An overview on animal/human biomass-derived carbon dots for optical sensing and bioimaging applications†

Prashant Dubey
Centre of Material Sciences, Institute of Interdisciplinary Studies (IIDS), University of Allahabad, Prayagraj-211002, Uttar Pradesh, India. E-mail: pdubey@allduniv.ac.in; pdubey.au@gmail.com

First published on 1st December 2023

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Prashant Dubey

Prashant Dubey received his PhD in Chemistry from the Indian Institute of Technology, Kanpur, India (2006) under the guidance of Professor Sabyasachi Sarkar. He also worked as a Postdoctoral Researcher with Professor C. J. Lee, School of Electrical Engineering, Korea University, South Korea. He is working as an Assistant Professor at the Centre of Material Sciences, University of Allahabad, Prayagraj, India since 03 November 2009. He has also been granted various fellowships (CSIR, DST, SSL, INSA, IASc, etc.) in his ongoing academic journey. His research interests include the development of low-dimensional nanomaterials for energy, environmental, and biological applications.

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1 Introduction

Carbon dots/quantum dots (CDs/CQDs) represent a family of zero-dimensional quasi-spherical carbon nanoparticles, which are typically less than 10 nm in size and primarily composed of a carbogenic backbone together with hydrogen (H), oxygen (O), and nitrogen (N)-containing surface functionalities.^1,2 Owing to their different structures and surface chemistry, CDs can be broadly categorized as carbon nanodots (CNDs), polymer carbon dots (PCDs), and graphene quantum dots (GQDs).^3,4 After the serendipitous discovery of nanosized CDs in 2004 during the purification of single-walled carbon nanotubes,⁵ they have attracted significant research attention in the scientific community as evidenced in Fig. 1. In 2006, Sun et al. observed bright luminescent emissions upon the surface passivation of acid treated carbon particles (obtained from laser ablation) by poly(ethylene glycol) (PEG), which, for the first time, were denoted as CDs.⁶ Since then, these emerging materials have become a rising star⁷ owing to their outstanding physiochemical properties (Fig. 2), such as multicolor photoluminescence (PL),^8,9 chemical inertness,¹⁰ and resistance to photo-bleaching.¹¹ Additionally, the aqueous/organic solvent dispersibility, high quantum yield (QY), low toxicity, good biocompatibility, and relatively inexpensive source for the low-cost, green synthesis of CDs further amplified their interest as an economical and environmentally sustainable class of fluorescent nanomaterials.^7,9,12–15 Consequently, the utility of CDs have been proven for diverse applications, including solar cells,¹⁶ optoelectronic devices,¹⁷ biosensing¹⁸ and chemical/metal sensing,^19,20 antibacterial agents,²¹ photocatalysis and electrocatalysis,²² displays,²³ nanothermometers,²⁴ drug delivery,²⁵ energy storage,²⁶ and live cell bioimaging²⁷ (Fig. 2). It has been demonstrated that synthetic methods, reaction parameters, and starting precursors are highly responsible for the specific characteristics of CDs.^7,28,29 Besides the conventional chemical precursors, there has been extensive research on the synthesis, properties, and applications of natural biomass/waste source-derived CDs as evidenced by the large number of review articles.^30–55

Most of the previous review articles described the synthesis, structural/optical properties, and different applications of biogenic CDs derived from diverse natural/waste sources, such as plant components (leave, stem, root, etc.), vegetables, fruits, foods, beverages, and wastes (agricultural, industrial, food, etc.), but rarely considered animal/human-derived precursors. For instance, Sharma et al.³⁰ discussed a variety of green source-derived CDs for sensing and bioimaging applications. Bhandari et al.³² presented the optoelectronic applications of CQDs/GQDs derived from various biomolecules including natural biomass. Meng et al.³³ highlighted the current developments in biogenic CDs synthesized from diverse natural sources. Fan et al.³⁴ focused on food waste-derived CQDs for food safety detection. Sekar et al.³⁷ reviewed the heavy metal ion detection capability of CNDs derived from various green resources. Desmond et al.⁴⁰ critically overviewed biomass-based CQDs for cancer therapy. Perumal et al.⁴¹ described the various applications of CDs derived from plant sources. The current developments in biomass-based CDs were also reviewed by Wareing et al.⁴² Chahal et al.⁴³ discussed green-synthesized CDs from natural/non-toxic chemicals. Shahraki et al.⁴⁶ presented the multifaceted applications of CDs particularly obtained from food waste. Ahuja et al.⁴⁷ outlined the energy and bioremediation applications of CQDs obtained from biomass waste. Kaur et al.⁴⁸ discussed the application of fruit waste-derived CDs in bioimaging. Manikandan et al.⁴⁹ discussed the environmental applications of green CQDs derived from plant/agro-industrial waste. Xiang et al.⁵⁰ critically reviewed CDs obtained from biomass/waste for biological and environmental applications. Fan et al.⁵² described biomass-derived CDs for sensing applications. Recently, Singh et al.⁵⁴ included CDs synthesized from a variety of biomass for the detection of hazardous ions. In another recent review article, Fang et al.⁵⁵ presented an overview of biomass-derived CDs, focusing on their preparation, property, and various applications. However, although there are numerous review articles related to biogenic CDs, a comprehensive overview of CDs derived from animal/human sources is limited in the literature. Natural biomass acquired from animal/human has attracted significant interest given that it is a minimal chemical intake, abundant, low-cost, and renewable green source. Moreover, the conversion of animal/human waste into value added products is an economical and sustainable approach to realize the waste-to-wealth initiative. Therefore, the assessment of animal/human biomass-derived CDs together with the recent achievements is paramount for future developments.

This review explicitly aims to present an overview of CDs synthesized from animal and human biomass for sensing and bioimaging applications. Initially, the diverse synthetic strategies, formation mechanisms, and various modifications associated with CDs are outlined. Furthermore, the comprehensive correlation/development of the size, QY, and elemental compositions of CDs derived from animal/human-based precursors using various preparation methods is presented with their structural and property description/relationship. Based on the preceding knowledge, the utilization of these animal/human biomass-derived CDs for metal ion/other analyte sensing and fluorescent biomarker applications is discussed together with a brief description of their other applications. Finally, this article is concluded by highlighting the achievements of these CDs in addition to identifying the future prospects of animal/human biomass as renewable resources and attempting to address the challenges/limitations in their practical implementation.

