Physics Reports 1043 (2023) 1–35 Contents lists available at ScienceDirect Physics Reports journal homepage: www.elsevier.com/locate/physrep Iron oxide nanoparticles (Fe3 O4 , γ -Fe2 O3 and FeO) as photothermal heat mediators in the first, second and third biological windows A.G. Roca a , J.F. Lopez-Barbera a , A. Lafuente a , F. Özel a,b , E. Fantechi a,c , ∗ J. Muro-Cruces a , M. Hémadi d , B. Sepulveda e , , J. Nogues a,f a Catalan Institute of Nanoscience and Nanotechnology (ICN2), CSIC and BIST, Campus UAB, Bellaterra, 08193 Barcelona, Spain b Department of Physics, Gebze Technical University, 41400 Gebze, Kocaeli, Turkey c Centro di Cristallografia Strutturale (CRIST), Università degli Studi di Firenze, Sesto Fiorentino 50019 Firenze, Italy d Université Paris Cité, CNRS-UMR 7086, Interfaces, Traitements, Organization et Dynamique des Systèmes (ITODYS), Paris, France e Instituto de Microelectrónica de Barcelona (IMB-CNM, CSIC), Campus UAB, Bellaterra, 08193 Barcelona, Spain f ICREA, Pg. Lluís Companys 23, 08010 Barcelona, Spain article info a b s t r a c t Article history: Nanotherapies are gaining increased interest for the treatment diverse diseases, par- Received 6 August 2023 ticularly cancer, since they target the affected area directly, presenting higher efficacy Accepted 6 October 2023 and reduced side effects than traditional therapies. A promising nanotherapy approach Available online 4 November 2023 is hyperthermia, where the nanoparticle can induce a local temperature increase by Editor: Gerrit E.W. Bauer an external stimulus in the sick tissue to selectively kill the malignant cells. Among Keywords: the diverse hyperthermia methods, photothermia is based on the absorption of light Iron oxides by the nanoparticles and further conversion into heat. Within the very wide range Photothermal mediators of nanostructured photothermal agents, iron oxides offer remarkable features since Photothermia they are already approved by the FDA/EMA for various biomedical applications, they Fe3 O4 , FeO are biodegradable, easily manipulated using magnetic fields and can be imaged by Wüstite diverse techniques. Here, we summarize the advantages of using the second biological γ -Fe2 O3 First biological window window, both from the perspective of the skin and the optical properties of iron Second biological window oxides. Further, we review the photothermal performance of iron oxide nanoparticles Absorption in the first, second and third biological windows. Overall, the results show that, for Photothermal efficiency different types of iron oxide nanoparticles (Fe3 O4 , γ -Fe2 O3 , wüstite-FeO), both the NIR-I, NIR-II heating capacity (i.e., induced temperature increase) and the photothermal conversion NIR-III efficiency, η, vary in a complex way with the light wavelength, depending critically on Nanotherapies the measurement conditions and physiochemical properties of the materials. Despite Photothermal applications the spread in the reported photothermal properties of iron oxides, Fe3 O4 particles tend to perform better than their γ -Fe2 O3 counterparts, particularly in the second biological window. Interestingly, FeO, which has not been exploited so far from a photothermal perspective, shows very appealing absorption properties. Our preliminary studies using FeO/Fe3 O4 core/shell nanoparticles evidence that they have excellent photothermal properties, outperforming Fe3 O4 in both first and second biological windows. Finally, some applications beyond cancer treatment of iron oxide nanoparticles, exploiting the enhanced properties in the second spectral window, are discussed. © 2023 The Author(s). Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). Contents 1. Introduction................................................................................................................................................................................... 2 ∗ Corresponding author. E-mail addresses: alejandro.gomez@icn2.cat (A.G. Roca), borja.sepulveda@csic.es (B. Sepulveda), josep.nogues@icn2.cat (J. Nogues). https://doi.org/10.1016/j.physrep.2023.10.003 0370-1573/© 2023 The Author(s). Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons. org/licenses/by-nc-nd/4.0/). A.G. Roca, J.F. Lopez-Barbera, A. Lafuente et al. Physics Reports 1043 (2023) 1–35 2. Optical considerations for photothermia ................................................................................................................................... 4 2.1. Optical absorption of the skin ........................................................................................................................................ 4 2.2. Optical absorption of the heat mediator: Fe3 O4 versus γ -Fe2 O3 ............................................................................... 5 3. Photothermal performance of Fe3 O4 in the first, second and third optical windows ......................................................... 7 3.1. First biological window ................................................................................................................................................... 7 3.2. Second biological window .............................................................................................................................................. 9 3.3. Third biological window ................................................................................................................................................. 10 4. In vitro and in vivo photothermal therapies of Fe3 O4 in the first and second optical windows ....................................... 11 5. FeO (wüstite) as a potential photothermal heat mediator...................................................................................................... 12 6. Other potential uses of iron oxide nanoparticles in the second biological window ........................................................... 14 6.1. Combined photothermal treatments for oncology....................................................................................................... 14 6.2. Non-oncological biomedical applications of photothermal therapy .......................................................................... 15 6.3. Diagnosis: Imaging agents and sensing......................................................................................................................... 15 6.4. Environment-related applications .................................................................................................................................. 15 6.5. Energy-related applications ............................................................................................................................................ 16 7. Conclusions.................................................................................................................................................................................... 16 Declaration of competing interest .............................................................................................................................................. 16 Acknowledgements....................................................................................................................................................................... 17 Annex A. Simulation of the absorption and scattering cross sections of different iron oxides .......................................................... 17 Annex B. Sample preparation ...................................................................................................................................................................... 17 B.1. Preparation of the nanoparticles. ................................................................................................................................... 17 B.2. Morphological characterization ...................................................................................................................................... 18 Annex C. Methods ......................................................................................................................................................................................... 18 C.1. Transmission electron microscopy................................................................................................................................. 18 C.2. Extinction measurements................................................................................................................................................ 18 C.3. Photothermal measurements.......................................................................................................................................... 19 Annex D. Water absorbance spectrum........................................................................................................................................................ 21 Annex E. Remote manipulation of the FeO/Fe3 O4 nanocubes by a magnetic gradient........................................................................ 21 References...................................................................................................................................................................................... 