Skip to main content

Advertisement

SpringerLink
Log in

Nanoparticles labeled with gamma-emitting radioisotopes: an attractive approach for in vivo tracking using SPECT imaging

  • Review Article
  • Published:
Drug Delivery and Translational Research Aims and scope Submit manuscript

Abstract

Providing accurate molecular imaging of the body and biological process is critical for diagnosing disease and personalizing treatment with the minimum side effects. Recently, diagnostic radiopharmaceuticals have gained more attention in precise molecular imaging due to their high sensitivity and appropriate tissue penetration depth. The fate of these radiopharmaceuticals throughout the body can be traced using nuclear imaging systems, including single-photon emission computed tomography (SPECT) and positron emission tomography (PET) modalities. In this regard, nanoparticles are attractive platforms for delivering radionuclides into targets because they can directly interfere with the cell membranes and subcellular organelles. Moreover, applying radiolabeled nanomaterials can decrease their toxicity concerns because radiopharmaceuticals are usually administrated at low doses. Therefore, incorporating gamma-emitting radionuclides into nanomaterials can provide imaging probes with valuable additional properties compared to the other carriers. Herein, we aim to review (1) the gamma-emitting radionuclides used for labeling different nanomaterials, (2) the approaches and conditions adopted for their radiolabeling, and (3) their application. This study can help researchers to compare different radiolabeling methods in terms of stability and efficiency and choose the best way for each nanosystem.

Graphical Abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

Availability of data and materials

No datasets were generated or analyzed during the current study.

Abbreviations

ADA:

Amino diatrizoic acid

APTES:

(3-Aminopropyl)triethoxysilane

APTMS:

3-Aminopropyltrimethoxysilane

AuNP:

Au nanoparticle

BAT:

6-[P-(bromoacetamido)benzyl]-1,4,8,11-tetraazacyclotetradecane-N,N′,N″,N″′-tetraacetic acid

BFC (BFCA):

Bifunctional chelating agent

BMEDA:

N,N-bis(2-mercaptoethyl)-N0,N0-diethyl-ethylenediamine

BSA:

Bovine serum albumin

CNS:

Carbon nanospheres

CNTs:

Carbon nanotubes

CT:

Computed tomography

CTAC:

Cetyltrimethylammonium chloride

CuS NPs:

Copper sulfide nanoparticles

Cys:

Cysteine

DAP:

Diaminopropionic acid

DARPins G3:

Designed ankyrin repeat proteins

DBCO:

Dibenzocyclooctyne

Df (DFO):

Deferoxamine

DO3A:

1,4,7-Tris(carboxymethylaza)cyclododecane-10-azaacetyl

DMSA:

Dimercaptosuccinic acid

DOTA:

(1,4,7,10-Tetra-azacyclododecane-1,4,7,10-tetraacetic acid)

DPA:

Dipicolylamine

DSPC:

1,2-Distearoyl-Sn-glycero-3-phosphocholine

DSPE:

1,2-Distearoyl-Sn-glycero-3-phosphorylethanolamine

DSPG:

1,2-Distearoyl-Sn-glycero-3-phosphoglycerol

DTC:

Dithiocarbamate

DTPA:

Diethylenetriaminepentaacetic acid

DTPA-PE:

DTPA-phosphatidylethanolamine

EDDA:

N,N-ethylene diamine diacetic acid

EDTA:

Ethylenediaminetetraacetic acid

EGFR:

Epidermal growth factor receptor

EPR:

Enhanced permeability and retention

[18F]-FCP:

[18F]-fluorinated carboplatin

[18F]-FDP :

3-[18F]-fluoro-1,2-dipalmitoylglycerol

[18F]FET:

[18F]fluoroethyl tosylate

FL:

Fluorescence

GGC:

Glycine glycine cysteine

Gly:

Glycine

GNGR:

Glycine-asparagine-glycine-aspartate

GO:

Graphene oxide

GSH:

Glutathione

HAS:

Human serum albumin

HMPAO:

Hexamethylpropyleneamine oxime

HYNIC-TOC:

Hydrazinonicotinyl-Tyr3-octreotide

IONPs:

Iron oxide nanoparticles

MnOx:

Manganese oxide

MNPs:

Magnetic nanoparticles

MRI:

Magnetic resonance imaging

MSH:

Alpha melanocyte stimulating hormone

MSNs:

Mesoporous silica nanoparticles

NETA-DBCO:

2,2′-((6-Amino-1-(4,7-bis(carboxymethyl)-1,4,7-triazonan-1-yl)hexan-2-yl) azanediyl) diacetic acid-dibenzocyclooctyne

NIR:

Near-infrared

NIRF:

Near-infrared fluorescence

NOC:

NaI(3)-octreotide

NODAGA:

1,4,7-Triazacyclononane,1-glutaric acid-4,7-acetic acid

NOTA:

1,4,7-Triazacyclononane-1,4,7-triacetic acid

NT:

Neurotensin

NTA:

Nitrilotriacetic acid

OPSS-PEG2K-NH:

Opyridyldisulfide-polyethylene glycol 2000-N-hydroxysuccinimide ester

PAT:

Photoacoustic tomography

PAMAM:

Polyamidoamine

PET:

Positron emission tomography

PEG:

Polyethylene glycol

PLA:

Polylactic acid

PLGA:

Polylactic-co-glycolic acid

PPAA:

Polymerized allylamine

PSMA:

Prostate specific membrane antigen

PTA:

Photo acoustic

PVP:

Polyvinyl phenol

PVP:

Polyvinylpyrrolidone

QDs:

Quantum dots

RBC:

Red blood cell

RE:

Radiolabeling efficiency

RGD:

Arginine-glycine-aspartic acid

RGO:

Reduced graphene oxide

SERS:

Surface-enhanced Raman scattering

sEVs:

Small extracellular vesicles

[18F]-SFB:

N-succinimidyl-4-[18F]-fluorobenzoate

SNPs:

Silica nanoparticles

SPECT:

Single-photon emission tomography

SPIONs:

Superparamagnetic iron oxide nanoparticles

SSNPs:

Solid silica nanoparticles

[18F]SteP2 :

1-[18F]fluoro-3,6-dioxatetracosane

UCNPs:

Upconversion nanoparticles

USPIONs:

Ultra-small superparamagnetic iron oxide nanoparticles

References

  1. Bhattacharyya S, Dixit M. Metallic radionuclides in the development of diagnostic and therapeutic radiopharmaceuticals. Dalton Trans. 2011;40(23):6112–28.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. McNamara K, Tofail SA. Nanoparticles in biomedical applications. ADV PHYS-X. 2017;2(1):54–88.

    CAS  Google Scholar 

  3. Xing Y, Zhu J, Zhao L, Xiong Z, Li Y, Wu S, et al. SPECT/CT imaging of chemotherapy-induced tumor apoptosis using 99mTc-labeled dendrimer-entrapped gold nanoparticles. Drug Deliv. 2018;25(1):1384–93.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Pellico J, Gawne PJ, de Rosales RT. Radiolabelling of nanomaterials for medical imaging and therapy. Chem Soc Rev. 2021;50(5):3355–423.

    Article  CAS  PubMed  Google Scholar 

  5. Dai W, Zhang J, Wang Y, Jiao C, Song Z, Ma Y et al (2021) Radiolabeling of nanomaterials: advantages and challenges. ftox 3

  6. Kumar R, Lal S. Synthesis of organic nanoparticles and their applications in drug delivery and food nanotechnology: a review. J Nanomater Mol Nanotechnol 3: 4. of. 2014;11:2.

  7. Kang KW, Song MG. Organic nanomaterials: liposomes, albumin, dendrimer, polymeric nanoparticles: Springer. 2018.

  8. Kim EE. Radionanomedicine: combined nuclear and nanomedicine. J Nucl Med. 2019;60(6):105–7.

    Article  Google Scholar 

  9. Maruyama K. Intracellular targeting delivery of liposomal drugs to solid tumors based on EPR effects. Adv Drug Del Rev. 2011;63(3):161–9.

    Article  CAS  Google Scholar 

  10. Phillips WT, Goins BA, Bao A. Radioactive liposomes. Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology. 2009;1(1):69–83.

    CAS  PubMed  Google Scholar 

  11. Aranda-Lara L, Morales-Avila E, Luna-Gutiérrez MA, Olivé-Alvarez E, Isaac-Olivé K. Radiolabeled liposomes and lipoproteins as lipidic nanoparticles for imaging and therapy. Chem Phys Lipid. 2020;230: 104934.

    Article  CAS  Google Scholar 

  12. Dams ETM, Oyen WJ, Boerman OC, Storm G, Laverman P, Kok PJ, et al. 99mTc-PEG liposomes for the scintigraphic detection of infection and inflammation: clinical evaluation. J Nucl Med. 2000;41(4):622–30.

    CAS  PubMed  Google Scholar 

  13. Hamoudeh M, Kamleh MA, Diab R, Fessi H. Radionuclides delivery systems for nuclear imaging and radiotherapy of cancer. Adv Drug Del Rev. 2008;60(12):1329–46.

    Article  CAS  Google Scholar 

  14. Jensen GM, Bunch TH. Conventional liposome performance and evaluation: lessons from the development of Vescan. J Liposome Res. 2007;17(3–4):121–37.

    Article  CAS  PubMed  Google Scholar 

  15. Li N, Yu Z, Pham TT, Blower PJ, Yan R. A generic 89Zr labeling method to quantify the in vivo pharmacokinetics of liposomal nanoparticles with positron emission tomography. Int J Nanomed. 2017;12:3281.

    Article  CAS  Google Scholar 

  16. Espinola L, Beaucaire J, Gottschalk A, Caride V. Radiolabeled liposomes as metabolic and scanning tracers in mice. II. In-111 oxine compared with Tc-99m DTPA, entrapped in multilamellar lipid vesicles. J Nucl Med. 1979;20(5):434–40.

  17. Man F, Gawne PJ, de Rosales RTM. Nuclear imaging of liposomal drug delivery systems: a critical review of radiolabelling methods and applications in nanomedicine. Adv Drug Del Rev. 2019;143:134–60.