2 Diverse strategies for the synthesis of CDs

Broadly, CDs can be synthesized either via the top-down or bottom-up approach using chemical or natural precursors as starting materials. A schematic illustration of the various top-down and bottom-up synthetic routes is shown in Fig. 3. Both synthetic strategies have their own merits/demerits and have been developed with time for the preparation of narrow-sized CDs with excellent optical properties.

2.1 Top-down approach

This approach involves the breaking of bigger carbon precursors into nano-sized carbon particles. Here, the synthesis of CDs using various top-down methods is highlighted with specific examples.

2.2 Bottom-up approach

The preparation of nano-sized CDs via the condensation of small carbon precursors can be broadly termed the ‘bottom-up’ route. Some common bottom-up methods for the synthesis of CDs include hydrothermal (HT), solvothermal (ST), microwave (MW), microwave-hydrothermal (MW-HT), pyrolysis, and thermal decomposition (TD) (Fig. 3).

3 Formation mechanism of CDs

The formation mechanism of CDs follows different routes in the top-down and bottom-up synthetic approaches.

3.1 Top-down pathway

In the top-down route, graphite,^56,58 MWCNTs,⁶⁰ and other bulk carbonaceous sources (e.g., activated carbon,⁸⁵ activated carbon fiber,⁸⁶ and coal feedstock⁶⁹) have been utilized as the starting source, which can be broken/cleaved into tiny CDs by employing physical, electrochemical or chemical oxidation method. The breaking/etching of inherent chemical bonds associated with bulk carbon drives the formation of CDs. This bulk to nano transformation can be induced either by high energy (arc discharge, laser ablation, ultrasonication-based acoustic cavitation, etc.) or chemical/electrochemical reaction (Fig. 3). Although the physical top-down strategy is less common for biomass-derived CDs, some researchers employed the chemical oxidation-based top-down formation route and natural/waste resources such as coal feedstock,⁶⁹ candle soot,⁸⁷ coal tar pitch,⁸⁸ and carbonized olive solid waste⁸⁹ to produce surface-passivated CDs. The harsh oxidizing environment (HNO₃, H₂SO₄/HNO₃, H₂O₂, etc.) eventually disrupts the bonding arrangements of bulk carbon, resulting in its breakdown into CDs. He et al.⁹⁰ demonstrated the one-step transformation of carbon nanotubes (CNTs) into CDs via a thiol–ene click reaction. The sp² carbon of CNTs reacted with thiomalic acid under reflux condition to produce –COOH-functionalized CDs for bioimaging application. The formation mechanism of coal-derived N,S-CDs is based on the breaking of the organic carbon linkage (binding bridge of crystalline fragments in the microstructure of coal) via ˙OH radicals (produced from H₂O₂). The oxidant can reach inside the interlayers of the graphitic structure (abundantly present in coal) to facilitate the disintegration of the bridging bonds such as –CH₂–CH₂–, –CH₂–O–, –O–, and –S–. Moreover, acoustic cavitation induced by ultrasonication favours the breaking of the bonds between the graphitic structure and polycyclic aromatic fragments. These aromatic components eventually fragment into C₂ units to form N,S-CDs via polymorphic reaction.⁶⁹

3.2 Bottom-up pathway

The bottom-up formation of CDs relies on the solution-phase condensation/carbonization of small carbon-containing molecules. Organic molecules (conjugated or non-conjugated) or natural biomass can be used to produce CDs via the bottom-up route.^91,92 The involvement of four stages (condensation, polymerization, carbonization, and passivation) is commonly speculated in the formation of CDs from small organic precursors (Fig. 3).^91,92 Initially, the starting organic molecules get condensed into a small chain-like structure, which subsequently polymerizes to form polymer-like aggregates or carbon clusters. Subsequently, the carbonization/aromatization of polymer-like aggregates generates a carbonaceous core (amorphous/graphitic) at elevated temperature, which has an outer surface containing various functional groups.^91,92 The reaction temperature/time plays a crucial role in determining the sp²/sp³ domains of CDs in the carbonization step.^91,92 He et al.⁹³ described the formation mechanism of MW-synthesized N-CDs, involving inter-and/or intra-molecular dehydration of an amide-rich organic precursor, followed by polymerization and carbonization to produce a carbon core possessing oxygen-containing functional groups. It was observed that the amount of core backbone increased with an increase in temperature and time, which is ascribed to the gradual transformation of the functional groups into a carbogenic core. Cao et al.⁹⁴ proposed the formation mechanism of N-CDs derived from o-phenylenediamine using the ST method. Initially, 2,3-diaminophenazine (oxidized/cyclised product of the precursor) aggregates (H-bonding and π interaction) into a polymeric cluster, which creates a core–shell type of preliminary structure in the subsequent carbonization step. With time, the shells collapse with the evolution of the graphitised core in the form of N-CDs. Recently, Mohammed et al.⁹⁵ investigated the effect of reaction time on the formation mechanism of N-CDs derived from 4-aminoantipyrine under HT condition. The spectroscopic results indicated the reduction and enhancement of the peak intensities in the aromatic and aliphatic/carbonyl group region, respectively, with the extension of the reaction time, indicating the structural changes during the synthesis process. These changes are correlated with the π–π interactions (non-covalent) of the benzene rings present in the precursor molecules. Moreover, the attachment of polar functional groups to the surface of N-CDs was accompanied by the hydrolysis of the pyrazole ring present in 4-aminoantipyrine.

Generally, biogenic CDs follow the bottom-up formation mechanism due to the abundance of organic molecules in the starting precursors. Although it is difficult to track the exact mechanism of these CDs due to the complex composition of their starting precursor, the decomposition of biomass into active components, followed by their polymerization, condensation, carbonization, and nucleation are the commonly accepted formation steps.^96,97 For example, Shewanella oneidensis MR-1 bacterial cells first decomposed to macromolecules (polysaccharides/proteins/lipids, etc.), followed by hydrolysis to produce a large number of small organic molecules (saccharides/peptides/amino acids/hydrocarbon etc.). These small organic fragments get polymerized, condensed, and carbonized in the subsequent steps to form doped CDs due to nuclear burst.⁹⁷

4 Modifications of CDs

The modification of CDs is vital for the improvement of physiochemical features, particularly their optical properties. Recently, Fan et al.⁹⁸ reviewed the metal ion sensing application of modified CDs. The inherent modifications in CDs can be achieved either by heteroatom doping or surface functionalization.

