Juveniles versus adults: differences in PGE2 levels in the gingival crevicular fluid during orthodontic tooth movement

Chibebe, Priscilla Campanatti; Starobinas, Nancy; Pallos, Debora

doi:10.1590/S1806-83242010000100018

Abstract

This study aimed to investigate age-related changes in the biosynthetic capacity of prostaglandin E2 (PGE2) in the gingival crevicular fluid (GCF) during one month of orthodontic treatment. Twenty-five juvenile subjects (mean age 13 ± 2.1 years) and 23 adults (mean age 24 ± 2.1 years) were included. GCF was collected immediately before the force application at the baseline, 2, 21 and 28 days, with periopaper inserted into the gingival crevice of the maxillary lateral incisors. The mediator levels were determined with an EIA kit. The results showed that the PGE2 concentrations were significantly elevated from the baseline to 21 days (129.35 and 198.84 pg/µL, p = 0.0169) in juvenile subjects and reduced from 21 to 28 days (198.84 to 112.60 pg/µL, p = 0.0032). Adults, however, had no significant changes in the PGE2 levels. The total amounts of PGE2 from both groups changed between the baseline to 21 and 21 to 28 days (p = 0.0119 and p = 0.0076, respectively). The PGE2 initial and final levels showed significant differences between the juveniles and adults, being higher in adults (baseline: juvenile = 129.35 pg/µL vs. adult = 163.20 pg/µL, p = 0.0379; t3: juvenile = 112.60 pg/µL and adult = 175.30 pg/µL, p = 0.0005). In conclusion, the results demonstrate the presence of variation in the PGE2 levels according to age and the orthodontic activation period, which can explain why the speed of orthodontics treatment may be different in adults vs. juveniles.

Prostaglandins; Gingival crevicular fluid; Orthodontics, corrective; Tooth movement; Cytokines

PERIODONTICS

Juveniles versus adults: differences in PGE₂ levels in the gingival crevicular fluid during orthodontic tooth movement

Priscilla Campanatti Chibebe^I; Nancy Starobinas^II; Debora Pallos^III

^IDDS, MS - Department of Periodontics, Taubaté University (UNITAU), Taubaté, SP, Brazil

^IIIDDS, PhD Department of Periodontics, Taubaté University (UNITAU), Taubaté, SP, Brazil

^IIPhD, Department of Imunogenetic, Butantan Institute, São Paulo, SP, Brazil

ABSTRACT

This study aimed to investigate age-related changes in the biosynthetic capacity of prostaglandin E₂ (PGE₂) in the gingival crevicular fluid (GCF) during one month of orthodontic treatment. Twenty-five juvenile subjects (mean age 13 ± 2.1 years) and 23 adults (mean age 24 ± 2.1 years) were included. GCF was collected immediately before the force application at the baseline, 2, 21 and 28 days, with periopaper inserted into the gingival crevice of the maxillary lateral incisors. The mediator levels were determined with an EIA kit. The results showed that the PGE₂concentrations were significantly elevated from the baseline to 21 days (129.35 and 198.84 pg/µL, p = 0.0169) in juvenile subjects and reduced from 21 to 28 days (198.84 to 112.60 pg/µL, p = 0.0032). Adults, however, had no significant changes in the PGE₂levels. The total amounts of PGE₂ from both groups changed between the baseline to 21 and 21 to 28 days (p = 0.0119 and p = 0.0076, respectively). The PGE₂ initial and final levels showed significant differences between the juveniles and adults, being higher in adults (baseline: juvenile = 129.35 pg/µL vs. adult = 163.20 pg/µL, p = 0.0379; t3: juvenile = 112.60 pg/µL and adult = 175.30 pg/µL, p = 0.0005). In conclusion, the results demonstrate the presence of variation in the PGE₂levels according to age and the orthodontic activation period, which can explain why the speed of orthodontics treatment may be different in adults vs. juveniles.

Descriptors: Prostaglandins; Gingival crevicular fluid; Orthodontics, corrective; Tooth movement; Cytokines.