  18. Richardson VJ, Jeyasingh K, Jewkes R, Ryman BE, Tattersall MH. Properties of [99mTc] technetium-labelled liposomes in normal and tumour-bearing rats. Biochem Soc Trans. 1977.

  19. Richardson V, Ryman B, Jewkes R, Jeyasingh K, Tattersall M, Newlands E, et al. Tissue distribution and tumour localization of 99m-technetium-labelled liposomes in cancer patients. Br J Cancer. 1979;40(1):35–43.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Marik J, Tartis MS, Zhang H, Fung JY, Kheirolomoom A, Sutcliffe JL, et al. Long-circulating liposomes radiolabeled with [18F] fluorodipalmitin ([18F] FDP). Nucl Med Biol. 2007;34(2):165–71.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Emmetiere F, Irwin C, Viola-Villegas NT, Longo V, Cheal SM, Zanzonico P, et al. 18F-labeled-bioorthogonal liposomes for in vivo targeting. Bioconjug Chem. 2013;24(11):1784–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Urakami T, Kawaguchi AT, Akai S, Hatanaka K, Koide H, Shimizu K, et al. In vivo distribution of liposome-encapsulated hemoglobin determined by positron emission tomography. Artif Organs. 2009;33(2):164–8.

    Article  CAS  PubMed  Google Scholar 

  23. Ahkong QF, Tilcock C. Attachment of 99mTc to lipid vesicles containing the lipophilic chelate dipalmitoylphosphatidylethanolamine-DTTA. International Journal of Radiation Applications and Instrumentation Part B Nuclear Medicine and Biology. 1992;19(8):831–40.

    Article  CAS  PubMed  Google Scholar 

  24. Helbok A, Decristoforo C, Dobrozemsky G, Rangger C, Diederen E, Stark B, et al. Radiolabeling of lipid-based nanoparticles for diagnostics and therapeutic applications: a comparison using different radiometals. J Liposome Res. 2010;20(3):219–27.

    Article  CAS  PubMed  Google Scholar 

  25. Elbayoumi TA, Torchilin VP. Enhanced accumulation of long-circulating liposomes modified with the nucleosome-specific monoclonal antibody 2C5 in various tumours in mice: gamma-imaging studies. Eur J Nucl Med Mol Imaging. 2006;33(10):1196–205.

    Article  CAS  PubMed  Google Scholar 

  26. Seo JW, Mahakian LM, Kheirolomoom A, Zhang H, Meares CF, Ferdani R, et al. Liposomal Cu-64 labeling method using bifunctional chelators: poly(ethylene glycol) spacer and chelator effects. Bioconjug Chem. 2010;21(7):1206–15.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Oku N, Namba Y, Takeda A, Okada S. Tumor imaging with technetium-99m-DTPA encapsulated in RES-avoiding liposomes. Nucl Med Biol. 1993;20(4):407–12.

    Article  CAS  PubMed  Google Scholar 

  28. Proffitt RT, Williams LE, Presant CA, Tin GW, Uliana JA, Gamble RC, et al. Tumor-imaging potential of liposomes loaded with In-111-NTA: biodistribution in mice. J Nucl Med. 1983;24(1):45–51.

    CAS  PubMed  Google Scholar 

  29. Harrington KJ, Rowlinson-Busza G, Syrigos KN, Uster PS, Vile RG, Stewart JSW. Pegylated liposomes have potential as vehicles for intratumoral and subcutaneous drug delivery. Clin Cancer Res. 2000;6(6):2528–37.

    CAS  PubMed  Google Scholar 

  30. Henriksen JR, Petersen AL, Hansen AE, Frankær CG, Harris P, Elema DR, et al. Remote loading of 64Cu2+ into liposomes without the use of ion transport enhancers. ACS Appl Mater Interfaces. 2015;7(41):22796–806.

    Article  CAS  PubMed  Google Scholar 

  31. Van Der Geest T, Laverman P, Gerrits D, Franssen GM, Metselaar JM, Storm G, et al. Comparison of three remote radiolabelling methods for long-circulating liposomes. J Control Release. 2015;220:239–44.

    Article  PubMed  Google Scholar 

  32. Gawne PJ, Clarke F, Turjeman K, Cope AP, Long NJ, Barenholz Y, et al. PET imaging of liposomal glucocorticoids using 89Zr-oxine: theranostic applications in inflammatory arthritis. Theranostics. 2020;10(9):3867.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Man F, Lim L, Volpe A, Gabizon A, Shmeeda H, Draper B, et al. In vivo PET tracking of 89Zr-labeled Vγ9Vδ2 T cells to mouse xenograft breast tumors activated with liposomal alendronate. Mol Ther. 2019;27(1):219–29.

    Article  CAS  PubMed  Google Scholar 

  34. Abraham SA, Edwards K, Karlsson G, MacIntosh S, Mayer LD, McKenzie C, et al. Formation of transition metal–doxorubicin complexes inside liposomes. Biochimica et Biophysica Acta (BBA)-Biomembranes. 2002;1565(1):41–54.

  35. Gawne P, Man F, Fonslet J, Radia R, Bordoloi J, Cleveland M, et al. Manganese-52: applications in cell radiolabelling and liposomal nanomedicine PET imaging using oxine (8-hydroxyquinoline) as an ionophore. Dalton Trans. 2018;47(28):9283–93.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Edmonds S, Volpe A, Shmeeda H, Parente-Pereira AC, Radia R, Baguña-Torres J, et al. Exploiting the metal-chelating properties of the drug cargo for in vivo positron emission tomography imaging of liposomal nanomedicines. ACS Nano. 2016;10(11):10294–307.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Bao A, Goins B, Klipper R, Negrete G, Mahindaratne M, Phillips WT. A novel liposome radiolabeling method using 99mTc-“SNS/S” complexes: in vitro and in vivo evaluation. J Pharm Sci. 2003;92(9):1893–904.

    Article  CAS  PubMed  Google Scholar 

  38. Li S, Goins B, Phillips WT, Bao A. Remote-loading labeling of liposomes with 99mTc-BMEDA and its stability evaluation: effects of lipid formulation and pH/chemical gradient. J Liposome Res. 2011;21(1):17–27.

    Article  CAS  PubMed  Google Scholar 

  39. Lee H, Zheng J, Gaddy D, Orcutt KD, Leonard S, Geretti E, et al. A gradient-loadable 64Cu-chelator for quantifying tumor deposition kinetics of nanoliposomal therapeutics by positron emission tomography. Nanomed Nanotechnol Biol Med. 2015;11(1):155–65.

    Article  CAS  Google Scholar 

  40. Lee H, Shields AF, Siegel BA, Miller KD, Krop I, Ma CX, et al. 64Cu-MM-302 positron emission tomography quantifies variability of enhanced permeability and retention of nanoparticles in relation to treatment response in patients with metastatic breast cancer. Clin Cancer Res. 2017;23(15):4190–202.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Engudar G, Schaarup-Jensen H, Fliedner FP, Hansen AE, Kempen P, Jølck RI, et al. Remote loading of liposomes with a 124I-radioiodinated compound and their in vivo evaluation by PET/CT in a murine tumor model. Theranostics. 2018;8(21):5828.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Afergan E, Epstein H, Koroukhov N, Klein M, Litchi A, Mishani E, et al. Biodistribution and imaging studies of 67Ga-labeled liposomes in rabbits with a vascular injury. J Drug Deliv Sci Technol. 2009;19(4):263–8.

    Article  CAS  Google Scholar 

  43. Abou DS, Thorek DL, Ramos NN, Pinkse MW, Wolterbeek HT, Carlin SD, et al. 89 Zr-labeled paramagnetic octreotide-liposomes for PET-MR imaging of cancer. Pharm Res. 2013;30(3):878–88.

    Article  CAS  PubMed  Google Scholar 

  44. Locke LW, Mayo MW, Yoo AD, Williams MB, Berr SS. PET imaging of tumor associated macrophages using mannose coated 64Cu liposomes. Biomaterials. 2012;33(31):7785–93.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Malinge J, Géraudie B, Savel P, Nataf V, Prignon A, Provost C, et al. Liposomes for PET and MR imaging and for dual targeting (magnetic field/glucose moiety): synthesis, properties, and in vivo studies. Mol Pharm. 2017;14(2):406–14.

    Article  CAS  PubMed  Google Scholar 

  46. Oku N, Yamashita M, Katayama Y, Urakami T, Hatanaka K, Shimizu K, et al. PET imaging of brain cancer with positron emitter-labeled liposomes. Int J Pharm. 2011;403(1):170–7.

    Article  CAS  PubMed  Google Scholar 

  47. Lamichhane N, Dewkar GK, Sundaresan G, Mahon RN, Zweit J. [18F]-fluorinated carboplatin and [111In]-liposome for image-guided drug delivery. Int J Mol Sci. 2017;18(5):1079.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Seo JW, Zhang H, Kukis DL, Meares CF, Ferrara KW. A novel method to label preformed liposomes with 64Cu for positron emission tomography (PET) imaging. Bioconjug Chem. 2008;19(12):2577–84.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Lee S-G, Gangangari K, Kalidindi TM, Punzalan B, Larson SM, Pillarsetty NVK. Copper-64 labeled liposomes for imaging bone marrow. Nucl Med Biol. 2016;43(12):781–7.

  50. Yu B, Goel S, Ni D, Ellison PA, Siamof CM, Jiang D, et al. Reassembly of 89Zr-labeled cancer cell membranes into multicompartment membrane-derived liposomes for PET-trackable tumor-targeted theranostics. Adv Mater. 2018;30(13):1704934.

    Article  Google Scholar 

  51. Jensen AI, Severin GW, Hansen AE, Fliedner FP, Eliasen R, Parhamifar L, et al. Remote-loading of liposomes with manganese-52 and in vivo evaluation of the stabilities of 52Mn-DOTA and 64Cu-DOTA using radiolabelled liposomes and PET imaging. J Control Release. 2018;269:100–9.

    Article  CAS  PubMed  Google Scholar 

  52. de Smet M, Langereis S, van den Bosch S, Bitter K, Hijnen NM, Heijman E, et al. SPECT/CT imaging of temperature-sensitive liposomes for MR-image guided drug delivery with high intensity focused ultrasound. J Control Release. 2013;169(1):82–90.

