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Year : 2020  |  Volume : 4  |  Issue : 2  |  Page : 93-99

Neutrophil equanimity: Function in health and diseases in periodontium

Department of Periodontics, Himachal Dental College, Sundernagar, Himachal Pradesh, India

Date of Submission25-Jul-2020
Date of Decision02-Sep-2020
Date of Acceptance05-Oct-2020
Date of Web Publication28-Jan-2021

Correspondence Address:
Dr. Komal Fanda
Department of Periodontics, Himachal Dental College, Sundernagar - 175 002, Himachal Pradesh
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/sidj.sidj_27_20

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The oral cavity is a distinct space where the microbiota is continually changing from the mechanical effort of eating and the incursion of foreign microorganisms such as bacteria, fungi, and viruses. There is a balance between symbiotic bacteria and the innate immune system in healthy gingival tissues, which is mainly maintained by neutrophils. Neutrophils are the essential killers of the body and have been recognized for a long time. However, rather than accurate snipers, neutrophils are often seen as crude and unrefined legionnaires, whose successful missions are usually liable for significant collateral damage. The excess of microorganisms in the biofilm creates an inflammatory state that leads to the recruitment of more immune cells, in which mainly neutrophils can be detected. However, the microbial pathogens within the gingival crevice cannot be abolished or controlled by neutrophils. Sometimes, neutrophil accumulation, rather than protecting and favoring periodontal tissue, can lead to a chronic inflammatory disease that can destroy the tooth-supporting tissues or the periodontium. Thus, it is imperative to maintain homeostasis between neutrophil function and microbe challenge to ensure periodontal health. This critical review article aims to discuss and outline the morphology of neutrophil function in periodontal inflammation, including neutrophils' action on biofilm and neutrophil dysfunction to prevent various syndromes related to it and its myriad potential novel therapeutic measures.

Keywords: Homeostasis, neutrophil, neutrophil extracellular traps, neutrophil abnormalities, periodontitis, Porphyromonas gingivalis

How to cite this article:
Sharma P, Fanda K, Jindal V, Malhotra R, Goel A, Thakur M, Vashisht S. Neutrophil equanimity: Function in health and diseases in periodontium. Saint Int Dent J 2020;4:93-9

How to cite this URL:
Sharma P, Fanda K, Jindal V, Malhotra R, Goel A, Thakur M, Vashisht S. Neutrophil equanimity: Function in health and diseases in periodontium. Saint Int Dent J [serial online] 2020 [cited 2023 Feb 2];4:93-9. Available from: https://www.sidj.org/text.asp?2020/4/2/93/308174

  Introduction Top

Neutrophils are a part of the innate immune system and an essential line of defense against bacteria. Neutrophils under homeostatic conditions, when enter the circulation and then migrate to tissues, where they complete their functions, and finally are eliminated by macrophages. The most abundant white blood cell (WBC) is found in the bloodstream comprising about 50%–70%. They are produced in the bone marrow in large numbers ~1011 cells per day.[1] PMNs in saliva are sometimes referred to as “orogranulocytes,”.[2] Periodontitis is one of the more advanced inflammatory forms of periodontal disease. Neutrophils are located in a high plethora within the periodontal tissues and the oral cavity that usually migrate from local capillaries toward gingival crevice within the periodontal tissues, followed by the highest concentration chemotactic gradient. The permanent presence of bacteria and biofilm-derived chemotactic and pro-inflammatory factors attract neutrophils from the circulation into the tissues.[3] Several mechanisms limit the exposure of the host to the factors produced by bacteria. First, the bacterial invasion is defined by a wall of neutrophils between the epithelium and the bacteria, thereby limiting the invasion of the tissues by bacteria. Second, a significant fluid flow emanates from the junctional epithelium's widened spaces, resulting in dilution of soluble products that could invade the periodontium's interstitial space. These proteinases from these bacteria in the tissues make it much more challenging to reach the critical concentration required for Sharpey's fibers' direct degradation.[4] Another prominent function of neutrophils is the release of pro-inflammatory compounds, including cytokines, chemokines, and digestive enzymes, stored in intracellular compartments and released through regulated exocytosis.[5] This review article will discuss neutrophils' homeostasis, function, and role of neutrophils in periodontal inflammation.