Introduction

In orthodontic tooth movement, mechanical stress appears to evoke biochemical and structural responses in a variety of cell types both in vivo and in vitro.^1-9 The early phase of orthodontic tooth movement involves an acute inflammatory response characterized by local tissue ischemia, periodontal vasodilatation and the migration of leukocytes through the periodontal ligament capillaries.^1-9 In this process, endothelial cells are activated, and cytokines and chemoattractants are produced that result in leukocyte activation. The interaction between activated endothelial cells and leukocytes plays an important role in the inflammatory process by producing proinflammatory and anti-inflammatory cytokines. These mediators are bioactive molecules that regulate the inflammatory process.^2-9 The mechanism of bone remodeling can also be related to the release of inflammatory mediators, such as prostaglandin E₂.^1-4

Prostaglandin E₂ (PGE₂) and interleukin IL-1β are key mediators involved in periodontal diseases, potent stimulators of bone resorption, and are produced by human periodontal ligament cells in response to mechanical stress. PGE₂ not only mediates inflammatory responses, such as increases in vascular permeability and dilatation, but also can act as a potent stimulator of bone resorption and formation. This dynamic mechanism can be affected according to the concentration of PGE₂.^6-10

Saito et al.⁹ showed that periodontal ligament cells respond to mechanical stress (in vivo and in vitro) by an increased production of PGE₂. Thus, after the application of mechanical forces, cells in the periodontal ligament produce sufficient amounts of mediators to diffuse into the gingival crevicular fluid. Grieve et al.⁷ showed that PGE₂ and IL-1β were significantly elevated after the initial tooth movement but returned to baseline levels after seven days. Ren et al.¹¹ showed that the concentrations were significantly elevated after 24 hours of activation in juvenile and adult patients, but concluded that the mediator levels in juvenile subjects are more responsive than the levels in adults.

Ren et al.⁵ showed that IL-8, IL-6, IL-1β and TNF-α play significant roles in the early stage of tooth movement, but not in the linear phase. This study suggests that once the microenvironment of the periodontal ligament is activated by orthodontic force, several key proinflammatory cytokines are produced to trigger a cascade of cellular events.

Although the severity of periodontal disease is known to be affected by the age of the host,¹² the role of aging in orthodontic tooth movement has not been well characterized. The production of PGE₂ in human periodontal ligament cells is increased by mechanical stress; however, the age-related changes in the susceptibility of periodontal ligament cells in response to mechanical stress remain unclear.¹³

Little information is available concerning the production of these mediators during orthodontic tooth movement in different ages and during a period of time around the reactivation of the orthodontic appliances in clinical treatment. The literature is limited regarding the best time to reactivate orthodontic appliances in different ages of periodontal cells, which can affect the severity of inflammation and bone resorption in response to the application of mechanical forces.

The level of PGE₂ in the gingival crevicular fluid can increase during orthodontic tooth movement, and its quantification provides a non-invasive model in vivo for investigating the dynamics of mediator production.^1,7,14-16 To investigate age-related changes in the biosynthetic capacity of PGE₂ in the periodontal ligament cells, we examined the effects of in vivo aging (juvenile and adults) with mechanical tension on the PGE₂ expression by periodontal ligament cells in the gingival crevicular fluid during the first month of orthodontic treatment.

Material and Methods

Study population

Forty-eight orthodontic patients were included in this study, with 25 juvenile subjects, and 23 adults. The juvenile group included the subjects between the ages of 11 and 17 years old, and the adults were from 21 to 27 years old. These subjects met the following criteria: good general health; no use of anti-inflammatory drugs in two month preceding the study; a lack of antibiotic therapy within the past six months; periodontally healthy, with generalized probing depths ≤ 3 mm and no radiographic evidence of periodontal bone loss; no smoking; and a requirement for buccal/labial tooth movement as part of their orthodontic treatment. The Ethics Committee of Research on Human Beings from Taubaté University approved the study. Informed consent was obtained from each individual.

Experimental design

The maxillary right lateral incisors were chosen as the experimental teeth. Orthodontic brackets (GAC International) were placed on the teeth and activated by an orthodontic wire (0.012 Nitinol- GAC International). This wire was custom-formed for each patient with varying amounts of buccal/labial offset to produce approximately 0.7 N of force at the baseline as measured with a calibrated orthodontic force gauge (Ortoply, Philadelphia, Pennsylvania, USA). The patients received oral hygiene instructions during all of this study to insure optimal control of bacterial plaque. The radiographic examination and clinical periodontal assessments, including the gingival index (GI),¹⁷ plaque index (PI),¹⁸ probing depth (PD) and clinical attachment level (CAL) were performed at the baseline and the end of experiment. At the mesio/buccal site of the experimental tooth, gingival crevicular fluid was collected immediately before activation (T0 = baseline) and after 2, 21 and 28 days.