21 1. Introduction Hyperthermal nanotherapies (e.g., magnetic hyperthermia and photothermia, among others) [1–4] mediated by nanometric thermal agents are gaining increasing interest as local therapies with minimal systemic side effects for cancer treatment [5–31]. The principle of the hyperthermal nanotherapies is to induce a local temperature increase by an external stimulus (e.g., light, magnetic field, ultrasounds, among others) only at the site of action (e.g., the tumor) to produce a controlled death of the malignant cells. The local character of the treatment is a result of the presence of heat-mediator nanostructures only inside the sick tissues, which heat up as a response to the external stimulus and the focused irradiation, only in the area of interest (see Fig. 1). The local character of the effect generates minimal effects in healthy neighbouring tissues, thus resulting in minimal side effects. The particular interest of hyperthermal therapies for cancer treatment is based on the fact that cancerous cells are more sensitive to heat than healthy cells [2]. In addition, the heat dissipation in tumors is less effective than in healthy tissues, making them more prone to heat-induced cell death [2]. In the case of photothermal therapies (PTT) in the near infrared (NIR) many different types of nanostructured mediators have been proposed, such as plasmonic nanoparticles (e.g., Au nanoparticles), carbon-based materials, organic dyes, transition metal oxide nanoparticles or chalcogenide nanostructured materials [5–23]. Interestingly, ferrimagnetic iron oxide nanoparticles (e.g., magnetite — Fe3 O4 and maghemite — γ -Fe2 O3 ) often form part of composite nanostructures accompanying classical photothermal mediators (e.g., Au plasmonic nanoparticles, carbon-based materials, organic mate- rials or chalcogenides) [32,33]. However, their role is not related to their potential photothermal properties, but to their magnetic properties. In fact, iron oxide nanoparticles have very appealing features, since their magnetic character allows them to be easily guided to and concentrated in tumors using magnetic field gradients [34,35], which can be appealing not only for hyperthermal treatments but also to deliver drugs to sick tissues [36]. Moreover, iron oxide nanoparticles can be tracked in vivo by different imaging techniques (e.g., magnetic resonance imaging, MRI – both in T2 and T1 modes – [37,38], magnetic particle imaging, MPI [39–41], magneto-acoustic imaging [42] and photo-acoustic imaging [43]) or they can be used as heat mediators for magnetic hyperthermia [44,45]. Although from the hyperthermia point of view iron oxide nanoparticles have been traditionally studied mainly as mediators for magnetic hyperthermia [44,45], in recent years, the importance of Fe3 O4 and γ -Fe2 O3 nanoparticles as stand-alone photothermal agents (i.e., without the presence of other photothermal mediators) has been put forward, thereby continuously increasing the interest in iron oxides (particularly Fe3 O4 ) for biomedical photothermia [46] (and other photothermal-related applications). Most of the photothermal applications of Fe3 O4 nanoparticles have been carried out in the so-called first biological window (wavelength λ between 650 nm and 950 nm; NIR-I; typically using λ = 808 nm, although other wavelengths have been used, such as 650, 660, 665, 671, 680, 690, 694, 730, 750, 785, 800, 810, 850, 885, 900 nm and even 980 nm) 2 A.G. Roca, J.F. Lopez-Barbera, A. Lafuente et al. Physics Reports 1043 (2023) 1–35 Fig. 1. (a) Schematic representation of the basic mechanism of the nanoparticle-mediated photothermal therapy. (b) Cartoon summarizing the advantages of using iron oxide nanoparticles in the second biological window (NIR-II). [47–349]. Interestingly, the optical absorption of Fe3 O4 in the second optical window (λ between 1000 nm and 1350 nm; NIR-II) is considerably higher than in the first biological window. This has triggered the interest in using iron oxides as photothermal mediators in the second NIR window, typically using λ = 1064 nm (although other wavelengths have been reported, e.g., 1000, 1053, 1090 or 1280 nm) [54,346–360]. Note also that although there are other biological windows (e.g., the third biological window, λ between 1550 nm and 1870 nm; NIR-III or even a possible fourth biological window, λ ∼2100 nm–2300 nm; NIR-IV) [361–363] no photothermal treatments using iron oxides in the NIR-III or NIR-IV ranges have been reported. Notably, there is a range of potential benefits of using iron oxide nanoparticles as stand-alone photothermal mediators instead of being one of the moieties in multicomponent particles, such as: (i) reduced complexity of the synthesis compared to composite, making the synthetic approach simpler, more reproducible and easier to scale-up [364–372] (ii) biodegradability, and avoidance of toxic materials [373] or materials not approved by the US Food and Drug Administration (FDA) or the European Medicines Agency (EMA) [374–376]; (iii) larger averaged magnetization, making easier the mag- netic manipulation of the particles (e.g., magnetic targeting and magnetic concentration inside the tumors) using lower fields than for composite materials; (iv) low cost and abundance of Fe (in contrast to, for example, Au); (v) robustness and endurance of oxide nanoparticles (particularly compared to, for example, organic or polymeric nanoparticles); (vi) far weaker sensitivity of the photothermal performance of iron oxide particles to size or shape dispersion than in other heat mediators (particularly, plasmonic nanoparticles); (vii) capacity to be used not only as heat mediators in magnetic hyperthermia [44,45], and photothermia [32,33,46], but also in microwave- or ultrasound-based hyperthermia [377–381]; (viii) capability of iron oxides for multimode imaging and sensing, which make them very powerful ‘‘single-particle’’ theranostic agents (therapy + diagnostic); (ix) long tradition of laser therapies (particularly in the NIR) for a myriad of health and cosmetic issues, ranging from neurological or retinal diseases to teeth cleaning or acne removal, in contrast to the therapeutic use of magnetic fields (e.g., magnetic hyperthermia); (x) additional mechanical therapeutic mode to induce cell lysis, by using non-spherical morphologies (particularly nanorods or platelets) of iron oxide nanoparticles that be efficiently rotated by magnetic fields [347]; (xi) enhanced internalization by cancer cells since they use iron for growth [382]; (xii) the additional ferroptosis-programmed cell death mechanism of Fe-based nanomaterials, which in combination with photothermally induced apoptosis can enhance nanoparticle-mediated cell death [46,383–385]; and (xiii) the very broad range of therapeutic uses of iron oxide nanoparticles, such as anti-bacterial, anti-inflammatory, anti-anemia, anti-viral, or even for neurological diseases, among others [386–392]. Interestingly, high quality iron oxide nanoparticles can be easily synthesized in a broad range of sizes and shapes (e.g., spheres, cubes, platelets, nanorods) and morphologies (like clusters, porous particles, urchin-like particles, hollow particles or chains of particles) [393–398]. However, the controlled growth of composite nanoparticles (e.g., dimers or core/shell structures) can be rather cumbersome and often difficult to scale up [364–372]. It is also important to emphasize that iron oxides (Fe3 O4 and γ -Fe2 O3 ) have already been extensively used in different biomedical applications [399–422] and are highly biocompatible and biodegradable, being their metabolic and secretion routes inside the body well known [423–425]. In fact, they are the only magnetic materials approved by the FDA and EMA for their use in humans [374–376]. Actually, iron oxides have already been proposed for the treatment of a great number of diseases and as diagnosis tools. As a matter of fact, several iron oxide-based treatments have been commercialized for diverse diagnostic and therapeutic uses [400,407,426,427]. 3 A.G. Roca, J.F. Lopez-Barbera, A. Lafuente et al. Physics Reports 1043 (2023) 1–35 Fig. 2. Dependence of (a) the absorption coefficient, µA , and (b) the optical penetration depth, δ , of the skin on the light wavelength. The shaded areas represent the first (NIR-I), second (NIR-II) and third (NIR-III) biological windows. The typical wavelengths used experimentally in photothermia in the NIR-I and NIR-II regions (λ = 808 nm and 1064 nm, respectively) are highlighted by vertical lines. Source: Adapted from Ref. [432]. Here, we review the use of iron oxide nanoparticles as independent photothermal mediators (for a broad range of applications) and discuss the advantages of Fe3 O4 and FeO/Fe3 O4 nanoparticles for photothermal applications in the second biological window. 2. Optical considerations for photothermia 2.1. Optical absorption of the skin As a first step for any photothermal cancer treatment it is important to establish how deeply light will penetrate into the organ of interest, since this will establish the viability of photothermia to treat the cancer. Since NIR light does not enter significantly into human tissues and organs, photothermia would be best suited for subcutaneous cancers. Nevertheless, for other types of cancers minimally invasive catheters with optical fibres to guide the light into the area of interest could be used. Remarkably, it is worth mentioning that novel approaches to enhance the penetration of light in biological tissues (like larger laser spots or optical clearing technology) are being investigated [428,429]. In the literature there are numerous studies of the optical properties (absorption, scattering, refractive index) of human skin, other organs and tissue components (e.g., blood, fat, bone) [430,431]. To a first approximation, the absorption coefficient would provide an indication of the penetration depth of light in the body, although tissue light scattering should also be considered. It is well established that NIR light penetrates deeper into the human body than visible light, which has led to the concept of NIR biological windows. In the particular case of the skin, light presents low absorption in the NIR-I and NIR-II ranges (λ = 600 nm–1300 nm; see Figure 2a) [432–435]. Interestingly, the absorption at λ = 808 nm (first biological window) is larger than at λ = 1064 nm (second biological window), where absorption has a local minimum. The lower absorption combined with the weaker scattering at λ = 1064 nm translates into a considerably higher penetration of light through the skin at this wavelength compared to λ = 808 nm (see Fig. 2b). Note that the optical penetration depth is given by 1 δ= √ 3µA (µA + µ′S ) where µA is the absorption coefficient and µ’S is the reduced scattering coefficient given by µ′S = µS (1 − g) where µS the scattering coefficient and g the anisotropy factor [432]. However, it has to be taken into account that different skin pigmentations and other tissues and organs may have different light absorption and scattering properties [430,431,434–436]. Thus, from the purely optical viewpoint of light penetration into the skin, λ = 1064 nm would be favoured over λ = 808 nm for photothermal treatments. 