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ORIGINAL ARTICLE
Year : 2009  |  Volume : 13  |  Issue : 3  |  Page : 145-149 Table of Contents   

Evaluation of plasma C-reactive protein levels in pregnant women with and without periodontal disease: A comparative study


1 Department of Periodontics, Postgraduate Student, A.B. Shetty Memorial Institute of Dental Sciences, Mangalore, India
2 Professor, A.B. Shetty Memorial Institute of Dental Sciences, Mangalore, India
3 Head and Professor, A.B. Shetty Memorial Institute of Dental Sciences, Mangalore, India

Date of Submission16-Feb-2009
Date of Acceptance14-Sep-2009
Date of Web Publication3-Mar-2010

Correspondence Address:
Anupriya Sharma
Department of Periodontics, A.B.Shetty Memorial Institute of Dental Sciences, Deralakatte, Mangalore, Karnataka - 575 018
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0972-124X.60227

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   Abstract 

Background and Objectives: Circulating C-reactive protein (CRP) levels are a marker of systemic inflammation and are associated with periodontal disease, a chronic bacterial infection associated with elevation of proinflammatory cytokines and prostaglandins. CRP has been associated with adverse pregnancy outcomes, including preterm delivery, preeclampsia, and intrauterine growth restriction. Furthermore, periodontal disease has been associated with increased risk of preterm low birth weight, low birth weight, and preterm birth. The present study was conducted to assess plasma CRP levels in pregnant women with and without periodontal disease; to evaluate the effect of periodontal therapy on the incidence of preterm delivery; and to compare the incidence of preterm delivery in pregnant women with and without periodontal disease. Materials and Methods: A total of 90 pregnant women aged between 18-35 years with gestational age between 12-28 weeks were recruited and divided into three equal groups (control group, study group, treatment group) of 30 each. Blood samples were taken for estimation of C-reactive protein levels from all groups at 12-20 weeks of gestation, determined using ultrasensitive turbidimetric immunoassay (QUANTIA-CRP US). The treatment group comprised plaque control, scaling, and root planning and daily rinsing with 0.2% chlorhexidine mouth before 28 weeks of gestation. Results: The mean value of C-reactive protein levels in subjects with periodontal disease was higher compared to control group i.e., 1.20 ± 0.247 mg/dl and 1.22 ± 0.250 mg/dl, respectively, compared to 0.713 ± 0.139 mg/ dl ( P = 0.001). The mean value of CRP levels before treatment was greater than the mean value after treatment i.e., 1.22 ± 0.25 compared to 0.84 ± 0.189 ( P < 0.001). The incidence of preterm delivery (< 37 weeks) was 31.7% in the periodontal disease group (study group) compared to 8.3% in the control group ( P = 0.001). The incidence of preterm delivery in the treatment group was 15.0% compared to 31.7% in the nontreatment group (study group). Conclusion: The findings from the study suggest that periodontal disease in pregnant women is associated with increased C- reactive protein levels in early pregnancy, incidence of preterm delivery is higher in pregnant women with periodontal disease compared to healthy controls, periodontal therapy during pregnancy reduces plasma CRP levels and there is decrease in incidence of preterm delivery after periodontal therapy.

Keywords: C-reactive protein, periodontal disease, preterm


How to cite this article:
Sharma A, Ramesh A, Thomas B. Evaluation of plasma C-reactive protein levels in pregnant women with and without periodontal disease: A comparative study. J Indian Soc Periodontol 2009;13:145-9

How to cite this URL:
Sharma A, Ramesh A, Thomas B. Evaluation of plasma C-reactive protein levels in pregnant women with and without periodontal disease: A comparative study. J Indian Soc Periodontol [serial online] 2009 [cited 2020 Jul 3];13:145-9. Available from: http://www.jisponline.com/text.asp?2009/13/3/145/60227