The gingival crevicular fluid collection and PGE₂ determination

The gingival crevicular fluid collection was performed as described by Grieve et al.⁷ Briefly, the mesio/buccal site of the maxillary right lateral incisor was isolated with cotton rolls and gently dried with an air syringe. A paper strip (Periopaper^, Harco. Tustin, CA, USA) was carefully inserted 1 mm into the gingival crevice and maintained for 30 seconds. Immediately, the periopaper strip was placed in an Eppendorf tube and sealed subsequently. The samples were stored at -70ºC until the analysis. To quantify the PGE₂ levels, duplicate samples from each site were evaluated with a competitive enzyme immunoassay (EIA) kit obtained from the Cayman Chemical Co. (Ann Arbor, Michigan, USA). The concentrations of mediator in the samples were calculated according to the reference calibration curves of the standards. The results were expressed as pg/µL.

The PGE₂ levels in the GCF were compared among the different periods of orthodontic tooth movement and age. The comparisons between the mean values of two groups were analyzed by analysis of variance and Student's t-tests (p < 0.05). The data were evaluated with the Bio Estat 2.0 software.

Results

No significant changes in the PI, GI or pocket depth were found in the 48 participants at any time throughout the experiment, suggesting a consistent level of oral hygiene. All of the experimental sites showed a stable and healthy gingival and periodontal status, with the PI and GI lower than 0.25 and pocket depths of 3 mm or less. There were no clinical signs of inflammation at any experimental time point. In relation to the force employed, the mean initial force in the juvenile group was 0.64 N (at the baseline), decreasing to 0.44 N (28 days). In adult group, the initial force was 0.67 N (at baseline), reducing to 0.45 N at the end of experiment. The mean of the CAL and PD and the initial and final force from the juvenile and adult group are shown in Table 1.

Thumbnail

The mean levels of PGE₂in both groups showed significant increases from the baseline to 21 days (p = 0.0119) and significant decreases from 21 to 28 days (p = 0.0076). However no significant differences were found between the baseline and 28 days (p = 0.8767) and 2 to 21 days (p = 0.5024). Graph 1 shows that the total PGE₂ levels at the end of experiment (143.95 pg/µL) returned to values similar to the baseline (146.28 pg/µL).

The comparison of the mean concentrations of PGE₂ of the two groups at each time point of study showed significant differences between the total amounts produced by the juveniles and adults at the baseline and the end of experiment. In adults, the amount produced was higher at both time points. At the baseline, the level in adults was 163.20 ± 70.11 pg/µL versus 129.35 ± 69.04 in the juveniles (p = 0.0379); at 28 days, the levels were 170.49 ± 68.14 pg/µL in adults and 112.60 ± 55.26 in juveniles (p = 0.0005).

In the juvenile group, a significant increase in PGE₂ was observed at 21 days after force had been applied (129.35 pg/µL to 198.84 pg/µL, p = 0.0169). The ANOVA test showed no significant increase between the baseline and 2 days (p = 0.1894) or 2 to 21 days (p = 0.2701). However, a significant decrease (56.6%) occurred at the end of experiment from 21 (198.84 pg/µL) to 28 days (112.60 pg/µL, p = 0.0032) (Graph 2).