  Neutrophils Top

Neutrophils are so named due to their neutral blurring with the Wright's stain, and neutrophils' diameter ranges from 12 to 15 μm. The nucleus is single, can be polygonal, and maybe in between 2 and 5 lobes. During maturation, the neutrophil drives through several stages, sequentially through the promyelocyte, namely myeloblast, myelocyte, metamyelocyte, band cell, and finally, PMN (segmented) cell.[4] The granules are of different types and are adapted to perform specific functions, which are broadly classified into three categories based on the ultrastructural and cytochemical characteristics: primary or azurophil granules, secondary (specific) granules, tertiary or secretory granules.[4]

  Neutrophil Homeostasis Top

Neutrophils are the predominantly WBCs formed in bone marrow in response to several cytokines drawn into the gingival crevice in the oral mucosa. Neutrophils exit the gingival blood vessels and travel through the gingival junction's epithelium until they reach the gingival crevice.[5] They form the primary line of defense against microorganisms present in dental plaque. Their absence or abundance leads to periodontal tissue damage as it is evident that neutrophil numbers and distribution play a fundamental role in preserving oral health.[5] Now let us understand the several mechanisms at the level of production, trafficking, and clearance.

Highlights of neutrophil production

Neutrophils are produced in the bone marrow's venous sinuses, subdivided into three pools (stem, mitotic, and postmitotic pool), which enter into the blood circulation and migrate to tissue to complete their function. Granulocyte colony-stimulating factor (G-CSF) is a prototypical neutrophil-mobilizing cytokine that plays an important role in the acute inflammation and neutrophil release. G-CSF induces neutrophils exiting from the bone marrow by interfering with the CXCR4-CXCL12 (coupled chemokine receptor) interaction. The large number of mature neutrophils in the bone marrow that is retained there by the interaction of the chemokine CXCL12 (stromal-derived factor-1/SDF-1) are produced by the bone marrow stromal cells, with the CXC chemokine receptor 4 (CXCR4) which is present on neutrophils. Interleukin-17 (IL-17) also promotes granulopoiesis and neutrophil release by upregulation of G-CSF. At chronic inflammation site, neutrophils attract IL-17-producing CD4+ T-lymphocytes (Th17 cells) which further help in the recruitment of neutrophils.[6] The production of IL-17 by neutrophils is also a part of this positive loop for neutrophil recruitment [Figure 1]. Neutrophils release CCL2 and CCL20 chemokines, which are ligands for the CCR2 and CCR6 chemokine receptors on Th17 cells, and thus, they are recruited to sites of neutrophil accumulation. In turn, Th17 cells recruit more neutrophils by producing more IL-17.[7]
Figure 1: Mechanism of neutrophil homeostasis (neurostat). Red arrows represent the release of cytokines and chemokines from cells and effect of these mediators on cells. Blue arrows represent the movement of cells[7]

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Neutrophil trafficking and its significance with periodontal tissue

Once neutrophils go into circulation, they can quickly move to sites of inflammation through a highly organized process known as the leukocyte adhesion cascade.[8] Integrins and selectins are the major adhesion molecules regulating the trafficking of neutrophils. After that, transmigration takes place in peripheral tissues. The role of these molecules in the emigration of neutrophils from the blood to sites of inflammation. After that transmigration take place in peripheral tissues. This leukocyte adhesion cascade can be controlled by tissue-derived cytokines, which control the expression of endothelial adhesion molecules, and by tissue-derived chemokines, which induce integrin conformational changes that result in their high affinity state. In this step, neutrophils transmigrate into peripheral tissue with the help of endothelial activated cells and in which it adheres with E- and P-selectins.

