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DOI: 10.1039/D4TB01357C (Paper) J. Mater. Chem. B, 2024, 12, 9030-9036

A superstable sandwich-type composite of a single-benzene-based fluorophore and chitosan as a fluorescent authentication barcode†

Jaehoon Kim a, Ji Hye Jin b, Ha Yeon Kim c, Joo Hee Hyun b, Sungnam Park c and Dokyoung Kim *abdefgh
aCollege of Medicine, Kyung Hee University, Seoul 02447, Republic of Korea. E-mail: dkim@khu.ac.kr
bDepartment of Biomedical Science, Graduate School, Kyung Hee University, Seoul 02447, Republic of Korea
cDepartment of Chemistry and Research Institute for Natural Science, Korea University, Seoul 02841, Republic of Korea
dDepartment of Precision Medicine, Graduate School, Kyung Hee University, Seoul 02447, Republic of Korea
eDepartment of Anatomy and Neurobiology, College of Medicine, Kyung Hee University, Seoul 02447, Republic of Korea
fCenter for Converging Humanities, Kyung Hee University, Seoul 02447, Republic of Korea
gKHU-KIST Department of Converging Science and Technology, Kyung Hee University, Seoul 02447, Republic of Korea
hMedical Research Center for Bioreaction to Reactive Oxygen Species and Biomedical Science Institute, Core Research Institute (CRI), Kyung Hee University, Seoul 02447, Republic of Korea

Received 21st June 2024 , Accepted 13th August 2024

First published on 14th August 2024

Abstract

Management of diseases through medication accounts for the largest portion of treatment, with people worldwide relying on a variety of medicines to treat and prevent minor to severe diseases in modern society. However, the recent increased use of counterfeit medicines rather than certified medication has emerged as a serious social concern. This study introduces a new hybrid material, named SBBF-chitosan (SC), which integrates a single-benzene-based fluorophore (SBBF) and chitosan, serving as a fluorescence-based authentication barcode for certified medication. The synthesis and characterization of SC, along with an analysis of its photophysical properties, were systematically conducted. SC demonstrated bright emission with high stability under various environmental conditions. In vitro analyses and in vivo animal experiment results further indicated the safety of SC for oral intake, even when directly incorporated into medicines. We are confident that this newly developed formulation SC provides a fundamental solution to address the challenges posed by counterfeit medicines, thereby safeguarding medication authenticity.


New concepts

Herein, we present a fluorescent authentication barcode as a new verification tool to distinguish counterfeit medicine, a global problem. The new fluorescent authentication barcode was synthesized based on single-benzene-based fluorophore (SBBF), chitosan, and SBBF-chitosan (SC) emitted bright orange fluorescence. SC further improved the high stability characteristic of SBBF and chitosan, demonstrating the superstable characteristics required as a fluorescent authentication barcode. SC emitted bright orange fluorescence without any change under various environmental conditions and also showed high stability, being released without any decomposition even after in vivo administration.

Introduction

Millions of people worldwide rely on medications to manage diseases and bodily conditions.1–4 However, people are faced with the threat of unwittingly consuming counterfeit medications daily.5–7 This reality extends even to developed countries that boast well-regulated healthcare systems.8–10 Counterfeit medicines have permeated various domains, including health supplements, contraceptive pills, treatments for erectile dysfunction and hair loss, and even medications combating life-threatening illnesses such as cancer.11–13 This phenomenon has evolved into a more serious social problem, instigating several side effects. What is more concerning is the inclusion of narcotic substances in these counterfeit medicines, leading many people into addiction without realization.7,14,15 Moreover, the emergence of online pharmacies, telemedicine services, and readily accessible online messenger apps exacerbates the problem.16–18

To solve the issue of counterfeit medicines, numerous preventive measures, such as scratch stickers, barcodes, and other identification methods printed on packaging, have been introduced.19–23 However, these tools have limitations as they can easily be replicated, and verifying the authenticity of the drug itself remains a challenge. To overcome these practical hurdles, the development of a new barcode system utilizing advanced materials is imperative to ensure clear distinction of certified drugs.

