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Carotenoids and Periodontal Infection

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Carotenoids and Periodontal Infection nutrients Communication Carotenoids and Periodontal Infection Koji Naruishi Department of Periodontology and Endodontology, Tokushima University Graduate School of Biomedical Sciences, 3-18-15 Kuramoto, Tokushima 770-8504, Japan; [email protected]; Tel.: +81-88-633-7344; Fax: +81-88-633-7345 Received: 13 December 2019; Accepted: 16 January 2020; Published: 20 January 2020 Abstract: Periodontitis is a polymicrobial infectious disease that leads to inflammation of the gingiva, resulting in teeth loss by various causes such as inflammation-mediated bone resorption. Recently, many investigators have reported that the periodontitis resulting from persistent low-grade infection of Gram-negative bacteria such as Porphyromonas gingivalis (Pg) is associated with increased atherosclerosis, diabetes mellitus, and other systemic diseases through blood stream. On the other hand, carotenoids belong among phytochemicals that are responsible for different colors of the foods. It is important to examine whether carotenoids are effective to the inhibition of periodontal infection/inflammation cascades. This review summarizes the advanced state of knowledge about suppression of periodontal infection by several carotenoids. A series of findings suggest that carotenoids intake may provide novel strategy for periodontitis treatment, although further study will be needed. Keywords: carotenoids; periodontitis; low-grade infection 1. Introduction Periodontitis is a chronic inflammatory disease affecting the supporting tissues of teeth [1]. The disease is caused by infection of specific microorganisms such as Porphyromonas gingivalis (Pg), which causes progressive destruction of the alveolar bone. More than 500 individual species of microbes have been identified in the human mouth [2], and the infection with periodontal bacteria causes humoral immunological/inflammatory responses [3]. Furthermore, periodontal inflammation induced by the bacterial infection exacerbates alveolar bone resorption. Since bone homeostasis is regulated by a balance of osteoblastic bone formation and osteoclastic bone resorption, the functional imbalance between osteoblasts and osteoclasts leads to the progression of periodontitis [1]. Recently, many reports showed that persistent low-grade infection of Pg in periodontitis lesions is associated with increased atherosclerosis, diabetes mellitus, and other systemic diseases disseminated through the blood stream [4,5]. Therefore, control of periodontal infection is not only important for oral health, it may also contribute to improve overall health. Clinically, the infection control by the adjunctive use of systemic or local antibiotics provide additional benefits in the treatment of periodontitis. However, dentists must consider the increase of risk of complications associated with antibiotics abuse, particularly those related to antimicrobial resistance. The use of natural antioxidant substances on treatment of this high prevalence disease instead of antibiotics may be effective. Carotenoids belong among the phytochemicals that are responsible for different colors of foods [6]. It is well known that these natural diet components are widely found in many fruits and vegetables, and exert a rich variety of physiological benefits and are beneficial for human health. This review summarizes the advanced knowledges about suppression of periodontal infection by carotenoids and the possibility of clinical use will be discussed. Nutrients 2020, 12, 269; doi:10.3390/nu12010269 www.mdpi.com/journal/nutrients Nutrients 2020, 12, 269 2 of 9 Nutrients 2020, 12, x FOR PEER REVIEW 2 of 9 2.2. Pathogenesis Pathogenesis of of Periodontitis Periodontitis PeriodontitisPeriodontitis is ais bacteriala bacterial infectious infectious disease, disease, and inflammationand inflammat cascadesion cascades in the periodontal in the periodontal lesions regulatelesions theregulate disease the pathogenesis disease pathogenesis [7,8]. Roles [7,8] of inflammatory. Roles of inflammatory cytokines such cytokines as interleukin such as (IL)-1 interleukinβ and IL-6(IL) in-1β periodontitis and IL-6 in have periodontitis been explored have by been targeting explored fibroblasts, by targeting epithelial fibroblasts, cells and macrophages epithelial cells [9, 10and]. Bothmacrophages IL-1β and IL-6[9,10] cause. Both tissue IL-1β destruction and IL-6 bycause inducing tissue the destruction production by of inducing matrix-metalloproteinase-1 the production of (MMP-1)matrix-metall in inflamedoproteinase periodontal-1 (MMP tissues-1) in [11 inflamed]. MMP-1 periodontal is released tissues into the [11] inflamed. MMP tissues,-1 is released and destroys into the theinflamed connective tissue tissuess, and by