    Article  PubMed  Google Scholar 

  53. Varga Z, Szigyártó IC, Gyurkó I, Dóczi R, Horváth I, Máthé D, et al. Radiolabeling and quantitative in vivo SPECT/CT imaging study of liposomes using the novel iminothiolane-99mTc-tricarbonyl complex. Contrast Media & Molecular Imaging. 2017;4693417.

  54. Sadri K, Momenypoor S, Dabbagh Kakhki VR, Sadeghi R, Aryana K, Johari Daha F, et al. Nano liposomes labeled with (99m)Tc-HMPAO, a novel agent for blood pool imaging. Iranian journal of pharmaceutical research : IJPR. 2015;14(4):981–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Soundararajan A, Bao A, Phillips WT, Perez R III, Goins BA. [186Re]Liposomal doxorubicin (Doxil): in vitro stability, pharmacokinetics, imaging and biodistribution in a head and neck squamous cell carcinoma xenograft model. Nucl Med Biol. 2009;36(5):515–24.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Soundararajan A, Dodd GD III, Bao A, Phillips WT, McManus LM, Prihoda TJ, et al. Chemoradionuclide therapy with 186Re-labeled liposomal doxorubicin in combination with radiofrequency ablation for effective treatment of head and neck cancer in a nude rat tumor xenograft model. Radiology. 2011;261(3):813–23.

    Article  PubMed  PubMed Central  Google Scholar 

  57. Li S, Goins B, Zhang L, Bao A. Novel multifunctional theranostic liposome drug delivery system: construction, characterization, and multimodality MR, near-infrared fluorescent, and nuclear imaging. Bioconjug Chem. 2012;23(6):1322–32.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Petersen AL, Henriksen JR, Binderup T, Elema DR, Rasmussen PH, Hag AM, et al. In vivo evaluation of PEGylated 64Cu-liposomes with theranostic and radiotherapeutic potential using micro PET/CT. Eur J Nucl Med Mol Imaging. 2016;43(5):941–52.

    Article  CAS  PubMed  Google Scholar 

  59. Uchegbu IF, Vyas SP. Non-ionic surfactant based vesicles (niosomes) in drug delivery. Int J Pharm. 1998;172(1–2):33–70.

    Article  CAS  Google Scholar 

  60. Singh TG, Sharma N. Chapter 7 - Nanobiomaterials in cosmetics: current status and future prospects: William Andrew Publishing. 2016.

  61. Almasi A, Shahhosseini S, Haeri A, Daha FJ, Geramifar P, Dadashzadeh S. Radiolabeling of preformed niosomes with [99m Tc]: in vitro stability, biodistribution, and in vivo performance. AAPS PharmSciTech. 2018;19(8):3859–70.

    Article  CAS  PubMed  Google Scholar 

  62. Akbar MU, Ahmad MR, Shaheen A, Mushtaq S. A review on evaluation of technetium-99m labeled radiopharmaceuticals. J Radioanal Nucl Chem. 2016;310(2):477–93.

    Article  CAS  Google Scholar 

  63. De Silva L, Fu J-Y, Htar TT, Muniyandy S, Kasbollah A, Wan Kamal WHB, et al. Characterization, optimization, and in vitro evaluation of Technetium-99m-labeled niosomes. Int J Nanomed. 2019;14:1101–17.

    Article  Google Scholar 

  64. Faruqu FN, Wang JT-W, Xu L, McNickle L, Chong EM-Y, Walters A, et al. Membrane radiolabelling of exosomes for comparative biodistribution analysis in immunocompetent and immunodeficient mice-a novel and universal approach. Theranostics. 2019;9(6):1666.

  65. Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol. 2013;200(4):373–83.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Molavipordanjani S, Khodashenas S, Abedi SM, Moghadam MF, Mardanshahi A, Hosseinimehr SJ. 99mTc-radiolabeled HER2 targeted exosome for tumor imaging. Eur J Pharm Sci. 2020;148: 105312.

    Article  CAS  PubMed  Google Scholar 

  67. van Dommelen SM, Vader P, Lakhal S, Kooijmans S, van Solinge WW, Wood MJ, et al. Microvesicles and exosomes: opportunities for cell-derived membrane vesicles in drug delivery. J Control Release. 2012;161(2):635–44.

    Article  PubMed  Google Scholar 

  68. Ohno S-I, Takanashi M, Sudo K, Ueda S, Ishikawa A, Matsuyama N, et al. Systemically injected exosomes targeted to EGFR deliver antitumor microRNA to breast cancer cells. Mol Ther. 2013;21(1):185–91.

  69. Biancone L, Bruno S, Deregibus MC, Tetta C, Camussi G. Therapeutic potential of mesenchymal stem cell-derived microvesicles. Nephrol Dial Transplant. 2012;27(8):3037–42.

    Article  CAS  PubMed  Google Scholar 

  70. Wiklander OP, Nordin JZ, O’Loughlin A, Gustafsson Y, Corso G, Mäger I, et al. Extracellular vesicle in vivo biodistribution is determined by cell source, route of administration and targeting. Journal of extracellular vesicles. 2015;4(1):26316.

    Article  PubMed  Google Scholar 

  71. Kim EE. Radionanomedicine: combined nuclear and nanomedicine. J Nucl Med. 2019;60(6):143–63.

    Article  Google Scholar 

  72. Elsharkasy OM, Nordin JZ, Hagey DW, de Jong OG, Schiffelers RM, Andaloussi SE, et al. Extracellular vesicles as drug delivery systems: why and how? Adv Drug Del Rev. 2020;159:332–43.

    Article  CAS  Google Scholar 

  73. Jeong J-M, Kim Y-J, Lee Y-S, Lee D-S, Chung J-K, Lee M-C. Radiolabeling of NOTA and DOTA with positron emitting 68Ga and investigation of in vitro properties. Nucl Med Mol Imaging. 2009;43(4):330–6.

    Google Scholar 

  74. Shi S, Li T, Wen X, Wu SY, Xiong C, Zhao J, et al. Copper-64 labeled PEGylated exosomes for in vivo positron emission tomography and enhanced tumor retention. Bioconjug Chem. 2019;30(10):2675–83.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Royo F, Cossío U, de Angulo AR, Llop J, Falcon-Perez JM. Modification of the glycosylation of extracellular vesicles alters their biodistribution in mice. Nanoscale. 2019;11(4):1531–7.

    Article  CAS  PubMed  Google Scholar 

  76. Rashid MH, Borin TF, Ara R, Angara K, Cai J, Achyut BR, et al. Differential in vivo biodistribution of 131I-labeled exosomes from diverse cellular origins and its implication for theranostic application. Nanomed Nanotechnol Biol Med. 2019;21: 102072.

    Article  CAS  Google Scholar 

  77. Jang SC, Kim OY, Yoon CM, Choi D-S, Roh T-Y, Park J, et al. Bioinspired exosome-mimetic nanovesicles for targeted delivery of chemotherapeutics to malignant tumors. ACS Nano. 2013;7(9):7698–710.

    Article  CAS  PubMed  Google Scholar 

  78. Choi H, Jang SC, Yoo MY, Park JY, Choi NE, Oh HJ, et al. Noninvasive imaging of radiolabeled exosome-mimetic nanovesicle using 99m Tc-HMPAO. Sci Rep. 2015;5(1):1–10.

    Google Scholar 

  79. Varga Z, Gyurkó I, Pálóczi K, Buzás EI, Horváth I, Hegedűs N, et al. Radiolabeling of extracellular vesicles with 99mTc for quantitative in vivo imaging studies. Cancer Biother Radiopharm. 2016;31(5):168–73.

    CAS  PubMed  Google Scholar 

  80. Hwang DW, Choi H, Jang SC, Yoo MY, Park JY, Choi NE, et al. Noninvasive imaging of radiolabeled exosome-mimetic nanovesicle using 99mTc-HMPAO. Sci Rep. 2015;5(1):15636.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Smyth T, Kullberg M, Malik N, Smith-Jones P, Graner MW, Anchordoquy TJ. Biodistribution and delivery efficiency of unmodified tumor-derived exosomes. J Control Release. 2015;199:145–55.

    Article  CAS  PubMed  Google Scholar 

  82. Khan A, Man F, Faruqu F, Kim J, Al-Salemee F, Volpe A, et al. [89Zr]Zr(oxinate)4 allows direct radiolabelling and PET imaging of small extracellular vesicles. chemrxiv. 2021.

  83. Cabral H, Miyata K, Osada K, Kataoka K. Block copolymer micelles in nanomedicine applications. Chem Rev. 2018;118(14):6844–92.

    Article  CAS  PubMed  Google Scholar 

  84. Cagel M, Tesan FC, Bernabeu E, Salgueiro MJ, Zubillaga MB, Moretton MA, et al. Polymeric mixed micelles as nanomedicines: achievements and perspectives. Eur J Pharm Biopharm. 2017;113:211–28.

    Article  CAS  PubMed  Google Scholar 

  85. Jain R, Nabar S, Dandekar P, Hassan P, Aswal V, Talmon Y, et al. Formulation and evaluation of novel micellar nanocarrier for nasal delivery of sumatriptan. Nanomedicine. 2010;5(4):575–87.

    Article  CAS  PubMed  Google Scholar 

  86. Abdelbary GA, Tadros MI. Brain targeting of olanzapine via intranasal delivery of core–shell difunctional block copolymer mixed nanomicellar carriers: in vitro characterization, ex vivo estimation of nasal toxicity and in vivo biodistribution studies. Int J Pharm. 2013;452(1–2):300–10.

    Article  CAS  PubMed  Google Scholar 

  87. Zhan C, Gu B, Xie C, Li J, Liu Y, Lu W. Cyclic RGD conjugated poly(ethylene glycol)-co-poly(lactic acid) micelle enhances paclitaxel anti-glioblastoma effect. J Control Release. 2010;143(1):136–42.