In this study, we disclosed a fluorescent sandwich-type composite consisting of a single-benzene-based fluorophore (SBBF) and chitosan, named SC, which holds the potential to prevent the problems associated with counterfeit medicines as a next-generation barcode material (Fig. 1).24,25 Chitosan, extracted from the outer skeletons of various marine organisms, is a representative bio-safe substance with significantly lower absorption rates in the living body.26–29 The chitosan-based composite SC is expected to exhibit high bio-sustainability and biosafety with successful in vivo excretion even after oral intakes an important consideration for orally ingested pills. The fluorescent chemical barcode SC, synthesized through the oxidative reduction of dimethyl 1,4-cyclohexanedione-2,5-dicarboxylate (DCD) and chitosan, exhibits a sandwich composite structure of SBBF embedded within chitosan layers.30SC holds several distinct advantages, including bright emission, superstability (non-degradable in various solvents), bio-safety, non-bioactivity, scalability, and cost-effectiveness important factors for developing a fluorescent barcode material for certified medicines.31,32 Leveraging these characteristics, SC can identify counterfeit medications (artificial tablets) by simple non-destructive fluorescence tracking. In vivo studies confirmed that when orally administered to mice, SC showed no absorption, distribution, or metabolism within the body and was completely excreted without any biotoxicity issues. The exceptional stability and bio-safety characteristics of SC indicate its suitability as a biomaterial for crafting new barcodes to distinguish certified medicines. We are confident that the newly engineered fluorescent barcode can establish itself as an excellent tool to curb the proliferation of counterfeit medicines.


image file: d4tb01357c-f1.tif
Fig. 1 Structure of SBBF-chitosan (SC), along with its advantages and development schematic, as a fluorescent chemical barcode for certified medicines.

Results and discussion

Materials characterization

SBBF-chitosan (SC) was prepared through an in situ one-pot synthesis involving DCD and chitosan under an open-air environment. Characterization of the synthesized SC was identified using various analytical tools, such as the attenuated total reflectance Fourier transform infrared spectroscopy (ATR-FTIR), Raman spectroscopy, 2D photoluminescence excitation (PLE) spectroscopy, and scanning electron microscopy (SEM). In the ATR-FTIR analysis, the ν(N–H) peak at 3200–3400 cm−1 and ν(C–H) peak at 2800–3000 cm−1 of chitosan were observed within the SC spectra (Fig. 2a).33–35 Additionally, the presence of the aromatic ester δ(C–O) peak at 1220 cm−1 was exclusively detected in the SC spectra.36 Raman spectroscopy results also confirmed the formation of benzene rings through the emergence of an ω(C–C) aromatic peak at 1588 cm−1 unique to SC a characteristic feature absent in pure DCD (Fig. 2b).37 ATR-FTIR and Raman spectroscopy results showed that aromatic rings and amine groups, which were not present in DCD, were formed in SC through a condensation reaction between DCD and the amine groups of chitosan, and that polymerization occurred through this process. Having validated the formation of SC through structural analysis, subsequent investigation delved into its photophysical properties. The excitation and emission spectra of SC were extracted from the photoluminescence excitation (PLE) spectrum (Fig. S1, ESI†). The solid-state absorption and emission spectra exhibited maximum peaks at 388 nm and 610 nm, respectively (Fig. 2c). Time-resolved fluorescence (TRF) signals of SC in the solid state were acquired using a time-correlated single-photon counting (TCSPC) method, revealing an average lifetime of 5.83 ns (Fig. 2d, excitation: 520 nm, TRF signals collection: 580 nm). In addition, the photoluminescence quantum yield of SC was confirmed to be 7.2 ± 2%. In comparison to chitosan, SC manifested an orange-colored powder when observed with the naked eye, and under UV, it displayed bright orange fluorescence, consistent with the solid-state fluorescence results (Fig. 2e). The quantum chemical calculations of the intermediate, representing a singular identically repeated sandwich structure of SBBF and chitosan within SC, yielded a HOMO–LUMO energy gap of 2.58 eV in the most optimized molecular conformation (B3LYP/6-31+G(3d) for the density functional theory (DFT) calculation).
image file: d4tb01357c-f2.tif
Fig. 2 Characterization of SC. (a) Attenuated total reflectance Fourier transform infrared (ATR-FTIR) spectra of DCD, chitosan, and SC. Symbols: ν = stretching; δ = bending. (b) Raman spectrum of DCD, chitosan, and SC. Excitation wavelength: 785 nm. Laser power: 36 mW. (c) Excitation and emission spectra of SC derived from solid-state 2D photoluminescence excitation (PLE) spectrum. Excitation wavelength: 360–600 nm. (d) Time-resolved fluorescence (TRF) signals of SC in the solid state. Experiments were carried out using a time-correlated single-photon counting (TCSPC) method. The sample was excited using a 380 nm pulse, and the corresponding TRF signals were collected at 610 nm. (e) Bright field and fluorescence images (under UV light, 365 nm) of chitosan and SC. (f) SEM images of chitosan and SC. Scale bar: 200 μm.

