cell carcinoma (KEYNOTE-040): a randomised, open-label, phase 3 study. Lancet (London, England). 2019;393:156–67.CrossRef
87.
go back to reference Seiwert TY, Burtness B, Mehra R, Weiss J, Berger R, Eder JP, et al. Safety and clinical activity of pembrolizumab for treatment of recurrent or metastatic squamous cell carcinoma of the head and neck (KEYNOTE-012): an open-label, multicentre, phase 1b trial. Lancet Oncol. 2016;17:956–65.PubMedCrossRef Seiwert TY, Burtness B, Mehra R, Weiss J, Berger R, Eder JP, et al. Safety and clinical activity of pembrolizumab for treatment of recurrent or metastatic squamous cell carcinoma of the head and neck (KEYNOTE-012): an open-label, multicentre, phase 1b trial. Lancet Oncol. 2016;17:956–65.PubMedCrossRef
88.
go back to reference Siu LL, Even C, Mesía R, Remenar E, Daste A, Delord J-P, et al. Safety and efficacy of durvalumab with or without tremelimumab in patients with PD-L1–low/negative recurrent or metastatic HNSCC. JAMA Oncol. 2019;5:195–203.PubMedCrossRef Siu LL, Even C, Mesía R, Remenar E, Daste A, Delord J-P, et al. Safety and efficacy of durvalumab with or without tremelimumab in patients with PD-L1–low/negative recurrent or metastatic HNSCC. JAMA Oncol. 2019;5:195–203.PubMedCrossRef
89.
go back to reference Herbst RS, Soria J-C, Kowanetz M, Fine GD, Hamid O, Gordon MS, et al. Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients. Nature. 2014;515:563–7.PubMedPubMedCentralCrossRef Herbst RS, Soria J-C, Kowanetz M, Fine GD, Hamid O, Gordon MS, et al. Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients. Nature. 2014;515:563–7.PubMedPubMedCentralCrossRef
90.
go back to reference Gentzler R, Hall R, Kunk PR, Gaughan E, Dillon P, Slingluff CL, et al. Beyond melanoma: inhibiting the PD-1/PD-L1 pathway in solid tumors. Immunotherapy. 2016;8:583–600.PubMedCrossRef Gentzler R, Hall R, Kunk PR, Gaughan E, Dillon P, Slingluff CL, et al. Beyond melanoma: inhibiting the PD-1/PD-L1 pathway in solid tumors. Immunotherapy. 2016;8:583–600.PubMedCrossRef
91.
go back to reference van der Veen EL, Bensch F, Glaudemans AWJM, Lub-de Hooge MN, de Vries EGE. Molecular imaging to enlighten cancer immunotherapies and underlying involved processes. Cancer Treat Rev. 2018;70:232–44.PubMedCrossRef van der Veen EL, Bensch F, Glaudemans AWJM, Lub-de Hooge MN, de Vries EGE. Molecular imaging to enlighten cancer immunotherapies and underlying involved processes. Cancer Treat Rev. 2018;70:232–44.PubMedCrossRef
92.
go back to reference England CG, Jiang D, Ehlerding EB, Rekoske BT, Ellison PA, Hernandez R, et al. 89Zr-labeled nivolumab for imaging of T-cell infiltration in a humanized murine model of lung cancer. Eur J Nucl Med Mol Imaging. 2018;45:110–20.PubMedCrossRef England CG, Jiang D, Ehlerding EB, Rekoske BT, Ellison PA, Hernandez R, et al. 89Zr-labeled nivolumab for imaging of T-cell infiltration in a humanized murine model of lung cancer. Eur J Nucl Med Mol Imaging. 2018;45:110–20.PubMedCrossRef
93.
go back to reference Li D, Cheng S, Zou S, Zhu D, Zhu T, Wang P, et al. Immuno-PET imaging of 89Zr labeled anti-PD-L1 domain antibody. Mol Pharm. 2018;15:1674–81.PubMedCrossRef Li D, Cheng S, Zou S, Zhu D, Zhu T, Wang P, et al. Immuno-PET imaging of 89Zr labeled anti-PD-L1 domain antibody. Mol Pharm. 2018;15:1674–81.PubMedCrossRef
94.
