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Table of Contents

    Topic review

    Antimicrobial Activity of Curcumin

    Subjects: Microbiology
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    Definition

    Curcumin (CUR) is a natural substance extracted from turmeric that has antimicrobial properties. Due to its ability to absorb light in the blue spectrum, CUR is also used as a photosensitizer (PS) in antimicrobial Photodynamic Therapy (aPDT). 

    1. Introduction

    The global changes arising from globalization and climate change have a profound impact on human health, including infectious diseases [1][2]. The increased mobility of people, urbanization, greenhouse-gas emissions, pollution, deforestation, global warming, loss of sea ice, sea-level rise, extreme weather events with droughts and flood, etc., have all contributed to affect the transmission, prevalence, and spread of existing infections, such as vector-borne diseases, and the emergence of new pathogens [1][2] . In some cases, these infections have resulted in epidemics such as dengue and pandemics such as COVID-19, which the world is currently facing [3].
    Notwithstanding the existence of anti-infective medications, other current concerns are the drug resistance arising from the misuse of antimicrobial agents and the emergence of multidrug-resistant species [4]. These problems are a challenge for humanity, especially when considering that the development of new drugs demands time and money. Thus, the repurposing of existing medications and alternative therapies, such as natural substances, has been investigated [5][6][7].
    Curcumin (CUR) is a yellow dye (diferuloylmethane—a natural polyphenol) found in turmeric (Curcuma longa), which is a plant native to India and Southeast Asia. Beyond its culinary use as food flavoring and coloring, CUR also has a potential application in medicine due to its therapeutic properties, which include antioxidant, anticancer, anti-inflammatory, and antimicrobial effects [8]. CUR is not toxic and, according to the Food and Drug Administration, it is “Generally Recognized as Safe” [9]. The literature shows a plethora of studies reporting the biological and pharmacological features of CUR on health. Comprehensive reviews are available on the anticancer [10], anti-inflammatory [8], and antimicrobial [11] effects of CUR.
    Nonetheless, CUR is not soluble in water, unstable in solutions, and shows low bioavailability, poor absorption, and rapid elimination from the body [11]. For these reasons, organic solvents such as ethanol, methanol, acetone, and dimethyl sulfoxide (DMSO) have been used to solubilize CUR [12]. These drawbacks hinder the in vivo use of CUR as a therapeutic agent. Thus, some approaches have been used to overcome the problems of CUR, such as the use of adjuvants and drug delivery systems. Piperine, a substance derived from black pepper, and lecithin, a phospholipid, have been associated with CUR to improve its bioavailability by blocking the metabolism of CUR and enhancing its gastrointestinal absorption [11]. Additionally, drug delivery systems have been used to solubilize CUR and protect it from degradation until it reaches the target tissue, where CUR is sustainably released [13].
    Nanotechnology has been a promising field in medicine (nanomedicine). Nanoscale structures show intrinsic physical and chemical properties, which have been exploited as diagnostic and therapeutic tools [13][14]. The present study reviews the drug delivery systems (DDS) used for CUR, aiming at its antimicrobial effect. Although comprehensive reviews about the antimicrobial effect of CUR (encapsulated or not) are found elsewhere [15][16][17][18], they describe only the antibacterial and antifungal activities of CUR in DDSs . Our review summarizes the DDSs used for CUR as an antiviral, antibacterial, and antifungal agent, encompassing different nanosystems (colloids and metals) and the relevant issues of antimicrobial resistance and the emergence of new pathogens.