4 A.G. Roca, J.F. Lopez-Barbera, A. Lafuente et al. Physics Reports 1043 (2023) 1–35 Fig. 3. Dependence of the skin maximum permissible exposure, MPE, of skin on the laser wavelength, λ. The shaded areas represent the first (NIR-I), second (NIR-II) and third (NIR-III) biological windows. The typical wavelengths used experimentally in photothermia in the NIR-I and NIR-II regions (λ = 808 nm and 1064 nm, respectively) are highlighted by vertical lines. Source: Adapted from Ref. [438]. Concerning the use of light on the skin (or other tissues) another factor which must be taken into account is the maximum permissible exposure (MPE). Namely, the highest light power which has a negligible probability for inducing damage to the irradiated region. It is important to highlight that the power used to excite the nanoparticles will determine the maximum heat that they can generate. According to the standard of the American National Standard for Safe Use of Lasers [437], the MPE depends on the wavelength and the duration of the irradiation exposure. As can be seen in Fig. 3, for human skin, in the NIR range and for durations longer than 10 s, the MPE is given by 0.2 × 102(λ/1000−0.7) W/m2 in the 700 nm–1050 nm range and 1 W/m2 (in the 1050 nm–1400 nm range) [438]. This implies that the MPE for λ = 808 nm (MPE = 0.33 W/cm2 ) is significantly lower than for λ = 1064 nm (MPE = 1.0 W/cm2 ) (see Fig. 3). Consequently, from the MPE viewpoint λ = 1064 nm would, again, be favoured over λ = 808 nm, since it allows the use of higher laser powers and, thus, the possibility of inducing a larger temperature increase. Consequently, from purely optical considerations of the human skin, the use of lasers in the second biological window (e.g., λ = 1064 nm) should be more efficient for photothermal treatments (Fig. 1b). Moreover, note that from the skin optics perspective, the use of the third biological window would, in principle, not be especially beneficial due to the limited light penetration (Fig. 2b) and the low MPE at these wavelengths (Fig. 3). 2.2. Optical absorption of the heat mediator: Fe3 O4 versus γ -Fe2 O3 Another important factor to take into consideration for photothermal applications is how much light the heat mediators can absorb since this will determine in the first instance the induced heat, although other factors like the scattering should also be considered [5–23]. Firstly, for Fe3 O4 and γ -Fe2 O3 , one has to bear in mind that although the two materials are structurally very similar (inverse spinel structure for both iron oxides), some of their physicochemical properties can differ considerably. In particular, while γ -Fe2 O3 is a semiconductor with a band gap of 2.0 eV, Fe3 O4 is almost metallic with a band gap of 0.1 eV [439]. Concerning their optical absorption, from a theoretical viewpoint, we have simulated (see Annex A for details) the absorption and scattering cross-sections of Fe3 O4 and γ -Fe2 O3 nanoparticles based on their bulk dielectric constants [440]. Notably, the simulations show remarkable differences between the two materials. Particularly, the absorption cross section, µA , for γ -Fe2 O3 decreases steadily in the NIR region. On the other hand, for Fe3 O4 , while the absorption decreases in the first NIR biological window, it increases considerably in the second NIR range, having a maximum around λ ∼1400 nm and slowly decreasing for longer wavelengths (in the third window) (Fig. 4a). Additionally, the scattering cross section (µS ) for γ -Fe2 O3 is remarkably larger than for Fe3 O4 in all the NIR regions (Fig. 4b). These marked differences between the two materials stem from the presence of Fe2+ ions in Fe3 O4 , where the charge-transfer transitions between Fe2+ and Fe3+ ions provide a wide and intense absorption band in the NIR region, which is not present in γ -Fe2 O3 [441,442]. It is also important to emphasize that experimentally, usually the extinction, µE , (absorption + scattering; µE = µA + µS ) rather than the absorption is measured. Moreover, although the experimental optical absorption/extinction of iron oxide nanoparticles (Fe3 O4 and γ -Fe2 O3 ) has been extensively studied, there are rather few studies extending over the three NIR biological windows. Nevertheless, some of the available experimental results confirm our simulation studies in 5 A.G. Roca, J.F. Lopez-Barbera, A. Lafuente et al. Physics Reports 1043 (2023) 1–35 Fig. 4. Dependence of the simulated (a) absorption, µA (Cabs ), and (b) scattering, µS (Cscat ), cross-sections for γ -Fe2 O3 and Fe3 O4 . (c,d) Experimental wavelength dependence of the extinction, µE , for 12.7 nm spherical nanoparticles of (c) Fe3 O4 and (d) γ -Fe2 O3 [352]. The shaded areas represent the first (NIR-I), second (NIR-II) and third (NIR-III) biological windows. The typical wavelengths used experimentally in photothermia in the NIR-I and NIR-II regions (λ = 808 nm and 1064 nm, respectively) are highlighted by vertical lines. the NIR-I and NIR-II ranges [54,346,351–353,443,444]. Namely, the extinction of γ -Fe2 O3 steadily decreases in the NIR region (Fig. 4c). On the other hand, although the extinction of Fe3 O4 decreases in the NIR-I, it shows a significant upturn in the NIR-II range (Fig. 4c). Notably, both the simulated µA and the experimental extinction of Fe3 O4 show a dip in the 700–800 nm region, which covers a large part of the NIR-I range. However, it is worth mentioning that in iron oxides the absorption in the NIR-I and NIR-II ranges could be enhanced by potential plasmonic effects, particularly for very small non-stoichiometric Fe3−x O4 nanoparticles [444]. The simulated and experimental absorption and extinction results have significant for photothermal applications. Namely, (i) γ -Fe2 O3 is expected to show poor light-induced heating in the whole NIR range, and (ii) a much higher temperature increase is expected for Fe3 O4 in the whole NIR region, with an important enhancement in the NIR-II/III regions. Consequently, based on these optical properties of iron oxides, Fe3 O4 would be favoured over γ -Fe2 O3 for photothermal applications. In addition, in the case of Fe3 O4 , NIR-II would be, in principle, more appealing for photothermal treatments. Importantly, given the rather strong dependence of the absorption in the NIR-II on the oxidation state of the iron oxide (see Figure 4) [440,441,445–447], the quality of the Fe3 O4 nanoparticles (e.g., degree of oxidation, vacancies, antiphase boundaries) may play a fundamental role on their photothermal performance. Interestingly, from the absorption viewpoint, the third biological window in Fe3 O4 may be an appealing alternative for certain applications, although, in principle it may not be so favourable from the skin optics perspective (Figures 2 and 3). Finally, it is important to highlight that comparing Fe3 O4 to Au nanoparticles (i.e., a typical PTT heat mediator), the complex refractive index, n = n′ + in ′′ , of Fe3 O4 relative to water (n′ ≳ 1.6) [448] is much higher than that of Au (n′ ≈ 10−1 ) [449]. Moreover, in the NIR the imaginary part for Fe3 O4 (relative to water), n′′ ≳ 0.4, is lower than that of Au, n′′ ≳ 1.5. These differences in n between Fe3 O4 and Au imply that while light penetrates in Fe3 O4 leading to an enhanced energy absorption, Au presents higher light scattering [450]. Consequently, even if µA is moderate for Fe3 O4 compared to other conventional photothermal heat mediators, its overall optical properties make it very attractive for photothermia. 6 A.G. Roca, J.F. Lopez-Barbera, A. Lafuente et al. Physics Reports 1043 (2023) 1–35 Fig. 5. Dependence of the increased temperature, ∆T, for (a) different concentrations (at 4 W/cm2 ) and (b) laser powers (at 3 nM; 1.68 · 10−7 mg/mL) for Fe3 O4 clusters (∼64 nm) using λ = 808 nm irradiation [50]. 3. Photothermal performance of Fe3 O4 in the first, second and third optical windows 3.1. First biological window There is a large number of studies of the photothermal efficiency of iron oxide nanoparticles (mostly Fe3 O4 ) in the first biological window (mostly using λ = 808 nm, although other wavelengths have also been used). Importantly, these studies do not only involve cancer treatment, but a myriad of other applications [47–349]. It is important to emphasize that many investigations, although they involve composite nanoparticles combining iron oxides and other heat mediators, show that the iron oxide counterpart accounts for a significant part of the heating properties of the composite [53,58,71,78,94,102, 107,110,115,116,120,122,125–128,130,132–134,138,143,147,149,150,158,166–168,170,172,173,178,189,191,197,221,223, 225,238,242,243,250,257,261,262,276,277,282,288,292,302,303,306,308,312,313,323,325,328,334,339,341–343]. In fact, many studies show that Fe3 O4 nanoparticles are relatively good heat mediators in the first optical window, with temperature increases, ∆T, typically above 20 ◦ C [47–51,56,59,61,63,69,71,75,77,79,84–97,101,102,105,107–109,113–117, 119,123,124,126,129,131,133,137,143,144,146–149,152–157,160–162,165,170–174,176,177,179,180,182,184,187,188,192, 193–196,198,199,203,207–211,213–219,222,224,227,230,232,237,241–244,247,250,252,253,255,258,260,261,263,264, 268–272,278–281,283,287,288,291,292,296,299,302,305–308,310,312,314,316,319–323,326,329,331,334,336,338,341,344, 345,347]. However, ∆T values expanding from 0 ◦ C to above 100 ◦ C can be found in the literature, depending on the experimental conditions (e.g., type of particle, concentration, laser power and so on) [47–349]. Interestingly, although ∆T increases linearly with nanoparticle concentration at low concentrations [53,61,82,92,95, 110,135,136,147,151,152,156,157,159,162,165,174,180,195,199,205,215,217,224,227,246,269,271,301,313,319,347] it tends towards saturation for higher concentrations (see Fig. 5a) [47–50,54,62,63,68,69,77,79,83,85–87,90–93,97,101,117, 123,131,137,141,146,153,155,156,159,162,168,176,180,182,185,193,195,199,203,213,215,217,219,222,227,250,252,253, 255,260,269,279,291,296,303,314,319,328,331,344,345]. This stems from the fact that at higher concentrations most of the light is absorbed before reaching the particles further away from the light source. Consequently, not all the particles contribute equally to ∆T at high concentrations. Nanoparticle size and shape could potentially affect ∆T, since both factors can affect the absorption