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Year : 2014  |  Volume : 25  |  Issue : 1  |  Page : 50-53
Periodontal status in infertile women attending in vitro fertilization clinics

Departments of Periodontics and Oral Implantology, GITAM Dental College and Hospital, Visakhapatnam, Andhra Pradesh, India

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Date of Submission20-Feb-2013
Date of Decision10-May-2013
Date of Acceptance19-Jan-2014
Date of Web Publication21-Apr-2014


Background and Aim: Throughout a woman's life, hormonal influences affect therapeutic decision making in periodontics. A woman undergoing infertility treatment is given drugs to stimulate the ovaries, which lead to sustained higher levels of female sex hormones. The differing levels of these hormones, either in infertile women or in women undergoing therapy for infertility or in women who have conceived and delivered naturally could suggest a differing periodontal status amongst these three groups. Hence, this cross-sectional study was undertaken to assess and compare the periodontal status in the above three groups.
Materials and Methods: 180 women including 60 women undergoing treatment for infertility (Group I), 60 women in whom infertility treatment had not yet been initiated (Group II) and 60 women who had conceived and delivered naturally (Group III-control group), of age range 25-35 years, were included. Clinical parameters including oral hygiene index simplified (OHI-S), gingival index, sulcus bleeding index (SBI) and clinical attachment loss (CAL) were assessed by a single examiner.
Results: Despite similar OHI-S scores (P > 0.05) in all groups, women of Group I had significantly higher gingival inflammation and SBI (P < 0.05) as compared to women of Group II and Group III. Furthermore, the women in Group I and Group II had statistically higher CAL (P < 0.05) as compared with the control group.
Conclusion: Within the limits of this study, it can be concluded that altered hormonal levels in infertile women undergoing assisted reproductive therapy and infertile women not undergoing this treatment can lead to increased attachment loss, suggesting that these women may require constant periodontal monitoring.

Keywords: Assisted reproductive therapy, clinical attachment loss, infertility, stress

How to cite this article:
Lalasa G, Murthy KV, Pavankumar S, Raju GR. Periodontal status in infertile women attending in vitro fertilization clinics. Indian J Dent Res 2014;25:50-3

How to cite this URL:
Lalasa G, Murthy KV, Pavankumar S, Raju GR. Periodontal status in infertile women attending in vitro fertilization clinics. Indian J Dent Res [serial online] 2014 [cited 2023 May 29];25:50-3. Available from:
Infertility is defined as the inability to conceive after 12 months of unprotected sexual intercourse. [1] Infertility is perceived as a problem across virtually all cultures and societies and affects an estimated 8-15% of couples of reproductive age. [2] Infertility can be attributed primarily to female factor in 58% couples, male factor in 25% couples and is unexplained in about 17% of couples. [1] This condition may be further classified as primary infertility, in which no previous pregnancies have occurred and secondary infertility, in which a prior pregnancy, although not necessarily a live birth, has occurred. [3]

In recent years, the number of couples seeking treatment for infertility has dramatically increased as a consequence of such as postponement of child bearing, development of newer and more successful techniques for infertility treatment and increasing awareness of available services. The development of assisted reproductive technologies has drastically altered the treatment of male and female infertility. [1] A woman undergoing infertility treatment is mainly given drugs to stimulate the ovaries to produce as many healthy follicles as possible, so as to increase the chances of ovulation and to control the timing of ovulation so that the eggs can be surgically retrieved and used for assisted reproductive therapy. [3],[4],[5]

Medications used for ovulation induction include clomiphene citrate, human chorionic gonadotropins, urofollitropins, menotropins, human menopausal gonadotropin and follicle stimulating hormone and pulsatile gonadotrophin releasing hormone. [6] Clomiphene citrate, the most commonly used drug is a non-steroidal estrogen antagonist that increases follicle stimulating hormone and luteinizing hormone levels by blocking estrogen negative feedback at the hypothalamus. A woman taking these medications produces double or triple the amount of progesterone and estrogen in that cycle compared to pre-treatment cycles. [7],[8]

Human gingiva has specific estrogen and progesterone receptors and there is direct biochemical evidence that this tissue may function as a target organ for sex hormones. [9],[10] Estrogen may regulate cellular proliferation, differentiation and keratinization, whereas progesterone influences the permeability of the microvasculature, alters the rate and pattern of collagen production and increases the metabolic breakdown of folate, which is necessary for tissue maintenance. [11],[12] Alterations in the composition of subgingival plaque, maternal immune responsiveness, sex hormones create a myriad of responses in the periodontium. [13],[14]

Chronic bacterial infections may affect reproduction, success and the outcome of infertility treatment. [1],[3] Hence, the aim of the present study was to compare the periodontal status of infertile women attending in vitro fertilization (IVF) clinics, infertile women in whom treatment had not yet been initiated and to compare the periodontal status of these women with women who had conceived and delivered naturally.