   Introduction Top


C-reactive protein (CRP) is an acute phase reactant produced by liver in response to diverse inflammatory stimuli, including heat, trauma, infection, and hypoxia. [1] Circulating CRP levels are a marker of systemic inflammation and are associated with periodontal disease, a chronic bacterial infection associated with elevation of proinflammatory cytokines and prostaglandins. CRP has been associated with adverse pregnancy outcomes, including preterm delivery, [2] preeclampsia, [3] and intrauterine growth restriction. [4] Furthermore, periodontal disease has been associated with increased risk of preterm low birth weight, [5] low birth weight, [6] and preterm birth. [7] Preterm birth is a major medical, social, and economic problem accounting for large proportion of maternal and especially, neonatal mortality and morbidity. Preterm infants are at elevated risk for death, neurodevelopment disabilities, cognitive impairment, and behavioral disorders. Therefore, CRP might be a plausible mediator of the association between periodontitis and adverse pregnancy outcomes. Elevated CRP could amplify the inflammatory response through complement activation, tissue damage, and induction of inflammatory cytokines in the monocytes and therefore may mediate the relationship between periodontitis and adverse pregnancy outcomes. [8] Alternatively, periodontal disease and CRP may share a common risk factor predisposing certain individuals to a hyper inflammatory response.

Objectives

This study was conducted with the following aims:

  1. To assess plasma CRP levels in pregnant women with and without periodontal disease.
  2. To evaluate the effect of periodontal therapy on the incidence of preterm delivery.
  3. To compare the incidence of preterm delivery in pregnant women with and without periodontal disease.

   Materials and Methods Top


Source of data

The study was designed as a prospective cohort study involving a sample size of 90 pregnant women, reporting to the Department of Periodontics, A. B. Shetty Memorial Institute of Dental Sciences and Department of Obstetric and Gynaecology, K. S. Hedge Medical Academy,Deralakatte, Mangalore, divided into three equal groups of 30 each: Group I: Control group, periodontally healthy pregnant women; group II: Study group, pregnant women diagnosed clinically as suffering from periodontal disease; group III: Treatment group, pregnant women diagnosed clinically as suffering from periodontal disease and periodontal therapy was given in second trimester.

Screening examination included: 1) medical history; 2) obstetric history; 3) dental history; 4) Russell's periodontal index.

Criteria for selection

Inclusion criteria

  1. Subjects with age group between 18-35 years.
  2. Subjects in good state of health without systemic disease.
  3. Subjects with gestational age between 12-28 weeks.
  4. Subjects were classified according to following criteria:
    1. Simple gingivitis (Russell's Periodontal Index Score: 0.3-0.9).
    2. Beginning destructive periodontal disease. (Russell's Periodontal Index Score: 0.7-1.9).
    3. Established destructive periodontal disease (Russell's Periodontal Index Score: 1.7-5.0).
  5. Subjects with minimum of 20 sound permanent teeth.
Exclusion criteria

  1. Subjects with systemic disease.
  2. Subjects with history of antibiotic intake during pregnancy.
  3. Subjects with multiple pregnancies.
  4. Subjects with diabetes prior to pregnancy.
  5. Subjects with intention to deliver at hospital other than that of the study.
  6. Other obstetric risk factors like smoking, alcohol consumption, drugs use, etc.
Periodontal disease activity was recorded at baseline for all groups using mouth mirror and UNC-15 probe. Blood samples were taken for estimation of C-reactive protein levels from all groups at 12-20 weeks of gestation. C-reactive protein levels were determined using ultrasensitive turbidimetric immunoassay (QUANTIA-CRP US), with a detection limit of 0.015 mg/dl. Periodontal therapy was done in the treatment group (Group III) consisting of plaque control, scaling and root planning, and daily rinsing with 0.2% chlorhexidine mouth before 28 weeks of gestation. Maintenance therapy was done in the control group (Group I) consisting of oral hygiene instructions and in the treatment group (Group III) consisting of oral hygiene instructions and supragingival plaque removal by instrumentation, as needed given every 2-3 weeks until delivery. Patients not maintaining oral hygiene in group I and group III were excluded from study. Incidence of preterm was compared in all groups.

Data analysis

The data obtained was subjected to statistical analysis using two sample t-test, paired t-test to compare C-reactive protein values in group III before and after treatment, unpaired t-test to compare C-reactive protein values for term and preterm cases in each group, chi-square test to compare the incidence of preterm in different groups, analysis of variance (ANOVA) to determine difference in age and C-reactive protein values in different groups.