4.1 Heteroatom doping

Various heteroatoms can be accommodated in the interior core or surface of CDs for the enhancement of their emission properties. Heteroatom-doped CDs usually possess abundant surface defects and active sites, resulting in the modification of their electronic structures via tuning of their initial band gap or formation of new energy levels.^3,42 Consequently, doped CDs show better possibility for diverse applications due to the improvement in their optical characteristics and QY.^3,42,98 N is one of the most common doping elements (atomic radius of C/N: 0.0914/0.092 nm), which is incorporated in CDs to improve their fluorescence properties.⁹⁹ A green precursor (glucose) was HT treated in the presence of NH₃ to produce N-CDs. The optimized N-CDs (N content: 10.94%) showed a significantly high PL emission with a QY of 9.6% compared to their undoped counterpart (QY: <1%), which is ascribed to the modifications in the surface/core electronic states of N-CDs. N-CDs were also used for the sensitive and selective detection of Cr⁶⁺.¹⁰⁰ Sulfur (S) is another heteroatom that can be incorporated in CDs to enhance their optical properties. For instance, S-CDs synthesized from a mixture of ascorbic acid (AA) and thioglycolic acid (TGA) using the HT method (180 °C, 6 h) showed a QY as high as 32.07%. Moreover, they could also recognize Fe²⁺/Fe³⁺ from a real oral ferrous gluconate sample.¹⁰¹ N and S elements are also codoped in biogenic CDs to enhance their fluorescence property and sensing application.¹⁰² CDs doped with boron (B) and phosphorous (P) heteroatoms are also known in the literature. For example, P-doped CDs derived from a trisodium citrate–phosphoric acid (H₃PO₄) mixture under HT condition showed a satisfactory QY (16.1%) and Fe³⁺ sensing ability via the quenching of their fluorescence signal.¹⁰³ Sadhanala et al.¹⁰⁴ developed B-doped CDs through the ST treatment of catechol (C source) and naphthalene boronic acid (B source). The violet luminescent B-doped CDs (QY: 39.4%) were implemented for the sensitive/selective detection of Mg²⁺. The choice of the natural precursor in the synthesis of doped CDs is advantageous for the self-incorporation of heteroatoms in their structure.¹⁰⁵ However, strategic doping can be achieved by using heteroatom-containing precursors together with the natural biomass. For example, the HT treatment of frozen tofu, EDA, and H₃PO₄ (210 °C, 4 h) produced N,P-codoped CDs, which were applied for sensing and bioimaging.¹⁰⁶

Wang et al.¹⁰⁷ firstly demonstrated the modification of CDs with metal ions (Mn²⁺) via the formation of Mn²⁺–coordination functional knots. Since then, a large number of metal ions has been used as doping agents for modifying the electronic state, charge density, and physiochemical properties of CDs.¹⁰⁸ For example, the simple room-temperature synthesis of Si-CDs was achieved using 5-sulfosalicylic acid and 3-aminopropyl triethoxysilane (APTES), which were also used for the detection of Hg²⁺.¹⁰⁹ The HT reaction between ethylenediamine tetraacetic acid disodium salt and FeCl₃·6H₂O yielded Fe-CDs with an Fe content as high as 13 wt%. Consequently, the Fe-CDs showed 2.6-times greater photocatalytic reduction ability (CO₂ to methanol) compared to the undoped CDs.¹¹⁰ Zhang et al.¹¹¹ used the traditional Chinese herb mulberry together with MgCl₂·6H₂O to synthesize Mg-CDs through the HT technique (200 °C, 10 h). The Mg-CDs were applied for in vitro osteoblastic differentiation and matrix mineralization.

4.2 Surface functionalization

The surface of CDs contains abundant functional groups, which can be modified with functional molecules either via covalent chemistry or non-covalent interaction.¹¹² Covalent modification involves the direct binding of additional molecules to the surface of CDs, whereas π interaction, electrostatic conjugation and van der Waals force direct non-covalent modification. The coupling of the abundant –COOH groups present on the surface of CDs with amine containing compounds via an amide linkage is one of the simplest covalent functionalization strategies to improve the fluorescence intensity and amphiphilic character of CDs.¹¹³ CDs derived from CA and diaminonaphthalene under ST condition showed an excellent QY of 70% ± 10%, which is attributed to the pronounced edge amination of the CDs to reduce the number of defect sites, therefore delaying non-radiative recombination.¹¹⁴ The acid-catalyzed esterification reaction between –COOH and –OH-containing compounds is another simple modification strategy. Lactose-derived CDs were modified with mercaptosuccinic acid (MSA) via the esterification protocol, which showed an improved QY (46%) in comparison to the unmodified CDs (21%). Furthermore, the MSA-CDs were also evaluated for Ag⁺ sensing application with good sensitivity and selectivity.¹¹⁵ Sulfonyl chloride compounds are attached to –NH₂-containing CDs via sulfonylation reaction. For example, amino-rich CDs (chitosan derived) were coupled with 4,4′-bis(1′′,1′′,1′′,2′′,2′′,3′′,3′′-heptafluoro-4′′,6′′-hexanedion-6′′-yl)chlorosulfo-o-terphenyl-Eu³⁺ (BHHCT-Eu³⁺) via sulfonylation reaction to fabricate a ratiometric fluorescent nanoprobe for the detection of Cu²⁺. Interestingly, the red fluorescence of BHHCT-Eu³⁺ (at ∼615 nm) was quenched in the presence of Cu²⁺ without affecting the blue fluorescence (at ∼410 nm) arising from CDs.¹¹⁶ The surface of CDs can also be redesigned with the silane moiety. For example, silylation chemistry was used to covalently functionalize CDs (CA derived) with tetraethyl orthosilicate and APTES, which possessed a large number of –NH₂ groups for the coupling of TGA-modified CdTe QDs. The resulting ratiometric fluorophore showed excellent Cu²⁺ sensing ability via quenching of the fluorescence signal originating from the CdTe QDs.¹¹⁷ Suzuki et al.¹¹⁸ grafted methyltriethoxysilane and 3-glycidyloxypropyltrimethoxysilane on –NH₂-containing CDs (prepared from CA and EDA using HT method) via epoxy-amine reaction, which were used to prepare organic–inorganic hybrid films for solid-state emitting devices. In a recent report, N-aminoethyl-γ-aminopropyltrimethoxysilane-functionalized CDs were applied for corrosion inhibition.¹¹⁹ Modification of the surface of CDs by copolymerization is advantageous to get a high molecular weight scaffold. For instance, Li et al.¹²⁰ used anionic ring-opening polymerization (monomer: glycidol) to conjugate hyperbranched polyglycerol (HPG) on the surface of –OH-containing CDs (derived from α-cyclodextrin via the HT process). Although the QY of HPG-g-CDs was estimated to be slightly lower (1.2%) than that of bare CDs (1.5%), they exhibited high water dispersibility and low cytotoxicity for cell labelling and imaging.

