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Article

Relationship between Acute Phase of Chronic Periodontitis and Meteorological Factors in the Maintenance Phase of Periodontal Treatment: A Pilot Study

1
Departments of Preventive Dentistry, Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, 2-5-1 Shikata-cho, Kita-ku, Okayama 700-8558, Japan
2
Advanced Research Center for Oral and Craniofacial Sciences, Okayama University Dental School, 2-5-1 Shikata-cho, Kita-ku, Okayama 700-8558, Japan
*
Author to whom correspondence should be addressed.
Int. J. Environ. Res. Public Health 2015, 12(8), 9119-9130; https://doi.org/10.3390/ijerph120809119
Submission received: 3 July 2015 / Revised: 27 July 2015 / Accepted: 31 July 2015 / Published: 5 August 2015

Abstract

:
The acute phase of chronic periodontitis may occur even in patients during supportive periodontal therapy. However, the details are not fully understood. Since the natural environment, including meteorology affects human health, we hypothesized that weather conditions may affect occurrence of acute phase of chronic periodontitis. The aim of this study was to investigate the relationship between weather conditions and acute phase of chronic periodontitis in patients under supportive periodontal therapy. Patients who were diagnosed with acute phase of chronic periodontitis under supportive periodontal therapy during 2011–2013 were selected for this study. We performed oral examinations and collected questionnaires and meteorological data. Of 369 patients who experienced acute phase of chronic periodontitis, 153 had acute phase of chronic periodontitis without direct-triggered episodes. When using the autoregressive integrated moving average model of time-series analysis, the independent covariant of maximum hourly range of barometric pressure, maximum hourly range of temperature, and maximum daily wind speed were significantly associated with occurrence of acute phase of chronic periodontitis (p < 0.05), and 3.1% of the variations in these occurrence over the study period were explained by these factors. Meteorological variables may predict occurrence of acute phase of chronic periodontitis.

1. Introduction

Periodontitis is one of the most widespread chronic diseases and is characterized by gingival bleeding, periodontal pocket formation, destruction of connective tissue attachment, and alveolar bone resorption. Based on a Japanese national survey, 42.5% of Japanese exhibited periodontitis [1]. The primary etiological agent for periodontitis is dental plaque bacteria [2,3]. The majority of periodontal tissue destruction is caused by abnormal host responses to these microorganisms and their products [4,5].
For the long-term stability of successfully treated periodontitis, supportive periodontal therapy (periodontal maintenance) is needed and is regarded as an integral part of overall periodontal management [6,7,8]. Although dentists have been making every effort to maintain periodontal health and prevent tooth loss during supportive periodontal therapy, acute phase of chronic periodontitis may occur in patients and has been regarded as one of the possible complications of supportive periodontal therapy [9]. A review [10] suggested that there were intraoral risk factors related to acute phase of chronic periodontitis. However, clinicians sometimes encounter patients suffering from periodontal abscess without any intraoral factors. Therefore, there may be a relationship between acute phase of chronic periodontitis and extraoral factors.
The natural environment including meteorology affects human health. Weather conditions have been found to be related to blood pressure [11,12,13], myocardial infarction [14,15], heatstroke [16], stroke [17], paediatric trauma [18], mortality [19], asthma [20,21], depression [22,23], rheumatoid arthritis [24,25], and pain in general [26]. In dentistry, some recent research suggests that meteorology is related to temporomandibular disorders [27] and oral pain [28].
Based on these findings, we hypothesized that weather conditions may cause occurrence of acute phase of chronic periodontitis. The aim of this study was to investigate the relationship between weather conditions and occurrence of acute phase of chronic periodontitis in patients under supportive periodontal therapy. Since meteorological variables influence one another [29], we chose temperature, rainfall, barometric pressure, wind speed, hours of sunlight, and humidity as meteorological variables.

2. Methods

2.1. Study Population

This study was performed at the Preventive Dentistry clinic in Okayama University Hospital in Japan from November 2011 to November 2013. In the clinic, all patients received supportive periodontal therapy that included non-surgical periodontal therapy consisting of oral examination, oral hygiene instructions, supra/sub-gingival debridement and scaling, and root-planing every 3–4 months [30]. The patients who were diagnosed with acute phase of chronic periodontitis under supportive periodontal therapy were selected for this study. Criteria for the acute phase of chronic periodontitis included at least two of the following clinical signs or symptoms; pain, swelling, redness or a feeling of warmth in the periodontal lesion [31,32]. Exclusion criteria were as follows: patients who had cancer, hospitalized patients, and patients with missing data. The patients who lived outside of Okayama’s local meteorological area were also excluded. This study was approved by the Ethics Committee of Okayama University Hospital (No. 502, 692). After obtaining written informed consent, the dentists completed a detailed medical questionnaire and oral examination as follows.