    Article  CAS  PubMed  Google Scholar 

  88. Shen J, Zhan C, Xie C, Meng Q, Gu B, Li C, et al. Poly(ethylene glycol)-block-poly(D, L-lactide acid) micelles anchored with angiopep-2 for brain-targeting delivery. J Drug Target. 2011;19(3):197–203.

    Article  CAS  PubMed  Google Scholar 

  89. Hoang B, Lee H, Reilly RM, Allen C. Noninvasive monitoring of the fate of 111In-labeled block copolymer micelles by high resolution and high sensitivity microSPECT/CT imaging. Mol Pharm. 2009;6(2):581–92.

    Article  CAS  PubMed  Google Scholar 

  90. Chen M-C, Wong H-S, Lin K-J, Chen H-L, Wey S-P, Sonaje K, et al. The characteristics, biodistribution and bioavailability of a chitosan-based nanoparticulate system for the oral delivery of heparin. Biomaterials. 2009;30(34):6629–37.

    Article  CAS  PubMed  Google Scholar 

  91. Fairclough M, Prenant C, Ellis B, Boutin H, McMahon A, Brown G, et al. A new technique for the radiolabelling of mixed leukocytes with zirconium-89 for inflammation imaging with positron emission tomography. J Labelled Compd Radiopharm. 2016;59(7):270–6.

    Article  CAS  Google Scholar 

  92. Dumoga S, Rai Y, Bhatt AN, Tiwari AK, Singh S, Mishra AK, et al. Block copolymer based nanoparticles for theranostic intervention of cervical cancer: synthesis, pharmacokinetics, and in vitro/in vivo evaluation in HeLa xenograft models. ACS Appl Mater Interfaces. 2017;9(27):22195–211.

    Article  CAS  PubMed  Google Scholar 

  93. Liu Y, Ibricevic A, Cohen JA, Cohen JL, Gunsten SP, Fréchet JM, et al. Impact of hydrogel nanoparticle size and functionalization on in vivo behavior for lung imaging and therapeutics. Mol Pharm. 2009;6(6):1891–902.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Zhong X, Yang K, Dong Z, Yi X, Wang Y, Ge C, et al. Polydopamine as a biocompatible multifunctional nanocarrier for combined radioisotope therapy and chemotherapy of cancer. Adv Funct Mater. 2015;25(47):7327–36.

    Article  CAS  Google Scholar 

  95. Silindir-Gunay M, Ozer AY. 99mTc-radiolabeled levofloxacin and micelles as infection and inflammation imaging agents. J Drug Deliv Sci Technol. 2020;56: 101571.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Fonge H, Huang H, Scollard D, Reilly RM, Allen C. Influence of formulation variables on the biodistribution of multifunctional block copolymer micelles. J Control Release. 2012;157(3):366–74.

    Article  CAS  PubMed  Google Scholar 

  97. Gill MR, Menon JU, Jarman PJ, Owen J, Skaripa-Koukelli I, Able S, et al. 111 In-labelled polymeric nanoparticles incorporating a ruthenium-based radiosensitizer for EGFR-targeted combination therapy in oesophageal cancer cells. Nanoscale. 2018;10(22):10596–608.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Arora G, Shukla J, Ghosh S, Maulik SK, Malhotra A, Bandopadhyaya G. PLGA nanoparticles for peptide receptor radionuclide therapy of neuroendocrine tumors: a novel approach towards reduction of renal radiation dose. PLoS ONE. 2012;7(3): e34019.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Pereira MA, Mosqueira VCF, Carmo VAS, Ferrari CS, Reis ECO, Ramaldes GA, et al. Biodistribution study and identification of inflammatory sites using nanocapsules labeled with 99mTc–HMPAO. Nucl Med Commun. 2009;30(9).

  100. Zielinska A, Carreiro F, Oliveira AM, Neves A, Pires B, Venkatesh DN, et al. Polymeric nanoparticles: production, characterization, toxicology and ecotoxicology. Molecules. 2020;25(16).

  101. Snehalatha M, Venugopal K, Saha RN, Babbar AK, Sharma RK. Etoposide loaded PLGA and PCL nanoparticles II: biodistribution and pharmacokinetics after radiolabeling with Tc-99m. Drug Deliv. 2008;15(5):277–87.

    Article  CAS  PubMed  Google Scholar 

  102. dos Santos SN, dos Reis SRR, Pinto SR, Cerqueira-Coutinho C, Nigro F, Barja-Fidalgo TC, et al. Anti-inflammatory/infection PLA nanoparticles labeled with technetium 99m for in vivo imaging. J Nanopart Res. 2017;19(10):1–8.

    Google Scholar 

  103. Polyák A, Hajdu I, Bodnár M, Trencsényi G, Pöstényi Z, Haász V, et al. 99mTc-labelled nanosystem as tumour imaging agent for SPECT and SPECT/CT modalities. Int J Pharm. 2013;449(1–2):10–7.

    Article  PubMed  Google Scholar 

  104. Wagener K, Moderegger D, Allmeroth M, Reibel A, Kramer S, Biesalski B, et al. Long-term biodistribution study of HPMA-ran-LMA copolymers in vivo by means of 131I-labeling. Nucl Med Biol. 2018;58:59–66.

    Article  CAS  PubMed  Google Scholar 

  105. Herth MM, Barz M, Moderegger D, Allmeroth M, Jahn M, Thews O, et al. Radioactive labeling of defined HPMA-based polymeric structures using [18F] FETos for in vivo imaging by positron emission tomography. Biomacromol. 2009;10(7):1697–703.

    Article  CAS  Google Scholar 

  106. Tang C, Edelstein J, Mikitsh JL, Xiao E, Hemphill AH, Pagels R, et al. Biodistribution and fate of core-labeled 125 I polymeric nanocarriers prepared by Flash NanoPrecipitation (FNP). J Mater Chem B. 2016;4(14):2428–34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Simone EA, Zern BJ, Chacko A-M, Mikitsh JL, Blankemeyer ER, Muro S, et al. Endothelial targeting of polymeric nanoparticles stably labeled with the PET imaging radioisotope iodine-124. Biomaterials. 2012;33(21):5406–13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Imlimthan S, Otaru S, Keinänen O, Correia A, Lintinen K, Santos HA, et al. Radiolabeled molecular imaging probes for the in vivo evaluation of cellulose nanocrystals for biomedical applications. Biomacromol. 2018;20(2):674–83.

    Article  Google Scholar 

  109. Pereira MA, Mosqueira VCF, Vilela JMC, Andrade MS, Ramaldes GA, Cardoso VN. PLA-PEG nanocapsules radiolabeled with 99mTechnetium-HMPAO: release properties and physicochemical characterization by atomic force microscopy and photon correlation spectroscopy. Eur J Pharm Sci. 2008;33(1):42–51.

    Article  CAS  PubMed  Google Scholar 

  110. Ding S, Zhang N, Lyu Z, Zhu W, Chang Y-C, Hu X, et al. Protein-based nanomaterials and nanosystems for biomedical applications: a review. Mater Today. 2020.

  111. Lohcharoenkal W, Wang L, Chen YC, Rojanasakul Y. Protein nanoparticles as drug delivery carriers for cancer therapy. Biomed Res Int. 2014;2014.

  112. Hawkins MJ, Soon-Shiong P, Desai N. Protein nanoparticles as drug carriers in clinical medicine. Adv Drug Del Rev. 2008;60(8):876–85.

    Article  CAS  Google Scholar 

  113. Schoonen L, van Hest JC. Functionalization of protein-based nanocages for drug delivery applications. Nanoscale. 2014;6(13):7124–41.

    Article  CAS  PubMed  Google Scholar 

  114. Miele E, Spinelli GP, Miele E, Tomao F, Tomao S. Albumin-bound formulation of paclitaxel (Abraxane® ABI-007) in the treatment of breast cancer. Int J Nanomed. 2009;4:99.

    CAS  Google Scholar 

  115. Sand KMK, Bern M, Nilsen J, Noordzij HT, Sandlie I, Andersen JT. Unraveling the interaction between FcRn and albumin: opportunities for design of albumin-based therapeutics. Front Immunol. 2015;5:682.

    Article  PubMed  PubMed Central  Google Scholar 

  116. Lesniak WG, Boinapally S, Banerjee SR, Behnam Azad B, Foss CA, Shen C, et al. Evaluation of PSMA-targeted PAMAM dendrimer nanoparticles in a murine model of prostate cancer. Mol Pharm. 2019;16(6):2590–604.

    Article  CAS  PubMed  Google Scholar 

  117. Jain S, Mathur R, Das M, Swarnakar NK, Mishra AK. Synthesis, pharmacoscintigraphic evaluation and antitumor efficacy of methotrexate-loaded, folate-conjugated, stealth albumin nanoparticles. Nanomedicine. 2011;6(10):1733–54.

    Article  CAS  PubMed  Google Scholar 

  118. Yi X, Zhou H, Zhang Z, Xiong S, Yang K. X-rays-optimized delivery of radiolabeled albumin for cancer theranostics. Biomaterials. 2020;233: 119764.

    Article  CAS  PubMed  Google Scholar 

  119. Woods A, Patel A, Spina D, Riffo-Vasquez Y, Babin-Morgan A, De Rosales R, et al. In vivo biocompatibility, clearance, and biodistribution of albumin vehicles for pulmonary drug delivery. J Control Release. 2015;210:1–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Feczkó T, Piiper A, Pleli T, Schmithals C, Denk D, Hehlgans S, et al. Theranostic sorafenib-loaded polymeric nanocarriers manufactured by enhanced gadolinium conjugation techniques. Pharmaceutics. 2019;11(10):489.

    Article  PubMed  PubMed Central  Google Scholar 

  121. Yang Y, Neef T, Mittelholzer C, Garayoa EG, Bläuenstein P, Schibli R, et al. The biodistribution of self-assembling protein nanoparticles shows they are promising vaccine platforms. J Nanobiotechnol. 2013;11(1):1–10.

    Article  CAS  Google Scholar 

  122. Pérez-Medina C, Tang J, Abdel-Atti D, Hogstad B, Merad M, Fisher EA, et al. PET imaging of tumor-associated macrophages with 89Zr-labeled high-density lipoprotein nanoparticles. J Nucl Med. 2015;56(8):1272–7.