and, particularly, the scattering of the nanoparticles. However, Chu et al. showed that the nanoparticle shape (spherical, hexagonal, nanorods) has little influence on ∆T despite the changes in the absorption among the different shapes [47,348]. Similarly, Wen et al. showed that for small spherical Fe3 O4 nanoparticles (2.1–9.5 nm), size had virtually no effect on ∆T [56], while Zhang et al., Guo et al., Gadora et al. and Lozano-Pedraza et al. evidenced that for larger particles, size had a only a small effect on ∆T [131,148,180,348]. Nevertheless, Peng et al. showed that 5 nm spherical nanoparticles had considerably smaller ∆T than 20 nm nanoparticles [213]. One possible origin of this effect may be because, as the size of Fe3 O4 nanoparticles is reduced, the surface of the particle, which is prone to oxidation to γ -Fe2 O3 , plays a much important role. However, additional systematic studies would be necessary to establish a clear correlation between size or shape and ∆T. In fact, one has to bear in mind that since the different nanoparticles being compared are often produced using diverse approaches, their oxidation state or number and type of defects could be distinctly different. In fact, the degree of crystallinity and the number and type of particle defects (which can strongly affect the optical properties) have been shown to influence ∆T, where more crystalline particles perform better [348,355]. In fact, it has been proposed that defects may have stronger impact on photothermia than other factors such as size or oxidation state [345,355]. In addition, Guo 7 A.G. Roca, J.F. Lopez-Barbera, A. Lafuente et al. Physics Reports 1043 (2023) 1–35 et al. showed that, in contrast to in vitro, the in vivo heating efficiency depended strongly on the nanoparticle size, probably due to the different degree of internalization or the extent of the aggregation of the nanoparticles inside the tumors [180]. Another parameter which influences ∆T is the degree of nanoparticle aggregation. Namely, in some cases the effect of the controlled aggregation of nanoparticles, which form small reproducible clusters, on photothermia has been investigated. Interestingly, most of the studies show that controlled aggregation improves ∆T [50,55,59,83,84,97,108,113, 144,149,164,219,289,348], although exceedingly large aggregates may be detrimental [51,55,59,111,162,169,219]. The im- provement of ∆T for aggregates may arise from the larger absorption of the aggregates as compared to individual particles, although there is probably a trade-off between enhanced absorption and increased scattering. Namely, larger aggregates should have stronger scattering, which is detrimental to the photothermal performance. However, as mentioned earlier, it has to be taken into account that the performance of nanoparticles or aggregates in suspension can be different than in vitro or in vivo, since smaller particles tend to agglomerate uncontrollably when they are inside the cells [169], which can drastically affect their photothermal behaviour [169]. In addition, ∆T is clearly influenced by the laser intensity. Most studies show that increasing the intensity of the laser results in larger ∆T. However, although usually ∆T is roughly proportional to the intensity [52,54,68,69,83,85,101,103, 119,129,136,147,152,165,171,223,224,227,266,269,283,291,316,319,344,348], in other cases the relationship is non-linear (Figure 5b) [48,50,62,75,78,79,109,164,172,185,190,218,246,278,287,292,331]. Nevertheless, it is important to highlight that most of the studies use laser powers well above the established MPE for λ = 808 nm of 0.33 W/cm2 . Given the non-linear dependence of ∆T on diverse parameters, it is somewhat complex to compare the various studies since they use different nanoparticle size and shape, degree of aggregation, capping layers, concentrations, laser power, initial temperatures, irradiated areas or irradiation times. However, to try to quantitatively compare the efficiencies of heat mediators under diverse conditions one can use the photothermal conversion efficiency parameter: hA (Tmax − Tamb ) − Q0 η= , I(1 − 10−Aλ ) where h is the heat transfer coefficient, A is the irradiated area, Tmax is the highest temperature obtained, Tamb is the ambient temperature, Q0 is heat dissipated from light absorbed by the sample holder and the medium, I is the incident laser power and Aλ is absorbance of the sample at the wavelength λ [451]. Namely, η gives an indication of how good a given material is in converting light into heat. However, η is not an intrinsic property of the material and depends on intrinsic and extrinsic factors, like the volume of the nanoparticle, the degree of aggregation or the coating of the particles, among other factors, indicating that parameters like light scattering may play an important role in η. Namely, there is a correlation between η and the ratio between the absorption and the extinction (absorption+scattering) at the given wavelength [55,452,453]. Despite the possibility of having a more quantitative comparison between samples than that given by ∆T, only a relatively small number of the studies evaluate η for Fe3 O4 nanoparticles. Remarkably, the reported conversion efficiency values for Fe3 O4 nanoparticles show a very broad variety of values, ranging between η = 2.2% and 90% [50,51,55, 59,62,68,79,83,85,89,95,97,100–103,108,113,126,127,137,149,151,152,158,159,162,165,166,178,197,204,213,214,217,219, 227,231,233,238,248,250,254,259,285,288,291,294,297,298,301,313,314,319,331,342,348]. This implies that this param- eter is not an intrinsic property of Fe3 O4 , but depends on the specific optical properties of the nanoparticles, which are related to the oxidation state and defects, and to some extent to the concentration, size, shape and degree of aggregation of the particles or other extrinsic parameters such as the capping layers or even the measurement conditions or the details of the efficiency calculations [51,55,62,66,68,97,108,113,149,162,165,227,297,348]. Nevertheless, it is important to highlight that many of the reported values for Fe3 O4 are similar or better than most of the state-of-the-art proposed heat mediators such as Au nanorods, carbon nanotubes or metal chalcogenides, among others [11]. Interestingly, in addition to the oxidation state or defects that affect the optical properties, doping or substitutions in Fe3 O4 nanoparticles with different ions can be used to tune their absorption spectrum, which can be used to enhance η; e.g., S doping has been reported to lead to η = 58% [454], or Znx Fe3−x O4 has been shown to have a higher η than similar Fe3 O4 nanoparticles [95]. However, it is important to emphasize that the figure of merit for photothermal treatments is the ∆T obtained for a given condition, where the aim is to minimize the laser power, the duration of the treatment and the concentration of the nano heat mediators. Notably, ∆T depends in a complex way on both µA (which is how much light is absorbed by the material) and η (which is how efficient is the material in converting the absorbed light into heat). Interestingly, a systematic study of the photothermal heating capacity of Fe3 O4 nanoparticles in the λ = 730 nm–840 nm spectral region has shown that there is not a one-to-one correlation between the experimental extinction and the ∆T [52]. In fact, the lack of a clear correlation between the absorption (extinction) and ∆T is corroborated in other studies comparing different wavelengths within the NIR-I [47,48,50,51,54,59,62,63,68,297,348]. This seems to indicate a complex correlation between the heating efficiency and not only to the absorption, but also to the scattering. Nevertheless, the role of the exact oxidation state of the nanoparticles, which determines both the absorption and the scattering, should also be considered when comparing different systems [348]. 8 A.G. Roca, J.F. Lopez-Barbera, A. Lafuente et al. Physics Reports 1043 (2023) 1–35 Fig. 6. Heating curves (Annex C) for different (a) concentrations (at 0.1 W/cm2 ) and (b) laser powers (at 0.1 mg/mL) for 16 nm Fe3 O4 nanocubes (see Annex B [394]) using λ = 1064 nm irradiation. Shown in the insets is the dependence of the intrinsic heating of the particles (∆TTotal - ∆TWater ) on the respective conditions. Note that ∆TWater is different at different powers. 3.2. Second biological window Remarkably, despite the rather promising optical properties of Fe3 O4 in the NIR-II and the advantages of using this wavelength range from the skin perspective (i.e., light penetration and MPE), there are relatively few studies of the heating efficiency of Fe3 O4 nanoparticles in the NIR-II range [54,346–360]. Similar to the studies in the NIR-I, there is a rather large spread of the reported ∆T values in the second biological window, ranging ∆T ∼1 ◦ C to 50 ◦ C [54,346–360], depending on the conditions (laser power, nanoparticle concentration, duration of the actuation, type of particles and so on). However, it is important to emphasize that the conditions used in the second biological windows are usually milder than the ones used in the NIR-I, for example, with small concentrations of nanoparticles or lower laser powers, within the MPE (1 W/cm2 for λ = 1064 nm) [54,346,347,352,355,360]. Our own measurements using 16 nm Fe3 O4 nanocubes (see Annex B [394]) evidence that, in concordance with the NIR-I experiments, ∆T depends on the concentration and the laser power (see Fig. 6). As, expected, the dependence of ∆T on the concentration shows that, while ∆T is proportional to the concentration for small concentrations [358], it tends to saturate for large concentrations (inset in Fig. 6a). On the other hand, in the range of powers used in our experiment the ∆T remains rather linear (inset in Fig. 6b), similar to other studies [358]. Concerning the efficiency, η, only a few studies have evaluated this parameter, with rather different η values, in the range 11%–90% [297,346,347,353,355]. To try to understand this broad range of η values, we studied the photothermal properties of three different iron oxide systems (16 nm nanocubes, 27 × 6 nm nanorods and 50 nm clusters composed of 5 nm particles; see Annex B). As can be seen in Fig. 7a, although the three systems were measured in the same conditions (0.35 