2.2. Oral Examination

All clinical procedures were performed by four trained and calibrated dentists (T.T., M.M., D.E., and N.T.). To distinguish other diseases including apical periodontitis, tooth fracture and trauma, acute phase of chronic periodontitis were confirmed by X-ray and or oral examination.

2.3. Questionnaires

The dentists took the history of acute phase of chronic periodontitis. They collected information about the date, place, and possible trigger that the patients were aware of, and any acute symptoms, such as physical stress, mental stress, occlusal trauma, insufficiency for oral hygiene, and so on. When the patients could not identify the trigger clearly and dentists could not determine the clinical factors affecting acute phase of chronic periodontitis, such cases were defined as acute phase of chronic periodontitis without direct-triggered episodes.

2.4. Meteorological Measurements

Meteorological data were acquired from the local meteorological office at Okayama City. The data included the following: (1) mean daily wind speed (m/s), (2) maximum daily wind speed (m/s), (3) minimum daily wind speed (m/s), (4) mean daily barometric pressure (hPa), (5) maximum daily barometric pressure (hPa), (6) minimum daily barometric pressure (hPa), (7) daily range of barometric pressure (hPa), (8) maximum hourly increase in barometric pressure (hPa), (9) maximum hourly decrease in barometric pressure (hPa), (10) total hours of sunlight, (11) total daily rainfall (mm), (12) mean daily temperature (°C), (13) maximum daily temperature (°C), (14) minimum daily temperature (°C), (15) daily range of temperature (°C), (16) maximum hourly increase in temperature (°C), (17) maximum hourly decrease in temperature (°C), (18) mean daily humidity (%), (19) maximum daily humidity (%), (20) minimum daily humidity (%), and (21) daily humidity range [29].

2.5. Statistical Analysis

A multivariate autoregressive integrated moving average model (ARIMA) was performed to identify whether meteorological variables might predict occurrence of acute phase of chronic periodontitis using Box-Jenkins methodology [29,33]. Models were identified by determining ARIMA model orders (p, d, q) using autocorrelation and partial autocorrelation. The model parameters were estimated by the unconditional least squares method. Finally, the adequacy of the model was checked and statistical significance of the parameters determined [33]. After identifying the multivariate transfer function models, the cross-correlation function was determined by estimating the correlations between occurrence of acute phase of chronic periodontitis at different time lags and metrological valuables. The final model was determined by the highest biological plausibility and determination coefficient (r2). All data were analyzed using the Statistical Package for the Social Sciences (21.0J for Windows; SPSS Japan, Tokyo, Japan). Values of p < 0.05 were considered to represent statistically significant differences.