destroy degradings the collagenconnective directly tissue ors by degrading activating thecollagen fibrinolytic directly protease or by activating cascades becausethe fibrinolytic type I collagen protease is accumulatedcascades because mainly type in periodontalI collagen is tissues accum [ulated11,12]. mainly Imbalance in periodontal of MMPs andtissues the inhibitors[11,12]. Imbalance such as tissue of MMPs inhibitors and ofthe MMPs inhibitors (TIMPs) such induces as tissue pathological inhibitors degradation of MMPs (TIMPs) of the collagensinduces pathological fiber in inflamed degradation periodontal of the tissues collagens [13]. fiber in inflamed periodontal tissues [13]. HumanHuman gingival gingival fibroblast fibroblast (HGF) (HGF) is is an an important important abundant abundantcell cellin in periodontal periodontaltissues tissues [14[14]]. AlthoughAlthough the the remodeling remodeling of of periodontal periodontal connective connective tissues tissues is is main main role role of of HGFs, HGFs HGFs, HGFs also also regulates regulates thethe inflammation inflammation cascades cascades in in periodontitis periodontitis lesions lesions [ 15[15,16],16].. In In addition, addition, Holden Holden et et al., al. reported, reported that that residentresident macrophages macrophages produce produce tumor tumor necrosis necrosis factor- αfactor(TNF--αα )(TNF and IL-10-α) and in response IL-10 in to response the subgingival to the microorganismssubgingival microorganisms such as fimbria such and as lipopolysaccharide fimbria and lipopolysaccharide (LPS) [17]. Thus, (LPS) macrophages [17]. Thus, m haveacrophages been involvedhave been in theinvolved inflammatory in the inflammatory responses of periodontitisresponses of [periodontitis18]. Cytokine [18] balance. Cytokine regulated balance by a crosstalkregulated betweenby a crosstalk tissue cellsbetween and immunetissue cells cells and plays immune important cells roles plays in important the stability roles and in progression the stability of theand diseaseprogression (Figure of1 ).the disease (Figure 1). FigureFigure 1. 1.Crosstalk Crosstalk of of HGFs HGFs and and inflammatory inflammatory cells: cells: Potential Potential biological biological mechanisms mechanisms of of periodontitis. periodontitis. InIn inflamed inflamed periodontal periodontal tissues, tissues, IL-1 IL-1 induces induces sIL-6R sIL-6R production production in in infiltrated infiltrated inflammatory inflammatory cells cells such such asas M. M. Furthermore, Furthermore, IL-1 IL-1 induces induces production production of of IL-6 IL-6 in in HGFs. HGFs. Finally, Finally, IL-6 IL-/6/sILsIL-6R-6R complexes complexes induce induce MMP-1,MMP-1, cathepsins, cathepsins, bFGF bFGF and and VEGF VEGF production production in in HGFs, HGFs, resulting resulting in in progression progression of of periodontitis. periodontitis. 2.1.2.1. Proteases Proteases and and Periodontitis Periodontitis ManyMany proteases proteases induce induce the the degradation degradation of of extracellular extracellular matrix matrix in in periodontitis periodontitis lesions, lesions and, and the the proteasesproteases contain contain MMPs MMPs and and cysteine cysteine proteases, proteases i.e.,, cathepsin i.e., cathepsin B and LB [19and]. AsL [19] described. As described above, MMP-1 above, isMMP released-1 is into released inflamed into periodontal inflamed periodontal tissues, and maytissue bes, involvedand may in be the involved destruction in the of collagen destruction fibers. of Sawadacollagen et al.,fibers reported. Sawada that et MMP-1 al., reported production that increased MMP-1 significantlyproduction increased in HGFs treated significantly with IL-1 inβ HGFsand IL-6treated/sIL-6R with [11 IL].- On1β and the otherIL-6/sIL hand,-6R cathepsin[11]. On the B andother L arehand, involved cathepsin in both B and intracellular L are involved proteolysis in both andintracellular extracellular proteolysis matrix degradation and extracellular so that matrix the proteases degradation induce so gingival that the tissue proteases destruction induce [gingival20]. In addition,tissue destruction although cathepsin[20]. In addition, B degrades although collagen cathepsin fibers directly, B degrades the cathepsin collagen B alsofibers contributes directly, tothe collagencathepsin degradation B also contributes indirectly to throughcollagenactivation degradation of MMP-1indirectly [19 through]. Previously, activation it has of been MMP shown-1 [19]. thatPreviously levels of, it cathepsin has been shown B and that L increase levels of in cathepsin the gingival B and crevicular L increase fluids in the (GCFs) gingival of crevicular patients withfluids periodontitis(GCFs) of patients [21]. We with reported periodontitis previously [21] that. We IL-6 reported/sIL-6R induced previously significantly that IL-6/sIL cathepsin-6R
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