Bismuth Oxychloride Nanomaterials in Biomedical Applications: History
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Contributor:
Rui Chen
,
Lili Wang
,
,
Yan Cheng

Photocatalytic nanomaterials (NMs) have been used for degrading pollution for a long time. As a typical photocatalytic NM, bismuth oxychloride (BiOCl) exhibits excellent photocatalytic performance due to its unique layered structure, electronic properties, optical properties, good photocatalytic activity, and stability. Some environmental pollutants, such as volatile organic compounds, antibiotics and their derivatives, heavy metal ions, pesticides, and microorganisms, could not only be detected but also be degraded by BiOCl-based NMs due to their excellent photocatalytic and photoelectrochemical properties. In particular, BiOCl-based NMs have been used as theranostic platforms because of their CT and photoacoustic imaging abilities, as well as photodynamic and photothermal performances.

  • BiOCl
  • photodegradation
  • photodynamic therapy
  • bismuth oxychloride

1. Introduction

Human health has been threatened by environmental pollution and various diseases for a long time. Photocatalytic technology is recognized as one of the most promising technologies, which has been widely used in the treatment of environmental pollution. Recently, this technology has been used for disease diagnosis and therapy. Photocatalysis is a process of producing free electrons and holes, which can induce oxidation and reduction reactions [1][2][3][4][5]. When the energy of the incident light is greater than or equal to the band gap energy (Eg) of the semiconductor, the electrons from the valence band (VB) of the semiconductor can be excited and transfer to the conduction band (CB), leaving holes on the VB. The photogenerated electrons have strong reduction ability, while the holes have strong oxidation ability [6]. Therefore, an effective photocatalyst could be used for solving environmental and healthcare problems.
Thus far, plenty of inorganic nanomaterials (NMs) have been developed as photocatalysts. Among these NMs, bismuth oxyhalide (BIOX, X = Cl, Br, I) has attracted more attention because of its excellent photoelectronic properties [7][8][9][10]. The VB of BIOX is hybridized by O 2p and Bi 6s orbitals, and the CB is composed of a Bi 6p orbital. The internal electric field formed between layers can promote the effective separation of photogenerated electron holes, which plays a key role in improving the photocatalytic performance of BIOX NMs. As one of the most important and representative BIOX NMs, bismuth oxychloride (BiOCl) crystals belong to the tetragonal crystal system structure, the space group is P4/nmm (No. 129), and its crystal structure parameters are a = b = 0.3891 nm, c = 0.7369 nm, α = β = γ = 90°, V0 = 0.1108 nm3, and Z = 2 [11]. From the van der Waals force analysis, there are weak non-bond orbits between the layers in the c-axis direction, but there is strong bonding in the (001) plane, the O2− and Cl− around Bi3+ form antisquare column coordination, the conical geometry structure with opposite direction and upper and lower asymmetry is formed, and the Cl− layer is a positive square coordination. The next layer is the positive square O2− layer, the Cl− layer and the O2− layers staggered at 45°, and intermediate sandwich Bi3+ layer. Under solar energy irradiation, electrons from the valence band Cl 3p orbital could jump to Bi 6p orbitals, and form photoinduction electrons and holes. The layered structure has enough space to polarize the atoms and the atomic orbits, prompt and induce the dipole moment, and effectively separate the electrons and holes, thus improving the photocatalytic performance.

2. BiOCl NMs Used as Theranostic Platform

Since the late 19th century, bismuth subsalicylate has been used to relieve nausea, diarrhea, and gastrointestinal discomfort. It can be hydrolyzed into BiOCl in the human body to effectively treat diarrhea and upset stomach [12][13], proving the excellent biocompatibility of BiOCl NMs. Recently, BiOCl NMs have been used as a theranostic platform, including for drug delivery [14], bioimaging [15][16][17], biosensors, Alzheimer’s disease [18], antibacterial, and anticancer applications [19][20].

2.1. Bioimaging

Bismuth-based NM has been used as an ideal X-ray computed tomography (CT) contrast agent due to the higher atomic numbers and X-ray attenuation coefficient of Bi elements [21]. As a typical Bismuth-based NM, BiOX NMs, such as BiOI [22], BiOBr [23], and BiOCl, have recently been used for spatial- and temporal-specific CT imaging of tumors. However, only a few studies on bioimaging of BiOCl NMs have been reported. As reported by Ye’s group [15], Se-doped BiOCl nanosheets were fabricated via a solvothermal method.