Discussion

In orthodontics, mechanical stress evokes a response in a variety of cell types. The early phase of orthodontic tooth movement involves an acute inflammatory response. The gingival crevicular fluid analysis has been proven as an effective method to study periodontal ligament and alveolar bone remodeling.⁵ Careful control of bacterially induced inflammation allowed the current research to focus on mediators associated with mechanically induced inflammation within the bone and periodontal ligament. Previous reports have demonstrated reduced or absent quantities of PGE in gingival crevicular fluid at non-inflamed sites.² However the increased levels of PGE₂ in gingival crevicular fluid are also associated with an increased severity of periodontal disease.^2,19-20

Prostaglandins, in particular PGE₂, are involved in the response of bone tissue and cells to stress.¹³ In this study, the PGE₂ levels in the initial samples compared to those observed after two days in juveniles did not show a significant difference according to the ANOVA analysis. These data do not agree with previous studies that showed an increase in the levels of PGE₂ in young individuals (17 years on average) after 24 and 48 hours, and a decrease after 168 hours of application of the orthodontic force.^11,21 In another study,⁵ in patients 11 to 27 years old, the levels of pro-inflammatory cytokines were significantly elevated in the early stage of tooth movement but at different time points, IL-6, IL-1β and TNFα at 24 hours and IL-8 at 1 month. However, during the linear stage of tooth movement, all cytokines were reduced to their baseline levels. The justification is that the periodontal system stabilizes at a new physiological homeostasis as indicated by the down-regulation of the initial stage of pro-inflammatory cytokines,⁵ which can be applied to this study too.

In the juvenile group, there was an increase in PGE₂ from the baseline to 21 days after the application of orthodontic force, while from 21 to 28 days (after a week) there was reduction in the PGE₂ levels. These data suggest differences in the PGE₂ levels according to the orthodontic movement phase, consistent with the role of PGE₂ as a potent stimulator of bone resorption and formation. This may also suggest that the difference in the PGE₂ activity might be partly affected by the local concentration of PGE₂.

No significant differences were found in the adult group samples at any time. Conversely, some studies showed an elevated PGE₂ production at 24 and 48 hours, but these studies are only 7 days in duration.^7,9,11 The finding of increased levels of gingival crevicular fluid adjacent to teeth undergoing orthodontic tooth movement indicates that the cells within the periodontium are producing increased PGE₂ in response to orthodontic force.

The mean PGE₂levels of both groups (total group) showed that the total amounts at the end of experiment returned to values similar to those of the baseline, suggesting that the inflammatory process returned to the normal status. This decreased level of PGE₂suggests that at 28 days there was no more cellular stress, indicating the optimal moment to re-activate the orthodontic appliance.

Lee et al. (2004)²² concluded that while continued strength has been provided, the levels of PGE₂ showed a significant increase in 24 hours and then decreased, showing a temporary increase, and forcefully stopped. The levels of PGE₂ increased significantly in 24 hours and remained high for a week In this study, force is continually applied with the NiTi orthodontic arch, with a gradual increase in the levels of PGE₂, peaking at 21 days then decreasing to levels close to the original.

Several factors could be considered when results are analyzed. First, the analysis of the gingival crevicular fluid is a useful and advantageous method, especially for human in vivo studies, because it is noninvasive, and repetitive sampling from the same site is achievable regardless of the number of samples. This enables the monitoring of change at a single site during a certain period.

Comparing the juvenile and adult data, it was possible to observe that juveniles showed greater changes in the PGE₂levels than the adults, in agreement with Ren et al.¹¹ In the absence of smoking or other periodontal disease, this may explain why the speed of orthodontic treatment may be different in adults versus juveniles. This suggests that, in juveniles, the inflammatory responses can react faster to local changes. In juveniles, sex hormones are related to an increased gingival response during orthodontic treatment,²³ however there are no studies that demonstrate the influence of these hormones on the periodontal ligament and alveolar bone in response to mechanical stress. Some studies^11,19,23-24showed that old periodontal ligament cells produced significantly higher amount of PGE₂compared with young cells in a time and magnitude-dependent manner when the cells were exposed to a cyclic tension force.

The orthodontic treatment of adults has increased dramatically in recent years. It has been shown that with increasing age there is a decrease in the proliferation of periodontal ligament cells, organic matrix production, the relative amount of soluble collagen and alkaline phosphates activity. Cellular differentiation is also affected, which results in a decreased number of osteoblasts and osteoblast-precursor cells.^11,19,25

The clinical significance of research regarding the mechanism of bone metabolism in orthodontic tooth movement is related to its potential pharmacologic modulation. This includes the effects of adjunctive PGE and IL-1β, as well as prostaglandin-inhibiting drugs, on the rate of tooth movement.⁷

Conclusions

The analysis of the GCF is an effective method in the study of inflammatory mediators in patients undergoing orthodontic treatment, as well as helpful in periodontal diagnosis. Studies on the mechanisms of the production of inflammatory mediators related to orthodontic therapy at different ages may provide useful information for monitoring the efficiency of tooth movement in the future and enable the establishment of drug regimens to improve the effectiveness of treatment.