    2. Free CUR

    The broad-spectrum activity of CUR as an antibacterial, antifungal, and antivirus agent was reviewed previously [15][16]. Thus, this section reviews recent studies not covered by these reviews about the antimicrobial activity of free (non-encapsulated) CUR (Table 1) before reporting the DDS used for CUR.
    Table 1. In vitro and in vivo studies using free CUR and curcuminoids as antimicrobial.
    Solvent Microorganism Culture Antimicrobial Method CUR
    Concentration
    Light/Ultrasonic Parameters Reference
    DMSO (0.4%) ZIKV Cell infection IC50 5.62–16.57 µM - [19]
    >DGEV >IC90
    N/R HPVA Cell infection Viral survival 0.015 mg/mL - [20]
    Tulane V
    N/R KSPV Infected cells EC50 Up to 6.68 µM - [21]
    Aqueous Piper nigrum seed extract SARS-CoV-2 Cell infection IC50 Plaque reduction 0.4 µg/mL - [22]
    DMSO (<0.4%) SARS-CoV-1 Cell infection Inhibiton of viral replication 20 µM - [23]
    N/R SARS-CoV In vitro Viral inhibition 23.5 µM - [24]
    N/R SARS-CoV In vitro papain-like inhibition 5.7 µM - [25]
    DMSO (1 w/v) S. aureus Planktonic Inhibition zone MIC 600 and - [26]
    E. coli 400 µg/mL
    DMSO MRSA Planktonic MIC
    FICI
    15.5 µg/mL - [27]
    N/R S. aureus Planktonic Colony count 100 µg/mL 8 or 20 J/cm2 [28]
    MSSA
    MRSA
    DMSO (10%) S. aureus Biofilm aPDT 20, 40, and 80 µM 5.28 J/cm2 [29]
    DMSO VRSA Biofilm/animal infection model MIC
    MBC
    156.25 µg/mL 20 J/cm2 [30]
    N/R S. aureus Animal infection model aPDT 78 µg/mL 60 J/cm2 [31]
    DMSO S. aureus Infected fruit Survival fraction 100 nM 1.5 and 9 J/cm2 [32]
    N/R S. aureus Planktonic PDI 40 and 80 µM 15 J/cm2 [33]
    E. coli
    Tween 80 (0.5%) S. aureus Planktonic CFU/mL 300 and 500 µM 0.03–0.05 W/cm2 [34]
    N/R S. aureus Biofilm Confocal microscope N/R 170 µmol m2 s1 [35]
    DMSO (0.5%) S. aureus Biofilm SDT
    aPDT
    SPDT
    80 µM 100 Hz
    15 and 70 J/cm2
    100 Hz, 15 and 70 J/cm2
    [36]
    DMSO E. coli Planktonic MIC
    Inhibition zone
    110, 220 and 330 µg/mL - [37]
    DMSO E. coli Planktonic OD600nm 8,16, 32, and 64 µg/mL - [38]
    N/R S. dysenteriae Planktonic MIC/MBC 256 and - [39]
    C. jejuni 512 µg/mL
    Edible alcohol E. coli Planktonic aPDT 5, 10, and 20 µM 3.6 J/cm2 [40]
    DMSO H. pylori Planktonic biofilm MIC
    MBC
    aPDT
    50 µg/mL 10 mW/cm2 [41]
    DMSO P. aeruginosa Biofilm aPDT
    CFU/mL
    N/R 5 and 10 J/cm2 [42]
    DMSO Imipenem-resistant
    A. baumannii
    Planktonic aPDT 25, 50, 100, and 200 µM 5.4 J/cm2 [43]
    DMSO (2%) P. aeruginosa, A. baumannii, K. pneumoniae, E. coli, E. faecalis Planktonic MIC/FICI 128-256 µg/mL - [44]
    N/R C. difficile, C. sticklandii, B. fragilis, P. bryantii Planktonic Viable cell number 10 µg/mL - [45]
    N/R B. subtillis, E. coli, S. carnosus, M. smegmatis Planktonic MIC/MBC Up to 25 µM - [46]
    N/R MRSA Planktonic/animal infection model MIC 4–16 μg/mL - [47]
    MSSA 2–8 μg/mL
    E. coli 8–32 μg/mL
    N/R E. faecalis, S. aureus, B. subtillis, P. aeruginosa, E. coli Planktonic MIC 156 μg/mL - [48]
    DMSO (0.5%) A. hydrophila, E. coli
    E. faecalis, K. pneumoniae, P. aeruginosa, S. aureus, C. albicans
    Planktonic MIC/MBC/
    FICI/aPDT
    37.5–150 µg/mL N/C [49]
    N/R E. faecalis Infection model CFU/mL 1 µg/mL - [50]
    Commercial solution E. faecalis Biofilm aPDT 1.5 g/mL 20.1 J/cm2 [51]
    Ethanol 99% A. hydrophila, V. parahaemolyticus Planktonic aPDT/SDT Up to 15 mg/L N/C [52]
    DMSO (10%) E. faecalis Biofilm MIC/MBC 120 mg/mL - [53]
    N/R S. mutans Planktonic aPDT 10 g/100cc N/C [54]
    DMSO: ethyl alcohol S. mutans, S. pyogenes Planktonic aPDT 3 mg/mL 28.8 J/cm2 [55]
    DMSO (0.8%) Caries isolated Biofilm aPDT 600 µg/mL 75 J/cm2 [56]
    DMSO S. mutans, C. albicans Biofilm single/dual MBEC 0.5 mM - [57]
    DMSO (0.05 M) A. actinomycetemcomitans Planktonic aPDT 40 µg/mL 300–420 J/cm2 [58]
    DMSO (<1%) P. gingivalis, A. actinomycetemcomitans Planktonic aPDT 20 µg/mL 6, 12 or 18 J/cm2 [59]
    DMSO (0.5%) P. gingivalis, A. actinomycetemcomitans, C. rectus, E. corrodens, F. nucleatum, P. intermedia, P. micra, T. denticola, T. forsythis Biofilm aPDT 100 mg/L - [60]
    N/R Subgingival plaque Biofilm aPDT 100 µg/mL 30 J/cm2 [61]
    DMSO P. gingivalis Planktonic MIC 12.5 µg/mL - [62]
    Ethanol: DMSO
    (99.9%: 0.1%)
    Periodontal pocket - aPDT 100 mg/mL 7.69 J/cm2 [63]
    Tween 80 Streptococcus spp, Staphylococcus spp, Enterobacteriaceae, C. albicans Clinical trail aPDT 0.75 mg/mL 20.1 J/cm2 [64]
    Sodium hydroxide: PBS C. albicans, C. parapsilosis, C. glabrata, C.dubliniensis Planktonic/biofilm MIC 0.1–0.5 mg/mL - [65]
    N/R C. albicans, S. aureus Planktonic
    Biofilm
    MIC/Biofilm percentag 200 µg/mL - [66]
    N/R C. albicans Biofilm aPDT 1.5 g/mL 20.1 J/cm2 [67]
    DMSO (10%) C. albicans Biofilm aPDT 20, 40, 60 and 80 µM 2.64, 5.28, 7.92, 10.56, and 13.2 J/cm2 [68]
    DMSO (1%) C. albicans Biofilm aPDT 40 and 80 mM 37.5 and 50 J/cm2 [69]
    N/R C. albicans Biofilm aPDT 100 µM 10 J/cm2 [70]
    DMSO (2.5%) Fluconazole-resistant C. albicans Planktonic/biofilm/infection model MIC/
    aPDT
    40 µM 5.28 J/cm2 [71]
    Fluconazole-susceptible C. albicans 80 µM 40.3 J/cm2
    DMSO C. albicans, F. oxysporum, A. flavus, A. niger, C. neoformans Planktonic MIC 137.5–200 μg/mL - [72]

    2.1. Antiviral Activity

    The antiviral activity of CUR has been described against enveloped and non-enveloped DNA and RNA viruses, such as HIV, Zika, chikungunya, dengue, influenza, hepatitis, respiratory syncytial viruses, herpesviruses, papillomavirus, arboviruses, and, noroviruses [11][73][74]. The action mechanism of CUR involves the inhibition of viral attachmentand penetration into the host cell and interference with viral replication machinery and the host cell signaling pathways used for viral replication. Moreover, CUR works as a virucidal substance, acting on the viral envelope or proteins [11][73][74]. CUR in 0.4%vol/vol DMSO was able to inhibit several strains of the Zika virus, including those causing human epidemics, inhibiting the viral attachment to the host cell [19]. The inhibitory effect was potentiated when CUR was combined with gossypol, which is another natural product. CUR also inhibited human strains of the dengue virus [19]. The combination of CUR with heat treatment reduced the time and temperature needed for inactivating the foodborne enteric virus (hepatitis A virus and Tulane virus—a cultivable surrogate of the human norovirus) [20]. CUR was able to inhibit the lytic replication of Kaposi’s sarcoma-associated herpesvirus (KSHV) as well as reduce its pathogenesis (neoangiogenesis and cell invasionof KSHV-infected mesenchymal stem cell from the periodontal ligament) [21].
    While the antiviral effect of CUR has been experimentally demonstrated, the effect of CUR against the new severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the etiologic agent of COVID-19, has been predicted by in silico studies using computational techniques, such as molecular docking [75][76][77][78][79][80][81][82]. These in silico studies showed the binding affinity of CUR to the spike protein of SARS-CoV-2 and the human receptors of the host cell, which could inhibit the viral infection into the human cells. The targets to which CUR may bind are the viral non-structural protein 9 (Nsp9) [77] and 15 (Nsp15) [81], main proteases of SARS-CoV-2 (important for viral replication) [75][80], receptor-binding domains (RBD) of the viral spike protein [76,78,82], human cell receptors angiotensin-converting enzyme2 (ACE2) [76][82], and glucose-regulating protein 78 (GRP78) [79], as well as the RBD/ACE complex [76]. Nevertheless, a virtual screening evaluated the interaction between potential functional foods and the main protease of SARS-CoV-2 and found that CUR showed lower docking affinity than flavonoids, vitamin, and β-sitosterol [83]. Omics approaches have been studied to identify infection pathways and propose drugs that could target these pathways. Thus, an integrative multiomics (interactome, proteome, transcriptome, andbibliome) analysis identified biological processes and SARS-CoV-2 infection pathways and proposed CUR as a potential prophylactic agent for blocking the SARS-CoV-2 infection [84].Although most investigations have evaluated the potential of CUR against SARS-CoV-2 by computational simulations, an in vitro study showed that an immunomodulatory herbal extract composed of CUR and piperine presented a virucidal effect (viral inhibitionof up to 92%) on SARS-CoV-2 [22]. Other in vitro studies showed the ability of CUR to inhibit its viral predecessor—the SARS-CoV-1 [23][24]. CUR in DMSO (<0.4%) inhibited by 25–50% the cytopathogenic effect of SARS-CoV-1 on Vero E6 cells and by 50% the viral replication and 3CL protease (main protease) [23]. Another study used CUR as a positive control for 3CL protease inhibition [24]. CUR also inhibited the papain-like protease, which is another protease used for SARS-CoV replication [25].