Besides, CDs are also modified with functional moieties via non-covalent interaction. The extended π system on the surface of CDs is advantageous to modify their surface via π–π interaction. For example, Si-CDs prepared from glycerol and APTES through the MW method were modified with dopamine (DA) via face-to-face π–π interaction. The resulting Si-CDs@DA was applied for the fabrication of an Ag⁺ sensor and intracellular visualization of Ag⁺.¹²¹ According to the surface functional groups/attached moieties, the CDs can impart surface charge (positive or negative) for the electrostatic interaction of targeting species. For instance, PEI-functionalized CDs were prepared via non-covalent adsorption/wrapping of a cationic polymer (PEI), which were further modified with FA via electrostatic interaction. The resulting FA-modified PEI-CDs were used as a fluorescent nanoprobe (turn-on, in vitro/in vivo) to target folate receptor-positive cancerous cells.¹²² Carrot juice-derived CDs were non-covalently modified (electrostatic interaction) with PEI and Nile blue chloride (organic dye) to assemble a two-photon fluorescent nanoprobe for the detection of Cu²⁺ (turn-on–off) and S²⁻ (turn-off–on).¹²³ The complexation/coordination strategy is also executed on CDs to attach functional species on their surface. For instance, when orange peel-derived CDs were modified with ethylenediamine tetraacetic acid (EDTA) via complexation, they showed higher sensitivity for the detection of Cr⁶⁺ compared to bare CDs due to the strong chelating ability of EDTA.¹²⁴

5 Developments in the precursors and synthetic methods for animal/human biomass-derived CDs

Besides plant-derived components as a natural resource, the use of animal- and human-based biomass has attracted tremendous interest over the past one decade for the synthesis of CDs and their doped counterparts. A representative illustration of the different animal/human-derived biomass used for the synthesis of CDs is shown in Fig. 4. These types of biomass are usually referred to as ‘green precursors’, which are sustainable, inexpensive, environmentally compatible, abundant, and renewable sources of carbon together with other elements. Moreover, the preparation of applied materials from these sustainable precursors is also a waste-to-wealth approach because many of them can be recognized as discarded biowaste. Although the synthesis of CDs from biomasses can be grouped into two broad categories, namely, top-down and bottom-up approach, the bottom-up protocol is widely implemented for this purpose. In this regard, the fusion of bio-derived organic precursor molecules under HT condition is one of the highly explored techniques; however, other methods such as pyrolysis, MW, alkaline hydrolysis, ultrasonication, MW-HT, thermal annealing, roasting (R)/grilling (G)/baking (B), acid carbonization, TD, autoclave TD (AT), and condensation are also adopted in the synthesis of biogenic CDs from various animal/human biomass (Table 1). Importantly, the bottom-up approach is advantageous compared to the top-down method for the production of CDs with a high yield, narrow size, heteroatom doping, good quality, and excellent property due to its simple and cost-effective operation. The AT calcination of grass at 180 °C and subsequent separation via centrifugation were probably the pioneering method for the synthesis of biogenic CDs.¹²⁵ The authors proposed that these CDs are photoluminescent polymer nano-dots because of their crystalline structure with considerably smaller lattice spacing (0.20 nm) than that of graphitic carbon (0.34 nm). This pioneer report on the use of a natural source started a new trend of utilizing green biogenic resources for the synthesis of CDs. In this section, we summarize the synthesis and structural/compositional developments of CDs obtained from different animal and human biomass in chronological order using various synthetic approaches.

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5.1 Animal-derived precursors

The components of animal derivatives include an abundance of proteins, fats, carbohydrates, amino acids, vitamins, and minerals. These constituents hold potential to serve as viable biosources for the synthesis of both CDs and their doped analogues.

5.2 Human-derived precursors

Besides animal biomass, various nontoxic human-derived raw/waste sources such as hair, urine, and fingernails have also been applied to produce fluorescent CDs and their doped counterparts.

5.3 Formation mechanism of CDs derived from animal/human biomass

Some research groups discussed the formation mechanism of animal/human-derived CDs in their reports. For instance, the formation mechanism of N-CDs from egg white begins with the hydrolysis of egg protein into peptides and amino acids during the HT process. Subsequently, partial polymerization, followed by the carbonization of amino acids results in the generation of a carbon core coated with oligomers. With the progression of the reaction, the oligomers are gradually eliminated from the core surface to form N-CDs with –OH and –COOH functionalities.¹²⁹ Subsequently, a similar formation mechanism was proposed for doped CDs derived from egg albumin/egg white using the alkaline hydrolysis/MW synthetic method.^130,133

He et al.¹³⁹ presented the combined effect of the top-down/bottom-up strategy in the formation of N-CDs from cocoon silk. The ˙OH radicals generated from H₂O₂ under HT condition cleave silk into small microrods. As the reaction proceeds, the fragments from the microrods get hydrolyzed into small molecules. Subsequently, the dehydration and polymerization of these molecules nucleate nanospheres for the formation of N-CDs via intermolecular dehydration/polymerization.