Acknowledgments

This work was supported by a grant from the São Paulo Research Foundation (FAPESP) 04/15395-1. Chibebe was supported by PROSUP- CAPES/UNITAU.

Received for publication on Sep 18, 2009

Accepted for publication on Dec 20, 2009

1. Griffiths GS. Formation, collection and significance of gingival crevice fluid. Periodontol 2000 2003; 31(1): 32-42.
2. Offenbacher S, Odle BM, Van Dyke TE. The use of crevice fluid prostaglandin E₂ levels as a predictor of periodontal attachment loss. J Periodontal Res 1986; Mar 21(2):101-12.
3. Roberts WE, Huja SS, Roberts JA. Bone modeling: biomechanics, molecular mechanisms, and clinical perspectives. Semin Orthod 2004; Jun 10(2):123-161.
4. Uitto VJ. Gingival crevice fluid- an introduction. Periodontol 2000 2003; Jan 31(1):9-11.
5. Ren Y, Hazemeijer H, Haan B, Qu N, Vos P. Cytokine profiles in crevice fluid during orthodontic tooth movement of short and long durations. J Periodontol 2007; Mar 78 (3):453-458.
6. Coetzee M, Haag M, Claassen N, Kruger MC. Stimulation of prostaglandin E2 (PGE2) production by arachidonic acid, oestrogen and parathyroid hormone in MG-63 and MC3T3-E1 osteoblast-like cells. Prostaglandins Leukot Essent Fatty Acids 2005; Dec 73(6): 423-430.
7. Grieve WG, Johnson GK, Moore RN, Reinhardt RA, Dubois LM. Prostaglandin E (PGE) and interleukin-1β (IL-1β) levels in gingival crevicular fluid during human orthodontic tooth movement. Am J Orthod Dentofacial Orthop 1994; Apr 105 (4):3 69-374.
8. Mitsui N, Suzuki N, Maeno M, Mayahara K, Yanagisawa M, Otsuka K, Shimizu N. Optimal compressive force induces bone formation via increasing bone sialoprotein and prostaglandin E₂ production appropriately. Life Sci 2005; Nov 77(25): 3168-3182.
9. Saito M, Saito S, Ngan PW, Shanfeld J, Davidovitch Z. Interleukin 1 beta and prostaglandin E are involved in the response of periodontal cells to mechanical stress in vivo and in vitro Am J Orthod Dentofacial Orthop 1991; Mar 99 (3): 226-240.
10. Sodek J, Mckee MD. Molecular and cellular biology of alveolar bone. Periodontol 2000 2000; Oct 24 (1):99-126.
11. Ren Y, Maltha JC, Van't Hof MA, Von Den Hoff JW, Kuijpers-Jagtman AM, Zhang D. Cytokine levels in crevice fluid are less responsive to orthodontic force in adults than in juveniles. J Clin Periodontol 2002; Aug 29(8): 757762.
12. Van Dyke TE, Sheilesh D. Risk factors for periodontitis. J Int Acad Periodontol 2005;Jan 7 (1):3-7.
13. Shimizu N, Yamaguchi M, Uesu K, Goseki T, Abiko Y. Stimulation of prostaglandin E2 and interleukin-1beta production from old rat periodontal ligament cells subjected to mechanical stress. J Gerontol A Biol Sci Med Sci. 2000; Oct 55(10):B489-95.
14. Burke JC, Evans CA, Crosby TR, Mednieks MI. . Expression of secretory proteins in oral fluid after orthodontic tooth movement. Am J Orthod Dentofacial Orthop 2002; Mar 121(3): 310-315.
15. Davidovitch Z. Tooth movement. Crit Rev Oral Biol Med 1991; 2(4): 411-450.
16. Kavadia-Tsatala S, Kaklamanos EG, Tsalikis L. Effects of orthodontic treatment on gingival crevicular fluid flow rate and composition: Clinical implications and applications. Int J Adult Orthodon Orthognath Surg 2002; Fall 17(3):191-205.
17. Löe H, Silness J. Periodontal disease in pregnancy. I. Prevalence and Severity Acta Odontol Scand Dec 1963; 21; 533-51
18. Silness J, Löe H. Periodontal disease in pregnancy. II. Correlation between oral hygiene and periodontal condtion. Acta Odontol Scand 1964; Fev 22: 121-35.
19. Ohzeki K, Yamaguchi M, Shimizu N, Abiko Y. Effect of cellular aging on the induction of cyclooxygenase-2 by mechanical stress in human periodontal ligament cells. Mech Ageing Dev 1999; May 108 (2): 151-163.
20. Tsai CC, Hong YC, Chen CC, Wu YM. Measurement of prostaglandin E₂ and leukotriene B₄ in the gingival crevice fluid. J Dent 1998; Mar 26 (2): 97-103.
21. Sari E, Olmez H, Gürton AU. Comparison of some effects of acetylsalicylic acid and rofecoxib during orthodontic tooth movement. Am J Orthod Dentofacial Orthop. 2004 Mar;125(3):310-5.
22. Lee KJ, Park YC, Yu HS, Choi SH, Yoo YJ. Effects of continuous and interrupted orthodontic force on interleukin-1beta and prostaglandin E2 production in gingival crevicular fluid. Am J Orthod Dentofacial Orthop. 2004; Feb 125(2):168-77.
23. Klein-Nulend J, Bacabac RG, Mullender MG. Mechanobiology of bone tissue. Pathol Biol 2005; Dec 53 (10):576-580.
24. Ren Y, Vissink A. Cytokines in crevicular fluid and orthodontic tooth movement Eur J Oral Sci, 2008; Apr 116 (2): 89-97.
25. Sari E, Ölmez H, Gürton AU. Comparison of some effects of acetylsalicylic acid and rofecoxib during orthodontic tooth movement. Am J Orthod Dentofacial Orthop 2004; Mar 125 (3): 310-315.