mg/mL and 0.793 W/cm2 ) the heating is quite different, where the nanocubes heat considerably more than the other two systems. Interestingly, the evaluation of η values from the ∆T curves leads to rather different values for the three systems. While the nanocubes have a moderate efficiency (η = 53%), nanorods and nanoclusters have lower efficiency (η = 24% and 20%, respectively). To clarify this issue, the extinction spectra were measured for the three systems (Fig. 7b). Although all three systems are nominally Fe3 O4 , their extinction spectra are quite different. As discussed earlier, this probably stems from the degree of oxidation towards γ - Fe2 O3 , different amounts and types of defects, and the contribution of the scattering, which is size and shape dependent. Interestingly, the ∆T and η values for the three samples show some degree of correlation between the extinction and their photothermal properties. Namely, the nanocubes with a larger extinction at λ = 1064 nm have a better photothermal performance. However, the correlation between the different parameters is not straightforward. Interestingly, Cabana et al. and Bertuit et al. have compared the performance of Fe3 O4 and γ -Fe2 O3 in the NIR-II range [352,355]. The results show that, in equal conditions of nanoparticle concentration and laser intensity, the ∆T reached by the γ -Fe2 O3 nanoparticles is considerably lower than for the Fe3 O4 ones, particularly at low concentrations, as expected from the difference in µE between both materials at λ = 1064 nm (see Fig. 4). However, Bertuit et al. emphasized the importance of the defects, rather than the stoichiometry, in the difference observed in their oxidized (γ -Fe2 O3 -like) nanoparticles [355]. Diverse studies measured the photothermal properties of the same type of particle under the same conditions (nanoparticle concentration and laser intensity) both at λ = 808 nm and 1064 nm [54,346–349]. Several of the results show that the heating power of the Fe3 O4 nanoparticles is considerably better in the second biological window [54,346, 347]. For example, Espinosa et al. found ∆T (808 nm) ∼6 ◦ C < ∆T (1064 nm) ∼8.5 ◦ C (using [Fe] 0.672 mg Fe/mL and 0.8 9 A.G. Roca, J.F. Lopez-Barbera, A. Lafuente et al. Physics Reports 1043 (2023) 1–35 Fig. 7. (a) Heating curves (Annex C) for 16 nm nanocubes, 27 × 6 nm nanorods and 50 nm clusters (see Annex B [394,455,456]) (using 0.35 mg/mL at 0.79 W/cm2 ) using λ = 1064 nm irradiation. Shown in the inset is the dependence of the intrinsic particle heating (∆TTotal - ∆TWater ) for the three systems. (b) Extinction spectra (Annex C) for the three systems. The shaded areas represent the first (NIR-I), second (NIR-II) and third (NIR-III) biological windows. The wavelengths used in the photothermia experiments (λ = 808 nm and 1064 nm, respectively) are highlighted by vertical lines. W/cm2 for 30 s) [54]. On the other hand, Huang et al. have reported an even greater ∆T improvement, ∆T (808 nm) ∼7 ◦ C << ∆T (1064 nm) ∼33 ◦ C (with a concentration about 0.375 mg Fe/mL and using 0.38 W/cm2 for 480 s) [346]. Similarly, Zhao et al. have reported ∆T (808 nm) ∼22 ◦ C < ∆T (1064 nm) ∼27 ◦ C (using 2 mg/mL and 1 W/cm2 during 600 s) [347]. However, Arranz et al. showed that ∆T is quite similar at either λ = 800 nm or 1053 nm [349]. Our own results, using 0.35 mg/mL of 16 nm Fe3 O4 nanocubes and 0.79 W/cm2 , show ∆T(808 nm) ∼7.6 ◦ C < ∆T (1064 nm) ∼11.2 ◦ C, similar to other studies. However, when the effect of water on ∆T is considered at the two wavelengths, the intrinsic heating of the particles becomes similar ∆TTotal – ∆TWater (808 nm) ∼7.3 ◦ C < ∆TTotal – ∆TWater (1064 nm) ∼7.9 ◦ C. In contrast, the difference in ∆T (after water correction) at λ = 808 nm and 1064 nm for the Fe3 O4 clusters is negligible (3.6 ◦ C vs 3.7 ◦ C), while for the nanorods, in fact, the heating is better at λ = 808 nm than at 1064 nm (4.1 ◦ C vs 1.7 ◦ C). Comparison the extinction of the nanocubes, nanocluster and nanorods (Fig. 7b), reveals no clear correlation between the extinction and ∆T, implying that other parameters apart for the absorption properties must enter into the ∆T of the different iron oxides. However, it is worth emphasizing that the laser power used for the two wavelengths is the same in all the studies. However, since the MPE for λ = 1064 nm is larger than that for λ = 808 nm, the difference in ∆T could be further enhanced if the MPEs corresponding to each λ were used. Lozano-Pedraza et al. studied η in the first and second biological widows and observed a larger η in the NIR-II, in agreement with the increased extinction of the nanoparticles in this range [348]. Our own study comparing η for the 16 nm nanocubes, 27 × 6 nm nanorods and 50 nm clusters (see Annex B) at 808 nm and 1064 nm show that our results do not follow the same trend, where, for example, for the nanocubes and the clusters η(808 nm) = 55% > η(1064 nm) = 52 % (nanocubes) and η(808 nm) = 40% > η(1064 nm) = 24% (clusters), respectively. Consequently, the results seem to indicate that the photothermal conversion efficiency of Fe3 O4 depends in a complex way on the extinction of the materials, and more systematic studies are necessary to understand these effects. However, since, ∆T (and not η) is what will ultimately determine the laser power and nanoparticle concentration required for an efficient treatment, it is clearly advantageous to use λ = 1064 nm for photothermal therapy for most iron oxide systems. 3.3. Third biological window Although from the skin optics perspective the third biological window does not appear optimal, more recent studies seem to indicate that, to properly account for the light penetration in the human body, subcutaneous tissues also need to be taken into account [361,362,434]. Consequently, the penetration of NIR-III light into the body may be adequate for photothermal applications. Thus, for the sake of completeness, we studied the performance of the Fe3 O4 nanocubes, nanorods and clusters (see Annex B) at λ = 1670 nm (in the NIR-III range) using 0.35 mg Fe/mL and 0.793 W/cm2 . As can be seen in Fig. 8, the ∆T of all the three systems is rather high, better that in the second biological window (Fig. 6). However, one should consider the heating of water which, in fact, for λ = 1670 nm accounts for greater part of ∆T. Although for some applications the effect of water heating would not be a problem, for biomedical uses, such a large heating of the medium surrounding the particles could induce unwanted side effects in healthy cells and tissues. Thus, 10 A.G. Roca, J.F. Lopez-Barbera, A. Lafuente et al. Physics Reports 1043 (2023) 1–35 Fig. 8. Heating curves (Annex C) for 16 nm nanocubes, 27 × 6 nm nanorods and 50 nm clusters (see Annex B) (0.35 mg/mL at 0.79 W/cm2 ) using λ = 1670 nm irradiation (NIR-III). The inset shows the dependence of the intrinsic particle heating (∆TTotal - ∆TWater ) for the three systems. although λ = 1670 nm is in the third biological window, implying that light absorption by water has a minimum in this range, its absorption is still considerably high (compared to 808 and 1064 nm; see Annex D), leading to a rather large temperature increase of water in this wavelength. Note that despite the somewhat low intrinsic heating of the three Fe3 O4 heat mediators, the efficiency of the Fe3 O4 nanocubes is rather good, reaching about η ∼70% for the current conditions. 4. In vitro and in vivo photothermal therapies of Fe3 O4 in the first and second optical windows There are numerous studies of the effects of photothermal treatments using iron oxide nanoparticles on cancerous cells in the first biological window. These in vitro NIR-I studies evidence that photothermia is an efficient way to destroy can- cer cells [47,48,52,59–62,68,76,77,84–88,90,92–94,97,98,101,108,113,119,124,133,137,141,151,153,155,157,162,169,175, 177,180,184,193,194,213,214,218,221,224,231,233,246,258,284,285,292,332]. For example, cancer cell death beyond 90% (i.e., cell viabilities below 10%) is achieved in many cases after laser irradiation [48,61,77,85,86,93,119,153,162,184,193, 213,224,258,285,332], even under rather mild irradiation conditions [85]. Some systematic studies evidence that the cell viability after the photothermal treatment is closely related to the nanoparticle concentration, the irradiation time and the laser power [47,52,56,59,61,87,88,90,92,94,97,98,113,117,124,137,153,155,157,162,184,193,194]. Importantly, many studies show that by controlling the irradiation conditions, apoptosis cell death (rather than necrosis, which can lead to side effects) can be induced [82,83,87,97,98,101,113,116,124,153,180,193,213,214,224,233,246,289,306,313,332]. Remarkably, many in vivo studies using Fe3 O4 nanoparticles or nanoparticle clusters show that the photothermal treatments in the NIR-I range can induce tumor growth inhibition, strong tumor regression, or even complete tumor removal, just a few days after the treatments [47–49,59,65,69,76,77,84–88,92,97,108,113,114,119,123,124,129,142,144, 152,155,157,158,177,180,193,194,196,213,222,224,233,247,258,285,286,301,313]. However, since the conditions of the diverse studies (e.g., different types of tumors, nanoparticle concentration, capping layers, laser power and spot size, laser wavelength, or irradiation duration) are not readily comparable, it is difficult to reach any general conclusions from these studies. Moreover, it is important to highlight that virtually all the in vivo studies use laser powers high above the recom- mended MPE of 0.33 W/cm2 at 808 nm, often above 1 W/cm2 and reaching values as high as 6.6 W/cm2 [48,49,59,84,86,88, 97,108,113,114,119,123,124,129,141,144,151,155,157,158,177,180,193,194,196,213,224,233,246,258,285,286,301] (with a few exceptions [47,69,87,221]). In contrast, despite the very promising perspectives of photothermal treatments in the NIR-II window, there are only a few in vitro studies in this range [346,347,352,354,356,359,360]. In agreement with what has been observed for the NIR-I, photothermia in the NIR-II range is an excellent approach to kill cancerous cells in vitro. For example, Huang et al. used ∼200 nm Fe3 O4 nanoclusters to treat HeLa cancer cells by irradiating with a λ = 1064 nm laser (0.38 W/cm2 ) for 10 min [346]. The treatment resulted