The MW-assisted transformation of silk sericin into N-CDs was studied through gas chromatography-mass spectrometry, which exhibited the release of various gases (CO₂, NH₃, N_xO_y, C_xH_yO_z, H₂O, etc.) during operational condition. The high/instant temperature and generated OH⁻ cleave sericin into amino acids and polypeptides. These active components get aggregated and carbonized in subsequent steps to form a graphitized carbon core attached with heteroatom-containing functional groups.¹⁴⁵ The N-CDs produced from silk sericin under pyrolysis condition underwent dehydration, depolymerisation, carbonization, and self-passivation to form a carbon core decorated with functional groups. It was also observed that the graphitization of the core carbon (I_D/I_G: 0.95/0.69/0.63/0.51) and average size of N-CDs (5.3/6.7/8.4/9.6 nm) increased with an increase in the pyrolysis temperature (150/200/250/300 °C).¹⁴⁶

Bi et al.¹⁵¹ discussed the formation mechanism of N-CDs extracted from pike eel at different roasting temperatures, indicating the intensified polymerization/carbonization of fish ingredients (carbohydrates, proteins, and lipids) at a higher roasting temperature. The light pink fish flesh (Fig. 8A) turned a golden colour (Fig. 8B) at 160 °C, which was composed of irregular microstructures (Fig. 8G) with weak fluorescence (Fig. 8M) due to its insufficient combustion. When the roasting temperature was increased to 200 °C, the flesh showed a brown/curled appearance (Fig. 8C) with the evolution of a few carbon nanoparticles in the microstructure (Fig. 8H) and weak fluorescence (Fig. 8N), indicating the disintegration of the large biopolymer clusters. The formation of char on the surface of the flesh (Fig. 8D) and shrinkage of the clusters (Fig. 8I) occurred at a roasting temperature of 230 °C due to the extension of carbonization, which also showed stronger fluorescence (Fig. 8O). A further increase in the roasting temperature (260 °C) resulted in more charred product on the flesh surface (Fig. 8E), possessing a large number of CDs (Fig. 8J) and intensified blue fluorescence (Fig. 8P). The disintegration of the biopolymer clusters was significant at this stage, which was further extended at 300 °C. Consequently, the flesh surface turned into charred mass (Fig. 8F) having small-sized CDs (Fig. 8K, 1.75–4.25 nm) with strong cyan fluorescence (Fig. 8Q). A similar observation/explanation of escalated carbonization at a higher processing temperature was also presented for N-CDs derived from duck¹⁵⁶ and chicken.¹⁵⁸

The growth mechanism of N-CDs derived from human hair using the AT/MW method starts with the cutting/unzipping of the tertiary structures present in hair to generate a significant amount of small hydrocarbon. Subsequently, the C–C bonds are disintegrated with the evolution of nitrogen (depolymerisation), followed by cross-linking to form N-CDs.²⁴²

6 Physiochemical properties of animal/human biomass-derived CDs

6.1 Structural characteristic and chemical composition

Structurally, most animal/human biomass-derived CDs are composed of a carbogenic core (predominantly sp²-hybridized carbon) and outer shell comprised of O- and/or N-containing functional groups attached to its surface. C, O, and N are found to be very common elements in these CDs; however, the successful doping of other elements (S, P, Fe, Zn, Mg, etc.) has also be reported, as shown in Table 1. There are numerous reports showing that the incorporation of heteroatoms significantly modifies the composition of CDs and effectively improves their QY (Table 1). The surface functionalities of the shell not only provide good aqueous solubility/dispersibility, but also tune the optical properties of animal/human biomass-derived CDs. Generally, surface zeta potential analysis is used to determine the strength of the electrostatic repulsion amongst CDs due to the presence of abundant surface charge. A large negative zeta potential value suggests strong electrostatic repulsion among the negatively charged functional groups and better stability of animal/human biomass-derived CDs in aqueous solution.^{128,129,131,132,140–142,144,185,189,191,197,203,207,208,215} Besides a negative zeta potential, animal/human-derived CDs with positive zeta potentials have also been reported.^{137,198,230,236,243} The functional groups and elemental compositions of animal/human biomass-derived CDs are often analyzed by Fourier transform infrared (FTIR) spectroscopy and XPS. Fig. 9a–d show the representative FTIR and XPS results of chicken breast-derived N-CDs, respectively.¹⁵⁹ The N-CDs obtained at a roasting temperature of 200/300 °C presented broad absorption peaks at ∼3267/3425 cm⁻¹ due to the stretching modes of the O–H or N–H bonds. The peaks at ∼2925/2932 cm⁻¹ were assigned to the –CH₂ stretching vibrations. The typical absorption peaks at ∼1593/1674 cm⁻¹, 1395 cm⁻¹, and ∼1121 cm⁻¹ were attributed to the CO stretching modes, vibrations corresponding to the C–N bonds, and C–O–C bonds, respectively. Interestingly, the peak intensities for the C–N and C–O–C bonds were low for the N-CDs extracted at 300 °C compared to that at 200 °C, which was ascribed to the partial breakdown of these bonds at a higher roasting temperature (Fig. 9a). Moreover, the XPS survey spectrum of the N-CDs synthesized at 300 °C exhibited C 1s (285.0 eV, 67.15%), N 1s (400.0 eV, 13.29%), and O 1s (531.0 eV, 18.80%) elements (Fig. 9b). The four deconvoluted peaks located at ∼284.5, 285.5, 286.4, and 288.6 eV in the C 1s core level peak are assigned to the CC, C–N, C–O, and CO bonds, respectively (Fig. 9c), while the high-resolution N 1s spectrum (Fig. 9d) showed two peaks at ∼398.1 eV (amide N bonds) and ∼398.6 eV (pyridinic N bonds). Many characterization techniques such as powder X-ray diffraction (PXRD), high-resolution transmission electron microscopy (HRTEM), and Raman spectroscopy are applied to investigate the crystalline nature and defect density of CDs. The PXRD spectra of CDs and doped CDs synthesized from animal/human biomass typically exhibit a diffraction peak in the 2θ range of 20° to 27°, which corresponds to the (002) graphitic plane. For example, the PXRD pattern of chicken cartilage-derived N-CDs showed an intense peak at 2θ = 23.2° due to the (002) graphitic planes (Fig. 9e).²¹⁷ Moreover, a nearly spherical shape (Fig. 9f), narrow size distribution (Fig. 9g), and high crystallinity with 0.24 nm lattice spacing corresponding to the (100) graphitic plane (inset of Fig. 9f) were also revealed for these N-CDs by TEM and HRTEM analyses.²¹⁷ Most animal/human biomass-derived CDs or their doped counterparts exhibit spherical/quasi-spherical shapes with a size of less than 10.0 nm (Table 1); however, the synthesis of large-sized CDs from animal biomass has also been reported. For example, CDs derived from silkworm chrysalis (∼19.0 nm),¹⁴⁰ goose/chicken feathers (∼21.5/35.0 nm),^205,206 pigeon manure (∼15.65 nm),²²¹ fish scale (∼61.0 nm),²²⁷ and shark cartilage (∼50.0 nm).²³² Biogenic CDs with an average size of above 10 nm were also prepared using human biomass such as human hair (∼11.0/78.0 nm)²⁴² and human urine (UPDs: 20.6 nm, CPDs: 11.4 nm, and APDs: 38.8 nm).²⁴⁴ Generally, the Raman spectrum of carbonaceous nanomaterials including CDs comprised of a G band (first-order Raman band due to the in-plane vibration of sp² carbon) and D band (defect centers induced by sp³ carbon). A high I_D/I_G ratio in nano-carbon indicates the presence of disordered structure. For example, the Raman spectra of OCDs and MCDs synthesized from human hair showed two typical peaks at ∼1316 cm⁻¹ (D band) and ∼1584 cm⁻¹ (G band) with I_D/I_G ratios of 1.12 and 1.14, respectively (Fig. 9h), suggesting the disordered structures of nano-carbon. Moreover, the shoulder peak at ∼1200 cm⁻¹ in the spectrum of OCDs (dotted circle in Fig. 9h) is ascribed to the π–π charge transfer between OCDs and NO rings.²⁴² The molecular weight and various functional groups/minute structural features of salmon fish-derived CDs were confirmed by matrix-assisted laser desorption ionization time-of-flight mass spectrometry (MALDI-TOF-MS) and ¹H nuclear magnetic resonance (NMR) and ¹³C NMR spectra.¹⁶³ The predominant peak at 1056 m/z indicated the small size of the isolated CDs (Fig. 9i). Moreover, the ¹H NMR signals at 1.23, 2.96, and 3.12 ppm were attributed to the alkyl, R³ N–C–H, and –O–C–H protons, while the peaks in the range of 3.82–4.1 ppm and 7.0–9.0 ppm were ascribed to the protons attached to the alcohol groups and aromatic protons, respectively (Fig. 10a). The peaks in the range of 10–30 ppm, 30–40 ppm, 40–65 ppm, 65–90 ppm, and 110–180 ppm in the ¹³C NMR spectrum are assigned to the carbon of the –CH₃ groups, carbon from the CH/C–/–C=C–O– groups, carbon in the –CN–/N–CH₃/C–N– structures, sp³ carbon of alcohols/ether groups, and aromatic carbon, respectively (Fig. 10b).