Corresponding author:

Debora Pallos

Rua Ásia, 173

São Paulo - SP - Brazil

CEP: 05413-030

E-mail:

dpallos@netpoint.com.br

Publication Dates

Publication in this collection
24 Mar 2010
Date of issue
Mar 2010

History

Received
18 Sept 2009
Accepted
20 Dec 2009

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

[1] 1. Griffiths GS. Formation, collection and significance of gingival crevice fluid. Periodontol 2000 2003; 31(1): 32-42.

[2] 2. Offenbacher S, Odle BM, Van Dyke TE. The use of crevice fluid prostaglandin E₂ levels as a predictor of periodontal attachment loss. J Periodontal Res 1986; Mar 21(2):101-12.

[3] 3. Roberts WE, Huja SS, Roberts JA. Bone modeling: biomechanics, molecular mechanisms, and clinical perspectives. Semin Orthod 2004; Jun 10(2):123-161.

[4] 4. Uitto VJ. Gingival crevice fluid- an introduction. Periodontol 2000 2003; Jan 31(1):9-11.

[5] 5. Ren Y, Hazemeijer H, Haan B, Qu N, Vos P. Cytokine profiles in crevice fluid during orthodontic tooth movement of short and long durations. J Periodontol 2007; Mar 78 (3):453-458.

[6] 6. Coetzee M, Haag M, Claassen N, Kruger MC. Stimulation of prostaglandin E2 (PGE2) production by arachidonic acid, oestrogen and parathyroid hormone in MG-63 and MC3T3-E1 osteoblast-like cells. Prostaglandins Leukot Essent Fatty Acids 2005; Dec 73(6): 423-430.

[7] 7. Grieve WG, Johnson GK, Moore RN, Reinhardt RA, Dubois LM. Prostaglandin E (PGE) and interleukin-1β (IL-1β) levels in gingival crevicular fluid during human orthodontic tooth movement. Am J Orthod Dentofacial Orthop 1994; Apr 105 (4):3 69-374.

[8] 8. Mitsui N, Suzuki N, Maeno M, Mayahara K, Yanagisawa M, Otsuka K, Shimizu N. Optimal compressive force induces bone formation via increasing bone sialoprotein and prostaglandin E₂ production appropriately. Life Sci 2005; Nov 77(25): 3168-3182.