    2.2. Antibacterial Activity

    The antibacterial effect of CUR has been demonstrated against Gram-positive and Gram-negative species, including strains responsible for human infections and showing antibiotic resistance [11][16][85][86]. CUR also inhibits bacterial biofilms, which are communities of cells embedded in a self-produced polymeric matrix tolerant to antimicrobial treatments [11][16][85][86]. The antibacterial mechanism of action of CUR involves damage to the cell wall or cell membrane, interference on cellular processes by targeting DNA and proteins, and inhibition of bacterial quorum sensing (communication process mediated by biochemical signals that regulate cell density and microbial behavior) [85]. Moreover, CUR affected the L-tryptophan metabolism in Staphylococcus aureus (Gram-positive) but not in Escherichia coli (Gram-negative), produced lipid peroxidation, and increased DNA fragmentation in both bacteria [26]. These results, along with the increased levels of total thiol and antioxidant capacity observed after bacterial cells were treated with CUR, suggested that oxidative stress may be the mechanism of antibacterial action of CUR [26].Therefore, these multiple targets make CUR an interesting option for antibiotic-resistant strains. CUR is effective in killing methicillin-resistant S. aureus (MRSA), which is a concerning pathogen responsible for nosocomial and community-associated infections [86]. CUR and another polyphenol, quercetin, inhibited the growth of MRSA and their combinationwas synergistic [27]. Moreover, CUR absorbs blue light (400–500 nm) and is used as anatural photosensitizer (PS) in antimicrobial Photodynamic Therapy (aPDT) [87]. CUR-mediated aPDT reduced the viability of reference strain of S. aureus and clinical isolates of methicillin-sensitive S. aureus (MSSA) and MRSA by 4 log10, while CUR alone reduced their survival by 2 log10 [28]. The aPDT mediated by CUR in 10% DMSO reduced the biofilm viability of S. aureus and MRSA by 3 and 2 log10, respectively, and their metabolicactivity by 94% and 89%, respectively [29]. The antibiofilm activity of CUR-mediated aPDT was also observed against clinical isolates of vancomycin-resistant S. aureus (VRSA),with reductions of 3.05 log10 in biofilm viability, 67.73% in biofilm biomass, and 47.94% in biofilm matrix [30]. Additionally, aPDT resulted in the eradication of VRSA in a rat model of skin infection [30]. The association of CUR-mediated aPDT with artificial skin resulted in a 4.14 log10 reduction in S. aureus from infected wounds in rats [31].
    The combination of CUR and another natural PS, hypocrellin B, increased the photoinactivation of S. aureus compared with the photodynamic effect of each PS alone [32]. Bacterial cells showed alteration in their membrane integrity and the dual-PS-mediatedaPDT also decontaminated apples with S. aureus [32]. The CUR-mediated aPDT was also effective in decontaminating food, reducing the number of S. aureus recovered from meatand fruit [33]. Compared to another natural PS, aloe-emodin, CUR was less effective inphotokilling S. aureus and E. coli [34]. Three-dimensional _cages fabricated with CURand resin monomer (pentaerythritol triacrylate) polymerized by infrared light were usedto entrap and kill S. aureus. Irradiation of µcages for 10 min with visible light resulted in a bacteria mortality rate of 95% [35]. Following the principles of aPDT, SonodynamicTherapy (SDT) associates a PS (also called sonosensitizer) with ultrasound (US) instead of light for the treatment of deeper lesions and infections, where light cannot reach [88].Both aPDT and SDT mediated by CUR, as well as the combination of both (SPDT, when the PS is activated by light and US simultaneously), reduced the viability of S. aureus biofilmS. SPDT promoted the highest reduction (3.48 log10), which was potentiated when CUR was combined with sodium dodecyl sulfate (7.43 log10) [36]. Regarding Gram-negative species, CUR alone was not able to inhibit the growth of an Enterotoxigenic E. coli, which is a strain that causes severe diarrhea and is resistant to antibiotics [37]. However, synergism was observed between CUR at 330 µg/mL and antibiotics (Ceftazidime, Amoxicillin/Clavulanic acid, Cefotaxime, and Ampicillin) [37]. CUR did not affect the growth of enteroaggregative (EAEC) and enteropathogenic (EPEC) diarrheagenic E. coli but inhibited the secretion and release of their virulence factors, Pet,and EspC, which are toxins produced by these strains [38]. Conversely, CUR alone and with ampicillin inhibited the growth of other species that caused diarrhea—Shigella dysenteriae and Campylobacter jejuni, including multidrug-resistant strains [39]. The aPDT mediated byCUR and light reduced the viability of E. coli by 3.5 log, increased membrane permeabilityof bacteria, and decontaminated oysters [40]. CUR-mediated aPDT reduced the viability of Helicobacter pylori and its virulence factors (motility, urease production, adhesion toerythrocytes, and biofilm formation) [41]. On Pseudomonas aeruginosa, aPDT potentiated the inhibitory effect of CUR, inhibited biofilm formation and matrix production, reduced biofilm thickness, and downregulated quorum sensing genes [42]. The photoinactivation of imipenem-resistant Acinetobacter baumannii reduced bacterial viability by 97.5% and shotgun proteomics analysis identified 70 carbonylated proteins modified after CUR mediated aPDT related to the membrane, translation, and response to oxidative stress [43].CUR inhibited the growth of antibiotic-resistant P. aeruginosa, A. baumannii, and Klebsiella pneumoniae isolated from burn wound infections and showed synergism with meropenem [44]. On gastrointestinal bacteria of human and bovine origin, CUR inhibited Firmicutes (Clostridioides difficile and Acetoanaerobium (Clostridium) sticklandii) but did not affect Bacteroidetes (Bacteroides fragilis and Prevotella bryantii) [45]. CUR was conjugated to triphenyl phosphonium resulting in a compound named Mitocurcumin, which inhibited the growth of Bacillus subtilis, E. coli, Staphylococcus carnosus, and Mycobacterium smegmatis, and induced morphological changes in B. subtilis [46]. Seventeen synthesized monocarbonyl curcuminoids showed high antibacterial activity against MSSA and MRSA and moderate activity against E. coli [47]. The four most effective curcuminoids were bacteriostatic at low concentrations and bactericidal at high concentrations against MRSA, which showed membrane damage. In an ex vivo mammalian co-culture infection model,two curcuminoids decreased the viability of MSSA internalized in the fibroblasts [47]. One of thirteen synthesized curcuminoids, 3,30-dihydroxycurcumin, showed antibacterial activity against S. aureus, B. subtilis, Enterococcus faecalis, and Mycobacterium tuberculosis, and produced membrane damage on B. subtilis [48]. Nonetheless, all the synthesized curcuminoids were not effective against Gram-negative species (P. aeruginosa and E. coli) [48]. CUR analogs (monocurcuminoids, MC) were synthesized and showed higher, lower, or similar antimicrobial activity than CUR against Aeromonas hydrophila, E. coli, E. faecalis, K. pneumoniae, P. aeruginosa, S. aureus, and the yeast Candida albicans [49]. Two MC and turmeric powder presented synergism against A. hydrophila, P. aeruginosa, and C. albicans. When aPDT was performed with UV light, two MC-mediated aPDT decreased the growth of E. faecalis, E. coli, and S. aureus, while aPDT with another MC and CUR increased the growth of A. hydrophila, E. faecalis, S. aureus, C. albicans, and P. aeruginosa [49]. CUR was more effective than other natural biomolecules (quercetin and resveratrol) in inhibiting thegrowth of E. faecalis in spermatozoa from rabbits, but less effective than antibiotics [50]. CUR-mediated aPDT also reduced the viability of E. faecalis biofilms grown in bovine bone cavities for 14 days by 1.92 log10 [51]. The aPDT and the combination of a nanobubble solution and the US reduced the viability of the aquatic pathogens Aeromonas hydrophila and Vibrio parahaemolyticus [52].
    CUR and aPDT have been used for dental infections and oral diseases. The Curcuma longa extract decreased the viability of 3-week-old E. faecalis biofilms formed on the root canal surface of human teeth [53]. The aPDT mediated by CUR and continuous laser irradiationeradicated planktonic cultures of Streptococcus mutans, which is the main etiologic factor of dental caries [54]. A formulation of syrup with curcuminoids and 30% sucrose wasused as a PS in aPDT, which reduced the viability of S. mutans, Streptococcus pyogenes, and aclinical isolate from a patient with pharyngotonsillitis [55]. Microbial samples from carious dentin were grown as microcosm biofilm and submitted to CUR-mediated aPDT, which reduced the vitality of 3-  and 5-day-old biofilms [56]. CUR alone decreased the biomass and the viability of mono- and dual-species biofilms of S. mutans and C. albicans, as well as the production of biofilm matrix and the expression of genes related to glucosyltransferaseand quorum sensing of S. mutans, and the adherence of C. albicans [57].The therapeutic effect of CUR on periodontal diseases was extensively investigated in animal models and clinical trials, which were reviewed [89]. Beyond its antibacterial activity, CUR-mediated aPDT also produced a bystander effect (behavior change of cellsexposed to treated target cells) on the periodontal pathogen Aggregatibacter actinomycetemcomitans, reducing its survival, metabolic activity, and the production of quorum sensing molecule [58]. The aPDT with CUR decreased the growth of both A. actinomycetemcomitans and Porphyromonas gingivalis, which is another pathogenic periodontal bacterium [59].Antimicrobial photothermal treatment promoted higher reduction than CUR-mediated aPDT in the viability of mixed biofilms of periodontal pathogens (P. gingivalis, A. actinomycetemcomitans, Campylobacter rectus, Eikenella corrodens, Fusobacterium nucleatum, Prevotella intermedia, Parvimonas micra, Treponema denticola, and Tannerella forsythia) grown on a titanium surface inside artificial periodontal pockets [60]. The aPDT mediated by different PS (methylene blue, CUR, and chlorin e6) eradicated the planktonic growth and reducedthe biofilm viability of metronidazole-resistant bacteria from the subgingival plaque [61].CUR alone inhibited the growth of P. gingivalis and CUR in gel was biocompatible when evaluated subcutaneously in rats [62].
    A randomized clinical trial showed that CUR-mediated aPDT associated with scaling and root planing improved the clinical attachment level gain of periodontal pockets in type-2 diabetic patients after three and six months [63]. The aPDT with CUR and LED applied in the mouth of 30 patients with acquired immune deficiency syndrome (AIDS) reduced the counts of Streptococcus spp., Staphylococcus spp., and total microorganismsfrom saliva, but not the number of Enterobacteriaceae and Candida spp. [64]. Additionally,there was no reduction in patients with CD8 lymphocytes lower than 25% [64].