This value corresponded with the excitation spectra of SC (Fig. S2, ESI†). The electron density of the intermediate exhibited greater localization in the donor moiety (chitosan) in the HOMO, whereas in the LUMO, it was more localized in the acceptor moieties (–COOMe). Upon electronic excitation, the SBBF in SC was expected to undergo intramolecular charge transfer, facilitating the migration of the partial charge from the donor to the acceptor moiety. Next, SEM imaging and elemental mapping (EDS) were performed to verify the actual structure and elements of SC (Fig. 2f and Fig. S3, ESI†). The SEM imaging and EDS mapping results confirmed that SC exhibited a structure highly similar to chitosan, with the elemental composition and quantity almost identical to those of chitosan, as evidenced by the SEM imaging findings.

Stability analysis of SC

The chemical stability of the material is of utmost importance in its application to certified medicines as a barcode, as any decomposition during the metabolic process or organ digestion, or its persistence within the body could potentially induce serious side effects. Therefore, we performed a comprehensive stability analysis of SC under various solvent conditions to evaluate its suitability as an oral uptake barcode material. To confirm stability across various solvent conditions, 1 mL of each solvent was added to 2 mg of SC. Following a certain period of time, the mixtures were centrifuged at 13[thin space (1/6-em)]000 rpm for 10 min, after which UV/vis absorption and emission spectra were measured. 1 mL of fresh solvent was replaced for each subsequent measurement to maintain accuracy and reliability throughout the analysis. Firstly, the analysis was conducted in various organic solvents, such as n-hexane (n-Hex), ethanol (EtOH), tetrahydrofuran (THF), ethyl acetate (EtOAc), dimethyl sulfoxide (DMSO), and acetonitrile (ACN) (Fig. 3a, b and Fig. S4, ESI†). The results demonstrated that SC remained intact and was not degraded in all tested solvents, even after 24 h of incubation. Next, the stability of SC was evaluated under various pH conditions representing those encountered in the body (Fig. 3c, d and Fig. S5, ESI†). The findings confirmed that SC did not dissolve across all conditions, including deionized water (DW, pH 7), phosphate-buffered saline (PBS, pH 7.4), pH 3, and pH 10, indicating that SC retained its formulation integrity without any degradation of dissolution in vivo. We also investigated the stability of SC in biological media under conditions encountered during gastrointestinal administration in vivo (Fig. 3e, f and Fig. S6, ESI†). To achieve this, simulated salivary fluids (SSF, pH 6.8), simulated gastric fluids (SGF, pH 2.0), and simulated intestinal fluids (SIF, pH 6.8) were prepared (see the composition in Table S1, ESI†). SC showed high stability in various biomimetic media and was stable even in simulated gastric fluids at pH 2.0, further confirming that it is stable under most pH conditions within the body. These results support the prediction that SC could be excreted without issue, retaining its integrity, even when passing through the gastrointestinal tract. In addition, in the thermal stability and optical stability results verified for use as a fluorescent barcode, SC showed the same fluorescence emission efficacy even when exposed to 150 °C for 1 h, and high fluorescence emission efficacy was also shown when irradiated with a 365 nm laser for 1 h (Fig. S7, ESI†). These stability results suggest that SC can maintain stability even when mixed with other drugs within the body and subsequently be excreted, making it an ideal barcode material with high fluorescence emission efficacy under various conditions.
image file: d4tb01357c-f3.tif
Fig. 3 The intensity plot of absorption (at 388 nm) and emission (at 610 nm) using the supernatant of SC-incubated suspension (2 mg mL−1) within (a) and (b) organic solvents, (c) and (d) aqueous solvents, and (e) and (f) simulated digestion fluids. n-Hex: normal hexane, THF: tetrahydrofuran, DMSO: dimethyl sulfoxide, EtOH: ethanol, EtOAc: ethyl acetate, ACN: acetonitrile, DW: deionized water, PBS: phosphate-buffered saline, SSF: simulated salivary fluids, SGF: simulated gastric fluids, SIF: simulated intestinal fluids. Inset: Images of SC in each solvent were captured under a bright field and UV chamber (365 nm).