Removal of neutrophils (clearance)

Neutrophils in tissues first undergo apoptosis, and then, their clearance takes place by native phagocytes, such as macrophages and dendritic cells. Neutrophils in the blood come back to the bone marrow for clearance after they increase the expression of CXCR4.[9] The clearance of apoptotic neutrophils not solely eliminates old cells but also is essential for controlling neutrophil production in the bone marrow. Phagocytosis of apoptotic neutrophil produces an anti-inflammatory response characterized by a decrease in IL-23 production by macrophages. IL-23 is one of the major cytokines for prompting IL-17 production by many immune system cells[10] [Figure 1]. Thus, reduced IL-17 levels lead to less G-CSF production and inconsequence less neutrophil production. This control loop has been known as a “neutrostat” (neutrophil rheostat) that maintains steady-state neutrophil in circulation.

  Antibacterial Activity of Neutrophils Top

The human junctional epithelium can never be sterile, meaning that even with optimal plaque control, neutrophils will be stimulated to exit the gingival microvasculature, so that it enters the periodontal tissues.[11] Neutrophil has multiple antibacterial or killing mechanisms that help them to fight a broad spectrum of bacteria. These mechanisms include phagocytosis, degranulation, and neutrophil extracellular traps (NETs) [Figure 2].
Figure 2: Neutrophil regulation of both innate and adaptive immunity. N: Neutrophil, FB: Fibroblast, APRIL: A proliferation-inducing ligand, B: B-cell, BLyS: B-lymphocyte stimulator, MMP: Matrix metalloproteinase, IL: Interleukin, OCP: Osteoclast precursor, P: Plasma cell, RANKL: Receptor activator of nuclear factor-kappa B ligand, ROS: Reactive oxygen species

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Neutrophils, composed of the skilled phagocytes, are endowed with a unique capacity to engulf and eliminate pathogens and cell debris.[11] Phagocytosis is a receptor-mediated process during which a particle is internalized by the cell into a vacuole called the phagosome. It requires the fusion of phagosome with the neutrophilic granules, which results in the discharge of granule contents into the phagosome, resulting in the intercellular killing of bacteria.[11] After the formation of the phagolysosome, the bacterial agents present in the neutrophil granules are released into it, and ingested microorganism is digested and killed. The neutrophil kills bacteria by oxygen-dependent or independent mechanisms.[11] Any alterations in this function can lead to localized juvenile periodontitis.


Degranulation is defined as intra- or extracellular release of granule contents such as enzymes and antimicrobial peptides. The exocytosis of granules and secretory vesicles plays a key role in most neutrophil functions, from initial activation to the destruction of phagocytosed microorganisms. Neutrophil's stimulation with phorbol myristate acetate prompts the complete release of gelatinase granules, controlled release of specific granules, and minimal exocytosis azurophil granules.[12] The recent observations found that neutrophils' degranulation depends on the activation of intracellular signaling pathways, including β-arrestins, Rho guanosine triphosphatase Rac2, soluble NSF-attachment protein receptors, src family of tyrosine kinases, and also the tyrosine phosphatase MEG2. In another way, neutrophil stimulation with fMLF prompts the release of mostly secretory vesicles without significant granule release.[11],[12]

Neutrophil extracellular traps

NETs are the extracellular, web-like structures composed of cytosolic and granule proteins present in a decondensed chromatin scaffold.[13] In this mechanism, the nuclear and mitochondrial DNA is released into the extracellular space. The chromatin forms a trap for pathogens that look like a web called NETs. The neutrophil extrudes a meshwork of chromatin fibers decorated, consisting of elastase; cathepsin G; myeloperoxidase, bactericidal/ permeability-inducing protein & BPI; lactoferrin; peptidoglycan recognition proteins; matrix metalloproteinase-9) that bind and kill bacteria and other pathogens, as well as destroying microbial virulence factors.[13] This process is also known as NETosis.[14] NETs provide a defense strategy to prevent bacteria's infiltration, which may be necessary for periodontal tissues. Conversely, NETs may also be harmful if produced in surplus or if they are not removed appropriately.[14] Various initiators of NETosis include bacterial cell wall components that can activate complement receptors, Fc receptors, or Toll-like receptors on the neutrophil surface.[14]