    2.3. Antifungal Activity

    The antifungal activity of CUR has been demonstrated mostly against Candida spp. by many in vitro and few in vivo studies [90]. CUR inhibited the growth of a reference strainand a clinical isolate of C. albicans, as well as reference strains of Candida parapsilosis, Candida glabrata, and Candida dubliniensis [65]. When biofilms of both C. albicans strains were evaluated, CUR reduced only the viability of the standard strain in a concentration-dependent effect, while the antifungal fluconazole did not inhibit the viability of either strain [65]. CUR and 2-aminobenzimidazole (2-ABI) inhibited the growth and adhesion of C. albicans and S. aureus to medical-grade silicone [66]. The combination of CUR and 2-ABI enhanced the inhibition of biofilm formation and reduced the viability of 48 h-old single and dual-species biofilms [66]. The aPDT mediated by CUR reduced the survival of 14-day-old biofilm of C. albicans in bone cavities, confirmed by fluorescence spectroscopy [67]. CUR-mediated aPDT reduced the metabolic activity of biofilms of C. albicans reference strain and clinical isolates from the oral cavity of patients with HIV and lichen planus [68]. Moreover, genes related to hyphae and biofilm formation were downregulated [68]. The aPDT mediatedby CUR and another PS, Photodithazine®, also resulted in the downregulation of genes involved in adhesion and oxidative stress response in C. albicans biofilms [69]. CUR alone and CUR-mediated aPDT, combined or not with an antibody-derived killer decapeptide,reduced the metabolic activity of an 18 h biofilm of C. albicans [70]. CUR showed synergism with fluconazole and CUR-mediated aPDT inhibited the planktonic growth and reduced the biofilm viability of fluconazole-resistant C. albicans [71]. CUR-mediated aPDT also increased the survival of Galleria mellonella infected with fluconazole-susceptible C. albicans, but did not affect the survival of larvae infected with fluconazole-resistant strain [71]. A library of 2-chloroquinoline incorporated monocarbonyl curcuminoids (MACs) was synthetized and most of the MACs exhibited strong or moderate antifungal activity compared with miconazole against C. albicans, Fusarium oxysporum, Aspergillus flavus, Aspergillus niger, and Cryptococcus neoformans [72]. To suggest a possible antifungal mechanism, a moleculardocking analysis showed that MACs had binding affinity to sterol 14α-demethylase(CYP51), leading to impaired fungal growth [72].

    3. Curcumin in DDSs (Colloidal, Metal, and Hybrid Nanosystems)

    3.1. CUR in Micelles

    Micelles are aggregates of surfactants or block polymers self-assembled in water solution. They are used as DDSs and formed by a hydrophilic domain named corona and a hydrophobic domain called core (Figure 1) [91], which stays in contact with hydrophobic drugs such as CUR [91]. Micelles have low toxicity, biocompatibility, and sustained release, which makes them an attractive DDS to carry CUR and to be used in medical applications [91]. Antimicrobial studies with CUR-loaded micelles are summarized in Table 2.
    Figure 1. Schematic representation of: (A) an amphiphilic molecule and (B) an assembled micelle.
    Table 2. Antimicrobial studies performed with CUR in micelles.
    Type of Micelles [CUR] Formulation Microorganism Type of
    Culture
    Antimicrobial Method Antimicrobial [CUR] Light/Ultrasonic Parameters Reference
    Mixed polymer micelles 1000 ppm E. coli, S. aureus, A. niger Planktonic MIC 350 and 275 µg/mL - [92]
    PCL-b-PAsp and Ag 2 mg/mL P. aeruginosa, S. aureus Planktonic OD600nm 8–500 µg/mL - [93]
    mPEG-OA 1:10 P. aeruginosa Planktonic MIC 400 µg/mL - [94]
    PEG-PCL 10 mg C. albicans Planktonic MIC 256 µg/mL - [95]
    PEG-PE 50 mM S. mutans Planktonic SACT 50 mM 1.56 W/cm2 [96]
    DAPMA, SPD, SPM 0.32 mg/mL P. aeruginosa Planktonic OD600nm and aPDT 250, 500 nM, 1 µM and 50, 100 nM 18 and 30 J/cm2 [97]
    P123 0.5% w/V S. aureus Planktonic aPDT 7.80 μmol/L 6.5 J/cm2 [98]
    PCL-b-PHMG-b-PCL, STES 10 mg S. aureus,E. coli Planktonic MIC 16 and 32 μg/mL * - [99]
    CUR-PLGA-DEX 1 mg/mL P. fluorescens, P. putida Planktonic biofilm OD600nm antibiofilm 0.625–5 mg/mL - [100]