    Article  PubMed  Google Scholar 

  123. Mason CA, Kossatz S, Carter LM, Pirovano G, Brand C, Guru N, et al. An 89Zr-HDL PET tracer monitors response to a CSF1R inhibitor. J Nucl Med. 2020;61(3):433–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Lin X, Xie J, Niu G, Zhang F, Gao H, Yang M, et al. Chimeric ferritin nanocages for multiple function loading and multimodal imaging. Nano Lett. 2011;11(2):814–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Yang Y, Neef T, Mittelholzer C, Garcia Garayoa E, Bläuenstein P, Schibli R, et al. The biodistribution of self-assembling protein nanoparticles shows they are promising vaccine platforms. J Nanobiotechnol. 2013;11(1):36.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Liang M, Tan H, Zhou J, Wang T, Duan D, Fan K, et al. Bioengineered H-ferritin nanocages for quantitative imaging of vulnerable plaques in atherosclerosis. ACS Nano. 2018;12(9):9300–8.

    Article  CAS  PubMed  Google Scholar 

  127. Yang S-G, Chang J-E, Shin B, Park S, Na K, Shim C-K. 99mTc-hematoporphyrin linked albumin nanoparticles for lung cancer targeted photodynamic therapy and imaging. J Mater Chem. 2010;20(41):9042–6.

    Article  CAS  Google Scholar 

  128. Gil AG, Irache JM, Peñuelas I, González Navarro CJ, López de Cerain A. Toxicity and biodistribution of orally administered casein nanoparticles. Food Chem Toxicol. 2017;106:477–86.

  129. Kesharwani P, Jain K, Jain NK. Dendrimer as nanocarrier for drug delivery. Prog Polym Sci. 2014;39(2):268–307.

    Article  CAS  Google Scholar 

  130. Kojima C, Regino C, Umeda Y, Kobayashi H, Kono K. Influence of dendrimer generation and polyethylene glycol length on the biodistribution of PEGylated dendrimers. Int J Pharm. 2010;383(1–2):293–6.

    Article  CAS  PubMed  Google Scholar 

  131. Niki Y, Ogawa M, Makiura R, Magata Y, Kojima C. Optimization of dendrimer structure for sentinel lymph node imaging: effects of generation and terminal group. Nanomed Nanotechnol Biol Med. 2015;11(8):2119–27.

    Article  CAS  Google Scholar 

  132. Katsumi H, Nishikawa M, Hirosaki R, Okuda T, Kawakami S, Yamashita F, et al. Development of PEGylated cysteine-modified lysine dendrimers with multiple reduced thiols to prevent hepatic ischemia/reperfusion injury. Mol Pharm. 2016;13(8):2867–73.

    Article  CAS  PubMed  Google Scholar 

  133. Sano K, Iwamiya Y, Kurosaki T, Ogawa M, Magata Y, Sasaki H, et al. Radiolabeled γ-polyglutamic acid complex as a nano-platform for sentinel lymph node imaging. J Control Release. 2014;194:310–5.

    Article  CAS  PubMed  Google Scholar 

  134. Kovacs L, Tassano M, Cabrera M, Zamboni CB, Fernández M, Anjos RM, et al. Development of 177Lu-DOTA-dendrimer and determination of Its effect on metal and ion levels in tumor tissue. Cancer Biother Radiopharm. 2015;30(10):405–10.

    CAS  PubMed  Google Scholar 

  135. Parrott MC, Benhabbour SR, Saab C, Lemon JA, Parker S, Valliant JF, et al. Synthesis, radiolabeling, and bio-imaging of high-generation polyester dendrimers. J Am Chem Soc. 2009;131(8):2906–16.

    Article  CAS  PubMed  Google Scholar 

  136. Price EW, Orvig C. Matching chelators to radiometals for radiopharmaceuticals. Chem Soc Rev. 2014;43(1):260–90.

    Article  CAS  PubMed  Google Scholar 

  137. Yang W, Barth RF, Adams DM, Ciesielski MJ, Fenstermaker RA, Shukla S, et al. Convection-enhanced delivery of boronated epidermal growth factor for molecular targeting of EGF receptor-positive gliomas. Cancer Res. 2002;62(22):6552–8.

    CAS  PubMed  Google Scholar 

  138. Thiagarajan G, Sadekar S, Greish K, Ray A, Ghandehari H. Evidence of oral translocation of anionic G6.5 dendrimers in mice. Mol Pharm. 2013;10(3):988–98.

  139. Wilbur DS, Pathare PM, Hamlin DK, Buhler KR, Vessella RL. Biotin reagents for antibody pretargeting. 3. Synthesis, radioiodination, and evaluation of biotinylated starburst dendrimers. Bioconjugate chemistry. 1998;9(6):813–25.

  140. Kurokawa Y, Sone H, Win-Shwe T-T, Zeng Y, Kimura H, Koyama Y, et al. Aggregation is a critical cause of poor transfer into the brain tissue of intravenously administered cationic PAMAM dendrimer nanoparticles. Int J Nanomed. 2017;12:3967.

    Article  CAS  Google Scholar 

  141. Orocio-Rodríguez E, Ferro-Flores G, Santos-Cuevas CL, Ramírez FdM, Ocampo-García BE, Azorín-Vega E, et al. Two novel nanosized radiolabeled analogues of somatostatin for neuroendocrine tumor imaging. Journal of nanoscience and nanotechnology. 2015;15(6):4159–69.

  142. Ghoreishi SM, Bitarafan-Rajabi A, Azar AD, Ardestani MS, Assadi A. Novel 99mTc-radiolabeled anionic linear globular PEG-based dendrimer-chlorambucil: non-invasive method for in-vivo biodistribution. Drug Res. 2017;67(03):149–55.

    CAS  Google Scholar 

  143. Ardestani MS, Bitarafan-Rajabi A, Mohammadzadeh P, Mortazavi-Derazkola S, Sabzevari O, Azar AD, et al. Synthesis and characterization of novel 99mTc-DGC nano-complexes for improvement of heart diagnostic. Bioorg Chem. 2020;96: 103572.

    Article  CAS  PubMed  Google Scholar 

  144. Xu X, Li Y, Cao T, Cheng J, Zhang Y. A novel, chelator-free method for 64 Cu labeling of dendrimers. J Nanopart Res. 2018;20(8):1–11.

    Article  Google Scholar 

  145. McNelles SA, Knight SD, Janzen N, Valliant JF, Adronov A. Synthesis, radiolabeling, and in vivo imaging of PEGylated high-generation polyester dendrimers. Biomacromol. 2015;16(9):3033–41.

    Article  CAS  Google Scholar 

  146. Gibbens-Bandala B, Morales-Avila E, Ferro-Flores G, Santos-Cuevas C, Luna-Gutiérrez M, Ramírez-Nava G, et al. Synthesis and evaluation of 177Lu-DOTA-DN(PTX)-BN for selective and concomitant radio and drug—therapeutic effect on breast cancer cells. Polymers. 2019;11(10).

  147. Lesniak WG, Chu C, Jablonska A, Azad BB, Zwaenepoel O, Zawadzki M, et al. PET imaging of distinct brain uptake of a nanobody and similarly-sized PAMAM dendrimers after intra-arterial administration. Eur J Nucl Med Mol Imaging. 2019;46(9):1940–51.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Zhou D, Kim SH, Carroll VM, Dence CS, Katzenellenbogen JA. Utilizing electrostatic interactions to facilitate F-18 radiolabeling of poly(amido)amine (PAMAM) dendrimers. Org Biomol Chem. 2014;12(43):8696–701.

    Article  CAS  PubMed  Google Scholar 

  149. Yoon HY, Jeon S, You DG, Park JH, Kwon IC, Koo H, et al. Inorganic nanoparticles for image-guided therapy. Bioconjug Chem. 2017;28(1):124–34.

    Article  CAS  PubMed  Google Scholar 

  150. Lee D. Radionanomedicine: combined nuclear and nanomedicine: Springer. 2019.

  151. Vivero-Escoto JL, Huxford-Phillips RC, Lin W. Silica-based nanoprobes for biomedical imaging and theranostic applications. Chem Soc Rev. 2012;41(7):2673–85.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  152. Li Z, Barnes JC, Bosoy A, Stoddart JF, Zink JI. Mesoporous silica nanoparticles in biomedical applications. Chem Soc Rev. 2012;41(7):2590–605.

    Article  CAS  PubMed  Google Scholar 

  153. Slowing II, Vivero-Escoto JL, Wu C-W, Lin VS-Y. Mesoporous silica nanoparticles as controlled release drug delivery and gene transfection carriers. Adv Drug Del Rev. 2008;60(11):1278–88.

  154. Liberman A, Mendez N, Trogler WC, Kummel AC. Synthesis and surface functionalization of silica nanoparticles for nanomedicine. Surf Sci Rep. 2014;69(2–3):132–58.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  155. Zarschler K, Rocks L, Licciardello N, Boselli L, Polo E, Garcia KP, et al. Ultrasmall inorganic nanoparticles: state-of-the-art and perspectives for biomedical applications. Nanomed Nanotechnol Biol Med. 2016;12(6):1663–701.

    Article  CAS  Google Scholar 

  156. Ehlerding EB, Chen F, Cai W. Biodegradable and renal clearable inorganic nanoparticles. Advanced Science. 2016;3(2):1500223.

    Article  PubMed  Google Scholar 

  157. Shaffer TM, Wall MA, Harmsen S, Longo VA, Drain CM, Kircher MF, et al. Silica nanoparticles as substrates for chelator-free labeling of oxophilic radioisotopes. Nano Lett. 2015;15(2):864–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Chen F, Ma K, Zhang L, Madajewski B, Zanzonico P, Sequeira S, et al. Target-or-clear zirconium-89 labeled silica nanoparticles for enhanced cancer-directed uptake in melanoma: a comparison of radiolabeling strategies. Chem Mater. 2017;29(19):8269–81.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  159. Shaffer TM, Harmsen S, Khwaja E, Kircher MF, Drain CM, Grimm J. Stable radiolabeling of sulfur-functionalized silica nanoparticles with copper-64. Nano Lett. 2016;16(9):5601–4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Lee JY, Vyas CK, Kim GG, Choi PS, Hur MG, Yang SD, et al. Red blood cell membrane bioengineered Zr-89 labelled hollow mesoporous silica nanosphere for overcoming phagocytosis. Sci Rep. 2019;9(1):1–9.