  Neutrophil Regulation of Both Innate and Adaptive Immunity Top

The typical antimicrobial function as the first defense line is neutrophils. It has significant versatility that enables them to engage in formerly unsuspected functions, such as regulating innate and adaptive immune leukocytes. The conversion from periodontal health to other diseases is associated with an intense shift from a symbiotic microbial community to dysbiotic communities and innate and adaptive immunity elements.[15] Neutrophils are activated by the dysbiotic microbiota directly or indirectly by complement activation products, primarily C5a. Neutrophils also interact with adaptive immune cells, such as B and plasma cells and Th17 cells, as indicated.[16] In periodontitis, activated neutrophil-derived reactive oxygen species and matrix metalloproteinases can directly cause connective tissue damage. Moreover, neutrophil interactions with adaptive immunity may contribute significantly to inflammatory events that eventually stimulate receptor activator of nuclear factor-kappa B-prompted osteoclastogenesis and bone resorption.[17] Neutrophils secrete cytokines that enhance B and plasma cells' survival, namely A proliferation-inducing ligand and B-lymphocyte stimulator, which we have associated with human periodontitis and causally linked to B-cell-dependent periodontal bone loss in mice.[18] Through the release of CCL2 and CCL20 chemokines, neutrophils can recruit CCR2- and CCR6-expressing Th17 cells, which are implicated in autoimmune and inflammatory conditions, including human and experimental animal periodontitis [Figure 2]. Reciprocally, by acting mainly through fibroblasts, Th17-derived IL-17 induces CXC chemokines (e.g., CXCL-8 and IL-8), which can influence the chemotactic recruitment of neutrophils to the periodontium.[15],[16]

  Neutrophil Role in Periodontitis Top

Neutrophils are the myeloid-derived professional antimicrobial phagocyte cells found in the crevice of periodontal tissue. Based on available previous literature, neutrophils form a wall between junctional epithelium and dental plaque. This neutrophil barrier wall works in periodontal tissue as reactive oxygen species merged with bactericidal protein and as a phagocytic apparatus, promoting tissue healing and inflammatory resolutions. The development of aggressive periodontitis is related to congenital deficiencies in neutrophil counts or their function and that neutrophil count is also important for maintaining a healthy periodontium. However, in contrast to all this, the presence of neutrophils is not necessarily protective. In fact, there is adequate evidence that a significant portion of the inflammatory destruction of the periodontium occurs as a result of collateral damage by hyperactive neutrophils.[19] Ryder, 2010 proposed the mechanisms that explain neutrophils' role in periodontal disease development.[20] These are the impaired neutrophil and hyperactive neutrophil. Another mechanistic category could also explain neutrophils' role in periodontal disease development, i.e., chronic recruitment and activation of the normal neutrophil.[20],[21]