    3.2. CUR in Liposomes

    Liposomes are biodegradable and biocompatible systems, which consist of hydrophobic and hydrophilic groups (Figure 2) [101]. The hydrophobic layer is mainly composed of phospholipids and cholesterol molecules. This lipid-based carrier is suitable for administering water-insoluble drugs, such as CUR [102]. Liposomes are classified into three groups: single unilamellar vesicles, large unilamellar vesicles, and multilamellar vesicles [103]. Drugs encapsulated in liposomes are protected from chemical degradation and show increased drug solubility [101]. Additionally, liposomes have advantageous properties such as better penetration into the skin, deposition, anti-melanoma, and antimicrobial activity [102]. Antimicrobial studies with CUR-loaded liposomes are summarized in Table 3.

    Figure 2. Schematic representation of the liposome structure.

    Table 3. Antimicrobial studies performed with CUR in liposomes and solid lipid nanoparticles (SLN).

    Type of Liposomes or SLN [CUR] Formulation Microorganism Type of Culture Antimicrobial Method Antimicrobial [CUR] Reference
    Lecithin and cholesterol 0.5 mg/mL A. sobria, C. violaceum, A. tumefaciens Planktonic biofilm MIC, antibiofilm 420, 400, and 460 μg/mL       [104]
    PCNL 60.65 ± 1.68 µg/µl B. subtilis, K. pneumoniae, C. violaceum, E. coli, M. smegmatis, A. niger, C. albicans, F. oxysporum Planktonic Disk diffusion assay N/R [105]
    Phosphocolines 100:1 M S. aureus Planktonic MIC 7 μg/mL [106]
    PLGA: triglycerides: F68 0.8 mg/mL E. coli, S. typhimurium, P. aeruginosa, S. aureus, B. sonorensis, B. licheniformis Planktonic MIC 75 and 100 μg/mL [107]
    Soya lecithin and menthol 0.5 mg/mL MRSA Planktonic, Biolfim MIC, microscopy, biomass 10 and 125 µg/mL [108]
    CurSLN 60 mg/500 mg lipid S. aureus, S. mutans, V. streptococci, L. acidophilus, E. coli, C. albicans Planktonic MIC, MBC 0.09375–3 and 1.5–6 mg/mL [109]

    [CUR]: CUR concentration. N/R: not reported.

    3.3. CUR in Solid Lipid Nanoparticles

    Solid lipid nanoparticles (SLN, Figure 3, Table 3) are a modern type of lipid-based carrier composed by solid biodegradable lipids and spherical solid lipid particles. SLNs are water colloidal or aqueous surfactant solution systems [102]. SLNs have advantages such as biocompatibility, biodegradability, greater drug absorption, and drug retention [18][102], thus they are an interesting system to carry CUR [14]. Currently, SLNs have become popular because they are used as carriers for COVID-19 vaccines based on RNA vaccine technology (Moderna and Pfizer–BioNTech).

    Figure 3. Schematic representation of solid lipid nanoparticle.

    3.4. CUR in Nanoemulsions

    Nanoemulsions (NE) are thermodynamically stable dispersions of oil and water (Figure 4) [110]. They are formed by a phospholipid monolayer composed of a surfactant and co-surfactant, which are important for nanoemulsion stabilization [110][111]. This system has thermodynamic stability and high solubilization characteristics, with improved drug release kinetics [112]. NE systems can be manufactured through emulsification, which can control the size of the drops and increase the drug solubility and efficacy. Moreover, the main disadvantage of NE is the high amount of surfactants in the formulation, which can lead to a potential toxic effect [111]. Antimicrobials studies with CUR-loaded NE are summarized in Table 4.

    Figure 4. Schematic diagram of oil-in-water nanoemulsion (A) and water-in-oil nanoemulsion (B), stabilized by surfactants.

    Table 4. Antimicrobial studies performed with curcumin/curcuminoid in emulsions.

    Type of

    Emulsion

    [CUR] Formulation Microorganisms  Type of culture Antimicrobial method  Antimicrobial Concentration  Light/Ultrasonic Paramet Reference 
    THC ME 5% HIV-1 Cell infection  IC50 0.9357 μM - [113]
    CUR-NE N/R HPV - aPDT 80 µM 50 J/cm2 [114]
    CUR-NE N/R DENV-1 to 4 Cell infection  Cell viability 1, 5, 10 µg/mL - [115]
    P60-CUR 4 mg/L E. coli Planktonic  OD595 nm N/R - [116]
    PE:CUR 0.566 mg/mL S. aureus, S. epidermidis, S. faecalis, C. albicans, E. coli Planktonic  Inhibition zone 1 mg/mL* - [117]
    cu-SEDDS 1% E. aureus, E. coli, P. aeruginosa, K. pneumonia  Planktonic  MIC 45–62 µg/mL - [118]
    CUR:NE in microbeads 0.5 mg/mL E. coli, S. typhmerium,Y. enterocolitica, P. aeruginosa, S, aureus, B. cereus, L. monocytogenes Planktonic  Inhibition zone 90 and 180 mg/mL* - [119]
    Lignin sulfomethylated 0.3 mg/mL S. aureus  Planktonic  OD600 nm 2.4 mg/mL* - [120]
    C14-EDA/GM/WC14-MEDA/GM/W N/R C. albicans  Planktonic, biofilm  Microdilution assay, antibiofilm 100 µg/mL, 20 µg - [121]

    [CUR]: CUR concentration. -: not performed. N/R: not reported. *: formulation concentration.

    3.5. CUR in Cyclodextrin

    Cyclodextrins (CDs) have revolutionized the pharmaceutical industry in recent years [122]. CDs consist of three naturally occurring oligosaccharides in a cyclic structure produced from starch [123][124][125]. The natural CDs have their nomenclature system and their chemical structure based on the number of glucose residues in their structure: 6, 7, or 8 glucose units, which are denominated α-CD, β-CD, and γ-CD, respectively [126][127]. Although the entire CD molecule is soluble in water, the interior is relatively non-polar and creates a hydrophobic microenvironment. Therefore, CDs are cup-shaped, hollow structures with an outer hydrophilic layer and an internal hydrophobic cavity (Figure 5) [126]. They can sequester insoluble compounds within their hydrophobic cavity, resulting in better solubility and consequently better chemical and enzymatic stability [124]. Due to the cavity size, β-CD forms appropriate inclusion complexes with molecules with aromatic rings [128], such as CUR [129]. Antimicrobial studies with CUR in CDs are summarized in Table 5.