    Google Scholar 

  161. Chen F, Hong H, Zhang Y, Valdovinos HF, Shi S, Kwon GS, et al. In vivo tumor targeting and image-guided drug delivery with antibody-conjugated, radiolabeled mesoporous silica nanoparticles. ACS Nano. 2013;7(10):9027–39.

    Article  CAS  PubMed  Google Scholar 

  162. Same S, Aghanejad A, Nakhjavani SA, Barar J, Omidi Y. Radiolabeled theranostics: magnetic and gold nanoparticles. BioImpacts: BI. 2016;6(3):169.

  163. Portilho FL, Helal-Neto E, Cabezas SS, Pinto SR, Dos Santos SN, Pozzo L, et al. Magnetic core mesoporous silica nanoparticles doped with dacarbazine and labelled with 99mTc for early and differential detection of metastatic melanoma by single photon emission computed tomography. Artif Cells Nanomed Biotechnol. 2018;46(sup1):1080–7.

    Article  CAS  PubMed  Google Scholar 

  164. Goel S, Chen F, Luan S, Valdovinos HF, Shi S, Graves SA, et al. Engineering intrinsically zirconium-89 radiolabeled self-destructing mesoporous silica nanostructures for in vivo biodistribution and tumor targeting studies. Advanced Science. 2016;3(11):1600122.

    Article  PubMed  PubMed Central  Google Scholar 

  165. Bindini E, Ramirez MdlA, Rios X, Cossío U, Simó C, Gomez‐Vallejo V, et al. In vivo tracking of the degradation of mesoporous silica through 89Zr radio‐labeled core–shell nanoparticles. Small. 2021:2101519.

  166. Fazaeli Y, Hosseini MA, Afrasyabi M, Ashtari P. 68Ga@ pyridine-functionalized MCM-41 mesoporous silica: a novel radio labeled composite for diagnostic applications. Radiochim Acta. 2019;107(2):157–64.

    Article  CAS  Google Scholar 

  167. Gao H, Liu X, Tang W, Niu D, Zhou B, Zhang H, et al. 99m Tc-conjugated manganese-based mesoporous silica nanoparticles for SPECT, pH-responsive MRI and anti-cancer drug delivery. Nanoscale. 2016;8(47):19573–80.

    Article  CAS  PubMed  Google Scholar 

  168. Rainone P, Riva B, Belloli S, Sudati F, Ripamonti M, Verderio P, et al. Development of 99mTc-radiolabeled nanosilica for targeted detection of HER2-positive breast cancer. Int J Nanomed. 2017;12:3447.

    Article  CAS  Google Scholar 

  169. Miller L, Winter G, Baur B, Witulla B, Solbach C, Reske S, et al. Synthesis, characterization, and biodistribution of multiple 89 Zr-labeled pore-expanded mesoporous silica nanoparticles for PET. Nanoscale. 2014;6(9):4928–35.

    Article  CAS  PubMed  Google Scholar 

  170. Zhang X, Chen F, Turker MZ, Ma K, Zanzonico P, Gallazzi F, et al. Targeted melanoma radiotherapy using ultrasmall 177Lu-labeled α-melanocyte stimulating hormone-functionalized core-shell silica nanoparticles. Biomaterials. 2020;241: 119858.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  171. Gao Y, Li Y, Wang Y, Chen Y, Gu J, Zhao W, et al. Controlled synthesis of multilayered gold nanoshells for enhanced photothermal therapy and SERS detection. Small. 2015;11(1):77–83.

    Article  CAS  PubMed  Google Scholar 

  172. Campbell JL, SoRelle ED, Ilovich O, Liba O, James ML, Qiu Z, et al. Multimodal assessment of SERS nanoparticle biodistribution post ingestion reveals new potential for clinical translation of Raman imaging. Biomaterials. 2017;135:42–52.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  173. Zhou C, Long M, Qin Y, Sun X, Zheng J. Luminescent gold nanoparticles with efficient renal clearance. Angew Chem Int Ed. 2011;50(14):3168–72.

    Article  CAS  Google Scholar 

  174. Liu J, Yu M, Ning X, Zhou C, Yang S, Zheng J. PEGylation and zwitterionization: pros and cons in the renal clearance and tumor targeting of near-IR-emitting gold nanoparticles. Angew Chem. 2013;125(48):12804–8.

    Article  Google Scholar 

  175. Tang S, Peng C, Xu J, Du B, Wang Q, Vinluan RD III, et al. Tailoring renal clearance and tumor targeting of ultrasmall metal nanoparticles with particle density. Angew Chem. 2016;128(52):16273–7.

    Article  Google Scholar 

  176. Jiménez-Mancilla N, Ferro-Flores G, Santos-Cuevas C, Ocampo-García B, Luna-Gutiérrez M, Azorín-Vega E, et al. Multifunctional targeted therapy system based on 99mTc/177Lu-labeled gold nanoparticles-Tat (49–57)-Lys3-bombesin internalized in nuclei of prostate cancer cells. J Labelled Compd Radiopharm. 2013;56(13):663–71.

    Article  Google Scholar 

  177. Ocampo-García BE, Ramírez FdM, Ferro-Flores G, De León-Rodríguez LM, Santos-Cuevas CL, Morales-Avila E, et al. 99mTc-labelled gold nanoparticles capped with HYNIC-peptide/mannose for sentinel lymph node detection. Nucl Med Biol. 2011;38(1):1–11.

  178. Karmani L, Labar D, Valembois V, Bouchat V, Nagaswaran PG, Bol A, et al. Antibody-functionalized nanoparticles for imaging cancer: influence of conjugation to gold nanoparticles on the biodistribution of 89Zr-labeled cetuximab in mice. Contrast Media Mol Imaging. 2013;8(5):402–8.

    Article  CAS  PubMed  Google Scholar 

  179. Sun X, Huang X, Yan X, Wang Y, Guo J, Jacobson O, et al. Chelator-free 64Cu-integrated gold nanomaterials for positron emission tomography imaging guided photothermal cancer therapy. ACS Nano. 2014;8(8):8438–46.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  180. Hu H, Huang P, Weiss OJ, Yan X, Yue X, Zhang MG, et al. PET and NIR optical imaging using self-illuminating 64Cu-doped chelator-free gold nanoclusters. Biomaterials. 2014;35(37):9868–76.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  181. Xie H, Wang ZJ, Bao A, Goins B, Phillips WT. In vivo PET imaging and biodistribution of radiolabeled gold nanoshells in rats with tumor xenografts. Int J Pharm. 2010;395(1–2):324–30.

    Article  CAS  PubMed  Google Scholar 

  182. Morales-Avila E, Ferro-Flores G, Ocampo-García BE, De León-Rodríguez LM, Santos-Cuevas CL, García-Becerra R, et al. Multimeric system of 99mTc-labeled gold nanoparticles conjugated to c[RGDfK(C)] for molecular imaging of tumor α(v)β(3) expression. Bioconjug Chem. 2011;22(5):913–22.

    Article  CAS  PubMed  Google Scholar 

  183. Jeon J, Choi MH. Synthesis of 68Ga-labeled gold nanoparticles for tumor targeted positron emission tomography imaging. Journal of Radiopharmaceuticals and Molecular Probes. 2015;1(1):46–52.

    Google Scholar 

  184. Chilug LE, Leonte RA, Patrascu MEB, Ion AC, Tuta CS, Raicu A, et al. In vitro binding kinetics study of gold nanoparticles functionalized with 68Ga-DOTA conjugated peptides. J Radioanal Nucl Chem. 2017;311(2):1485–93.

    Article  CAS  Google Scholar 

  185. Vilchis-Juárez A, Ferro-Flores G, Santos-Cuevas C, Morales-Avila E, Ocampo-García B, Díaz-Nieto L, et al. Molecular targeting radiotherapy with cyclo-RGDFK(C) peptides conjugated to 177Lu-labeled gold nanoparticles in tumor-bearing mice. J Biomed Nanotechnol. 2014;10(3):393–404.

    Article  PubMed  Google Scholar 

  186. Karmani L, Bouchat V, Bouzin C, Levêque P, Labar D, Bol A, et al. 89Zr-labeled anti-endoglin antibody-targeted gold nanoparticles for imaging cancer: implications for future cancer therapy. Nanomedicine. 2014;9(13):1923–37.

    Article  CAS  PubMed  Google Scholar 

  187. Guerrero S, Herance JR, Rojas S, Mena JF, Gispert JD, Acosta GA, et al. Synthesis and in vivo evaluation of the biodistribution of a 18F-labeled conjugate gold-nanoparticle-peptide with potential biomedical application. Bioconjug Chem. 2012;23(3):399–408.

    Article  CAS  PubMed  Google Scholar 

  188. El-Ghareb WI, Swidan MM, Ibrahim IT, Abd El-Bary A, Tadros MI, Sakr TM. 99mTc-Doxorubicin-loaded gallic acid-gold nanoparticles (99mTc-DOX-loaded GA-Au NPs) as a multifunctional theranostic agent. Int J Pharm. 2020;586: 119514.

    Article  CAS  PubMed  Google Scholar 

  189. Goel S, Chen F, Ehlerding EB, Cai W. Intrinsically radiolabeled nanoparticles: an emerging paradigm. Small. 2014;10(19):3825–30.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  190. Zhou M, Zhang R, Huang M, Lu W, Song S, Melancon MP, et al. A chelator-free multifunctional [64Cu] CuS nanoparticle platform for simultaneous micro-PET/CT imaging and photothermal ablation therapy. J Am Chem Soc. 2010;132(43):15351–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  191. Zhou B, Zhao J, Qiao Y, Wei Q, He J, Li W, et al. Simultaneous multimodal imaging and photothermal therapy via renal-clearable manganese-doped copper sulfide nanodots. Appl Mater Today. 2018;13:285–97.