6.2 Optical properties

The remarkable optical features of CDs such as their absorption, emission wavelength, excitation-tunable emission, QY, lifetime, photo and chemical stability are crucial for their potential applications. Table S1† clearly reveals that most animal/human biomass-derived CDs are comprised of a distinct absorption in the UV range (200–400 nm) and tails extended into the visible region. The lower wavelength peak is mainly due to the core domain of CDs (featured by the sp²-hybridized carbon framework of conjugated π electrons), and generally recognized as the π → π* transitions of the extended aromatic rings and CC segments (Table S1†). Meanwhile, the peak/shoulder at a relatively higher wavelength in the UV region is correlated with the low energy n → π* transitions of CO bonds/other functional groups attached to the surface or trapped excited state energy on the surface/edge (Table S1†). Therefore, it can be concluded that irrespective of the animal/human biomass utilized as the starting precursor, the optical absorption of CDs originates from their core and/or surface defects/surface states/functional groups. For example, Mohamed et al.²⁰⁰ observed two sharp absorption peaks at ∼230 nm and ∼315 nm, corresponding to the π → π* transitions of CC and n → π* transition of the CO bonds in N,S-CDs derived from a mixture of milk and methionine (Fig. 11a). Additional modifications in the surface functional groups are also directed to improve the optical absorption of CDs. For example, when crab shell-derived N-CDs were conjugated with FA via EDS/NHS coupling reaction, it resulted in strong peak at ∼210 nm and higher absorption at ∼280 nm in comparison to the bare N-CDs (λ_abs = 260 nm).¹⁷⁹

PL is one of the most fascinating features of CDs, which determines their utility in sensing and bioimaging applications. Particularly, the excitation-wavelength dependent (EWD) emission of CDs is important for multicolor imaging applications. The PL emissions in most animal/human biomass-derived CDs exhibit the typical Stokes-type behavior (down-conversion, Table S1†). It was observed that some animal-derived CDs showed emission spectra with good symmetry and narrow full-width at half-maxima, which were correlated with the narrower size distributions of the CDs.^130,201 Moreover, depending on the physiochemical characteristics of animal/human biomass-derived CDs, their PL spectra may follow either EWD emission or EWID behavior (Table S1†). The PL behavior of CDs is still under debate; however, there are some hypotheses for its origin, as follows: (i) core-based emission due to the band gap transitions in the conjugated π-skeletons, which is determined by the size of the carbogenic core (quantum size effect) and degree of graphitization; (ii) surface state-based emission (or trapping of excited state energy at the surface/edge states) induced by the surface/edge defects and/or passivation of the core surface via the attachment of functional groups; and (iii) molecular state-type emission due to the fluorophores (free or bonded) present in the CDs. A closer look at the emissions behavior and structural features of animal/human biomass-derived CDs indicated that either of the first two factors or their combination may influence the PL feature of CDs; however, one of them may be dominant in some cases (Table S1†). Fig. 11b shows the typical profile of the EWD-dependent PL spectra of N-CDs (egg yolk derived) in the λ_ex range of 320 to 420 nm and maximum emission intensity at 340 nm excitation.¹³⁷ Most of the animal/human source-derived CDs showed blue (inset of Fig. 11a) or blue-green luminescence under the irradiation of UV light (λ_ex = 365 nm) (Table S1†). The EWD emission is a distinct observation (Table S1†); however, EWID emissions^{135,145,185,200,212,215,227,231} or the combination of both EWD and EWID^223,225 were also noticed in animal biomass-derived CDs (Table S1†). For example, recently synthesized N,S-CDs (from a mixture of milk powder and methionine) exhibited EWID emission (λ_em = ∼ 470 nm) in the λ_ex range of 360–410 nm and maximum emission intensity at λ_ex = 383 nm (Fig. 11c).²⁰⁰ Interestingly, Ca-self-doped CDs specifically derived from animal bones (without additional purification steps) showed EWID behavior.^212,215 The authors speculated that the functional groups attached to the surface of the CDs effectively passivated the surface defects, and therefore the EWID characteristics originated from the single radiative transition of the core sp² carbon.