    Figure 5. Schematic representation of CUR in CD.

    Table 5. Antimicrobial studies performed with CUR in CDs.

    Type of CD [CUR] Formulation Microorganism Type of Culture Antimicrobial Method Antimicrobial [CUR] Light/Ultrasonic Parameters Reference
    PEG-based β-CD or γ-CD 10 µM E. coli, E. faecalis Planktonic aPDT 10 µM 4.8, 29 J/cm2 [130]
    HPMC-stabilized hydroxypro pyl-β-CD 7.64 × 10−3 M E. coli Planktonic aPDT 10, 25 µM 5, 14, 28 J/cm2 [131]
    methyl-β-CD hyaluronic acid HPMC 7.64 × 10−3 M E. faecalis, E. coli Planktonic aPDT 0.5–25 µM 11, 16, 32 J/cm2 [132]
    carboxymethyl-β-CD 20 µM E. coli Planktonic aPDT 0.7 ± 0.1 to 4.1 ± 1.6  nmole cm−2 1050 ± 250 lx [133]
    hydrogel with CUR in hydroxypropyl-β-CD 15.8 mg/mL S. aureus Planktonic Inhibition zone 2% (w/v) - [134]
    α- and β-CD 1 mol/L E. coli, S. aureus Planktonic MIC, OD600 nm 0.25 and 0.31 mg/mL - [135]
    β-CD or γ-CD in CS 0.06 mM E. coli, S. aureus Planktonic MIC, Zone of inhibition 64 and 32 µg/mL - [136]
    γ-CD 25 mg/L T. rubrum Planktonic MIC, aPDT N/R 45 J/cm2 [137]
    hydroxypropyl-β-CD 1:1 B. subtillis, S. aureus, S. pyrogenes, P. aeruginosa, C. difficile, C. butyricum, L. monocytogenes, E. faecalis, E. coli, K. pneumoniae, P. mirabilis, S. typhimurium, E. aerogens, C. kusei, C. albicans Planktonic Inhibition zone 25 mg/mL - [138]
    methyl-β-CD 20 mM E. coli Planktonic MIC, MBC, aPDT 500, 90 µM 9 J/cm2 [139]

    [CUR]: CUR concentration. -: not performed. N/R: not reported.

    3.6. CUR in Chitosan

    Chitin is a natural polysaccharide commonly found in the exoskeleton of marine crustaceans such as shrimps, prawns, lobsters, and crabs. Chitosan (CS) derives from the acetylation of chitin and has a linear structure of D-glucosamine (deacetylated monomer) linked to N-acetyl-D-glucosamine (acetylated monomer) through β-1,4 bonds [140]. The main advantages that make CS a promising drug carrier include biocompatibility, biodegradability, non-toxicity, controlled release system, mucoadhesive properties, and low cost [140][141]. Moreover, CS is soluble in aqueous solutions and is the only pseudo-natural polymer with a positive charge (cationic) [142], which can interact with negatively-charged DNA, membranes of microbial cells, and biofilm matrix [143]. Antimicrobial studies with CUR in CS are summarized in Table 6.

    Table 6. Antimicrobial studies performed with CUR in CS.

    Type ofCS [CUR] Formulation Microorganism Type of Culture Antimicrobial Method Antimicrobial [CUR] Reference
    PEG-CS 4.4%, 5 mg/mL MRSA, P. aeruginosa Planktonic, Animal model OD600nm, CFU 5 and 10 mg/mL * [144]
    CCS microspheres 12.27 mg/mL, 1 mol S. aureus, E. coli Planktonic Zone of inhibition, MIC N/R [145]
    CS nanoparticles 1.06 mg/mL S. mutans Planktonic, Biofilm MIC 0.114 mg/mL [146]
    CS-CMS-MMT 0.0004–0.004 g S. mutans Planktonic, Biofilm MIC 0.101 mg/mL [147]
    CS-GP-CUR 148.09 ± 5.01 µg S. aureus Planktonic Zone of inhibition, tissue bacteria count N/C [148]
    PVA-CS-CUR N/C E. coli, P. aeruginosa, S. aureus, B. subtilis Planktonic Zone of inhibition N/R [149]
    PVA-CS-CUR 10, 20, 30 mg P. multocida, S. aureus, E. coli, B. subtilis Planktonic Zone of inhibition 10, 20, 30 mg [150]
    CS NPs 2, 4, 8, 16% C. albicans, S. aureus Planktonic, Biofilm MIC, Colony count 400 mg/mL [151]
    CS NPs 4 mg/mL HCV-4 N/R Antiviral assay 15 µg/mL [152]
    CS/milk protein nanocomposites 100 mg PVY Plant infection Antiviral activity 500, 1000, 1500 mg/100 mL [153]
    [CUR]: CUR concentration. N/R: not reported. N/C: not clear. *: formulation concentration.

    3.7. CUR in Other Polymeric DDS

    Antimicrobial studies with CUR loaded in other polymeric DDSs are summarized in Table 7.

    Table 7. Antimicrobial studies performed with curcumin in polymeric drug delivery systems.

    Type of Polymeric DDS [CUR] Formulation Microorganism Type of Culture Antimicrobial Method Antimicrobial [CUR] Light/Ultrasonic Parameters Reference
    PEG 400γ-CD and PEG + β-CD 0.18% E. faecalis, E. coli Planktonic CFU/mL aPDT N/R 9.7 J/cm2 29 J/cm2 [154]
    CUR-NP without polymer 100 mg S. aureus, B. subtillis, E. coli, P. aeruginosa, P. notatum, A. niger Planktonic MIC Inhibition zone 100 mg, 0.27 mmol - [155]
    CUR-NP without polymer 100 mg M. lutues, S. aureus, E. coli, P. aeruginosa Planktonic MBC N/R - [156]
    Mixed polymer NP 5 mM E. coli Planktonic MIC 400–500 μM - [157]
    CTABTween 20Sodium dodecylsulfate 100 mg/mL L. monicytogenes Planktonic Inhibition zone N/R - [158]
    PLA/dextran sulfate 4 mg/mL MRSA, C. albicans, S. mutans Planktonic/mono- and –mixed biofilm aPDT 260 μM 43.2 J/cm2 [159]
    PLA/dextran sulfate 0.4% C. albicans Animal model aPDT 260 μM 37.5 J/cm2 [160]
    Nanocurcumin N/R P. aeruginosa (isolates) and standard strain Planktonic MIC 128 µg/mL - [161]
    PLGA 5 mg S. saprophyticus subsp. Bovis, E. coli Planktonic aPDT 50 µg/mL 13.2 J/cm2 [162]
    Eudragit L-100 N/C L. monocytogenes Planktonic Animal model infection N/R - [163]
    nCUR N/R S. mutans PlanktonicBiofilm Inhibition zoneaPDT N/R 300–420 J/cm2 [164]
    nCUR combined with indocyanine 100 mg E. faecalis Biofilm Metabolic activity N/R 500 mW/cm2 [165]
    PVAc-CUR-PET-PVDC 0.02 g S. aureus, S. tiphimurium Planktonic aPDT N/R 24, 48, and 72 J/cm2 [166]
    MOA.CUR-PLGA-NP Up to 10% S. mutans Biofilm aPDT 7% wt 45 J/cm2 [167]
    CS- β-CD N/C S. aureus, E. coli Planktonic Colony count Up to 0.03% - [168]
    [CUR]: CUR concentration. -: not performed. N/R: not reported. N/C: not clear.