There is some strong evidence that neutrophils from localized or generalized periodontitis with a rapid progression rate demonstrate defective chemotaxis and phagocytosis. The consensus is that the chemotaxis defect may involve faulty surface receptors for chemotactic stimulants.[18] The hyperactive neutrophil is also known as “primed neutrophils,” which increases neutrophils' activity or function.[20] In recent studies, much of the data published have supported that a hyperactive/primed neutrophil concluded leads to increased tissue destruction in aggressive forms of periodontitis.[21],[22] Researchers have found that myeloperoxidase levels in the GCF with increased elastase levels were observed in patients with aggressive periodontitis compared to healthy patients or control groups.[21] The authors have imputed this difference to priming events. These are proteolytic enzymes and may also inhibit the host defense mechanisms. These enzymes' increase was thought to result from a priming response that enabled a cell to release an excess amount of these enzymes at the inflammation site.[22] The superoxide generation by neutrophils is also enhanced due to exposure to f-Met-Leu-Phe and preincubation with Porphyromonas gingivalis. The priming substance in serum may be a microbial product. One study identified three aggressive periodontitis-related genes involved in neutrophil adhesion and expression of tumor necrosis factor-alpha.[23] In some published works of literature, we also found that an increase in gene expression was associated with NADPH oxidase, which is responsible for synthesizing oxidative burst products in both chronic and aggressive forms of periodontitis.[22]

  Neutrophil Abnormalities and Polymorphisms Associated With Aggressive Periodontitis Top

It has been widely observed that neutrophils may be responsible for both host defense and host tissue damage. Many genetic neutrophil defects, such as a defect in chemotaxis, adhesion, and phagocytosis, often lead to severe inflammatory periodontal disease. Some oral manifestations of neutrophil defects are listed in [Table 1].
Table 1: Oral manifestations associated with neutrophil abnormalities

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  Microbial Subversion of Neutrophil Function Top

The studies presented above clearly demonstrated that more neutrophils with a prosurvival phenotype are present with severe forms of periodontitis.[9] As crevicular neutrophils maintain their viability and capacity to stimulate immune responses, the persistence of uncontrolled biofilms could be attributed, at least in part, to the ability of the bacteria to subvert neutrophil functions in ways that impede immune-mediated killing.[7] Now let's understand how periodontitis-associated bacteria can get the “best of both worlds” (protection through impaired immunity and growth through enhanced inflammation).[15] Some of these bacteria show a survival mechanism that controls neutrophil functions, prevents microbial killing, and promotes inflammation. This subversion of neutrophils has been described in great detail molecularly level.

A P. gingivalis is a keystone pathogen in periodontitis that can disengage bacterial clearance from inflammation and contribute to the persistence of microbial communities that drive periodontitis.[25] P. gingivalis can manipulate both TLR signaling and complement to induce bacterial resistance. P.[26] gingivalis expresses ligands that activate the Toll-like receptor-2 and produce enzymes gingipains (HRgpA and RgpB) that function as complement C5 convertases with high concentrations of C5a ligand. Thus, the C5a coactivates or binds with C5a receptor and Toll-like receptor-2 in neutrophils leads to ubiquitination and proteasomal degradation of the Toll-like receptor-2 adaptor myeloid differentiation primary response protein 88 (MyD88).[27],[28] As MyD88 pathway utilized by TLR2 (Toll Like Receptors 2) is not only involve in the signal transduction but also a pro-inflammatory pathway, thereby inhibiting a host protective antimicrobial response. P. gingivalis also induces inflammation from the neutrophil by the same strategy [Figure 3]. Binding to the TLR2, an alternative signaling pathway involves the adaptor molecule Mal, the enzyme phosphatidylinositol 3-kinase (PI-3K) and pro-inflammatory cytokines, such as TNF, IL-1b, and IL-6. Moreover, the same pathway can prevent actin polymerization through the small GTPase RhoA and block phagocytosis.[9],[15] The integrated, subversive strategy provides P. gingivalis; in addition, it protects other bystander bacteria from neutrophil microbial mechanisms. As a result, P. gingivalis controls neutrophil function by two means that together ensure bacterial survival and continuation of inflammation.
Figure 3: Microbial subversion of neutrophil function leads to periodontal inflammation. Mal: Myeloid differentiation primary response protein 88 adaptor-like, C5aR: C5a complement fragment binds to its receptor, MyD88: Myeloid differentiation primary response protein 88, PI3K: Phosphoinositide 3-kinase, PKA: Protein kinase A, TLR: Toll-like receptor[7]