3. Results

Table 1 presents the characteristics of the study population. Of a total of 20,034 patients who had received supportive periodontal therapy at the hospital clinic, 369 patients developed acute phase of chronic periodontitis (1.84% of all patients). The number of acute phase of chronic periodontitis without direct-triggered episodes was 153 (0.76%) and the mean age of patients was 68.7 years (SD = 11.2). The proportion of females was 73.9%.
Table 1. Characteristics of the study population.
Table 1. Characteristics of the study population.
AgeMaleFemaleTotal
Patients Who Had Received Supportive Periodontal Therapy
20–29114138252
30–39135444579
40–494349221356
50–5972622352961
60–69196247666728
70–79184240315873
80–94213432285
Total615513,87920,034
Patients with Acute Phase of Chronic Periodontitis
20–29000
30–39145
40–493912
50–5992534
60–6933114147
70–793489123
80–133548
Total93276369
Patients with Acute Phase of Chronic Periodontitis without Direct-Triggered Episodes
20–29000
30–39022
40–49145
50–596713
60–69104858
70–79184058
80–51217
Total40113153
The mean probing pocket depth at teeth with occurrence of acute phase of chronic periodontitis was 5.1 ± 2.5 mm among patients without direct-triggered episodes. The number of teeth with mobility was 37 (24.2%).
The correlation between occurrence of acute phase of chronic periodontitis without direct-triggered episodes and meteorological parameters is shown in Table 2. Based on the correlation of the results, the final model was predicted using the ARIMA model (Table 3). The independent covariants, namely maximum hourly range (decrease) of barometric pressure, maximum hourly range (increase) of temperature, and maximum daily wind speed were significantly associated with occurrence of acute phase of chronic periodontitis without direct-triggered episodes (p < 0.05). The determination coefficient (r2) of the final model was 0.031% or 3.1% of the variations in occurrence of acute phase of chronic periodontitis without direct-triggered episodes over the study period were explained by the factors included in the model.
Table 2. Significant cross correlations with acute phase of chronic periodontitis without direct-triggered episodes.
Table 2. Significant cross correlations with acute phase of chronic periodontitis without direct-triggered episodes.
ParameterrP Value
Wind speed (m/s)
Mean daily wind speed0.062<0.001
Maximum daily wind speed−0.0150.027
Minimum daily wind speedOmitted
Barometric pressure (hPa)
Mean daily barometric pressureOmitted
Maximum daily barometric pressureOmitted
Minimum daily barometric pressureOmitted
Daily range of barometric pressure0.019<0.001
Maximum hourly increase in barometric pressure0.1330.002
Maximum hourly decrease in barometric pressure0.099<0.001
Total hours of bright daily sunshine (h)Omitted
Total daily rainfall (mm)Omitted
Temperature (°C)
Mean daily temperature−0.0050.015
Maximum daily temperature−0.0050.009
Minimum daily temperature−0.0040.015
Daily range of temperatureOmitted
Maximum hourly increase in temperature−0.050.018
Maximum hourly decrease in temperatureOmitted
Humidity (%)
Mean daily humidityOmitted
Maximum daily humidityOmitted
Minimum daily humidityOmitted
Daily humidity rangeOmitted
Table 3. Multivariate time-series analysis model for acute phase of chronic periodontitis without direct-triggered episodes (r2 = 0.031).
Table 3. Multivariate time-series analysis model for acute phase of chronic periodontitis without direct-triggered episodes (r2 = 0.031).
TermLag Time aCoefficient (S.E.) bT RatioP Value
Maximum hourly decrease in barometric pressure20.098 (0.031)3.1560.002
Maximum hourly increase in temperature10.046 (0.018)2.4730.014
Maximum daily wind speed3−0.015 (0.006)−2.5010.013
a Represents the delay necessary to observe the effect (in days).b Indicates the size and the direction of the effect.

4. Discussion

To the best of our knowledge, this is the first epidemiological study to assess the relationship between occurrence of acute phase of chronic periodontitis and meteorological variables during the maintenance phase of periodontal treatment. In this study, ARIMA model analysis showed that maximum hourly decrease in barometric pressure, maximum hourly increase in temperature, and maximum daily wind speed were significantly associated with occurrence of acute phase of chronic periodontitis. In this model, 3.1% of the variations in occurrence of acute phase of chronic periodontitis over the study period were explained by these factors. Our results provide new findings in the acute phase of chronic periodontitis development. In addition, occurrence of acute phase of chronic periodontitis seems to occur one to three days after changes in meteorological variables. It is feasible that there is a response time lag in which meteorological variables induce pathological changes in periodontal tissue. In the occurrence of acute phase of chronic periodontitis, the first step may be the invasion of bacteria into the soft tissues surrounding the periodontal pocket, which will develop an inflammatory process [34]. Bacterial pathogens attract inflammatory cells to induce chemokines and cytokines, and modulate the inflammatory response during 2–72 h [35,36,37,38]. These findings might support the time lag.