   Materials and Methods Top

A total of 180 women satisfying the inclusion and exclusion criteria were included in the study. All subjects provided written informed consent. The study protocol was approved by the institution review boards of Gandhi Institute of Technology and Management Dental College and Hospital, Krishna IVF Clinic and King George Hospital, Visakhapatnam. Subjects were divided into three groups of 60 women each.

Group I: 60 women who were undergoing infertility treatment at the Krishna IVF clinic, Visakhapatnam.

Group II: 60 women with a history of infertility but in whom treatment had not yet been initiated.

Group III (Control group): 60 women who had conceived and delivered naturally.

Subjects of Group II and III were examined at King George Hospital, Visakhapatnam.

The inclusion criteria were:

  • Women in the age group of 25-35 years
  • For Group I and II: women with history of primary infertility
  • For Group III: women who conceived and delivered naturally.

Patients were excluded if the following conditions were observed:

  • Presence of complicating systemic conditions
  • Women suffering from secondary infertility
  • Male factor responsible for the infertility
  • Smoking
  • Periodontal treatment undertaken within the previous 6 months
  • Use of systemic antibiotics or non-steroidal anti-inflammatory drugs in 3 months prior to enrollment in the study.

All individuals were interviewed about their age, occupation, educational level, marital age, medical history, family history and oral hygiene practice.

Clinical examination

The clinical parameters assessed included: Simplified oral hygiene index (Greene and Vermillion; 1964), [15] gingival index (GI) (Lφe; 1967), [16] sulcus bleeding index (SBI) (Mόhlemann and Son; 1971), [17] and clinical attachment loss (CAL). [18] Measurements for all the teeth except third molars were recorded. All periodontal measurements were assessed at four sites on each tooth (mesio-buccal, disto-buccal, mesio-lingual, disto-lingual). All measurements were performed by a single examiner using a mouth mirror and a community periodontal index of treatment need probe. Hu-Friedy, Chicago, IL, USA.

Statistical analysis

Comparison of groups individually with respect to each clinical parameter was analyzed by Kruskal - Wallis one-way ANOVA test. Pair wise comparison of three groups with respect to each clinical parameter was analyzed using the Mann-Whitney U test. Relationship between marital age and clinical parameters in every group was analyzed by Karl Pearson's correlation coefficient method. P < 0.05 was considered statistically significant. Statistical analysis was performed using a statistical package SPSS version 17.0; IBM. Statistical Package for the Social Sciences Version 17.0 International Business Machines Corporation.

   Results Top

Oral hygiene index simplified (OHI-S): Oral hygiene status did not differ significantly (P > 0.05) when the mean values of OHI-S scores of Group I, II and III were compared, indicating that the oral hygiene status was similar in all the groups [Table 1].
Table 1: Comparison of OHI-S, GI, SBI and CAL among groups

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GI: When compared to Group II and Group III, Group I had significantly higher scores of GI (P < 0.05). However, GI did not show statistically significant difference between Group II and Group III [Table 1].

SBI: On comparison of mean values of the percentage of sulcus bleeding sites, scores were significantly higher in Group I (P < 0.05) when compared to Group II and III. There was no significant difference between the scores of Group II and III [Table 1].

CAL: CAL was significantly higher in Group I and Group II (P < 0.05) compared to Group III. Furthermore, CAL did not differ significantly between Group I and Group II (P > 0.05) [Table 1].

   Discussion Top

Among the different systemic factors and conditions, sex hormones have been suggested as an important modifying factor that may influence the pathogenesis of periodontal disease. [19] This study was performed to assess gingival inflammation and periodontal status in women undergoing infertility treatment and to compare this group of women with women having a history of infertility, but not undergoing treatment and with a control group comprising of women who had conceived and delivered naturally. The study groups were matched for factors such as age, socio-economic status, education level, marital age [Table 2] and oral hygiene practice to eliminate their effect on the periodontium.
Table 2: Summary statistics for age, marital age and education level in the study population (mean ± SD)

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In spite of similar plaque scores, women who were undergoing infertility treatment (Group I) had significantly higher gingival inflammation and bleeding, compared to Group II and Group III [Table 1]. This effect may be attributed to increased levels of estrogen and progesterone. There is biochemical evidence that specific estrogen and progesterone receptors are present in the gingival tissue. [9] Increased levels of estrogen may regulate cellular proliferation and keratinization while progesterone alters the microvasculature and collagen production. [9],[11] Estrogen promotes the growth of periodontal pathogens especially prevotella intermedia. In addition, an increased level of estrogen and progesterone alters the host defense mechanism, depresses neutrophil chemotaxis and phagocytosis, reduces antibody and T-cell responses and stimulates prostaglandin production. [11]