    3.8. CUR with Metallic Nanoparticles

    Metal complexation plays an important role in the therapeutic properties of CUR. The β-diketone moiety in the CUR chemical structure enables it to form complexes with metal ions [169]. A previous review summarized the antimicrobial activity of CUR and curcuminoid complexes with metals, such as boron, Ca2+, Cd2+, Cr3+, Co2+, Cu2+, Fe3+, Ga3+, Hg2+, In3+, Mn2+, Ni2+, Pd2+, Sn2+, Y3+, and Zn2+ against viruses, bacteria, and fungi [169]. Metals have also been combined with polymers to improve the biological effects of CUR and to be used as films, hydrogels, dressings, and other pharmaceutical formulations [170][171]. In this context, silver NPs (AgNPs) have been extensively used due to their antimicrobial activity (Figure 6) [172]. Antimicrobial studies with CUR complexes with metals are summarized in Table 8.

    Figure 6. Schematic representation of CUR in silver nanoparticles.

    Table 8. Antimicrobial studies performed with CUR complexes with metallic NPs.

    Type of Metallic Material [CUR] Formulation Microorganism Type of Culture Antimicrobial Method Antimicrobial [CUR] Reference
    CUR-AgNPs 20 mg/mL P. aeruginosa, E. coli, B. subtilis, S. aureus Planktonic MIC 20 mg/mL [173]
    Ag-CUR-nanoconjugates 0.1 mM E. coli, Salmonella spp., Fusarium spp., S. aureus Planktonic Zone of Inhibition 0.1 mM [174]
    AgCURNPs 500 mg P. aeruginosaS. aureus Biofilm CLSM SEM Up to 400 μg/mL [175]
    AgNPs 7 mg E. coli Planktonic Turbidimetric Assay 0.005 µM [176]
    cAgNPs 7 mg E. coliB. subtilis Planktonic MIC, CFU/mL 7 mg [177]
    Ru II complex 0.092 g E. coli, S. aureus, K. pneumoniae, A. baumannii, P. aeruginosa, Enterococcus sp. Plakntonic MIC/FICI >64 µg/mL [178]
    SCMC SNCF nanocomposites with CUR 0.25 mg/mL E. coli Planktonic Disc Method Count Method 2 mg/mL [179]
    CSCL CUR-AgNP 0.092 g E. coli, B. subtilis Planktonic Zone of Inhibition 10 and 20 μM [180]
    nSnH 10% S. aureus, E. coli. Planktonic CFU/mL N/R [181]
    Nanocomposite of CUR and ZnO NPs N/C S. epidermidis, S. hemolyticus, S. saprophyticus Planktonic Zone of Inhibition 1000, 750, 500, 250 μg/mL [182]
    Thermo-responsive hydrogels N/C S. aureusP. aeruginosaE. coli Planktonic MIC 400 μg/mL [183]
    CUR-AgNPs 5 mg/mL C. albicans, C. glabrata, C. tropicalis, C. parapsilosis, C. krusei, C. kefyr Planktonic Zone of Inhibition, MIC 32.2–250 μg/mL [184]
    Gel-CUR-Ag 20 mg P. aeruginosa, S. aureus Planktonic MIC, MBC 20 mg [185]
    HGZ-CUR N/C S. aureus, T. rubrum Planktonic Zone of Inhibition N/C [186]
    CHG-ZnO-CUR N/C S. aureus, T. rubrum Planktonic Zone of Inhibition N/C [187]
    Copper (II) oxide NPs 1 g E. faecalis, P. aeruginosa Planktonic Zone of Inhibition CFU/mL 1 mg/mL [188]
    OA-Ag-C 1 g P. aeruginosa, S. aureus Planktonic OD600nm 2.5 mg/mL [189]
    Ag-NP-β-CD-BC 0.79 g P. aeruginosa, S. aureus, C. auris Planktonic Zone of Inhibition N/R [190]
    Cotton fabrics coated ZnO-NP 2.71 × 10−3 M S. aureus, E. coli Planktonic Bacterial Count N/R [191]
    CS-ZnO-CUR 0.2 g S. aureus, E. coli Planktonic MIC, MBC Up to 50 μg/mL [192]
    CUR-TiO2 -CS 100–300 mg S. aureus, E. coli Planktonic Animal infection MIC 10 mg [193]
    CUR-Au-NPs 1 mg/mL E. coli, B. subtilis, S. aureus, P. aeruginosa Planktonic Zone of Inhibition 100, 200, 300 μg/mL [194]
    [CUR]: CUR concentration. N/R: not reported. N/C: not clear.

    3.9. CUR in Mesoporous Particles

    Porous materials are structures with ordered pores ranging from nanometer to micrometers, which are classified as microporous (less 2 nm), mesoporous (from 2 up to 50 nm), and macroporous (above 50 nm) [195]. Porous materials can be synthesized using carbon, silica, and metal oxides [196]. Mesoporous silica nanoparticles (MSN, Figure 7) are inorganic scaffolds [197], which seemed ideal carriers for hydrophobic drugs due to their well-defined structure, large specific surface area, and versatile chemistry for functionalization [198]. The pore size and volume and the surface area, as well as the surface functionalization of the mesoporous material, determine the drug load and release [199]. Moreover, mesoporous materials can be modified or functionalized to control drug release under environmental stimuli, such as pH, temperature, or light. These stimuli-responsive DDS, or smart DDS, prevent undesirable drug release before reaching the target tissue (“zero premature release”) [199]. Antimicrobial studies with CUR in porous DDSs are summarized in Table 9.

    Figure 7. Schematic representation of a porous particle.

    Table 9. Antimicrobial studies performed with CUR in porous DDSs.

    Porous DDS [CUR] Formulation Microorganism Type of Culture Antimicrobial Method Antimicrobial [CUR] Light/Ultrasonic Parameters Reference
    Cu-SNP/Ag 1.0 mmol E. coli Planktonic aPDT N/R 72 J/cm2 [200]
    Bionanocomposite silica/chitosan 100 mg E. coli, S. aureus Planktonic Zone of inhibition N/R - [201]
    NCIP 1 mg HIV-1 Transfected cells Immuno fluorescent staining 5–8 mg/mL - [202]
    Lollipop-like MSN 30 mg L−1 E. coli, S. aureus Planktonic OD600nm N/R - [203]
    SBA-15/PDA/Ag 2 mg E. coli, S. aureus Planktonic CFU/mL 50 mM - [204]
    [CUR]: CUR concentration. -: not performed. N/R: not reported.

    3.10. CUR in Quantum Dots

    Quantum dots (QDs) are semiconductor particles at nanosize (up to 10 nm) with electrical and photoluminescence properties of biotechnological and biomedical applications, such as bioimaging and DDS [205]. Carbon dots are divided into carbon QD and graphene QD and are produced by top-down and bottom-up methods using bulk carbon material and molecular precursors, respectively [205]. Antimicrobial studies with CUR in QDs are summarized in Table 10.

    Table 10. Antimicrobial studies performed with CUR in quantum dots (QDs).