In this study, maximum hourly decrease in barometric pressure was related to occurrence of acute phase of chronic periodontitis. A case report suggested that sudden decreases in barometric pressure when on an airplane can influence the disease activity of patients with acute apical periodontitis [39], which supports our findings. Barometric pressure may have an effect on myopia [40], passenger discomfort on aircrafts [41], sleep disordered breathing [42], deep venous thrombosis [43], and oral pain [28,44]. In an animal model, decreases in barometric pressure induce pain and increase blood pressure and heart rate, suggesting the direct effects of barometric pressure on sympathetic nerve activity and the indirect effects of activation of the peripheral nociceptive and/or mechano-receptive fibers [45]. Although it is difficult to explain the relationship between barometric pressure and occurrence of acute phase of chronic periodontitis, there may be a possible mechanism or hormonal changes [46]. Decreases in barometric pressure possibly modulate the environment of hormones such as adrenaline [46]. Some hormones have direct effects on the growth of periodontitis-related bacteria in vitro [47]. Thus, decreases in barometric pressure might indirectly contribute to occurrence of acute phase of chronic periodontitis. However, further studies are required.
Changes in temperatures contribute to the observed temperature-related mortality [48,49,50,51] and increased cardiovascular and respiratory risk [52,53]. Occurrence of acute phase of chronic periodontitis was also related to maximum hourly increase in temperature in this study. Changes in temperature can control blood biomarkers. For example, cumulative increases in fibrinogen and plasminogen activator inhibitor type 1 in diabetes patients are observed in association with a 5 °C temperature decrement [54]. It is also known that increased C-reactive protein and interleukin-6 occur with a 10 °C temperature decrement [55]. Therefore, the inflammatory process in periodontal tissue may be partially affected by the temperature-related changes in blood biomarkers. Further studies are required to explore the exact mechanisms that promote the association between occurrence of acute phase of chronic periodontitis and changes in temperature.
Wind speed may have an indirect effect on the severity and frequency of air pollution occurrence in respiratory allergic disease [56]. It is also reported that higher wind speed provides a small increase in the risk of back pain [57]. In the present study, occurrence of acute phase of chronic periodontitis was negatively related to maximum daily wind speed. This supports the concept that not only barometric pressure and temperature but also wind speed can affect health, including periodontal condition.
The present comprehensive epidemiological study describes the influence of changes in meteorological valuables on occurrence of acute phase of chronic periodontitis and yields evidence that this can be a phenomenon of everyday life. It is commonly accepted that the weather itself may influence the well-being of individuals. Therefore, dentists should be aware of the relationship and inform their patients about the weather being one of the probable reasons for certain complaints.
In this study, the acute phase of chronic periodontitis during supportive periodontal therapy was 1.84% of all patients. Previous studies report that the prevalence of periodontal abscess is 1.04%–27.5% [34,58,59,60,61,62]. The prevalence in this study was within the range, which suggests that participants were not limited to a specific group and the results may be generalized to a various populations.
Our study has some limitations. First, the experimental period (two years) may be too short to investigate the seasonal effects. A long-term study will be required to clarify it. Second, the number of patients was small in this study. Future study needs a large number of patients. Third, meteorological data were only acquired from one area. Because other areas where occurrence occurred were quite few, we selected cases in a limited area. A multicenter study including more areas will be required. Fourth, 3.1% of the variations in occurrence of acute phase of chronic periodontitis without direct-triggered episodes were explained by meteorological factors. However, since 41.4% of occurrence was of unknown origin in this study, other explanation such as a minor shift in the microorganisms should be considered. Further studies are needed to clarify the details of acute phase of chronic periodontitis without direct-triggered episodes.