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  Potential Therapeutic Approaches Top

In this review article we have also tried to discuss how both reduction and increase in neutrophil counts can exacerbate oral diseases. Because in both conditions IL-17 Mediated inflammation & bone loss may be a primary cause of periodontitis. It can be therefore assumed that IL-17R inhibitors may be promising for the treatment of periodontal diseases.[18],[29],[30] In chronic periodontitis, periodontal bacteria activate neutrophil subversion pathways, as discussed above, that allow bacteria to escape neutrophil killing. These bacterial products could be neutralized with antibodies or novel pharmaceutical drugs to prevent neutrophils' adverse effects.[29] Del-1 is another important molecule to be used therapeutically to prevent neutrophil recruitment and bone loss associated with periodontal inflammation as Del-1 blocks LFA-1 binding to its ligand ICAM-1 and prevents neutrophil transmigration. Local administration of Del-1 also prevented inflammatory bone loss.[18]

  Conclusion Top

Neutrophils are specialized phagocytes that coordinate and accomplish inflammation. Alterations in the neutrophil homeostasis can lead to periodontal diseases. It is also studied that hyperactive neutrophils can exacerbate and even leads to autoimmune and inflammatory diseases. Neutrophils can also contribute to tissue destruction in periodontitis, at least in part due to their subversion by microbes in ways that dysregulate their antimicrobial and inflammatory responses. New potential therapeutic approaches have been identified. They promise relief from periodontitis and perhaps other inflammatory disorders.

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Conflicts of interest

There are no conflicts of interest.

  References Top

Rosales C, Uribe-Querol E. Neutrophil role in perio-dontal disease. In: Abbas M, editor. Role of Neutrophils in Disease Pathogenesis. London: Intech Open; 2017. p. 67-88.  Back to cited text no. 1
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Dennison DK, Van Dyke TE. The acute inflammatory response and the role of phagocytic cells in periodontal health and disease. Periodontol 2000 1997;14:54-78.  Back to cited text no. 3
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Delima AJ, Van Dyke TE. Origin and function of the cellular components in gingival crevice fluid. Periodontol 2000 2003;31:55-76.  Back to cited text no. 5
Hajishengallis E, Hajishengallis G. Neutrophil homeostasis and periodontal health in children and adults. J Dent Res 2014;93:231-7.  Back to cited text no. 6
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Chavakis E, Choi EY, Chavakis T. Novel aspects in the regulation of the leukocyte adhesion cascade. Thromb Haemost 2009;102:191-7.  Back to cited text no. 8
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Saroch N. Role of neutrophils in host microbial interactions. Periobasics A Textbook of Periodontics and Implantology. 2nd ed. Himachal Pradesh, India: Sushrut Publications; 2017. p. 150-6.  Back to cited text no. 11
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Lacy P. Mechanisms of degranulation in neutrophils. Allergy Asthma Clin Immunol 2006;2:98-108.  Back to cited text no. 13
Papayannopoulos V. Neutrophil extracellular traps in immunity and disease. Nat Rev Immunol 2018;18:134-47.  Back to cited text no. 14
Kaplan MJ, Radic M. Neutrophil extracellular traps: Double-edged swords of innate immunity. J Immunol 2012;189:2689-95.  Back to cited text no. 15
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Abe T, AlSarhan M, Benakanakere MR, Maekawa T, Kinane DF, Cancro MP, et al. The B cell-stimulatory cytokines BLyS and APRIL are elevated in human periodontitis and are required for B cell-dependent bone loss in experimental murine periodontitis. J Immunol 2015;195:1427-35.  Back to cited text no. 19
Ryder MI. Comparison of neutrophil functions in aggressive and chronic periodontitis. Periodontol 2000 2010;53:124-37.  Back to cited text no. 20
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[PUBMED]  [Full text]  
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  [Figure 1], [Figure 2], [Figure 3]

  [Table 1]


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