7 Applications of animal/human biomass-derived CDs

Due to the unique properties of animal/human biomass-derived CDs such as small size, abundant surface functionality, low toxicity, aqueous solubility/dispersibility, and biocompatibility, they may function as excellent nanoprobes for sensing and biological applications.

7.1 Sensor application

When foreign species/analytes (metal ions, biomolecules, drugs, etc.) come in contact with CDs, they preferably interact with their surface functional groups, resulting in either a reduction/enhancement in their emission intensity (light-down/light-up) or shift in their PL peak or change in their absorption behavior. Therefore, it is desirable for the optical signal of CDs to be altered after the addition of the analyte to construct an efficient sensor probe. In this case, “turn on–off” of the fluorescence signal is the most common approach (Fig. 12a); however, the “turn on–off–on” approach (Fig. 12b) is also employed to design sensor platforms using animal/human biomass-derived CDs (Table 2). Moreover, the involvement of several quenching mechanisms in the sensing process such as static quenching effect (SQE), dynamic quenching effect (DQE), fluorescence resonance energy transfer (FRET), IFE, electron transfer (ET), aggregate-induced quenching (AIQ), coordination/interaction-induced quenching (CIQ/IIQ), and PET is also revealed in Table 2.

---

7.2 Bioimaging application

Compared to metal-based QDs, fluorescent CDs are found to be more suitable for bio-applications due to their small size, high water dispersibility/solubility, low cytotoxicity, superior cell viability, high photo-stability, and good bio-degradability. Multimodal bioimaging through CDs is an effective approach for diagnosis and cell labeling. It is known that CDs may have critical effects on living cells and model organisms.^261–263 Therefore, before applying CDs in various bio-environments, it is necessary to understand their in vitro and/or in vivo cytotoxicity as well as bio-distribution and cellular uptake for safety purpose. In this section, the toxic evaluation, bio-distribution, cell uptake, and bioimaging applications of animal/human biomass-derived CDs are summarized.

7.3 Other applications

The promotion of plant growth using animal biomass-derived CDs is another growing area of interest.^168,169,172 For instance, bee pollen-derived EBCDs exhibited better promotion capability on the growth of the classical Arabidopsis plant model in comparison to WBCDs. The high growth-promoting ability of EBCDs was ascribed to their high content of N- and O-heteroatoms, which resulted in greater biocompatibility and bioactivity.¹⁷²

The antimicrobial activity of animal-derived CDs has also been investigated.^171,181,184 For example, crab shell-derived CDs were used as an antibacterial agent against highly noxious human pathogenic bacteria (Escherichia coli (E. coli) and Klebsiella pneumonia). The high inhibition activity of CDs in this study was ascribed to the effective damage of the cell membrane via the generation of ROS on the surface of CDs.¹⁸¹

Animal biomass-derived CDs have also been investigated for therapeutic application.^132,220 For example, boronic acid-functionalized PBA-CDs (derived from cow manure) were employed as an immunotherapy agent to treat melanoma skin cancer-bearing mice, which exhibited interaction with tumour tissues and stimulated the immune system against the disease. The histopathological imaging of the cancer-bearing mice after treatment with PBA-CDs exhibited no obvious damage to the brain and kidney tissues, while the liver, spleen, and lung tissues showed inflammatory focus, white pulp hyperplasis, and fibrosis/inflammatory infiltrate, respectively. The histological analyses also revealed necrosis and inflammatory infiltrate on large areas of tumour tissues after PBA-CD treatment.²²⁰

The drug delivery applications of doped CDs derived from dried shrimps,¹⁷⁷ crab shell,¹⁷⁸ and pasteurized milk²⁰¹ are also appreciable. For instance, magneto-fluorescent Gd-CDs (derived from a mixture of crab shell and GdCl₃) showed potential for diagnostic and theranostic application. FA@Gd-CDs specifically targeted HeLa cells (folate receptor-positive) via folate receptor-mediated endocytosis. Moreover, doxorubicin (DOX, anti-cancer drug) conjugated with FA@Gd-CDs (∼74.5% loading) exhibited higher release kinetics at low pH (5.0) in comparison to high pH (7.4), which was ascribed to the weakened DOX binding with CDs due to the protonation of the –NH₂ groups present in DOX.¹⁷⁸

Animal-derived CDs have also been employed to prepare fluorescent ink for multi-colour coating, patterning, and word writing, which is vital for staining, information encryption, and anti-counterfeiting applications.^{126,145,166,193,202,204,221,235} Li et al.¹⁴⁵ employed silk sericin-derived N-CDs to prepare multimodal quick response/bar security codes and Morse code-based encryption, which could be recognized under UV irradiation and immediately after switching-off of the UV light. Moreover, the N-CD ink coated on different fabrics (silk, cotton, and terylene) was visible once the UV light is turned-off after exposure.

The catalytic and photocatalytic applications of animal/human biomass-derived CDs have also been investigated.^{148,167,206,228,249} Recently, Din et al.²⁰⁶ demonstrated 92% degradation of methylene blue (MB) by chicken feather-derived CDs during 60 min exposure to sunlight. The catalyst also showed reusability of up to 5 cycles. The photo-generated electrons/holes on the surface of the CDs induced the formation of superoxide anion radical (O₂˙⁻)/˙OH, which eventually decomposed the aromatic structure of the dye molecules.