5. Conclusions

Maximum hourly decrease in barometric pressure, maximum hourly increase in temperature, and maximum daily wind speed were significantly associated with occurrence of acute phase of chronic periodontitis without direct-triggered episodes. In the model, 3.1% of the variations in the occurrence of acute phase of chronic periodontitis over the study period could be explained by these factors.

Acknowledgments

The authors are grateful to Keiko Kimura for data analysis. This work was supported by Grants-in-Aid for Scientific Research (No. 40157904 and No. 25670892) from the Ministry of Education, Culture, Sports, Science and Technology, Tokyo, Japan.

Author Contributions

N.T., D.E., T.T. and M.M. conceived and planned the project and wrote the manuscript. They also conducted oral examinations. N.T. performed data entry and conducted statistical analysis.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Ojima, M.; Hanioka, T.; Tanaka, K.; Inoshita, E.; Aoyama, H. Relationship between smoking status and periodontal conditions: Findings from national databases in Japan. J. Periodont. Res. 2006, 41, 573–579. [Google Scholar] [CrossRef] [PubMed]
  2. Madianos, P.N.; Bobetsis, Y.A.; Kinane, D.F. Generation of inflammatory stimuli: How bacteria set up inflammatory responses in the gingiva. J. Clin. Periodontol. 2005, 32, 57–71. [Google Scholar] [CrossRef] [PubMed]
  3. Colombo, A.P.; Boches, S.K.; Cotton, S.L.; Goodson, J.M.; Kent, R.; Haffajee, A.D.; Socransky, S.S.; Hasturk, H.; van Dyke, T.E.; Dewhirst, F.; et al. Comparisons of subgingival microbial profiles of refractory periodontitis, severe periodontitis, and periodontal health using the human oral microbe identification microarray. J. Periodontol. 2009, 80, 1421–1432. [Google Scholar] [CrossRef] [PubMed]
  4. Page, R.C.; Kornman, K.S. The pathogenesis of human periodontitis: An introduction. Periodontology 2000 1997, 14, 9–11. [Google Scholar] [CrossRef] [PubMed]
  5. Benakanakere, M.; Kinane, D.F. Innate cellular responses to the periodontal biofilm. Front. Oral Biol. 2012, 15, 41–55. [Google Scholar] [PubMed]
  6. Parameter on periodontal maintenance. American Academy of Periodontology. J. Periodontol. 2000, 71, 849–850.
  7. Cohen, R.E. Research, Science and Therapy Committee, American Academy of Periodontology. Position paper: Periodontal maintenance. J. Periodontol. 2003, 74, 1395–1401. [Google Scholar] [PubMed]
  8. Gaunt, F.; Devine, M.; Pennington, M.; Vernazza, C.; Gwynnett, E.; Steen, N.; Heasman, P. The cost-effectiveness of supportive periodontal care for patients with chronic periodontitis. J. Clin. Periodontol. 2008, 35, 67–82. [Google Scholar] [CrossRef] [PubMed]
  9. Silva, G.L.; Soares, R.V.; Zenóbio, E.G. Periodontal abscess during supportive periodontal therapy: A review of the literature. J. Contemp. Dent. Pract. 2008, 9, 82–91. [Google Scholar] [PubMed]
  10. Herrera, D.; Roldán, S.; Sanz, M. The periodontal abscess: A review. J. Clin. Periodontol. 2000, 27, 377–386. [Google Scholar] [CrossRef] [PubMed]
  11. Argilés, A.; Mourad, G.; Mion, C. Seasonal changes in blood pressure in patients with end-stage renal disease treated with hemodialysis. N. Engl. J. Med. 1998, 339, 1364–1370. [Google Scholar] [CrossRef] [PubMed]
  12. Modesti, P.A.; Morabito, M.; Bertolozzi, I.; Massetti, L.; Panci, G.; Lumachi, C.; Giglio, A.; Bilo, G.; Caldara, G.; Lonati, L.; et al. Weather-related changes in 24-hour blood pressure profile: effects of age and implications for hypertension management. Hypertension 2006, 47, 155–161. [Google Scholar] [CrossRef] [PubMed]
  13. Morabito, M.; Crisci, A.; Orlandini, S.; Maracchi, G.; Gensini, G.F.; Modesti, P.A. A synoptic approach to weather conditions discloses a relationship with ambulatory blood pressure in hypertensives. Am. J. Hypertens. 2008, 21, 748–752. [Google Scholar] [CrossRef] [PubMed]
  14. Ruhenstroth-Bauer, G.; Baumer, H.; Burkel, E.M.; Sönning, W.; Filipiak, B. Myocardial infarction and the weather: A significant positive correlation between the onset of heart infarct and 28 KHz atmospherics—A pilot study. Clin. Cardiol. 1985, 8, 149–151. [Google Scholar] [PubMed]