   Results Top


In this study, an attempt was made to evaluate the CRP levels in pregnant women with and without periodontal disease and healthy control using ultrasensitive measurement of CRP, with a detection limit of 0.015 mg/dl. There was a statistically significant difference in mean CRP levels in different groups (P = 0.001) [Table 1]a. To further compare which particular pairs of groups were statistically significant, a post-hoc comparison test was carried out. There was a significant difference in group 1 and group 2, group 1 and group 3 (P < .001) but there was no significant difference between group 2 and group 3 (P > 0.05) [Table 1]b. Post-hoc pairwise comparison of adjusted mean showed a significantly higher mean CRP values (1.204 and 1.22) in periodontal disease groups compared to control group (0.713) [Table 1]c. A statistically significant difference was observed in mean value of CRP plasma levels ( P < .001) in group III before and after treatment [Table 2].The mean values of CRP levels in group I subjects with preterm delivery was 0.912 ± 0.697 (mean ± S.D) and term delivery 0.674 ± 0.113 (mean ± S.D). A significant difference was found in mean values of CRP levels ( P < .001) in preterm and term delivery in group I subjects .

The mean value of CRP levels in group II subjects with preterm delivery was 1.30 ± 0.201 (mean ± SD) and normal delivery was 1.037 ± 0.238 (mean ± SD). A significant difference was found in mean values of CRP levels ( P = .003) in preterm and term delivery in group II subjects . The mean values of CRP levels before treatment in group III subjects with preterm delivery was 1.25 ± 0.248 (mean ± SD) and normal delivery was 1.21 ± 0.255 (mean ± SD). There was no significant difference in mean values of CRP levels ( P = 0.653) in preterm and term delivery subjects before treatment. The mean values of CRP levels after treatment in group III subjects with preterm delivery was 0.99 ± 0.167 (mean ± SD) and term delivery was 0.78 ± 0.162 (mean ± SD). A significant difference was found in mean values of CRP levels ( P = .003) in preterm and term delivery subjects after treatment [Table 3]. The incidence of preterm and term delivery in group I was 8.3% and 41.7%, respectively (OR = 0.30, 95% CI = 0.134-0.674); and in group II was 31.7% and 18.3%, respectively (OR = 2.5,95% CI = 1.52-4.41). A significant difference was found in incidence of preterm and term delivery in group I and group II ( P = 0.001) [Table 4]. The incidence of preterm and term delivery in group II was 31.7% and 18.3%, respectively (OR = 1.97, 95% CI = 1.14-3.39) and group III was 15.0% and 35.0%, respectively (OR = 0.49, 95% CI = 0.27-0.88). A significant difference was found in incidence preterm and term delivery in group II and group III (P = 0.010) [Table 5].


   Discussion Top


The results of this cohort study demonstrated the elevated CRP levels in pregnant women with periodontal disease compared to healthy controls and preterm delivery rate was higher in women with periodontal disease compared to control group. Significantly elevated CRP levels were found in subjects with periodontal disease. The results of the study are consistent with outcomes of recent investigations which reported an elevation of CRP levels in periodontitis patients. [9],[10],[11],[12] Several underlying pathogenic mechanism for observation are possible. Periodontal pathogens do not induce only local inflammation and tissue destruction; they are involved in systemic increase in inflammatory and immune response. [13] Low levels of bacteremia, LPS, and other bacterial components may provide a stimulus for systemic inflammatory responses such as increased production of CRP due to activation of the cascade of inflammatory cytokines production by monocytes and other cells in periodontal tissues. [14]