The severity of gingival effects was strongly correlated with the duration of usage of drugs like clomiphene citrate used in the infertility treatment. This was due to the cumulative effect of these drugs on both hormone levels and on inflammation, when used in subsequent cycles. [6]

The CAL was significantly higher in the infertile women (Group I and Group II) as compared to women in the control group (Group III). This finding may be attributed to psychological stress invariably associated with infertility. Psychosocial stress is a significant risk indicator for periodontal disease. [20] Stress induced release of cortisol and neurotransmitters results in an immunosuppression that increases the potential for destruction by periodontal pathogens. [11],[21]

The present interest in the association of periodontal diseases and pregnancy outcome is based on the infection hypothesis, which states that microbes themselves or microbial toxins (lipopolysaccharides) and inflammatory cytokines enter the uterine cavity by the blood borne route from a non-genital focus such as periodontal disease, [22] causing increased plasma levels of inflammatory cytokines [23],[24] and leading to unsuccessful embryo development and implantation failure in IVF patients. [25],[26] This suggests that periodontal diseases, which are chronic infections, may cause bacteremia, [27] endotoxemia, [28] increased plasma levels of inflammatory cytokines [22],[27] all which have proved to be significantly associated with reproductive failure. [25],[26]

Gingival inflammation or periodontal disease induced by ovulation drugs may affect the success of infertility treatment. [6] Therefore, effective plaque control during the infertility treatment could minimize the effect of gingival inflammation on the success of infertility treatment. Patients should be motivated to practice meticulous oral hygiene and routine professional prophylaxis should be performed at the beginning of each menstrual cycle to ensure healthy periodontium on the ovulation day on which assisted reproductive therapy is performed. Furthermore, low levels of plaque should be maintained even after pregnancy is achieved to reduce the risk of pre-term labor and low birth weight.

The limitations of the study were that hormonal levels were not recorded nor were a bacteriological or immunological assay carried out. The study also did not assess the psychological stress in the subjects. Stress has been suggested a risk indicator for periodontal disease owing to an increase in cortisol production resulting in the depression of immunity. [19] Hence, these factors should be assessed in further studies.

   Conclusion Top

From the analysis of the results and within the limitations of the study, it can be concluded that infertility treatment exacerbates gingival inflammation and periodontal disease process. Since periodontitis is a modifiable risk factor associated with adverse pregnancy outcomes, further interventional prospective studies are needed to confirm the effects of periodontitis and periodontal treatment on the outcome of infertility treatment. Furthermore, this study may lead to effective interventional strategies that minimize or negate the effect of elevated hormonal levels as a contributor to periodontal disease and in turn infertility treatment.

   Acknowledgments Top

Dr. Santha Rao, Superintendent of King George Hospital, Visakhapatnam. Dr. Subha Devi, Head of the Department, Obstetrics and Gynecology, King George Hospital, Visakhapatnam.