go back to reference Maute RL, Gordon SR, Mayer AT, McCracken MN, Natarajan A, Ring NG, et al. Engineering high-affinity PD-1 variants for optimized immunotherapy and immuno-PET imaging. Proc Natl Acad Sci USA. 2015;112:E6506–14.PubMedPubMedCentralCrossRef Maute RL, Gordon SR, Mayer AT, McCracken MN, Natarajan A, Ring NG, et al. Engineering high-affinity PD-1 variants for optimized immunotherapy and immuno-PET imaging. Proc Natl Acad Sci USA. 2015;112:E6506–14.PubMedPubMedCentralCrossRef
95.
go back to reference Bensch F, van der Veen EL, Lub-de Hooge MN, Jorritsma-Smit A, Boellaard R, Kok IC, et al. (89)Zr-atezolizumab imaging as a non-invasive approach to assess clinical response to PD-L1 blockade in cancer. Nat Med. 2018;24:1852–8.PubMedCrossRef Bensch F, van der Veen EL, Lub-de Hooge MN, Jorritsma-Smit A, Boellaard R, Kok IC, et al. (89)Zr-atezolizumab imaging as a non-invasive approach to assess clinical response to PD-L1 blockade in cancer. Nat Med. 2018;24:1852–8.PubMedCrossRef
96.
go back to reference Li D, Li X, Yang J, Shi Z, Zhang L, Li R, et al. Nivolumab-DTPA-based PD-1 imaging reveals structural and pathological changes in colorectal carcinoma. Front Bioeng Biotechnol. 2022;10: 839756.PubMedPubMedCentralCrossRef Li D, Li X, Yang J, Shi Z, Zhang L, Li R, et al. Nivolumab-DTPA-based PD-1 imaging reveals structural and pathological changes in colorectal carcinoma. Front Bioeng Biotechnol. 2022;10: 839756.PubMedPubMedCentralCrossRef
97.
go back to reference Li D, Wang C, Zhang D, Peng Y, Ren S, Li X, et al. Preliminary application of 125I–nivolumab to detect PD-1 expression in colon cancer via SPECT. J Radioanal Nucl Chem. 2018;318:1237–42.CrossRef Li D, Wang C, Zhang D, Peng Y, Ren S, Li X, et al. Preliminary application of 125I–nivolumab to detect PD-1 expression in colon cancer via SPECT. J Radioanal Nucl Chem. 2018;318:1237–42.CrossRef
99.
go back to reference Oweida A, Lennon S, Calame D, Korpela S, Bhatia S, Sharma J, et al. Ionizing radiation sensitizes tumors to PD-L1 immune checkpoint blockade in orthotopic murine head and neck squamous cell carcinoma. Oncoimmunology. 2017;6: e1356153.PubMedPubMedCentralCrossRef Oweida A, Lennon S, Calame D, Korpela S, Bhatia S, Sharma J, et al. Ionizing radiation sensitizes tumors to PD-L1 immune checkpoint blockade in orthotopic murine head and neck squamous cell carcinoma. Oncoimmunology. 2017;6: e1356153.PubMedPubMedCentralCrossRef
100.
go back to reference Oweida A, Hararah MK, Phan A, Binder D, Bhatia S, Lennon S, et al. Resistance to radiotherapy and PD-L1 blockade is mediated by TIM-3 upregulation and regulatory T-Cell infiltration. Clin Cancer Res. 2018;24:5368–80.PubMedPubMedCentralCrossRef Oweida A, Hararah MK, Phan A, Binder D, Bhatia S, Lennon S, et al. Resistance to radiotherapy and PD-L1 blockade is mediated by TIM-3 upregulation and regulatory T-Cell infiltration. Clin Cancer Res. 2018;24:5368–80.PubMedPubMedCentralCrossRef
101.
go back to reference Kikuchi M, Clump DA, Srivastava RM, Sun L, Zeng D, Diaz-Perez JA, et al. Preclinical immunoPET/CT imaging using Zr-89-labeled anti-PD-L1 monoclonal antibody for assessing radiation-induced PD-L1 upregulation in head and neck cancer and melanoma. Oncoimmunology. 2017;6: e1329071.PubMedPubMedCentralCrossRef Kikuchi M, Clump DA, Srivastava RM, Sun L, Zeng D, Diaz-Perez JA, et al. Preclinical immunoPET/CT imaging using Zr-89-labeled anti-PD-L1 monoclonal antibody for assessing radiation-induced PD-L1 upregulation in head and neck cancer and melanoma. Oncoimmunology. 2017;6: e1329071.PubMedPubMedCentralCrossRef
102.