in a decrease of the cell viability to 59% after one day, which was further reduced after 3 days to 18%. This significant decrease in cell viability after a few days suggests an apoptotic cell death rather than necrotic. Moreover, it is worth emphasizing that rather mild irradiation conditions were used, with a laser intensity 11 A.G. Roca, J.F. Lopez-Barbera, A. Lafuente et al. Physics Reports 1043 (2023) 1–35 Fig. 9. (a) Metabolic/cytotoxicity tests of PC3 prostatic cancer cells treated with a λ = 1064 nm laser at a power density of 0.3 W/cm2 for 10 min using four different types of iron oxide nanoparticles as heat mediators; 12.7 nm γ -Fe2 O3 nanoparticles — Maghemite NanoSpheres; 27 nm γ -Fe2 O3 clusters — Maghemite NanoFlowers; 12.7 nm Fe3 O4 nanoparticles — Magnetite NanoSpheres; 27 nm Fe3 O4 clusters — Magnetite NanoFlowers. (b) Annexin V/propidium iodide apoptosis assay for cells treated with magnetite nanoflowers after laser irradiation. Source: Adapted from Ref. [352]. well below the MPE for λ = 1064 nm (1 W/cm2 ) [346]. Interestingly, the cell mortality can be further increased when using a magnet to concentrate the nanoparticles in the irradiation area [346]. On the other hand, Cabana et al. used four different types of particles (Fe3 O4 and γ -Fe2 O3 ; see Fig. 9) to treat PC3 cancer cells with a λ = 1064 nm laser (0.3 W/cm2 ) for 10 min [352]. The results using Fe3 O4 nanoclusters show that a cell viability as low as 5% can be obtained after one day [352]. This is rather remarkable considering that the laser power was only 0.3 W/cm2 , i.e., below the 1 W/cm2 MPE for λ = 1064 nm. However, in this case the cell death was found to be mostly by necrosis (60%). Notably, the treatments using γ -Fe2 O3 -based particles (nanoparticles and clusters) resulted in poorer results than the corresponding particles based on Fe3 O4 (Fig. 9), consistent with the worse photothermal performance of the former [352]. Zhao et al. have shown a reduction of the cell viability to 65% after λ = 1064 nm irradiation when using chains of Fe3 O4 nanoparticle aggregates. Interestingly, the cell viability can be further reduced (to 25%) when NIR-II irradiation, anticancer drugs and mechanical cell lysis using alternating magnetic fields are combined [347]. Finally, Wang et al. have reported cell viabilities of about 18% after using hollow ∼200 nm Fe3 O4 nanoclusters, again, under rather mild conditions (i.e., λ = 1064 nm laser power at 0.8 W/cm2 and 0.5 mg Fe/mL) [354]. Interestingly, Li et al. formed soft robots using Fe3 O4 nanoparticles and used them to effectively kill cancerous cells. However, the power used (2.5 W/cm2 ) was well above the MPE for λ = 1064 nm [356]. Unfortunately, there are very few in vivo investigations based on Fe3 O4 nanoparticles in the NIR-II range. Zhao et al. have shown that using chains of Fe3 O4 nanoparticle aggregates, irradiation at 1064 nm irradiation produces a reduction of the tumor growth rate (Fig. 10). However, to induce complete tumor destruction, additional therapeutic modes (anticancer drugs and mechanical cell lysis) are required [347]. Yet, note that the extinction of these aggregates does not show the expected increase in the NIR-II region [347], which may indicate the presence γ -Fe2 O3 rather than Fe3 O4 . This may explain the somewhat weak effect of the NIR-II irradiation in these particles, both in vitro and in vivo. On the other hand, Wang et al. have again reported a substantial tumor growth inhibition using hollow ∼200 nm Fe3 O4 nanoclusters and λ = 1064 nm irradiation at 0.8 W/cm2 . To completely eradicate the tumor, they needed to encapsulate the anticancer drug DOX inside the hollow structure of the clusters [354]. On the other hand, Qin et al. have shown only a rather small tumor growth reduction WHEN ∼116 nm Fe3 O4 nanoparticles and λ = 1064 nm irradiation at 0.75 W/cm2 were used [359]. Unfortunately, similar to the study by Zhao et al. [347], the extinction of the nanoparticles in Wang et al. and Quin et al. studies does not show an increase in the second biological window, which may explain the limited efficiency of the NIR-II treatment when Fe3 O4 nanoparticles are used alone [354,359]. In view of the rather few in vitro and in vivo studies for NIR-II, this is certainly a field with great potential yet to be explored. 5. FeO (wüstite) as a potential photothermal heat mediator FeO (wüstite) is another interesting constituent of the family of iron oxides. However, contrary to Fe3 O4 or γ -Fe2 O3 , it is not ferrimagnetic at room temperature. Although FeO has been far less studied than other iron oxides, FeO-based nanoparticles have been assessed for their use in diverse biomedical applications [360,457–464]. However, from the optic viewpoint, the simulated absorption properties of FeO (see Annex A) [465] are quite appealing since they present a rather 12 A.G. Roca, J.F. Lopez-Barbera, A. Lafuente et al. Physics Reports 1043 (2023) 1–35 Fig. 10. Evolution of the relative tumor volume after different treatments using one-dimensional polycation-coated nanohybrids Fe3 O4 @Dex-PGEA (1D FDP) [347]. [AFM — alternating magnetic field; p53 — antioncogene p53; NIR — 1064 nm irradiation]. Fig. 11. Dependence of the theoretical (a) absorption, µA (Cabs ), and (b) scattering, µS (Cscat ), cross-sections for spherical FeO and Fe3 O4 nanoparticles (diameter 25 nm). (c) Experimental wavelength dependence of the extinction (Annex C), for 40 nm FeO/Fe3 O4 nanocubes and 16 nm Fe3 O4 nanocubes (see Annex B) [394,466,467]. The shaded areas represent the first (NIR-I), second (NIR-II) and third (NIR-III) biological windows. The typical wavelengths used experimentally in photothermia in the NIR-I and NIR-II regions (λ = 808 nm and 1064 nm, respectively) are highlighted by vertical lines. 13 A.G. Roca, J.F. Lopez-Barbera, A. Lafuente et al. Physics Reports 1043 (2023) 1–35 Fig. 12. Heating curves (Annex C) for 40 nm FeO/Fe3 O4 core/shell nanocubes and 16 nm Fe3 O4 nanocubes (see Annex B) [394,466] (0.35 mg/mL and 0.79 W/cm2 ) using (a) λ = 808 nm and (b) λ = 1064 nm irradiation. high µA in both the first, second and third biological windows, significantly better than Fe3 O4 (Fig. 11). Additionally, the scattering, µS is also rather low for small (25 nm) FeO nanospheres. Remarkably, FeO is not stable under ambient conditions, and in nanoparticle form it partially oxidizes to Fe3 O4 , typically leading to FeO/Fe3 O4 core/shell nanoparticles [466,468–471], which is a rather stable structure for sufficiently large particles [466]. This fact offers the possibility of exploiting the appealing optical absorption properties of both FeO and Fe3 O4 while maintaining the overall magnetic character due to the presence of Fe3 O4 . In fact, this type of particle can be easily manipulated using magnets [467] (see Annex E) or can be used in magnetic hyperthermia [457,458]. The FeO/Fe3 O4 core/shell nanoparticles indeed show experimentally a rather strong extinction spectrum [471]. Our results show that the shape of the extinction curve of FeO/Fe3 O4 core/shell nanoparticles is similar to that of pure Fe3 O4 since it combines the properties of the Fe3 O4 shell and the FeO core. However, due to the presence of the FeO core, the extinction of the FeO/Fe3 O4 nanoparticles is considerably stronger than that of the pure Fe3 O4 nanocubes (Fig. 11c). Remarkably, as can be seen in Fig. 12, the FeO/Fe3 O4 nanoparticles outperforms the pure Fe3 O4 nanocubes in terms of ∆T both in the NIR-I and NIR-II ranges. In addition, the efficiency extracted from Fig. 12 shows that η of the FeO/Fe3 O4 nanocubes is rather high in both biological windows, surpassing many state-of-the-art photothermal mediators [15]. In fact, its efficiency is clearly better than that for the Fe3 O4 nanocubes both at λ = 808 nm (55% - Fe3 O4 vs 68% - FeO/Fe3 O4 ) and at λ = 1064 nm (53% - Fe3 O4 vs 79% - FeO/Fe3 O4 ). Thus, the photothermal performance (∆T and η) correlates nicely to the higher extinction coefficient of the FeO/Fe3 O4 nanocubes. These results clearly reveal the great potential of FeO/Fe3 O4 nanoparticles for different types of photothermal-based applications, thus encouraging in vitro and in vivo investigations. 6. Other potential uses of iron oxide nanoparticles in the second biological window Although we have focused on the use of photothermia for cancer therapy using iron oxide nanoparticles (mainly Fe3 O4 ) exploiting the enhanced light absorption and the excellent heating performance of the Fe3 O4 and FeO/Fe3 O4 nanoparticles in the second biological window and the overall advantages of this wavelength range, other possible applications of iron oxide nanoparticles using NIR-II light can be envisaged. 6.1. Combined photothermal treatments for oncology Combining photothermal treatments in the NIR-II range with other therapy modes can lead to an enhancement of the therapeutic effect. For example, combining photothermia and magnetic hyperthermia has been shown to be a very powerful synergetic combination for cancer treatment. However, although the enhanced efficiency of the photo/magnetic- hyperthermia has been demonstrated in the NIR-I region [54,82,98,136,140,312], it has not been systematically explored in the second biological window. An additional interesting cancer (or other diseases) treatment which could be improved using NIR-II light, is the controlled photo-induced drug delivery in nanoparticle-based chemotherapy approaches [56,96,99,101,105,117, 123,137,144,146,156,176,182,184,195,203,204,214,218,231,258–260,267,271,279,295,320,321,325,347,354]. Namely, the enhanced heat induced by the NIR-II light would probably allow more efficient on-demand triggering of the drug release carried by the Fe3 O4 nanoparticles when they reach the site of action [472]. In fact, it has been proposed that the heat induced in Fe3 O4 -based photothermal experiments could lead to cell poration, which would lead to a better absorption of the drugs carried by the heat mediators [261]. 