    Article  Google Scholar 

  192. Chen F, Hong H, Goel S, Graves SA, Orbay H, Ehlerding EB, et al. In vivo tumor vasculature targeting of CuS@MSN based theranostic nanomedicine. ACS Nano. 2015;9(4):3926–34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  193. Cai H, Xie F, Mulgaonkar A, Chen L, Sun X, Hsieh J-T, et al. Bombesin functionalized 64Cu-copper sulfide nanoparticles for targeted imaging of orthotopic prostate cancer. Nanomedicine. 2018;13(14):1695–705.

    Article  PubMed  Google Scholar 

  194. Liu Q, Zhou M, Li P, Ku G, Huang G, Li C, et al. 64CuS-labeled nanoparticles: a new sentinel-lymph-node-mapping agent for PET–CT and photoacoustic tomography. Contrast Media Mol Imaging. 2016;11(6):475–81.

    Article  CAS  PubMed  Google Scholar 

  195. Zhou M, Chen Y, Adachi M, Wen X, Erwin B, Mawlawi O, et al. Single agent nanoparticle for radiotherapy and radio-photothermal therapy in anaplastic thyroid cancer. Biomaterials. 2015;57:41–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  196. Zhou M, Melancon M, Stafford RJ, Li J, Nick AM, Tian M, et al. Precision nanomedicine using dual PET and MR temperature imaging–guided photothermal therapy. J Nucl Med. 2016;57(11):1778–83.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  197. Yi X, Shen M, Liu X, Gu J, Jiang Z, Xu L, et al. Diagnostic radionuclides labeled on biomimetic nanoparticles for enhanced follow‐up photothermal therapy of cancer. Adv Healthc Mater. 2021:2100860.

  198. Sun M, Leong B, Gobalakrishnan S, Wang L, Vijayaragavan V, McDonagh P, et al. Zirconium-89 doped copper sulfide nanoparticle for PET and photoacoustic imaging. Soc Nuclear Med. 2016.

  199. Rieffel J, Chen F, Kim J, Chen G, Shao W, Shao S, et al. Hexamodal imaging with porphyrin-phospholipid-coated upconversion nanoparticles. Adv Mater. 2015;27(10):1785–90.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  200. Seo HJ, Nam SH, Im H-J, Park J-Y, Lee JY, Yoo B, et al. Rapid hepatobiliary excretion of micelle-encapsulated/radiolabeled upconverting nanoparticles as an integrated form. Sci Rep. 2015;5(1):1–12.

  201. Sun Y, Yu M, Liang S, Zhang Y, Li C, Mou T, et al. Fluorine-18 labeled rare-earth nanoparticles for positron emission tomography (PET) imaging of sentinel lymph node. Biomaterials. 2011;32(11):2999–3007.

    Article  CAS  PubMed  Google Scholar 

  202. Liu Q, Chen M, Sun Y, Chen G, Yang T, Gao Y, et al. Multifunctional rare-earth self-assembled nanosystem for tri-modal upconversion luminescence/fluorescence/positron emission tomography imaging. Biomaterials. 2011;32(32):8243–53.

    Article  CAS  PubMed  Google Scholar 

  203. Gallo J, Alam IS, Jin J, Gu Y-J, Aboagye EO, Wong W-T, et al. PET imaging with multimodal upconversion nanoparticles. Dalton Trans. 2014;43(14):5535–45.

    Article  CAS  PubMed  Google Scholar 

  204. Fang H, Li M, Liu Q, Gai Y, Yuan L, Wang S, et al. Ultra-sensitive nanoprobe modified with tumor cell membrane for UCL/MRI/PET multimodality precise imaging of triple-negative breast cancer. Nano-micro letters. 2020;12(1):1–14.

    Article  Google Scholar 

  205. Sun X, Huang X, Guo J, Zhu W, Ding Y, Niu G, et al. Self-illuminating 64Cu-doped CdSe/ZnS nanocrystals for in vivo tumor imaging. J Am Chem Soc. 2014;136(5):1706–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  206. Guo W, Sun X, Jacobson O, Yan X, Min K, Srivatsan A, et al. Intrinsically radioactive [64Cu] CuInS/ZnS quantum dots for PET and optical imaging: improved radiochemical stability and controllable Cerenkov luminescence. ACS Nano. 2015;9(1):488–95.

    Article  CAS  PubMed  Google Scholar 

  207. Felber M, Bauwens M, Mateos JM, Imstepf S, Mottaghy FM, Alberto R. 99mTc radiolabeling and biological evaluation of nanoparticles functionalized with a versatile coating ligand. Chemistry–A European Journal. 2015;21(16):6090–9.

  208. Patt M, Schildan A, Habermann B, Mishchenko O, Patt J, Sabri O. 18F-and 11C-labelling of quantum dots with nca [18F]fluoroethyltosylate and [11C]methyliodide: a feasibility study. J Radioanal Nucl Chem. 2010;283(2):487–91.

    Article  CAS  Google Scholar 

  209. Tang T, Wei Y, Yang Q, Yang Y, Sailor MJ, Pang H-B. Rapid chelator-free radiolabeling of quantum dots for in vivo imaging. Nanoscale. 2019;11(46):22248–54.

    Article  CAS  PubMed  Google Scholar 

  210. Sun M, Sundaresan G, Jose P, Yang L, Hoffman D, Lamichhane N, et al. Highly stable intrinsically radiolabeled indium-111 quantum dots with multidentate zwitterionic surface coating: dual modality tool for biological imaging. J Mater Chem B. 2014;2(28):4456–66.

    Article  CAS  PubMed  Google Scholar 

  211. Cai W, Chen K, Li Z-B, Gambhir SS, Chen X. Dual-function probe for PET and near-infrared fluorescence imaging of tumor vasculature. J Nucl Med. 2007;48(11):1862–70.

    Article  CAS  PubMed  Google Scholar 

  212. Mathur R, Bag N, Varshney R, Hussain F, Kaul A, Kumari N, et al. Enhanced in vivo tumour imaging by EDTA-bis-GNGR functionalized core shell CdSe: ZnS quantum dot: synergistic effect of active passive targeting. RSC Adv. 2016;6(16):13562–71.

    Article  CAS  Google Scholar 

  213. Bag N, Mathur R, Singh S, Hussain F, Chauhan RP, Chuttani K, et al. Design, synthesis and evaluation of the QD-DTC–bisbiotin nanobioconjugate as a potential optical-SPECT imaging agent. MedChemComm. 2015;6(2):363–71.

    Article  CAS  Google Scholar 

  214. Tu C, Ma X, House A, Kauzlarich SM, Louie AY. PET imaging and biodistribution of silicon quantum dots in mice. ACS Med Chem Lett. 2011;2(4):285–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  215. Fazaeli Y, Zare H, Karimi S, Feizi S. 68Ga CdTe/CdS fluorescent quantum dots for detection of tumors: investigation on the effect of nanoparticle size on stability and in vivo pharmacokinetics. Radiochim Acta. 2020;108(7):565–72.

    Article  CAS  Google Scholar 

  216. Zhao Y, Shaffer TM, Das S, Pérez-Medina C, Mulder WJ, Grimm J. Near-infrared quantum dot and 89Zr dual-labeled nanoparticles for in vivo Cerenkov imaging. Bioconjug Chem. 2017;28(2):600–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  217. Madru R, Kjellman P, Olsson F, Wingårdh K, Ingvar C, Ståhlberg F, et al. 99mTc-labeled superparamagnetic iron oxide nanoparticles for multimodality SPECT/MRI of sentinel lymph nodes. J Nucl Med. 2012;53(3):459–63.

    Article  CAS  PubMed  Google Scholar 

  218. Sandiford L, Phinikaridou A, Protti A, Meszaros LK, Cui X, Yan Y, et al. Bisphosphonate-anchored PEGylation and radiolabeling of superparamagnetic iron oxide: long-circulating nanoparticles for in vivo multimodal (T1 MRI-SPECT) imaging. ACS Nano. 2013;7(1):500–12.

    Article  CAS  PubMed  Google Scholar 

  219. Chen F, Ellison PA, Lewis CM, Hong H, Zhang Y, Shi S, et al. Chelator-free synthesis of a dual-modality PET/MRI agent. Angew Chem Int Ed. 2013;52(50):13319–23.

    Article  CAS  Google Scholar 

  220. Israel LL, Karimi F, Bianchessi S, Scanziani E, Passoni L, Matteoli M, et al. Surface metal cation doping of maghemite nanoparticles: modulation of MRI relaxivity features and chelator-free 68Ga-radiolabelling for dual MRI-PET imaging. Materials Research Express. 2015;2(9): 095009.

    Article  Google Scholar 

  221. Pellico J, Ruiz-Cabello J, Saiz-Alía M, del Rosario G, Caja S, Montoya M, et al. Fast synthesis and bioconjugation of 68Ga core-doped extremely small iron oxide nanoparticles for PET/MR imaging. Contrast Media Mol Imaging. 2016;11(3):203–10.

    Article  CAS  PubMed  Google Scholar 

  222. Chakravarty R, Valdovinos HF, Chen F, Lewis CM, Ellison PA, Luo H, et al. Intrinsically germanium-69-labeled iron oxide nanoparticles: synthesis and in-vivo dual-modality PET/MR imaging. Adv Mater. 2014;26(30):5119–23.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  223. Lee H-Y, Li Z, Chen K, Hsu AR, Xu C, Xie J, et al. PET/MRI dual-modality tumor imaging using arginine-glycine-aspartic (RGD)–conjugated radiolabeled iron oxide nanoparticles. J Nucl Med. 2008;49(8):1371–9.

    Article  CAS  PubMed  Google Scholar 

  224. Gholipour N, Akhlaghi M, Kheirabadi AM, Geramifar P, Beiki D. Development of Ga-68 labeled, biotinylated thiosemicarbazone dextran-coated iron oxide nanoparticles as multimodal PET/MRI probe. Int J Biol Macromol. 2020;148:932–41.