2.2. Biosensor

The release of pesticide residue and antibiotics has become a public health concern. Therefore, the detection of biomarkers, pesticides, and antibiotics has a significant impact on human health. Photoelectrochemical sensing is becoming an innovative technique due to its simple detection equipment, rapid analysis, and high sensitivity abilities [24]. A series of BiOCl-based NMs have been developed to detect various substances, such as pesticides, antibiotics, and biomarkers, due to the faster separation efficiency of photogenerated carriers. Antibiotics, such as ciprofloxacin, chloramphenicol, kanamycin, and lincomycin, have been widely used for the treatment of bacterial infections and showed good therapeutic effects. However, they cannot be fully absorbed and degraded, leading to environmental and water pollution, or even worse to adverse effects on the health of humans. For instance, the release of ciprofloxacin has caused serious threats to human health. Yuan’s group [25][26] first designed a BiOCl-based PEC senor for the detection of ciprofloxacin though monitoring the changes of photocurrents produced by BiOCl under irradiation. In order to improve the sensitivity of the BiOCl-based PEC senor, graphitic carbon nitride or metallic Bi were used to form heterostructures with BiOCl NMs to separate photogenerated carriers. Both of these heterostructures show much higher photocurrents than BiOCl alone, thus leading to higher detection ranges and limits. In order to obtain a PEC senor with high selectivity, the aptamer, which serves as a specific biometric molecule due to its biological affinity and specific recognition with a specific analyte, was usually decorated on the surface to form PEC aptasenor. Li et al. [27] designed an aptamer-modified BiOCl-Bi24O31Cl10 PEC aptasenor, which can be applied to the determination of ciprofloxacin in water with good selectivity and reproducibility. The residues and metabolites of chloramphenicol also cause damage to the human hematopoietic and gastrointestinal system. Li’s group [28] designed Ag nanoparticles modified with a BiOCl NM (BiOCl-Ag) PEC aptasenor, which could effectively improve the absorption of incident light and promote the migration and separation of photogenerated carriers due to the surface plasmon resonance (SPR) of Ag NMs. After decorating with the aptamer, there were obvious changes to the photocurrent when incubating the BiOCl-Ag PEC aptasenor with chloramphenicol, while no changes were observed in the other subjects, such as tetracycline, lincomycin, oxytetracycline, bisphenol A, norfloxacin, and hexafluorobisphenol A, proving the good selectivity due to the specific binding of the chloramphenico-aptamer. In addition, other antibiotics, such as kanamycin and lincomycin, were also detected by the BiOCl-MnO2 and BiOCl-Au-CdS heterostructure PEC aptasenor, with excellent sensitivity and selectivity, respectively [29][30].

2.3. Antibacterial

One of the serious threats to the world’s public health is bacterial invasion, which could induce cholera, pneumonia, influenza, tuberculosis, measles, meningitis, etc. Therefore, bacteria inactivation is significant. However, traditional antibiotics bring bacterial resistance, and moreover, the antibiotic itself is toxic to animals and humans. Due to the capability of ROS generation, there were some studies on the photocatalytic antibacterial abilities of BiOCl-based NMs. In fact, BiOCl NMs hydrolyzed by bismuth subsalicylate have been reported to act upon enteric pathogens without light irradiation in the gastrointestinal tract [12]. In order to study the mechanism of the antimicrobial properties of bismuth subsalicylate [31], Jan et al. investigated the antimicrobial effects of bismuth subsalicylate and BiOCl on Clostridium difficile, Salmonella, Shigella, Shiga toxin-producing Escherichia coli strains, and norovirus. The results indicated that bismuth subsalicylate and BiOCl have similar antimicrobial effects on a wide range of diarrhea-causing pathogens. Inspired by the excellent ROS generation ability, BiOCl-based NMs have been used to kill both Gram-positive and Gram-negative bacteria, including Staphylococcus aureus, Enterococcus faecalis, Escherichia coli, and Pseudomonas aeruginosa [32]. To enhance antibacterial efficacy, Ag nanoparticles are usually used to couple with BiOCl NMs [33][34]. On the one hand, Ag could not only enhance the light absorption ability due to the SPR effect, but also separate photoinduced electrons and holes as a result of heterostructure; on the other hand, Ag nanoparticles could release Ag+, which could kill bacteria effectively [35]. Forming a semiconductor heterostructure could also improve antibacterial efficacy. For example, BiOCl-AgCl [36], BiOCl-Bi3O4Cl [37], and BiOCl-BiO1.84H0.08 [38] heterostructures were designed, and showed that effective visible light triggered antibacterial performance. The binding between bacteria and antibacterial agents is another important key to improving the efficacy of bacterial inactivation. In order to regulate the binding ability with bacteria, Yu’s group [39] used PEG (MW = 10000) and cetrimonium bromide (CTAB) as a template to prepare two vacancy types of BiOCl microspheres. Fourier transform infrared spectroscopy showed no peaks of these two templates, which ruled out the effect of templates on the following bioeffects of the microspheres. The positron lifetime spectra and zeta potential proved that PEG-modified BiOCl microspheres exhibited one negative charge (−1.58 mV), while CTAB-modified BiOCl microspheres possessed ten negative charges (−15.95 mV).