14 A.G. Roca, J.F. Lopez-Barbera, A. Lafuente et al. Physics Reports 1043 (2023) 1–35 Fig. 13. Schematic diagram of the free radicals or reactive oxygen species (ROS) by Fe3 O4 nanoparticles [477]. Moreover, another approach often used in cancer treatment is photodynamic therapy, where free radicals or reactive oxygen species (ROS) are used to kill malignant cells [473,474]. Fe3 O4 nanoparticles have also the potential to generate photodynamic effects (Fig. 13) [475–477]. Namely, the Fenton reaction can be triggered by the Fe2+ ions that react with H2 O2 (usually present inside cells) leading to highly reactive hydroxyl (• OH) and superoxide (O− · 2 ) radicals though the Haber–Weiss reaction [476,477]. In fact, these reactions are enhanced at higher temperatures [478–480] as observed also for Fe3 O4 nanoparticles [215,318,345]. Therefore, the enhanced photothermia in the second biological window could be beneficial for ROS generation. In principle, the larger amount of Fe2+ ions in FeO nanoparticles could enhance the photodynamic and photothermal synergistic actuation, although this effect has not been explored yet. Additionally, as shown for NIR-I, iron oxides are often combined with other materials to increase the production of H2 O2 or to hinder the reduction of the Fenton reaction with time and, thus, enhance the efficiency of the photodynamic treatments [57,81,110,116,118,119,140,277,291,295]. Interestingly, the ferroptosis cell death mechanism has also been proposed to be enhanced by photothermal temper- ature increases [215,252], which could potentially be enhanced in the second biological window. 6.2. Non-oncological biomedical applications of photothermal therapy The first obvious uses of iron oxide-photothermia would be in other biomedical applications beyond cancer, like the treatment of other diseases, where the application of local heat may be advantageous, such as atherosclerosis or even neurological diseases [481]. Interestingly, iron oxide-based photothermia can be used for antibacterial treatments, including biofilm eradication or wound disinfection, which have already been demonstrated in the first optical window using Fe3 O4 nanoparticles [91, 131,159,167,173,190,198,237,243,257,263,276,287,288,291,311,314,325,345,482,483]. 6.3. Diagnosis: Imaging agents and sensing The second biological window could not only improve the therapy aspects of iron oxide nanoparticles, but also their diagnostic characteristics. For example, the increased induced heat in the NIR-II could improve different light- induced imaging modes proposed for Fe3 O4 nanoparticles, which have already been demonstrated in the first biological window, like photoacoustic imaging [123,133,177,180,222,233], photothermal optical coherence tomography [484,485], or photothermal microscopy [213,486]. A different diagnostic feature of Fe3 O4 nanoparticles which may be improved is sensing, for example, in thermal sensing [135,154,166,174,238,283,303,483,487]. In addition, given their strong absorption in the NIR-II and their magnetic character, Fe3 O4 nanoparticles could potentially be used for in situ photo-magnetic temperature sensing in the second biological window [488]. 6.4. Environment-related applications Beyond biomedical applications there are other fields where the enhanced NIR absorption and the outstanding photothermal performance of Fe3 O4 nanoparticles in the second biological window may be appealing. For example, Fe3 O4 nanoparticles have long been used for environmental remediation via, for example, the Fenton reaction (Fig. 13), where the free radicals or reactive oxygen species (ROS) degrade many organic pollutants [489–491]. In principle, the heat induced by 15 A.G. Roca, J.F. Lopez-Barbera, A. Lafuente et al. Physics Reports 1043 (2023) 1–35 the NIR-II irradiation could improve the efficiency of these processes [318,345]. In addition, iron oxide nanoparticles can absorb metal ions in solution [492,493]. Since this process is thermally activated [494], it could potentially be enhanced by the photoinduced temperature increase. Another proposed use of Fe3 O4 nanoparticles as photothermal mediators is as insecticides, where the generated heat is used to kill insect larvae [292]. Iron oxide nanoparticles have been used for solar water heating, purification, sterilization, desalinization or even anti- freezing or de-icing coatings [280,287,495–500]. Given that solar light is composed of about 50% infrared irradiation, raising the absorption in the NIR-II region using Fe3 O4 nanoparticles, rather than γ -Fe2 O3 , would enhance the absorption of solar light for diverse applications [495–500]. Notably, the intense and rather flat absorption spectrum of the FeO nanoparticles in the visible and NIR could also find environmental applications exploiting the whole sunlight spectrum. 6.5. Energy-related applications The photothermal effect could also be exploited in the broad concept of photothermal catalysis, in which light- induced heat is used to drive chemical reactions [501–503], and the strong NIR-II heating can be used to activate certain reactions [331,358]. In addition, the strong absorption of Fe3 O4 or FeO/Fe3 O4 nanoparticles in the NIR-II range may be beneficial for non- linear optics and absorbing applications [504–506], where the robustness of oxides compared to other optically non-linear materials [507] may be an advantage for many optical applications. The local photothermal heating can also be exploited to drive the movement of Fe3 O4 -based nanomotors [283]. Moreover, the enhanced absorption in the NIR of Fe3 O4 has also been used to design more efficient windows [53,508,509]. On the other hand, the photothermal heat generated by Fe3 O4 nanoparticles when they are embedded in different types of thermosensitive matrices can be used for very widespread applications, ranging from friction control to energy storage in phase-change materials [160,179,187,188,202,207,216,220,230,232,236,240,241,247,263,264,268,275,278,281, 305,307,326,329,337,338,340,346,356,510,511]. These applications are based on the photothermally induced generation of physiochemical changes in the matrix [512] (e.g., a solid–liquid phase transition, changes in viscosity) that can be exploited for diverse uses, like soft robots, actuators, shape-memory materials, energy storage, light-controlled ferrofluids, tribological applications, artificial muscles, wireless-controlled switches or energy harvesters among many others. In fact, there are probably many other uses of Fe3 O4 nanoparticles which could benefit from an enhanced absorption and/or large photothermal effects in the NIR-II. 7. Conclusions Summarizing, iron oxides (Fe3 O4 , γ -Fe2 O3 and FeO) are excellent photothermal agents for biomedical and other appli- cations both in the first (NIR-I) and second (NIR-II) biological windows. Iron oxides are biocompatible and biodegradable, and their metabolic route is very well known. As iron is an abundant element in the Earth’s crust, the synthesis of these nanoparticles is relatively cheap. Moreover, due to their magnetophoretic properties, they can be guided inside the body and concentrated at the target organ/tissue boosting the efficiency of the photothermally activated treatment. However, the spread of the photothermal performance results, both in terms of ∆T and η, indicates that the correlation between the physicochemical properties of the iron oxide nanoparticles and photothermia is not straightforward, and more systematic studies are needed to fully elucidate the efficiency of this type of system. There are several parameters that seems to affect the photothermal performance of the iron oxides for photothermal applications. On the one hand, there are intrinsic properties of the particles such as the iron oxide phase, particle size, morphology, aggregate size and defects which clearly affect their performance. On the other hand, the wide spread of the conditions used in the measurement settings reported in the literature (defined by the laser intensity, spot size and wavelength, among others) represent the main drawback for the comparison of the results reported in the results, i.e., the lack of standardization. Remarkably, despite the evident advantages of Fe3 O4 and FeO/Fe3 O4 nanoparticles in the NIR-II region for a broad range of photothermal applications, this field is still relatively unexplored. The enhanced absorption at the NIR-II and the higher MPE limit are, in principle, sufficient arguments to encourage work in this wavelength range. However, more studies are necessary to unravel the full potential of iron oxides beyond the first biological window. Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. 16 A.G. Roca, J.F. Lopez-Barbera, A. Lafuente et al. Physics Reports 1043 (2023) 1–35 Acknowledgements This work was financially supported form grants No MAT2016-77391-R, PID2019-106229RB-I00, PDC2021-121303- I00, PDC2022-133036-I00, RTI2018-095495-J-I00 and RYC2019-027449-I funded by MCIN/AEI/10.13039/501100011033. We thank the Ramon Areces foundation through grant CIVP19A5922. Funding from Generalitat de Catalunya through the 2021-SGR-00651 project is also acknowledged. FÖ acknowledges the support of TUBITAK (The Scientific and Tech- nological Research Council of Turkey) through the Project No. 1059B192000021. ICN2 is funded by the CERCA pro- gramme/Generalitat de Catalunya. The ICN2 is supported by the Severo Ochoa Centres of Excellence programme, Grant CEX2021-001214-S, funded by MCIN/AEI/10.13039.501100011033. The authors thank Iris Nogués for preparing Fig. 1. Annex A. Simulation of the absorption and scattering cross sections of different iron oxides The absorption and scattering cross section simulations of spherical γ -Fe2 O3 , Fe3 O4 and FeO nanoparticles with a diameter of 25 nm were carried out by finite different time domain (FDTD) simulations using the Lumerical software, using literature values for their optical constants [440,465]. A mesh size of 1 nm was imposed in the nanoparticle region. As external medium in the calculations, it was assumed water (refractive index 1.33), without considering the water absorption coefficient to show just the spectral contribution of the nanoparticles. Annex B. Sample preparation B.1. Preparation of the nanoparticles. All the nanoparticles were prepared through thermal decomposition, which leads to uniform and highly crystalline nanoparticles with well-defined morphology. The 16 nm magnetite nanocubes were synthesized following the method reported by Muro-Cruces et al. [394]. Iron (III) acetylacetonate (0.446 g; 1.27 