There are very few studies to evaluate the association between periodontal disease and CRP levels in pregnant women. It has been shown that high CRP levels at the beginning of the pregnancy is associated with nearly two-fold increased risk if preterm delivery. [15] Moreover, CRP levels exceeding the threshold were associated with increased risk of preterm delivery. [2] In the present study, the mean value of reported CRP levels correlated with high incidence of preterm delivery. Subjects with preterm delivery have high mean CRP values compared to subjects with normal delivery. Periodontal treatment before 28 weeks of gestation resulted in significant decrease in mean CRP levels. Randomized trials of periodontal treatment have indicated that treatment of periodontal infections can significantly lower serum levels of CRP. [16-19] This study is in support to the reports of previous trails. [16],[17],[18],[19] The data from this study showed that the incidence of preterm delivery was greater in subjects with periodontal disease compared to control group. This association was initially suggested by Offenbacher et al., 1996 and was further confirmed in various other studies. [20] Incidence of preterm delivery in treatment group was 19.0% compared to 31.7% in the study group. There was a significant reduction in incidence after treatment which showed that the treatment resulted in decrease in incidence of preterm delivery. Studies have indicated that periodontal treatment improves periodontal health and is safe, [21],[22],[23] and periodontal treatment reduces the incidence of PT/LBW rate. [24],[17] Results obtained in the present study are consistent with previous studies. [17],[24],[25] In this study, the association observed between CRP and periodontal disease in pregnancy may or may not be causal. Periodontitis may increase CRP levels in pregnancy. CRP could amplify the inflammatory response through complement activation, tissue damage, and induction of inflammatory cytokines in monocytes, [26] and therefore, may mediate the association between periodontitis and adverse pregnancy outcomes. Periodontal treatment resulted in decrease in CRP levels and incidence of preterm delivery. This raises the possibility that CRP may mediate association between periodontal disease and preterm delivery. Further study on the maternal and fetal immune response to chronic oral infection and on placental pathology in women with periodontal disease has to be done to determine whether the relationship between periodontal disease and preterm is causal or simply associative.

However, since there has been no previous report on plasma CRP levels in pregnant women with and without periodontal disease and related incidence of preterm delivery in Indian population, the present study provides ground work data regarding the above correlation and promotes further studies in this direction.


   Acknowledgments Top


We would like to acknowledge the assistance of all the members of department of biochemistry, Fr. Muller medical College and hospital and all the faculty and staff of Department of Obstetrics& Gynecology, KSHEMA.