Athika et al.²⁰³ investigated denatured milk-derived CDs for supercapacitor application. The rectangular shape of the cyclic voltammetry curves and almost symmetrical galvanostatic charge-discharge (GCD) profiles implied the existence of double layer capacitance. The specific capacitance was estimated to be 95.0 F g⁻¹ together with 100% columbic efficiency/cyclic stability during 1000 GCD cycles at 0.12 A g⁻¹.

The free radical scavenging activity of animal source-derived CDs is also remarkable.^153,161 Mackerel fish-derived N-CDs were utilized for unique free radical (˙OH and ˙CH₃) scavenging activity, which showed potential to protect against oxidative stress under biological condition. The scavenging of ˙OH radicals via Fenton reaction resulted in strong fluorescence quenching due to the changes in the energy levels of the N-CDs. The dose-dependent scavenging exhibited 90% disappearance of the ˙OH signal using 15.0 mg mL⁻¹ N-CDs. Additionally, the 41.4% decrease in the reaction rate constant implied the remarkable reduction of the MB (source of ˙CH₃ generation by visible-light photosensitization) degradation rate via ˙CH₃ scavenging.¹⁶¹

The non-linear optical (NLO) phenomenon refers to a process that non-linearly depends on the excitation light parameters. An aqueous dispersion of N,S-codoped CDs (obtained from a mixture of honey, garlic extract, and NH₃) showed a self-defocusing and strong NLO response. The third-order NLO susceptibility was estimated to be significantly high (2.29 × 10⁻⁶ esu) together with reverse saturable absorption in the open aperture curve, which indicated the suitability of doped CDs for NLO application.¹⁷¹

8 Challenges and future prospects

Considering the significant utilization of animal/human biomass in the synthesis and potential applications of sustainable CDs, there are several challenges and prospects that require attention in the foreseeable future, as follows:

(1) Exploring novel precursors capable of self-doping and surface passivation, coupled with refined bottom-up synthetic protocols can potentially enhance both the performance and fluorescent QY of CDs.

(2) Attaining precise control of the size distribution, degree of graphitization, and surface functionalization remains crucial for achieving exceptional optical properties in CDs, necessitating further improvement.

(3) The presence of impurities in CDs has the potential to impede the desired performance outcomes. Therefore, developing new, uncomplicated, and cost-effective purification protocols is essential to achieve optimal results.

(4) Although the applications of animal/human biomass-derived CDs have shown promise at the laboratory scale, achieving their commercial-scale production has proven to be a challenge. Thus, comprehensive research is needed to enable the large-scale synthesis of CDs from these readily available precursors while retaining their inherent small-scale properties.

(5) Despite the clear influence of synthetic parameters and starting sources, the actual underlying growth mechanism of these CDs remains unknown, requiring comprehensive understanding through empirical/in situ experimental evidence.

(6) The precise origins of the PL and EWD/EWID features in these CDs still need to be elucidated, making it a pivotal area for in-depth investigation.

(7) In addition to the common down-conversion fluorescence, some animal/human biomass-derived CDs exhibit UCPL (Table S1†), which holds potential for near infrared (NIR) cellular imaging via two-photon luminescence and catalyst fabrication for energy-related applications. Consequently, these application areas offer fertile ground for new research.

(8) The design of CDs with long λ_em using animal/human biomass remains uncharted. Therefore, dedicated efforts should be devoted to creating CDs with NIR absorption and emission properties, leveraging the low biotoxicity and efficient tissue penetration capabilities of NIR light.

(9) Many sensors for metal ions and their tracking in biological systems using these CDs rely on light-down (fluorescence quenching) mechanisms. However, the development of light-up (fluorescence enhancement, Table 2) phenomena in the presence of analytes can be a valuable advancement, addressing the challenges posed by the high background fluorescence in biological environments.

(10) Opportunities exist to enhance the sensitivity and selectivity of analyte detection and tracking in real samples and biological systems by producing CD nanoprobe sensors using new precursors or modifying chemical composition/structure. Furthermore, there is untapped potential to develop sensing platforms for various toxic metal ions such as Mn²⁺, Pb²⁺, As³⁺, Po³⁺, and other unexplored analytes using these CDs in the future.

(11) Investigation of the long-term acute toxicity of animal/human-derived CDs on vertebrates and humans is insufficient. Moreover, advancement in the in situ tracking of these CDs may facilitate the in depth understanding and assessment of the metabolic process.

9 Conclusions

This review article presented a comprehensive overview of CDs synthesized from biomass of animal and human origin, aiming to provide researchers with insights for novel experimental implications and advancements in this field. This type of biomass, which is often considered inexpensive or waste materials, offers a sustainable and eco-friendly resource that can be converted into value-added products. The choice of precursor and synthetic method significantly influences the fundamental structure, heteroatom doping, and surface functional groups of the resulting CDs. Consequently, both the CDs and their doped counterparts can benefit from size control, leading to an enhanced QY. Many of these CDs exhibit self-passivation through various functional groups, offering opportunities for tailored modifications catering to specific applications. Notably, the optical properties of these CDs are closely related to their structure and chemical composition. In addition to the common emission known as EWD fluorescence, these CDs display EWID and UCPL behaviours. Their EWD fluorescence properties are primarily influenced by the quantum size effect of the core structure, the presence of surface emission centers arising from the presence of functional groups or defect sites, and the radiative recombination of excitons trapped at the surface. Conversely, their UCPL characteristics stem from a multi-photon activation process. The outstanding PL properties of these CDs combined with their attributes such as photo-stability, low cytotoxicity, and high biocompatibility make them promising candidates for various sensing, bioimaging, and many more applications. Consequently, the utilization of animal and human biomass has potential to emerge as a sustainable and eco-friendly platform for creating fluorescent CDs characterized by excellent optical properties, thereby opening diverse avenues for their application.

Conflicts of interest

There are no conflicts to declare for financial interests or personal relationships.

Acknowledgements

PD thanks to University of Allahabad, Prayagraj, India for infrastructural facility and Science & Engineering Board (SERB), New Delhi, India for financial support through the fast track grant (SB/FT/CS-190/2011). He also thanks to Mr Shishir Singh, IIT Kanpur and Professor S. K. Pandey, Department of Chemistry, BHU to provide unsubscribed contents used in this article.

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Footnote

† Electronic supplementary information (ESI) available. See DOI: https://doi.org/10.1039/d3ra06976a

This journal is © The Royal Society of Chemistry 2023