103.
go back to reference Debordeaux F, Chansel-Debordeaux L, Pinaquy J-B, Fernandez P, Schulz J. What about αvβ3 integrins in molecular imaging in oncology? Nucl Med Biol. 2018;62–63:31–46.PubMedCrossRef Debordeaux F, Chansel-Debordeaux L, Pinaquy J-B, Fernandez P, Schulz J. What about αvβ3 integrins in molecular imaging in oncology? Nucl Med Biol. 2018;62–63:31–46.PubMedCrossRef
104.
go back to reference Fabricius E-M, Wildner G-P, Kruse-Boitschenko U, Hoffmeister B, Goodman SL, Raguse J-D. Immunohistochemical analysis of integrins αvβ3, αvβ5 and α5β1, and their ligands, fibrinogen, fibronectin, osteopontin and vitronectin, in frozen sections of human oral head and neck squamous cell carcinomas. Exp Ther Med. 2011;2:9–19.PubMedCrossRef Fabricius E-M, Wildner G-P, Kruse-Boitschenko U, Hoffmeister B, Goodman SL, Raguse J-D. Immunohistochemical analysis of integrins αvβ3, αvβ5 and α5β1, and their ligands, fibrinogen, fibronectin, osteopontin and vitronectin, in frozen sections of human oral head and neck squamous cell carcinomas. Exp Ther Med. 2011;2:9–19.PubMedCrossRef
105.
go back to reference Ahmedah HT, Patterson LH, Shnyder SD, Sheldrake HM. RGD-binding integrins in head and neck cancers. Cancers (Basel). 2017;9:56.PubMedCentralCrossRef Ahmedah HT, Patterson LH, Shnyder SD, Sheldrake HM. RGD-binding integrins in head and neck cancers. Cancers (Basel). 2017;9:56.PubMedCentralCrossRef
106.
go back to reference Nieberler M, Reuning U, Reichart F, Notni J, Wester H-J, Schwaiger M, et al. Exploring the role of RGD-recognizing integrins in cancer. Cancers. 2017;9:116.PubMedCentralCrossRef Nieberler M, Reuning U, Reichart F, Notni J, Wester H-J, Schwaiger M, et al. Exploring the role of RGD-recognizing integrins in cancer. Cancers. 2017;9:116.PubMedCentralCrossRef
107.
go back to reference Beer AJ, Grosu A-L, Carlsen J, Kolk A, Sarbia M, Stangier I, et al. [18F]galacto-RGD positron emission tomography for imaging of alphavbeta3 expression on the neovasculature in patients with squamous cell carcinoma of the head and neck. Clin Cancer Res Offl J Am Assoc Cancer Res. 2007;13:6610–6.CrossRef Beer AJ, Grosu A-L, Carlsen J, Kolk A, Sarbia M, Stangier I, et al. [18F]galacto-RGD positron emission tomography for imaging of alphavbeta3 expression on the neovasculature in patients with squamous cell carcinoma of the head and neck. Clin Cancer Res Offl J Am Assoc Cancer Res. 2007;13:6610–6.CrossRef
108.
go back to reference Lobeek D, Rijpkema M, Terry SYA, Molkenboer-Kuenen JDM, Joosten L, van Genugten EAJ, et al. Imaging angiogenesis in patients with head and neck squamous cell carcinomas by [68Ga]Ga-DOTA-E-[c(RGDfK)]2 PET/CT. Eur J Nucl Med Mol Imaging. 2020;47:2647–55.PubMedPubMedCentralCrossRef Lobeek D, Rijpkema M, Terry SYA, Molkenboer-Kuenen JDM, Joosten L, van Genugten EAJ, et al. Imaging angiogenesis in patients with head and neck squamous cell carcinomas by [68Ga]Ga-DOTA-E-[c(RGDfK)]2 PET/CT. Eur J Nucl Med Mol Imaging. 2020;47:2647–55.PubMedPubMedCentralCrossRef
109.