   References Top

1.Longo DL, Fauci AS, Kasper DL, Hauser SL, Jameson JL, Loscalzo J. Harrisson's Principles of Internal Medicine. 18 th ed., Vol. 2. NewYork: Mc Graw Hill Companies Inc.; 2012.  Back to cited text no. 1
2.David AW, Timothy MC, John DF. Oxford Textbook of Medicine. 5 th ed. United States: Oxford University Press; 2010.  Back to cited text no. 2
3.Novak ER, Jones GS, Jones HW. Textbook of Gynaecology. 7 th ed. Edinburgh and London: E and S. Livingstone Ltd.; 1965.  Back to cited text no. 3
4.Office of Technology Assessment. Infertility: Medical and Social Choices, Publication OTA-BA-358. Washington, DC: U.S. Government Printing Office; 1988.  Back to cited text no. 4
5.Pelinck MJ, Hoek A, Simons AH, Heineman MJ. Efficacy of natural cycle IVF: A review of the literature. Hum Reprod Update 2002;8:129-39.  Back to cited text no. 5
6.Haytaç MC, Cetin T, Seydaoglu G. The effects of ovulation induction during infertility treatment on gingival inflammation. J Periodontol 2004;75:805-10.  Back to cited text no. 6
7.Kousta E, White DM, Franks S. Modern use of clomiphene citrate in induction of ovulation. Hum Reprod Update 1997;3:359-65.  Back to cited text no. 7
8.Fritz MA, Holmes RT, Keenan EJ. Effect of clomiphene citrate treatment on endometrial estrogen and progesterone receptor induction in women. Am J Obstet Gynecol 1991;165:177-85.  Back to cited text no. 8
9.Rose LF, Genco RJ, Mealey BL, Cohen DW. Periodontal Medicine. Hamilton: B.C.Decker Inc.; 2000.  Back to cited text no. 9
10.Raber-Durlacher JE, van Steenbergen TJ, Van der Velden U, de Graaff J, Abraham-Inpijn L. Experimental gingivitis during pregnancy and post-partum: Clinical, endocrinological, and microbiological aspects. J Clin Periodontol 1994;21:549-58.  Back to cited text no. 10
11.Newman MG, Takei HH, Klokkevold PR, Carranza FA. Clinical Periodontology. 10 th ed. St. Louis, Missouri: Saunders; 2006.  Back to cited text no. 11
12.Mealey BL, Moritz AJ. Hormonal influences: Effects of diabetes mellitus and endogenous female sex steroid hormones on the periodontium. Periodontol 2000 2003;32:59-81.  Back to cited text no. 12
13.Nakagawa S, Fujii H, Machida Y, Okuda K. A longitudinal study from prepuberty to puberty of gingivitis. Correlation between the occurrence of Prevotella intermedia and sex hormones. J Clin Periodontol 1994;21:658-65.  Back to cited text no. 13
14.Lapp CA, Thomas ME, Lewis JB. Modulation by progesterone of interleukin-6 production by gingival fibroblasts. J Periodontol 1995;66:279-84.  Back to cited text no. 14
15.Greene JC, Vermillion JR. The simplified oral hygiene index. J Am Dent Assoc 1964;68:7-13.  Back to cited text no. 15
16.Löe H. The Gingival Index, the Plaque Index and the Retention Index Systems. J Periodontol 1967;38:Suppl:610-6.  Back to cited text no. 16
17.Mühlemann HR, Son S. Gingival sulcus bleeding - A leading symptom in initial gingivitis. Helv Odontol Acta 1971;15:107-13.  Back to cited text no. 17
18.Clark DC, Chin Quee T, Bergeron MJ, Chan EC, Lautar-Lemay C, de Gruchy K. Reliability of attachment level measurements using the cementoenamel junction and a plastic stent. J Periodontol 1987;58:115-8.  Back to cited text no. 18
19.Mascarenhas P, Gapski R, Al-Shammari K, Wang HL. Influence of sex hormones on the periodontium. J Clin Periodontol 2003;30:671-81.  Back to cited text no. 19
20.Genco RJ, Ho AW, Grossi SG, Dunford RG, Tedesco LA. Relationship of stress, distress and inadequate coping behaviors to periodontal disease. J Periodontol 1999;70:711-23.  Back to cited text no. 20
21.LeResche L, Dworkin SF. The role of stress in inflammatory disease, including periodontal disease: Review of concepts and current findings. Periodontol 2000 2002;30:91-103.  Back to cited text no. 21
22.Gibbs RS. The relationship between infections and adverse pregnancy outcomes: An overview. Ann Periodontol 2001;6:153-63.  Back to cited text no. 22
23.Neuer A, Spandorfer SD, Giraldo P, Dieterle S, Rosenwaks Z, Witkin SS. The role of heat shock proteins in reproduction. Hum Reprod Update 2000;6:149-59.  Back to cited text no. 23
24.Abramov Y, Schenker JG, Lewin A, Friedler S, Nisman B, Barak V. Plasma inflammatory cytokines correlate to the ovarian hyperstimulation syndrome. Hum Reprod 1996;11:1381-6.  Back to cited text no. 24
25.Spandorfer SD, Neuer A, LaVerda D, Byrne G, Liu HC, Rosenwaks Z, et al. Previously undetected Chlamydia trachomatis infection, immunity to heat shock proteins and tubal occlusion in women undergoing in-vitro fertilization. Hum Reprod 1999;14:60-4.  Back to cited text no. 25
26.Neuer A, Mele C, Liu HC, Rosenwaks Z, Witkin SS. Monoclonal antibodies to mammalian heat shock proteins impair mouse embryo development in vitro. Hum Reprod 1998;13:987-90.  Back to cited text no. 26
27.Scannapieco FA. Position paper of The American Academy of Periodontology: Periodontal disease as a potential risk factor for systemic diseases. J Periodontol 1998;69:841-50.  Back to cited text no. 27
28.Geerts SO, Nys M, De MP, Charpentier J, Albert A, Legrand V, et al. Systemic release of endotoxins induced by gentle mastication: Association with periodontitis severity. J Periodontol 2002;73:73-8.  Back to cited text no. 28

Correspondence Address:
Godavarthi Lalasa
Departments of Periodontics and Oral Implantology, GITAM Dental College and Hospital, Visakhapatnam, Andhra Pradesh
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/0970-9290.131055

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