Practical application of SC

To validate the actual efficacy of SC as a fluorescent authentication barcode for medicines, we introduced SC to the medicine surface. As a result, it was confirmed that SC showed high fluorescence intensity even when it was present in more than 2 mg based on a tablet with a diameter of 1 cm (Fig. S8, ESI†). In addition, to verify whether this fluorescent authentication efficacy can be identified as a fluorescent barcode even when it is present inside the drug rather than attached to the outside, SC was mixed into the formulation with Eudragit EPO, an excipient commonly used in actual medicines. This SC/Eudragit formulation was produced using a tablet press (Fig. 4a). The corresponding formulation was 1 cm in diameter and exhibited bright orange emission at 365 nm. Subsequently, the emission depth of SC within the SC/Eudragit formulation was investigated. The formulation was placed under chicken tenderloins of varying thicknesses, and fluorescence tissue imaging system (FTIS) images were captured (Fig. 4b). The results confirmed that the SC/Eudragit formulation showed robust emission efficacy, penetrating tissue thickness of up to 6 mm while exhibiting weak emission only beyond a tissue thickness over 10 mm. This affirms the detectability of emission even when SC is incorporated into most medicine formulations. Additionally, the feasibility of fluorescence tracking for SC injected into most skin in vivo was demonstrated. Based on the emission depth test results of SC, an evaluation was conducted to assess the practical utility of SC as a fluorescent barcode for certified medicines. To this end, white tablets resembling actual medicines were manufactured (Fig. 4c). These tablets consist of an SC/Eudragit formulation encapsulated with Eudragit EPO. Various tablets were manufactured, with each formulation containing different amounts of the SC/Eudragit. Upon examination in a bright field, only the white color of Eudragit was observed, with no visible orange coloration indicative of SC presence (Fig. 4d). On the contrary, tablets with high amounts of SC showed distinctive emission differences when examined with FTIS images. Specifically, the control group devoid of SC showed no emission, whereas tablets containing SC displayed high emission intensities. This trend of heightened emission intensity tended to rise with the increase in SC content. These results clearly demonstrate that SC can function not only as a fluorescent barcode (on the outside of a tablet) but also as a means of certifying authenticated medicines by selectively incorporating SC in locations where genuine medicines are manufactured.
image file: d4tb01357c-f4.tif
Fig. 4 (a) Schematic illustration of the preparation of SC/Eudragit formulation (tablet) and fluorescence images under UV light (365 nm). (b) Bright field and fluorescence tissue images of SC/Eudragit tablet (half-size) under chicken tenderloins. (c) Schematic illustration of certified medicine authentication using SC/Eudragit tablet as a fluorescent chemical barcode. (d) Bright field and fluorescence images of SC/Eudragit tablets depending on the SC amounts. The fluorescent imaging was conducted at the PE detection channel (390–490 nm excitation, 575–640 nm detection). Scale bar: 1 cm.