go back to reference Durante S, Dunet V, Gorostidi F, Mitsakis P, Schaefer N, Delage J, et al. Head and neck tumors angiogenesis imaging with 68Ga-NODAGA-RGD in comparison to 18F-FDG PET/CT: a pilot study. EJNMMI Res. 2020;10:47.PubMedPubMedCentralCrossRef Durante S, Dunet V, Gorostidi F, Mitsakis P, Schaefer N, Delage J, et al. Head and neck tumors angiogenesis imaging with 68Ga-NODAGA-RGD in comparison to 18F-FDG PET/CT: a pilot study. EJNMMI Res. 2020;10:47.PubMedPubMedCentralCrossRef
110.
go back to reference Ansari MJ, Bokov D, Markov A, Jalil AT, Shalaby MN, Suksatan W, et al. Cancer combination therapies by angiogenesis inhibitors; a comprehensive review. Cell Commun Signal. 2022;20:49.PubMedPubMedCentralCrossRef Ansari MJ, Bokov D, Markov A, Jalil AT, Shalaby MN, Suksatan W, et al. Cancer combination therapies by angiogenesis inhibitors; a comprehensive review. Cell Commun Signal. 2022;20:49.PubMedPubMedCentralCrossRef
111.
go back to reference Terry SYA, Abiraj K, Lok J, Gerrits D, Franssen GM, Oyen WJG, et al. Can 111In-RGD2 monitor response to therapy in head and neck tumor xenografts? J Nucl Med Offl Publ Soc Nucl Med. 2014;55:1849–55. Terry SYA, Abiraj K, Lok J, Gerrits D, Franssen GM, Oyen WJG, et al. Can 111In-RGD2 monitor response to therapy in head and neck tumor xenografts? J Nucl Med Offl Publ Soc Nucl Med. 2014;55:1849–55.
112.
go back to reference Rylova SN, Barnucz E, Fani M, Braun F, Werner M, Lassmann S, et al. Does imaging αvβ3 integrin expression with PET detect changes in angiogenesis during bevacizumab therapy? J Nucl Med Offl Publ Soc Nucl Med. 2014;55:1878–84. Rylova SN, Barnucz E, Fani M, Braun F, Werner M, Lassmann S, et al. Does imaging αvβ3 integrin expression with PET detect changes in angiogenesis during bevacizumab therapy? J Nucl Med Offl Publ Soc Nucl Med. 2014;55:1878–84.
113.
go back to reference Chen S-H, Wang H-M, Lin C-Y, Chang JT-C, Hsieh C-H, Liao C-T, et al. RGD-K5 PET/CT in patients with advanced head and neck cancer treated with concurrent chemoradiotherapy: Results from a pilot study. Eur J Nucl Med Mol Imaging. 2016;43:1621–9.PubMedCrossRef Chen S-H, Wang H-M, Lin C-Y, Chang JT-C, Hsieh C-H, Liao C-T, et al. RGD-K5 PET/CT in patients with advanced head and neck cancer treated with concurrent chemoradiotherapy: Results from a pilot study. Eur J Nucl Med Mol Imaging. 2016;43:1621–9.PubMedCrossRef
114.
go back to reference Roesch S, Lindner T, Sauter M, Loktev A, Flechsig P, Müller M, et al. Comparison of the RGD motif-containing αvβ6 integrin-binding peptides SFLAP3 and SFITGv6 for diagnostic application in HNSCC. J Nucl Med Offl Publ Soc Nucl Med. 2018;59:1679–85. Roesch S, Lindner T, Sauter M, Loktev A, Flechsig P, Müller M, et al. Comparison of the RGD motif-containing αvβ6 integrin-binding peptides SFLAP3 and SFITGv6 for diagnostic application in HNSCC. J Nucl Med Offl Publ Soc Nucl Med. 2018;59:1679–85.
115.
go back to reference Quigley NG, Steiger K, Hoberück S, Czech N, Zierke MA, Kossatz S, et al. PET/CT imaging of head-and-neck and pancreatic cancer in humans by targeting the "Cancer Integrin" αvβ6 with Ga-68-Trivehexin. Eur J Nucl Med Mol Imaging. 2021. Quigley NG, Steiger K, Hoberück S, Czech N, Zierke MA, Kossatz S, et al. PET/CT imaging of head-and-neck and pancreatic cancer in humans by targeting the "Cancer Integrin" αvβ6 with Ga-68-Trivehexin. Eur J Nucl Med Mol Imaging. 2021.