    Article  CAS  PubMed  Google Scholar 

  225. Unak P, Tekin V, Guldu OK, Aras O. 89Zr labeled Fe3O4@TiO2 nanoparticles: in vitro afffinities with breast and prostate cancer cells. Appl Organomet Chem. 2020;34(5): e5616.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  226. Tsoukalas C, Psimadas D, Kastis GA, Koutoulidis V, Harris AL, Paravatou-Petsotas M, et al. A novel metal-based imaging probe for targeted dual-modality SPECT/MR imaging of angiogenesis. Front Chem. 2018;6:224.

    Article  PubMed  PubMed Central  Google Scholar 

  227. McDevitt MR, Chattopadhyay D, Jaggi JS, Finn RD, Zanzonico PB, Villa C, et al. PET imaging of soluble yttrium-86-labeled carbon nanotubes in mice. PLoS ONE. 2007;2(9): e907.

    Article  PubMed  PubMed Central  Google Scholar 

  228. Cornelissen B, Able S, Kersemans V, Waghorn PA, Myhra S, Jurkshat K, et al. Nanographene oxide-based radioimmunoconstructs for in vivo targeting and SPECT imaging of HER2-positive tumors. Biomaterials. 2013;34(4):1146–54.

    Article  CAS  PubMed  Google Scholar 

  229. Shi S, Xu C, Yang K, Goel S, Valdovinos HF, Luo H, et al. Chelator-free radiolabeling of nanographene: breaking the stereotype of chelation. Angew Chem Int Ed. 2017;56(11):2889–92.

    Article  CAS  Google Scholar 

  230. Sarpaki S, Cortezon-Tamarit F, De Aguiar S, Exner R, Divall D, Arrowsmith R, et al. Radio-and nano-chemistry of aqueous Ga(III) ions anchored onto graphene oxide-modified complexes. Nanoscale. 2020;12(12):6603–8.

    Article  CAS  PubMed  Google Scholar 

  231. Wei Q, Zhan L, Juanjuan B, Jing W, Jianjun W, Taoli S, et al. Biodistribution of co-exposure to multi-walled carbon nanotubes and nanodiamonds in mice. Nanoscale Res Lett. 2012;7(1):1–9.

    Article  Google Scholar 

  232. Satpati D, Satpati A, Pamale Y, Kumar C, Sharma R, Sarma HD, et al. 177 Lu-labeled carbon nanospheres: a new entry in the field of targeted radionanomedicine. RSC Adv. 2016;6(56):50761–9.

    Article  CAS  Google Scholar 

  233. Ormsby RW, McNally T, Mitchell CA, Musumeci A, Schiller T, Halley P, et al. Chemical modification of multiwalled carbon nanotube with a bifunctional caged ligand for radioactive labelling. Acta Mater. 2014;64:54–61.

    Article  CAS  Google Scholar 

  234. Ruggiero A, Villa CH, Holland JP, Sprinkle SR, May C, Lewis JS, et al. Imaging and treating tumor vasculature with targeted radiolabeled carbon nanotubes. Int J Nanomed. 2010;5:783.

    CAS  Google Scholar 

  235. Biagiotti G, Pisaneschi F, Gammon ST, Machetti F, Ligi MC, Giambastiani G, et al. Multiwalled carbon nanotubes for combination therapy: a biodistribution and efficacy pilot study. J Mater Chem B. 2019;7(16):2678–87.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  236. Liu Z, Cai W, He L, Nakayama N, Chen K, Sun X, et al. In vivo biodistribution and highly efficient tumour targeting of carbon nanotubes in mice. Nat Nanotechnol. 2007;2(1):47–52.

    Article  CAS  PubMed  Google Scholar 

  237. Ahmadi M, Ebrahimnia M, Shahbazi M-A, Keçili R, Ghorbani-Bidkorbeh F. Microporous metal–organic frameworks: synthesis and applications. J Ind Eng Chem. 2022;115:1–11.

    Article  CAS  Google Scholar 

  238. Ahmadi M, Ayyoubzadeh SM, Ghorbani-Bidkorbeh F, Shahhosseini S, Dadashzadeh S, Asadian E, et al. An investigation of affecting factors on MOF characteristics for biomedical applications: a systematic review. Heliyon. 2021;7(4): e06914.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  239. Masoudifar R, Pouyanfar N, Liu D, Ahmadi M, Landi B, Akbari M, et al. Surface engineered metal-organic frameworks as active targeting nanomedicines for mono- and multi-therapy. Appl Mater Today. 2022;29: 101646.

    Article  Google Scholar 

  240. deKrafft KE, Xie Z, Cao G, Tran S, Ma L, Zhou OZ, et al. Iodinated nanoscale coordination polymers as potential contrast agents for computed tomography. Angew Chem. 2009;121(52):10085–8.

    Article  Google Scholar 

  241. Taylor KM, Rieter WJ, Lin W. Manganese-based nanoscale metal–organic frameworks for magnetic resonance imaging. J Am Chem Soc. 2008;130(44):14358–9.

    Article  CAS  PubMed  Google Scholar 

  242. Zanzonico P. Principles of nuclear medicine imaging: planar, SPECT, PET, multi-modality, and autoradiography systems. Radiat Res. 2012;177(4):349–64.

    Article  CAS  PubMed  Google Scholar 

  243. Chen D, Yang D, Dougherty CA, Lu W, Wu H, He X, et al. In vivo targeting and positron emission tomography imaging of tumor with intrinsically radioactive metal–organic frameworks nanomaterials. ACS Nano. 2017;11(4):4315–27.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  244. Zhu W, Yang Y, Jin Q, Chao Y, Tian L, Liu J, et al. Two-dimensional metal-organic-framework as a unique theranostic nano-platform for nuclear imaging and chemo-photodynamic cancer therapy. Nano Res. 2019;12(6):1307–12.

    Article  CAS  Google Scholar 

  245. Tao Y, Sun Y, Shi K, Pei P, Ge F, Yang K, et al. Versatile labeling of multiple radionuclides onto a nanoscale metal–organic framework for tumor imaging and radioisotope therapy. Biomaterials Science. 2021;9(8):2947–54.

    Article  CAS  PubMed  Google Scholar 

  246. Goins BA. Radiolabeled lipid nanoparticles for diagnostic imaging. Expert Opin Med Diagn. 2008;2(7):853–73.

    Article  CAS  PubMed  Google Scholar 

  247. Thakor AS, Jokerst JV, Ghanouni P, Campbell JL, Mittra E, Gambhir SS. Clinically approved nanoparticle imaging agents. J Nucl Med. 2016;57(12):1833–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  248. Phillips E, Penate-Medina O, Zanzonico PB, Carvajal RD, Mohan P, Ye Y, et al. Clinical translation of an ultrasmall inorganic optical-PET imaging nanoparticle probe. Sci Transl Med. 2014;6(260):260ra149–260ra149.

  249. Benezra M, Penate-Medina O, Zanzonico PB, Schaer D, Ow H, Burns A, et al. Multimodal silica nanoparticles are effective cancer-targeted probes in a model of human melanoma. J Clin Investig. 2011;121(7):2768–80.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  250. Ow H, Larson DR, Srivastava M, Baird BA, Webb WW, Wiesner U. Bright and stable core− shell fluorescent silica nanoparticles. Nano Lett. 2005;5(1):113–7.

    Article  CAS  PubMed  Google Scholar 

  251. Rietbergen DD, Meershoek P, KleinJan GH, Donswijk M, Olmos RAV, van Leeuwen FW, et al. Head-to-head comparison of the hybrid tracer indocyanine green-99mTc-nanocolloid with 99mTc-Senti-Scint using sentinel node lymphoscintigraphy and single-photon emission computed tomography combined with computer tomography in melanoma. Nucl Med Commun. 2020;41(10):1010–7.

    Article  CAS  PubMed  Google Scholar 

  252. Tokin CA, Cope FO, Metz WL, Blue MS, Potter BM, Abbruzzese BC, et al. The efficacy of Tilmanocept in sentinel lymph mode mapping and identification in breast cancer patients: a comparative review and meta-analysis of the 99mTc-labeled nanocolloid human serum albumin standard of care. Clin Exp Metastasis. 2012;29(7):681–6.

    Article  CAS  PubMed  Google Scholar 

  253. Thakor AS, Jokerst JV, Ghanouni P, Campbell JL, Mittra E, Gambhir SS. Clinically approved nanoparticle imaging agents. Soc Nuclear Med. 2016;57(12):1833–7.

  254. Phillips E, Penate-Medina O, Zanzonico PB, Carvajal RD, Mohan P, Ye Y, et al. Clinical translation of an ultrasmall inorganic optical-PET imaging nanoparticle probe. Science. 2014;6(260):260ra149–260ra149.

Download references

Acknowledgements

The authors would like to thank the research deputy of Shahid Beheshti University of Medical Sciences.

Author information

Authors and Affiliations

  1. Department of Pharmaceutics and Pharmaceutical Nanotechnology, School of Pharmacy, Shahid Beheshti University of Medical Sciences, Tehran, Iran

    Mahnaz Ahmadi & Marjan Emzhik

  2. Department of Pharmaceutical Chemistry and Radiopharmacy, School of Pharmacy, Shahid Beheshti University of Medical Sciences, Niayesh Junction, Vali-E-Asr Ave, Tehran, 14155-6153, Iran

    Mona Mosayebnia

Authors
  1. Mahnaz Ahmadi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marjan Emzhik
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mona Mosayebnia
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

The study conception was carried out by Mosayebnia M. All authors equally contributed to the material preparation, article collection, and writing of the first draft of the manuscript. All authors read and approved the final manuscript as well.

Corresponding author

Correspondence to Mona Mosayebnia.

Ethics declarations

Ethics approval and consent to participate

Not applicable

Consent for publication

Not applicable

Competing interests

The authors declare no competing interests.

Additional information

Publisher's Note

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

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ahmadi, M., Emzhik, M. & Mosayebnia, M. Nanoparticles labeled with gamma-emitting radioisotopes: an attractive approach for in vivo tracking using SPECT imaging. Drug Deliv. and Transl. Res. 13, 1546–1583 (2023). https://doi.org/10.1007/s13346-023-01291-1

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13346-023-01291-1

Keywords

Search

Navigation