2.4. Anticancer

The incidence rate and mortality rate of cancer are increasing year by year. According to the latest report from the World Health Organization, in 2020 there were 19.29 million new cancer cases and 9.96 million deaths [40]. As a non-invasive treatment technology, some new therapeutic methods based on nanotechnology, such as photodynamic therapy (PDT), photothermal therapy (PTT), and sonodynamic therapy (SDT), are widely used due to their advantages of strong tissue penetration, high efficiency, low side effects, and broad-spectrum anticancer applications. As semiconductors, more and more bismuth-based semiconductor NMs, such as bismuth sulfide [41][42], BiOBr [43], and Cu3BiS3 [44], have been used as PDT agents due to their ROS generation capabilities under light irradiation. Based on the excellent photocatalytic activity, Wu et al. first applied layered BiOCl NMs toward cancer PDT [45]. BiOCl nanosheets and nanoplates were synthesized through a hydrothermal method. Both of them have square shapes and have ideal dispersion stability after ultrasonic dispersion and polyetherimide (PEI) modification. Compared with the commonly used photocatalyst (P25), both BiOCl nanosheets and nanoplates could effectively degrade methyl violet and kill tumor cells with UV light irradiation.
In addition to PDT agents, bismuth-based NMs have also been used as other therapeutic agents, including SDT, PTT, and radiotherapy agents. NIR-activated PTT are a promising technology for tumor ablation. Usually, the photothermal properties are generated from localized surface plasmon resonances or narrow bandgaps (smaller than 1.53 eV) [21][46]. However, photothermal performance has also been observed for semiconductor bandgaps greater than 1.53 eV, the photothermal properties of which may originate from various defects, such as deep level defects in bismuth sulfide [47], hydrogen impurity in TiO2 [48], and oxygen vacancies in manganese dioxide [49] or bismuth tungstate [50]. Inspired by oxygen-vacancy-induced photothermal performance, oxygen vacancies have been introduced to BiOCl to endow them photothermal properties [16].
Considering the tissue penetration capability, ultrasound and X-ray are also used for irradiating semiconductors through different mechanisms. With ultrasound irradiation (20 kHz~1 GHz), the microbubbles (cavitation nuclei) existing in the liquid will vibrate, grow, and continuously gather the sound field energy. When the energy reaches the threshold, the cavitation nuclei will collapse and release the energy, producing local high temperature and high pressure (5000 K, 1800 ATM), thus resulting in the decomposition of water molecules and the fracture of chemical bonds. When these broken chemical bonds are recombined, they will release energy and produce luminescence (sonoluminescence). The emitted light is mainly ultraviolet light, which can be used to stimulate most semiconductor materials to generate ROS [51]. Therefore, BiOCl NMs could be excited by ultrasound to produce ROS.
X-ray is another method for stimulating semiconductors to produce ROS, due to its higher energy. This is especially true for bismuth-based semiconductors, as they have stronger X-ray absorption abilities due to high atomic numbers (83) and the X-ray attenuation coefficient (4.3 cm2 g−1 at 100 keV) of Bi elements. In fact, there have been some bismuth-based NMs used for radiation therapy, such as Bi2S3 [52], Bi2Se3 [53], Bi2O3 [54], BiOI [22], pure Bi [55], and BiOCl NMs [56]. However, the radiation therapy efficacy has been limited by the tumor microenvironment of solid tumors, such as hypoxia and antioxidative GSH. In order to improve therapeutic efficacy, Li’s group designed hydrogen peroxide (H2O2)-loaded Cu-doped BiOCl nanocomposites (BCHN) to improve the synergistic effect of radiation and chemodynamic therapy through modulating the tumor microenvironment [56]. BCHN were fabricated through a stepwise method. First, Na0.2Bi0.8O0.35F1.91 (NBOF) was obtained through co-precipitation of sodium nitrate, bismuth nitrate, and ammonium fluoride. Then, Cu2+ was absorbed on the surface of NBOF. After adding sodium hydroxide and H2O2, BCHN monodispersed mesoporous nanospheres were obtained, as proved by the XRD patternand SEM image. The existence of Cu2+ and H2O2 in BCHN has been confirmed by Cu 2p high-resolution XPS spectrum and the redox reaction of potassium permanganate and H2O2. Intracellular GSH and O2 levels showed that BCHN could effectively deplete GSH and produce O2 through Fenton-like reactions among Cu2+, GSH, and H2O2. Therefore, without radiation, BCHN alone could kill some cancer cells due to the chemodynamic property, as well as change the antioxidant and hypoxic microenvironment, while with radiation, BCHN could effectively produce ROS to kill the other cancer cells. In vivo experiments further proved that BCHN could be used as a synergistic radiation therapy/chemotherapy agent with good biocompatibility.

This entry is adapted from the peer-reviewed paper 10.3390/cryst12040491

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