117.
go back to reference Virgolini I, Decristoforo C, Haug A, Fanti S, Uprimny C. Current status of theranostics in prostate cancer. Eur J Nucl Med Mol Imaging. 2018;45:471–95.PubMedCrossRef Virgolini I, Decristoforo C, Haug A, Fanti S, Uprimny C. Current status of theranostics in prostate cancer. Eur J Nucl Med Mol Imaging. 2018;45:471–95.PubMedCrossRef
118.
go back to reference Chang SS, O’Keefe DS, Bacich DJ, Reuter VE, Heston WDW, Gaudin PB. Prostate-specific membrane antigen is produced in tumor- associated neovasculature. Clin Cancer Res. 1999;5(10):2674–81.PubMed Chang SS, O’Keefe DS, Bacich DJ, Reuter VE, Heston WDW, Gaudin PB. Prostate-specific membrane antigen is produced in tumor- associated neovasculature. Clin Cancer Res. 1999;5(10):2674–81.PubMed
119.
go back to reference Haffner MC, Laimer J, Chaux A, Schäfer G, Obrist P, Brunner A, et al. High expression of prostate-specific membrane antigen in the tumor-associated neo-vasculature is associated with worse prognosis in squamous cell carcinoma of the oral cavity. Mod Pathol. 2012;25:1079–85.PubMedCrossRef Haffner MC, Laimer J, Chaux A, Schäfer G, Obrist P, Brunner A, et al. High expression of prostate-specific membrane antigen in the tumor-associated neo-vasculature is associated with worse prognosis in squamous cell carcinoma of the oral cavity. Mod Pathol. 2012;25:1079–85.PubMedCrossRef
120.
go back to reference Pandit-Taskar N, O’Donoghue JA, Divgi CR, Wills EA, Schwartz L, Gönen M, et al. Indium 111-labeled J591 anti-PSMA antibody for vascular targeted imaging in progressive solid tumors. EJNMMI Res. 2015;5:28.PubMedPubMedCentralCrossRef Pandit-Taskar N, O’Donoghue JA, Divgi CR, Wills EA, Schwartz L, Gönen M, et al. Indium 111-labeled J591 anti-PSMA antibody for vascular targeted imaging in progressive solid tumors. EJNMMI Res. 2015;5:28.PubMedPubMedCentralCrossRef
121.
go back to reference Lawhn-Heath C, Flavell RR, Glastonbury C, Hope TA, Behr SC. Incidental detection of head and neck squamous cell carcinoma on 68Ga-PSMA-11 PET/CT. Clin Nucl Med. 2017;42:e218–20.PubMedCrossRef Lawhn-Heath C, Flavell RR, Glastonbury C, Hope TA, Behr SC. Incidental detection of head and neck squamous cell carcinoma on 68Ga-PSMA-11 PET/CT. Clin Nucl Med. 2017;42:e218–20.PubMedCrossRef
122.
go back to reference Osman MM, Iravani A, Hicks RJ, Hofman MS. Detection of synchronous primary malignancies with 68Ga-labeled prostate-specific membrane antigen PET/CT in patients with prostate cancer: frequency in 764 patients. J Nucl Med. 2017;58:1938–42.PubMedCrossRef Osman MM, Iravani A, Hicks RJ, Hofman MS. Detection of synchronous primary malignancies with 68Ga-labeled prostate-specific membrane antigen PET/CT in patients with prostate cancer: frequency in 764 patients. J Nucl Med. 2017;58:1938–42.PubMedCrossRef
Metadata
Title
Advances in nuclear medicine-based molecular imaging in head and neck squamous cell carcinoma
Authors
Danni Li
Xuran Li
Jun Zhao
Fei Tan
Publication date
01-12-2022
Publisher
BioMed Central
Published in
Journal of Translational Medicine / Issue 1/2022
Electronic ISSN: 1479-5876
DOI
https://doi.org/10.1186/s12967-022-03559-5

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