  15. Morabito, M.; Modesti, P.A.; Cecchi, L.; Crisci, A.; Orlandini, S.; Maracchi, G.; Gensini, G.F. Relationships between weather and myocardial infarction: A biometeorological approach. Int. J. Cardiol. 2005, 105, 288–293. [Google Scholar] [CrossRef] [PubMed]
  16. Shanks, N.J.; Papworth, G. Environmental factors and heatstroke. Occupational Med. 2001, 51, 45–49. [Google Scholar] [CrossRef]
  17. Ohshige, K.; Hori, Y.; Tochikubo, O.; Sugiyama, M. Influence of weather on emergency transport events coded as stroke: Population-based study in Japan. Int. J. Biometeorol. 2006, 50, 305–311. [Google Scholar] [CrossRef] [PubMed]
  18. Macgregor, D.M. Effect of weather on attendance with injury at a paediatric emergency department. Emerg. Med. J. 2003, 20, 204–205. [Google Scholar] [CrossRef] [PubMed]
  19. Plavcová, E.; Kyselý, J. Relationships between sudden weather changes in summer and mortality in the Czech Republic, 1986–2005. Int. J. Biometeorol. 2010, 54, 539–551. [Google Scholar] [CrossRef] [PubMed]
  20. Hanashiro, K.; Tamaki, N.; Kosugi, T.; Kakazu, T.; Kaneshima, H.; Saito, A. The correlation between the outbreaks of asthma attack and meteorologic parameters in Okinawa. Arerugi 1998, 47, 434–448. [Google Scholar] [PubMed]
  21. Suarez-Varela, M.M.; Alvarez, L.G.M.; Kogan, M.D.; Gonzalez, A.L.; Gimeno, A.M.; Ontoso, I.A.; Diaz, C.G.; Pena, A.A.; Aurrecoechea, B.D.; Monge, R.M.B.; et al. Climate and prevalence of atopic eczema in 6- to 7-year-old school children in Spain. ISAAC Phase Ш. Int. J. Biometeorol. 2008, 52, 833–840. [Google Scholar] [CrossRef] [PubMed]
  22. Yang, A.C.; Huang, N.E.; Peng, C.-K.; Tsai, S.-J. Do seasons have an influence on the incidence of depression? The use of an internet search engine query data as a proxy of human affect. PLoS One 2010, 5, e13728. [Google Scholar] [CrossRef] [PubMed]
  23. Henríquez-Sánchez, P.; Doreste-Alonso, J.; Martínez-González, M.A.; Bes-Rastrollo, M.; Gea, A.; Sánchez-Villegas, A. Geographical and climatic factors and depression risk in the SUN project. Eur. J. Public Health 2014, 24, 626–631. [Google Scholar] [CrossRef] [PubMed]
  24. Drane, D.; Berry, G.; Bieri, D.; McFarlane, A.C.; Brooks, P. The association between external weather conditions and pain and stiffness in women with rheumatoid arthritis. J. Rheumatol. 1997, 24, 1309–1316. [Google Scholar] [PubMed]
  25. Strusberg, I.; Mendelberg, R.C.; Serra, H.A.; Strusberg, A.M. Influence of weather conditions on rheumatic pain. J. Rheumatol. 2002, 29, 335–338. [Google Scholar] [PubMed]
  26. Macfarlane, T.V.; McBeth, J.; Jones, G.T.; Nicholl, B.; Macfarlane, G.J. Whether the weather influences pain? Results from the EpiFunD study in North West England. Rheumatology 2010, 49, 1513–1520. [Google Scholar] [CrossRef] [PubMed]
  27. Edefonti, V.; Bravi, F.; Cioffi, I.; Capuozzo, R.; Ammendola, L.; Abate, G.; Decarli, A.; Ferraroni, M.; Farella, M.; Michelotti, A. Chronic pain and weather conditions in patients suffering from temporomandibular disorders: a pilot study. Community Dent. Oral Epidemiol. 2012, 40, 56–64. [Google Scholar] [CrossRef] [PubMed]
  28. Kloss-Brandstätter, A.; Hächl, O.; Leitgeb, P.C.; Buchner, A.; Coassin, S.; Rasse, M.; Kronenberg, F.; Kloss, F.R. Epidemiologic evidence of barometric pressure changes inducing increased reporting of oral pain. Eur. J. Pain 2011, 15, 880–844. [Google Scholar] [CrossRef] [PubMed]
  29. McWilliams, S.; Kinsella, A.; O’Callaghan, E. The effects of daily weather variables on psychosis admissions to psychiatric hospitals. Int. J. Biometeorol. 2013, 57, 497–508. [Google Scholar] [CrossRef] [PubMed]
  30. Machida, T.; Tomofuji, T.; Ekuni, D.; Yamane, M.; Yoneda, T.; Kawabata, Y.; Kataoka, K.; Tamaki, N.; Morita, M. Longitudinal relationship between plasma reactive oxygen metabolites and periodontal condition in the maintenance phase of periodontal treatment. Dis. Markers 2014, 2014. [Google Scholar] [CrossRef] [PubMed]
  31. Armitage, G.C. Development of a classification system for periodontal diseases and conditions. Ann. Periodontol. 1999, 4, 1–6. [Google Scholar] [CrossRef] [PubMed]