[9] 9. Saito M, Saito S, Ngan PW, Shanfeld J, Davidovitch Z. Interleukin 1 beta and prostaglandin E are involved in the response of periodontal cells to mechanical stress in vivo and in vitro Am J Orthod Dentofacial Orthop 1991; Mar 99 (3): 226-240.

[10] 10. Sodek J, Mckee MD. Molecular and cellular biology of alveolar bone. Periodontol 2000 2000; Oct 24 (1):99-126.

[11] 11. Ren Y, Maltha JC, Van't Hof MA, Von Den Hoff JW, Kuijpers-Jagtman AM, Zhang D. Cytokine levels in crevice fluid are less responsive to orthodontic force in adults than in juveniles. J Clin Periodontol 2002; Aug 29(8): 757762.

[12] 12. Van Dyke TE, Sheilesh D. Risk factors for periodontitis. J Int Acad Periodontol 2005;Jan 7 (1):3-7.

[13] 13. Shimizu N, Yamaguchi M, Uesu K, Goseki T, Abiko Y. Stimulation of prostaglandin E2 and interleukin-1beta production from old rat periodontal ligament cells subjected to mechanical stress. J Gerontol A Biol Sci Med Sci. 2000; Oct 55(10):B489-95.

[14] 14. Burke JC, Evans CA, Crosby TR, Mednieks MI. . Expression of secretory proteins in oral fluid after orthodontic tooth movement. Am J Orthod Dentofacial Orthop 2002; Mar 121(3): 310-315.

[15] 15. Davidovitch Z. Tooth movement. Crit Rev Oral Biol Med 1991; 2(4): 411-450.

[16] 16. Kavadia-Tsatala S, Kaklamanos EG, Tsalikis L. Effects of orthodontic treatment on gingival crevicular fluid flow rate and composition: Clinical implications and applications. Int J Adult Orthodon Orthognath Surg 2002; Fall 17(3):191-205.

[17] 17. Löe H, Silness J. Periodontal disease in pregnancy. I. Prevalence and Severity Acta Odontol Scand Dec 1963; 21; 533-51

[18] 18. Silness J, Löe H. Periodontal disease in pregnancy. II. Correlation between oral hygiene and periodontal condtion. Acta Odontol Scand 1964; Fev 22: 121-35.

[19] 19. Ohzeki K, Yamaguchi M, Shimizu N, Abiko Y. Effect of cellular aging on the induction of cyclooxygenase-2 by mechanical stress in human periodontal ligament cells. Mech Ageing Dev 1999; May 108 (2): 151-163.

[20] 20. Tsai CC, Hong YC, Chen CC, Wu YM. Measurement of prostaglandin E₂ and leukotriene B₄ in the gingival crevice fluid. J Dent 1998; Mar 26 (2): 97-103.

[21] 21. Sari E, Olmez H, Gürton AU. Comparison of some effects of acetylsalicylic acid and rofecoxib during orthodontic tooth movement. Am J Orthod Dentofacial Orthop. 2004 Mar;125(3):310-5.

[22] 22. Lee KJ, Park YC, Yu HS, Choi SH, Yoo YJ. Effects of continuous and interrupted orthodontic force on interleukin-1beta and prostaglandin E2 production in gingival crevicular fluid. Am J Orthod Dentofacial Orthop. 2004; Feb 125(2):168-77.

[23] 23. Klein-Nulend J, Bacabac RG, Mullender MG. Mechanobiology of bone tissue. Pathol Biol 2005; Dec 53 (10):576-580.

[24] 24. Ren Y, Vissink A. Cytokines in crevicular fluid and orthodontic tooth movement Eur J Oral Sci, 2008; Apr 116 (2): 89-97.

[25] 25. Sari E, Ölmez H, Gürton AU. Comparison of some effects of acetylsalicylic acid and rofecoxib during orthodontic tooth movement. Am J Orthod Dentofacial Orthop 2004; Mar 125 (3): 310-315.

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Juveniles versus adults: differences in PGE2 levels in the gingival crevicular fluid during orthodontic tooth movement

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History