Pharmacokinetic analysis of SC

Based on the various in vitro analyses and emission efficacy results for SC as a fluorescent authentication barcode, we further conducted a pharmacokinetic analysis to explore the movement of SC upon entry into the body. As depicted in Fig. 5a, the experiment involved dividing mice into two sets: set A (control group) and set B (SC-treated group). In set B, SC was dispersed within a carboxymethyl cellulose (CMC) solution (5 mg mL−1). CMC solution is currently one of the most essential food additives and is used in various foods, and is widely used in oral delivery systems because of its property of uniformly suspending substances.38 Conversely, only the CMC solution was administered to the control group (set A). After the administration (p.o.), mice in each set were sacrificed at certain time points (0, 1, 2, and 6 h), and their organs were harvested for analysis. The results of the absorption and distribution of SC over time revealed no emission of SC in the major organs of the body: brain, heart, lung, spleen, liver, and kidney (Fig. 5b). On the other hand, SC was exclusively detected in the intestines and was confirmed to gradually move from the stomach to the rectum over time (Fig. 5c). The hemolysis activity of SC was additionally conducted in the blood of mice to confirm the effect of SC in the blood. As a result, it was confirmed that SC showed negligible hemolysis activity up to a concentration of 10 mg mL−1, which is higher than the administered concentration of 5 mg mL−1 (Fig. S9, ESI†). In addition, upon collection and examination of the stools of the mice after 6 h, a bright orange coloration was observed in the stools in a bright field. When checked using FTIS imaging, high emission was confirmed solely in the stools of the mice from set B, without any traces detected in the bodies of mice (Fig. 5d). This pharmacokinetic analysis, based on SC emission tracking within the mouse body, confirmed that SC remained intact and was neither decomposed nor dissolved in the stomach or cecum, where digestive juices are predominantly secreted in the intestine. On the other hand, as shown in the ex vivo image, no fluorescence changes were observed in urine since SC did not move to the kidney (Fig. S10, ESI†). Instead, SC was excreted from the intestine without any absorption and distribution. Moreover, to confirm the spectroscopic property changes of SC after in vivo administration, an emission spectra comparison of the administered SC and the SC metabolites obtained directly from the sigmoid colon of the mice was performed. As with the stool, the FTIS image results showed that fluorescence emission from the SC metabolites and the administered SC was observed in the same filter, and the emission spectra of both groups were confirmed to show almost the same spectra (Fig. S11, ESI†). No changes in mouse weight, the shape of harvested mouse organs, or signs of acute toxicity were observed in the SC-treated set. Additionally, no fatalities occurred within 48 h after administration, confirming that SC does not induce any toxic effects in the body. These results signify that SC can be safely used, supported by its high stability within the body. This attribute presents a significant advantage of SC as a fluorescent barcode, particularly in the context of oral administration of certified medications.
image file: d4tb01357c-f5.tif
Fig. 5 (a) Experimental scheme of pharmacokinetic testing of SCvia oral administration. CMC: carboxymethyl cellulose. (b) FTIS image of six main organs and (c) gastrointestinal tract over time in the SC-administered mice. The images were acquired by tracking the signals of SC (PE channel: 390–490 nm excitation, 575–640 nm detection). (d) Bright field image and FTIS image of stool obtained from set A and set B. The FTIS images were acquired by tracking the signals of SC (PE channel: 390–490 nm excitation, 575–640 nm detection).

Conclusions

A novel sandwich-type composite of a single-benzene-based fluorophore and chitosan, named SC, is disclosed, along with its practical applications in addressing the issue of counterfeit medicines. SC could be synthesized on a large scale through a one-pot method with high yield. It exhibited bright emission characteristics in the solid state, even when encapsulated within drugs. Various in vitro analyses have indicated that SC has high stability in organic solvents and biological media across broad pH ranges. Through in vivo verification, SC was confirmed to be highly stable and bio-safe, as it was excreted from the body over time without any absorption or distribution in the body. We are confident that these characteristics of SC offer significant advantages as a fluorescent authentication barcode for insertion into medicines, overcoming the pressing global issue of counterfeit medicines. We believe that SC holds great potential to revolutionize the pharmaceutical market in the future.

Author contributions

Jaehoon Kim: conceptualization, methodology, investigation, visualization, writing – original draft, writing – review & editing. Ji Hye Jin: conceptualization, methodology, investigation, visualization, writing – original draft. Ha Yeon Kim: investigation, visualization. Joo Hee Hyun: investigation. Sungnam Park: supervision. Dokyoung Kim: conceptualization, funding acquisition, project administration, supervision, writing – review & editing

Data availability

The data that support the findings of this study are available from the corresponding author, upon reasonable request.

Conflicts of interest

The authors are listed as inventors on a pending patent application related to the technology described in this work.

Acknowledgements

This work was supported by grants from the National Research Foundation (NRF) of Korea (2022-R1F1A1069954) and the Bio & Medical Technology Development Program of the NRF of Korea (2021-M3A9I5030523). This research was also supported by the Core Research Institute (CRI) Program, the Basic Science Research Program through the NRF of Korea, Ministry of Education (2018-R1A6A1A03025124).

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Footnote

† Electronic supplementary information (ESI) available. See DOI: https://doi.org/10.1039/d4tb01357c
This journal is © The Royal Society of Chemistry 2024