  32. Tomita, S.; Kasai, S.; Imamura, K.; Ihara, Y.; Kita, D.; Ota, K.; Sekino, J.; Nakagawa, T.; Saito, A. Changes in antimicrobial susceptibility profile and prevalence of quinolone low-sensitive strains in subgingival plaque from acute periodontal lesions after systemic administration of sitafloxacin. Microb. Pathog. 2015, 79, 41–46. [Google Scholar] [CrossRef] [PubMed]
  33. Aldeyab, M.A.; Harbarth, S.; Vernaz, N.; Kearney, M.P.; Scott, M.G.; DarwishElhajji, F.W.; Aldiab, M.A.; McElnay, J.C. The impact of antibiotic use on the incidence and resistance pattern of extended-spectrum beta-lactamase-producing bacteria in primary and secondary healthcare settings. Br. J. Clin. Pharmacol. 2012, 74, 171–179. [Google Scholar] [CrossRef] [PubMed]
  34. Herrera, D.; Alonso, B.; de Arriba, L.; Santa Cruz, I.; Serrano, C.; Sanz, M. Acute periodontal lesions. Periodontology 2000 2014, 65, 149–177. [Google Scholar] [CrossRef] [PubMed]
  35. Zhou, Q.; Amar, S. Identification of proteins differentially expressed in human monocytes exposed to Porphyromonas gingivalis and its purified components by high-throughput immunoblotting. Infect. Immun. 2006, 74, 1204–1214. [Google Scholar] [CrossRef] [PubMed]
  36. Gokyu, M.; Kobayashi, H.; Nanbara, H.; Sudo, T.; Ikeda, Y.; Suda, T.; Izumi, Y. Thrombospondin-1 production is enhanced by Porphyromonas gingivalis lipopolysaccharide in THP-1 cells. PLoS One 2014, 9, e115107. [Google Scholar] [CrossRef] [PubMed]
  37. Barksby, H.E.; Nile, C.J.; Jaedicke, K.M.; Taylor, J.J.; Preshaw, P.M. Differential expression of immunoregulatory genes in monocytes in response to Porphyromonas gingivalis and escherichia coli lipopolysaccharide. Clin. Exp. Immunol. 2009, 156, 479–487. [Google Scholar] [CrossRef] [PubMed]
  38. Thurnheer, T.; Belibasakis, G.N.; Bostanci, N. Colonisation of gingival epithelia by subgingival biofilms in vitro: Role of “red complex” bacteria. Arch Oral Biol. 2014, 59, 977–986. [Google Scholar] [CrossRef] [PubMed]
  39. Hodges, F.R. Barodontalgia at 12,000 feet. J. Am. Dent. Assoc. 1978, 97, 66–68. [Google Scholar] [CrossRef] [PubMed]
  40. Fledelius, H.C. High atmospheric pressure and myopic shift in caisson workers. Lancet 2003, 361, 362. [Google Scholar] [CrossRef]
  41. Muhm, J.M.; Rock, P.B.; McMullin, D.L.; Jones, S.P.; Lu, I.L.; Eilers, K.D.; Space, D.R.; McMullen, A. Effect of aircraft-cabin altitude on passenger discomfort. N. Engl. J. Med. 2007, 357, 18–27. [Google Scholar] [CrossRef] [PubMed]
  42. Doherty, M.J.; Youn, C.E.; Haltiner, A.M.; Watson, N.F. Do weather-related ambient atmospheric-pressure changes influence sleep disordered breathing? J. Clin. Sleep Med. 2010, 6, 152–156. [Google Scholar] [PubMed]
  43. Brown, H.K.; Simpson, A.J.; Murchison, J.T. The influence of meteorological variables on the development of deep venous thrombosis. Thromb. Haemost. 2009, 102, 676–682. [Google Scholar] [PubMed]
  44. Zadik, Y. Barodontalgia. J. Endod. 2009, 35, 481–485. [Google Scholar] [CrossRef] [PubMed]
  45. Sato, J.; Takanari, K.; Omura, S.; Mizumura, K. Effects of lowering barometric pressure on guarding behavior, heart rate and blood pressure in a rat model of neuropathic pain. Neurosci. Lett. 2001, 299, 17–20. [Google Scholar] [CrossRef]
  46. Funakubo, M.; Sato, J.; Honda, T.; Mizumura, K. The inner ear is involved in the aggravation of nociceptive behavior induced by lowering barometric pressure of nerve injured rats. Eur. J. Pain. 2010, 14, 32–39. [Google Scholar] [CrossRef] [PubMed]
  47. Jentsch, H.F.; März, D.; Krüger, M. The effects of stress hormones on growth of selected periodontitis related bacteria. Anaerobe 2013, 24, 49–54. [Google Scholar] [CrossRef] [PubMed]
  48. Analitis, A.; Katsouyanni, K.; Biggeri, A.; Baccini, M.; Forsberg, B.; Bisanti, L.; Kirchmayer, U.; Ballester, F.; Cadum, E.; Goodman, P.G.; et al. Effects of cold weather on mortality: Results from 15 European cities within the PHEWE project. Am. J. Epidemiol. 2008, 168, 1397–1408. [Google Scholar] [CrossRef] [PubMed]
  49. Basu, R. High ambient temperature and mortality: A review of epidemiologic studies from 2001 to 2008. Environ. Health 2009, 8, 40. [Google Scholar] [CrossRef] [PubMed]