 
   References Top

1.Pepys MB, Baltz ML. Acute phase proteins with special reference to C-reactive protein and related proteins (pentaxins) and serum amyloid A protein. Adv Immunol 1983;34:141-212.  Back to cited text no. 1      
2.Pitiphat W, Gillman MW, Joshipura KJ, Williams PL, Douglass CW, Rich-Edwards JW. Plasma C-reactive protein in early pregnancy and preterm delivery. Am J Epidemiol 2005;162:1108-113.  Back to cited text no. 2      
3.Teran E, Escudero C, Moya W, Flores M, Vallance P, Lopez-Jaramillo P. Elevated C-reactive protein and pro-inflammatory cytokines in Andean women with pre-eclampsia. Int J Gynaecol Obstet 2001;75:243-9.  Back to cited text no. 3      
4.Tjoa ML, van Vugt JM, Go AT, Blankenstein MA, Oudejans CB, van Wijk IJ. Elevated C-reactive protein levels during first trimester of pregnancy are indicative of preeclampsia and intrauterine growth restriction. J Reprod Immunol 2003;59:29-37.   Back to cited text no. 4      
5.Offenbacher S, Katz V, Fertik G, Collins J, Boyd D, Maynor G, et al. Periodontal infection as a possible risk factor for preterm low birth weight. J Periodontol 1996;67:1103-13.  Back to cited text no. 5      
6.Dasanayake AP. Poor periodontal health of the pregnant woman as a risk factor for low birth weight. Ann Periodontol 1998;3:206-12.  Back to cited text no. 6      
7.Jeffcoat MK, Geurs NC, Reddy MS, Cliver S, Goldenberg RL, Hauth JC. Periodontal infection and preterm birth: Results of a prospective study. J Am Dent Assoc 2001;132:875-80.  Back to cited text no. 7      
8.Cermak J, Key NS, Bach RR, Balla J, Jacob HS, Vercellotti GM. C-reactive protein induces human peripheral blood monocytes to synthesize tissue factor. Blood 1993;82:513-20.  Back to cited text no. 8      
9.Kushner J. The acute phase reactants and erythrocyte sedimentation rate. Text book of rheumatology. Philadelphia: W.B. Saunders Co; 1981. p. 669.  Back to cited text no. 9      
10.Noack B, Genco RJ, Trevisan M, Grossi S, Zambon JJ, de Nardin E. Periodontal infections contribute to elevated systemic C-reactive protein level. J Periodontol 2001;72:1221-7.  Back to cited text no. 10      
11.Salzberg TN, Overstreet BT, Rogers JD, Califano JV, Best AM, Schenkein HA. C-reactive protein levels in patients with aggressive periodontitis. J Periodontol 2006;77:933-9.  Back to cited text no. 11      
12.Paraskevas S, Huizinga JD, Loos BG. Systematic review and meta-analyses on C-reactive protein in relation to periodontitis. J Clin Periodontol 2008;35:277-90.  Back to cited text no. 12      
13.Beck J, Garcia R, Heiss G, Vokonas PS, Offenbacher S. Periodontal disease and cardiovascular disease. J Periodontal 1996;67:1123-37.  Back to cited text no. 13      
14.Noack B, Genco RJ, Trevisan M, Grossi S. Periodontal infections contribute to elevated systemic C-reactive protein level. J Periodontol 2001;72:1221-7.   Back to cited text no. 14      
15.Hvilsom GB, Thorsen P, Jeune B, Bakketeig LS. C-reactive protein: A serological marker for preterm delivery? Acta Obstet Gynecol Scand 2002;81:424-8.  Back to cited text no. 15      
16.Jeffcoat MK, Hauth JC, Geurs NC, Reddy MS, Cliver SP, Hodgkins PM, et al. Periodontal disease and preterm birth: Results of a pilot intervention study. J Periodontol 2003;74:1214-8.  Back to cited text no. 16      
17.Sadatmansouri S, Sedighpoor N. Effects of periodontal treatment phase I on birth term and birth weight. J Indian Soc Pedod Prev Dent 2006;24:23-6.  Back to cited text no. 17  [PUBMED]  Medknow Journal  
18.Ioannidou E, Malekzadeh T, Dongari-Bagtzoglou A. Effect of periodontal treatment on serum C-reactive protein levels: A systematic review and meta-analysis. J Periodontol 2006;77:1635-42.  Back to cited text no. 18      
19.D'Aiuto F, Nibali L, Parkar M, Suvan J, Tonetti MS. Short-term effects of intensive periodontal therapy on serum inflammatory markers and cholesterol. J Dent Res 2005;84:269-73.  Back to cited text no. 19      
20.Lopez NJ, Smith PC, Gutierrez. Higher risk of preterm birth and low birth weight in women with periodontal disease. J Dent R ES 2002;81:58-63.  Back to cited text no. 20      
21.Offenbacher S, Boggess KA, Murtha AP, Jared HL, Lieff S, McKaig RG, et al. Progressive periodontal disease and risk of very preterm delivery. Obstet Gynecol 2006;107:29-36.   Back to cited text no. 21      
22.Michalowicz BS, Hodges JS, DiAngelis AJ, Lupo VR, Novak MJ, Ferguson JE, et al. OPT study. Treatment of periodontal disease and the risk of preterm birth. N Engl J Med 2006;355:1885-94.  Back to cited text no. 22      
23.Lopez R. Periodontal treatment in pregnant women improves periodontal disease but does not alter rates of preterm birth. N Engl J Med 2006;355:1885-94.   Back to cited text no. 23      
24.Lopez NJ, Da Silva I, Ipinza J, Gutierrez J. Periodontal therapy reduces the rate of preterm low birth weight in women with pregnancy-associated gingivitis. J Periodontol 2005;76:2144-53.  Back to cited text no. 24      
25.Lopez NJ, Smith NC, Gutierrez J. Periodontal therapy may reduce the risk of preterm low birth weight in women with periodontal disease: A randomized control trial. J Periodontal 2002;73:911-24.  Back to cited text no. 25      
26.Gabay C, Kushner I. Acute-phase proteins and other systemic responses to inflammation. N Engl J Med 1999;40:448-54.  Back to cited text no. 26      



 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]


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