    Type of
    Material
    [CUR]
    Formulation
    Microorganism Type of
    Culture
    Antimicrobial
    Method
    Antimicrobial
    [CUR]
    Light/Ultrasonic
    Parameters
    Reference
    CUR-cQDs 0.6 S. aureus
    MRSA
    E. faecalis
    E. coli
    K. pneumoniae
    P. aeruginosa
    Planktonic
    Biofilm
    Grown
    inhibition
    Biomass
    evaluation
    Confocal
    microscopy
    3.91–
    7.825 µg/mL
    - [206]
    CUR-cQDs 200 mg EV-71 Cell infection
    Animal
    infection
    MIC
    Plaque assay
    TC IC50 assay
    Western blot
    PCR
    5 µg/mL - [207]
    CUR-MQD 2:1 wt% K. pneumoniae
    P. aeruginosa
    S. aureus
    Planktonic MIC
    MBC
    Confocal
    microscopy
    Fluorescence
    microscopy
    Flow
    cytometry
    <0.00625–
    0.125 µg/mL
    - [208]
    CUR-GQDs N/C A. actinomycetemcomitans
    P. gingivalis
    P. intermedia
    Mixed biofilm aPDT 100 µg/mL 60–80 J/cm2 [209]

    3.11. CUR in Films, Hydrogels, and Other Nanomaterials

    Antimicrobial studies with CUR in films, hydrogels, and other nanomaterials are summarized in Table 11.

    Table 11. Antimicrobial studies performed with CUR in films, hydrogels, and other nanomaterials.

    Type of Material [CUR] Formulation Microorganism Type of Culture Antimicrobial Method Antimicrobial [CUR] Light/Ultrasonic Parameters Reference
    CuR-SiNPs 20 mg S. aureus, P. aeruginosa Planktonic, Biofilm aPDT 50 μg/mL, 1 mg/mL 20 J/cm2 [210]
    CUR-HNT-DX 10 mg S. marcescens, E. coli Planktonic, Infection model Grown inhibition, Confocal microscopy Up to 0.5 mg/mL - [211]
    Exosomes N/R HIV-1 infection - Flow cytometry N/R - [212]
    Electrospun nanofibers 100 mg/mL Actinomyces naeslundii Biofilm aPDT 2.5 and 5 mg/mL 1200 mW/cm2 [213]
    Ga NFCD-GO NF 0.1 mol B. cereus, E. coli Planktonic Zone of inhibition, MIC Up to 63.25 µg/mL - [214]
    Multinanofibers-film 1, 2.5, and 5 mg/mL S. aureusE. coli Planktonic UFC/mL, Confocal microscopy 1 mg/mL - [215]
    Nanofibers scaffolds 4.0 wt% S. aureus Pseudomonassp. Planktonic Colony count N/R ,- [216]
    Nanofibrous scaffold 5% S. aureus, E. coli Planktonic Colony count 20 mg - [217]
    Nanofibers 5 and 10%wt S. aureusE. coli Planktonic OD600nm Up to 212.5 µg/mL - [218]
    CSDG 1 w/w S. aureus, E. coli Planktonic, Infection model Colony count, Microscopy N/R - [219]
    Gelatin film 0, 0.25, 0.5, 1.0, and 1.5 wt% E. coli, L. monocytogenes Planktonic UFC/mL 0.25 and 1.5 wt% - [220]
    ZnO-CMC film 0.5 and 1.0 wt% E. coli, L. monocytogenes Planktonic UFC/mL 1 wt% - [221]
    Pectin film 40 mg E. coli, L. monocytogenes Planktonic UFC/mL N/R - [222]
    Edible film 0.4% (w/v) E. coli, B. subtilis Planktonic Zone of inhibition 1% wt. - [223]
    [CUR]: CUR concentration. -: not performed. N/R: not reported. N/C: not clear

    4. Conclusions and Future Perspectives

    CUR has a broad-spectrum antimicrobial activity against viruses, bacteria, and fungi, including resistant and emergent pathogens. However, some species such as Gram-negative bacteria are less susceptible to CUR and aPDT. For those, the combination of CUR with antibiotics has been suggested, especially for antibiotic-resistant strains [220]. CUR showed synergism with polymyxin and protection against the side effects of polymyxin treatment, nephrotoxicity, and neurotoxicity [224]. Nonetheless, the evaluation of synergism requires accurate methods to study drug interaction, considering potential differences between the dose–response relationship of individual drugs and avoiding over- or under-estimation of interactions. For example, while the time–kill curve of C. jejuni treated with both cinnamon oil and ZnO NPs resulted in the over-estimation of synergism between the antimicrobials, the fractional inhibitory concentration index (FICI) method showed no synergism but only an additive effect [225]. The FICI method was not able to detect the synergism between binary combinations of antimicrobials (cinnamon oil, ZnO NPs, and CUR encapsulated in starch) at sub-MIC, which resulted in the non-turbidity of C. jejuni. In turn, mathematical modeling using isobolograms and median-effect curves showed synergism when CUR in starch was combined with other antimicrobials against C. jejuni, with bacterial reductions of 3 log for the binary combination and over 8 log for the tertiary combination. The mathematical modeling suggested that CUR in starch was the main antimicrobial responsible for the synergistic interaction [225].

    In addition to the antimicrobial evaluation, in vitro and in vivo studies have demonstrated the cytocompatibility and biocompatibility of CUR in DDSs [108][113][114][115][118][121][144][145][152][156][168][185][192][202][209], suggesting that CUR-loaded DDSs might be safe. Although a plethora of DDSs has been developed to circumvent the hydrophobicity, instability in solution, and low bioavailability of CUR, several studies are still performed with free CUR dissolved in organic solvents [19][20][21][22][23][24][25][26][27][28][29][30][31][32][33][34][35][36][37][38][39][40][41][42][43][44][45][46][47][48][49][50][51][52][53][54][55][56][57][58][59][60][61][62][63][64][65][66][67][68][69][70][71][72][85][86][87][88][89][90]. Furthermore, compared to several in vitro investigations, few in vivo studies using animal infection models and scarce clinical trials have been reported. A randomized clinical trial showed that aPDT mediated by free CUR improved gingivitis in adolescents under fixed orthodontic treatment but did not reduce dental plaque accumulation after 1 month [226]. Clinical improvements after CUR-mediated aPDT were also observed for periodontal diseases, although few studies have evaluated the microbiological parameters [63][89]. Therefore, the improvement of clinical parameters might be due to the anti-inflammatory effect of CUR/aPDT instead of their in vivo antimicrobial activity. Nonetheless, randomized clinical trials evaluating CUR in DDSs against infections are required.

    As a note on the future use of CUR, the incorporation of CUR in DDS and other pharmaceutical formulations allows its clinical use especially as an adjuvant agent to conventional antimicrobial agents. Such a combination can be an important weapon in the battle against resistant strains and emergent pathogens. The use of stimuli-responsive (or smart) DDS can also improve CUR delivery and its therapeutic effect on the target tissue. The combination of polymeric and metallic carriers may also enhance the therapeutic activity of CUR. Nonetheless, the degradation of DDS and its clearance from the body are other issues that require further investigation [18]. The evidence produced so far about the antimicrobial activity of CUR in DDSs supports future in vivo and clinical studies, which may pave the way for industrial production.

    The entry is from 10.3390/ijms22137130

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