  50. Goldberg, M.S.; Gasparrini, A.; Armstrong, B.; Valois, M.F. The short-term influence of temperature on daily mortality in the temperate climate of Montreal, Canada. Environ. Res. 2011, 111, 853–860. [Google Scholar] [CrossRef] [PubMed]
  51. Breitner, S.; Wolf, K.; Devlin, R.B.; Diaz-Sanchez, D.; Peters, A.; Schneider, A. Short-term effects of air temperature on mortality and effect modification by air pollution in three cities of Bavaria, Germany: A time-series analysis. Sci. Total Environ. 2014, 485–486, 49–61. [Google Scholar] [CrossRef] [PubMed]
  52. Koken, P.J.; Piver, W.T.; Ye, F.; Elixhauser, A.; Olsen, L.M.; Portier, C.J. Temperature, air pollution, and hospitalization for cardiovascular diseases among elderly people in Denver. Environ. Health Perspect. 2003, 111, 1312–1317. [Google Scholar] [CrossRef] [PubMed]
  53. Barnett, A.G.; Dobson, A.J.; McElduff, P.; Salomaa, V.; Kuulasmaa, K.; Sans, S. Cold periods and coronary events: An analysis of populations worldwide. J. Epidemiol. Community Health 2005, 59, 551–557. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  54. Schäuble, C.L.; Hampel, R.; Breitner, S.; Rückerl, R.; Phipps, R.; Diaz-Sanchez, D.; Devlin, R.B.; Carter, J.D.; Soukup, J.; Silbajoris, R.; et al. Short-term effects of air temperature on blood markers of coagulation and inflammation in potentially susceptible individuals. Occup. Environ. Med. 2012, 69, 670–678. [Google Scholar] [CrossRef] [PubMed]
  55. Schneider, A.; Panagiotakos, D.; Picciotto, S.; Katsouyanni, K.; Löwel, H.; Jacquemin, B.; Lanki, T.; Stafoggia, M.; Bellander, T.; Koenig, W.; et al. Air temperature and inflammatory responses in myocardial infarction survivors. Epidemiology 2008, 19, 391–400. [Google Scholar] [CrossRef] [PubMed]
  56. D’Amato, G.; Cecchi, L. Effects of climate change on environmental factors in respiratory allergic diseases. Clin. Exp. Allergy 2008, 38, 1264–1274. [Google Scholar] [CrossRef] [PubMed]
  57. Steffens, D.; Maher, C.G.; Li, Q.; Ferreira, M.L.; Pereira, L.S.M.; Koes, B.W.; Latimer, J. Effect of weather on back pain: Results from a case-crossover study. Arthritis Care Res. 2014, 66, 1867–1872. [Google Scholar] [CrossRef] [PubMed]
  58. Ahl, D.R.; Hilgeman, J.L.; Snyder, J.D. Periodontal emergencies. Dent. Clin. North Am. 1986, 30, 459–472. [Google Scholar] [PubMed]
  59. Lewis, M.A.; Meechan, C.; MacFarlane, T.W.; Lamey, P.J.; Kay, E. Presentation and antimicrobial treatment of acute orofacial infections in general dental practice. Br. J. Oral Maxillofac. Surg. 1989, 166, 41–45. [Google Scholar] [CrossRef]
  60. Gray, J.L.; Flanary, D.B.; Newell, D.H. The prevalence of periodontal abscess. J. Indiana Dent. Assoc. 1994, 73, 18–23. [Google Scholar] [PubMed]
  61. Kaldahl, W.B.; Kalkwarf, K.L.; Patil, K.D.; Molvar, M.P.; Dyer, J.K. Long term evaluation of periodontal therapy (I). Response to 4 therapeutic modalities. J. Periodontol. 1996, 67, 93–102. [Google Scholar] [CrossRef] [PubMed]
  62. McLeod, D.E.; Lainson, P.A.; Spivey, J.D. Tooth loss due to periodontal abscess: A retrospective study. J. Periodontol. 1997, 68, 963–966. [Google Scholar] [CrossRef] [PubMed]

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MDPI and ACS Style

Takeuchi, N.; Ekuni, D.; Tomofuji, T.; Morita, M. Relationship between Acute Phase of Chronic Periodontitis and Meteorological Factors in the Maintenance Phase of Periodontal Treatment: A Pilot Study. Int. J. Environ. Res. Public Health 2015, 12, 9119-9130. https://doi.org/10.3390/ijerph120809119

AMA Style

Takeuchi N, Ekuni D, Tomofuji T, Morita M. Relationship between Acute Phase of Chronic Periodontitis and Meteorological Factors in the Maintenance Phase of Periodontal Treatment: A Pilot Study. International Journal of Environmental Research and Public Health. 2015; 12(8):9119-9130. https://doi.org/10.3390/ijerph120809119

Chicago/Turabian Style

Takeuchi, Noriko, Daisuke Ekuni, Takaaki Tomofuji, and Manabu Morita. 2015. "Relationship between Acute Phase of Chronic Periodontitis and Meteorological Factors in the Maintenance Phase of Periodontal Treatment: A Pilot Study" International Journal of Environmental Research and Public Health 12, no. 8: 9119-9130. https://doi.org/10.3390/ijerph120809119

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