mmol), sodium oleate (0.23 g; 0.80 mmol) and oleic acid (1.48 g; 5.20 mmol) were dissolved to a mixture of 1-octadecene (10 mL), benzyl ether (10 mL) and 1-tetradecene (3 mL) in a 100 mL three-neck round flask. This mixture was sonicated and then heated up to 60 ◦ C under vacuum for one hour. Next, the reaction mixture was heated to 190 ◦ C at 3 ◦ C/min under Ar flow. Finally, Ar was removed and the reaction was kept at reflux for 1 h being cooled down to room temperature afterwards by removing the heating mantle. The magnetite nanocubes were purified by centrifugation. The reaction mixture was mixed with a mixture of isopropanol, ethanol and methanol and centrifuged for 10 min at 10600 g. Then, the supernatant was discarded and the pellet redispersed in chloroform, mixed with isopropanol and methanol and centrifuged again (10 min, 10600 g). To obtain a dispersion stable in water, the magnetite nanocubes were coated by PMAO [poly (maleic anhydride-alt-1- octadecene)]. Magnetite nanocubes were redispersed and sonicated in 50 mL of chloroform. In parallel, 20 mg PMAO were dissolved in 5 mL in chloroform and added to the nanocube solution. The dispersion was gently stirred and 50 mL of buffer borate (pH 9) was added to the solution. The suspension was sonicated for several minutes using an ultrasonic probe until a milky solution (denoting the formation of a microemulsion) was formed. Then, the suspension was rota-evaporated at 45 ◦ C for several minutes until the chloroform was evaporated and the nanocubes were transferred to water. Finally, the suspension was centrifuged for 1 h at 10600 g to remove the excess of PMAO and the pellet was redispersed in water. The 40 nm core/shell FeO/Fe3 O4 nanocubes were synthesized following the procedure reported by Ichikawa et al. [466]. This procedure consists of two steps: (1) synthesis of iron (III) oleate and (2) thermal decomposition of iron (III) oleate in eicosane under the presence of oleic acid and sodium oleate. The iron (III) oleate was synthesized refluxing iron (III) chloride and sodium oleate in a mixture of hexane, water and ethanol [393]. In the second step, iron (III) oleate (10.25 g, 11.4 mmol), oleic acid (1.44 g, 5.12 mmol) and sodium oleate (1.56 g, 5.12 mmol) were mixed with 26 g of eicosane and degassed at room temperature prior to heating up to 70 ◦ C for 2 h under Ar atmosphere to dissolve the sodium oleate. Then, the reaction mixture was heated up to 350 ◦ C at 3 ◦ C/min under Ar flow and kept for 30 min. Finally, the reaction was cooled down to room temperature under Ar flow. Purification of the particles was carried out by several cycles of centrifugation with ethanol. Finally, the particles were dispersed in chloroform. The FeO/Fe3 O4 nanocubes were transferred to water following the same procedure described for the Fe3 O4 nanocubes. The hydrophilic 50 nm magnetic nanoclusters were synthesized using the solvothermal method [94]. In a typical process, 0.8 g sodium acetate, 0.03 g polyacrylic acid, 0.27 g iron(III) chloride hexahydrate were dissolved in a solvent mixture composed by 4 mL diethylene glycol and 6 mL N- methyldiethanolamine. The mixture was transferred to Teflon- lined autoclave and maintained at 200 ◦ C for 12 h. After the autoclave was cooled to room temperature, the nanoclusters were obtained by magnetic separation using a magnet and then washed with ethanol and water for several times. Note that the as obtained nanoclusters are readily dispersible in water, thus there no extra steps are required to transfer them to water. The synthesis approach for the growth of the 27 ×6 nm magnetic nanorods is based on the method published by Sun et al. [455]. A mixture of 1.79 g oleic acid, 0.83 g hexadecylamine and 11 mL 1-octanol is stirred and heated up to 55 ◦ C for 30 min to completely dissolve the hexadecylamine. Subsequently, the mixture is cooled down to room temperature 17 A.G. Roca, J.F. Lopez-Barbera, A. Lafuente et al. Physics Reports 1043 (2023) 1–35 Fig. 14. TEM images (Annex C) of the FeO/Fe3 O4 nanocubes, (b) the Fe3 O4 nanocubes, (c) the Fe3 O4 nanorods and (d) the Fe3 O4 clusters. and 2.75 mL iron(0) pentacarbonyl is added to the system and stirred for an additional 30 min. Then, the reaction mixture is transferred to a 23 mL autoclave with a Teflon lining and heated up to 200 ◦ C for 6 h. After cooling the reactor to room temperature, the sample was washed with ethanol and centrifuged for 10 min at 10600 g twice. Then the nanorods are redispersed in chloroform and separated with a magnet. The nanorods were transferred to water following the same procedure described for the Fe3 O4 nanocubes. B.2. Morphological characterization The average particle size and the corresponding size distribution was estimated from the dimensions obtained from at least 200 particles. In the case of the FeO/Fe3 O4 nanocubes the particle dimension was defined as the edge length. The average size of the nanocubes was 40 nm with a standard deviation of 5 nm (see Fig. 14). The thickness of the Fe3 O4 shell is around 7 nm. In the case of the Fe3 O4 nanocubes, the average particle size (edge length) was 16.5 nm with a standard devi- ation of 1.9 nm (see Fig. 14). The nanorod dimensions were defined by their length and diameter, being 27 ± 8 nm for the length and 5.6 ± 1.5 nm for the diameter, respectively (see Fig. 14). This leads to an aspect ratio of around 5. Finally, the di- mensions of the nanoclusters were defined by the diameter of a circle completely comprising the cluster. Thus, the average cluster diameter was 50 ± 8 nm. Moreover, the size of the nanoparticles forming the cluster was about 5.3 ± 1.0 nm. Annex C. Methods C.1. Transmission electron microscopy Transmission electron microscopy (TEM) images were collected in a JEM 1400 (JEOL) microscope operating at 120 keV. A small amount of particles was suspended in hexane and a few drops were placed on a carbon-coated copper grid. C.2. Extinction measurements The visible-near-infrared (vis–NIR) spectroscopy studies of the nanoparticle dispersions were carried out using a UV– VIS Cary 5 (Agilent) in the 400 to 1800 nm range, covering the visible light and near-infrared regions. Measurements were carried out using 0.7 mL quartz cuvettes with an optical length of 0.2 mm. The nanoparticle dispersion concentration was 0.350 mg Fe/mL. 18 A.G. Roca, J.F. Lopez-Barbera, A. Lafuente et al. Physics Reports 1043 (2023) 1–35 Fig. 15. Experimental setup designed to performed photothermal measurements. Fig. 16. Experimental absorbance (Annex C) of pure liquid water. The shaded areas represent the first (NIR-I), second (NIR-II) and third (NIR-III) biological windows. The circles highlight the absorption at the wavelengths used in our experiments (λ = 808 nm, 1064 nm and 1670 nm, respectively). C.3. Photothermal measurements The heating curves under laser irradiation were obtained using a custom-made photothermal testing system. The system consisted of: (i) a NIR laser diode with the selected emission wavelength (808 nm, K808F11FA, BWT Beijing Ltd; 1064 nm, KA64FAMFA, BWT Beijing Ltd.; and 1670 nm 4PN-135, Seminex) driven by a laser diode controller (ITC4005, Thorlabs), (ii) an optical collimating and aligning system, (iii) an infrared camera (ETS320, FLIR) to monitor the temperature variations at the liquid surface, (iv) a power meter (PM100D, Thorlabs), and (v) a computer with the data acquisition software. The laser incident power upon the samples was typically set to 100 mW and the laser spot size was about 4 mm in diameter leading to a laser intensity of 0.793 W/m2 . The laser beam incident perpendicularly to the cuvette wall, and the infrared camera is located on top of the cuvette to measure the temperature at the liquid interface. The nanoparticle suspension was placed onto a 1.5 mL polystyrene cuvette. The photothermal laser set up schematics is represented in Fig. 15. The total volume of the dispersion was 0.75 mL. The ambient temperature was set to 23 ± 1 ◦ C. 19 A.G. Roca, J.F. Lopez-Barbera, A. Lafuente et al. Physics Reports 1043 (2023) 1–35 Fig. 17. (a) Different mages showing the trapping of FeO/Fe3 O4 nanocubes by a magnet after flowing the nanoparticle suspension at different rates. (b) UV–VIS spectra of the nanoparticle suspension after flowing through the magnet at different rates. (c) Trapping efficiency calculated for the different flowing rates. The photothermal conversion efficiency η was calculated as follows [451]: hS(Tmax − Tamb ) − Qdis η= (1) I(1 − 10−Ax ) where h is the heat transfer coefficient, S the laser irradiating surface, Tmax is the maximum optically induced temperature change, Tamb is the temperature in the lab, Qdis the heat dissipation due to the experimental set up, I the laser incident power (100 mW) and Ax the absorbance at the irradiated wavelength (x = 808 nm, 1064 nm or 1670 nm). In order to get the value of η, hS for heat dissipation should be calculated. During the cooling process, since there is no light irradiating the nanoparticles, the dispersion will reach Tamb : ∑ dT Qdiss = mi Cp,i = hS (T − Tamb ) (2) dt i Here we can define the time constant τs and the dimensionless parameter θ to simplify the integral as follows: ∑ mi Cp,i T − Tamb τs = i and θ = hS Tmax − Tamb dθ 1 = θ (3) dt τs 20 A.G. Roca, J.F. Lopez-Barbera, A. Lafuente et al. Physics Reports 1043 (2023) 1–35 Setting the boundary conditions for the cooling process: t = 0, θ = 1, the equation can be solved as (4) from which a linear relationship can be deduce to obtain τs value, consequently, hS can be calculated and introduced in (1) to calculate the photothermal efficiency. 1 θ = e τs t (4) Annex D. Water absorbance spectrum See Fig. 16. Annex E. Remote manipulation of the FeO/Fe3 O4 nanocubes by a magnetic gradient To demonstrate that the FeO/Fe3 O4 nanoparticle can be easily manipulated using magnetic fields, magnetic trapping experiments were performed by setting a spherical 19 mm diameter FeNdB permanent magnet (7.1 kOe at the surface) attached to a narrow microfluidic channel (3 mm in diameter) (see Fig. 17) [472]. A FeO/Fe3 O4 nanoparticle dispersion of 0.3 mg Fe/mL (total volume of 1 mL) was controllably flowed by a syringe pump through the microfluidic channel at different flow rates. 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