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Comparative Evaluation of Periodontal Alteration in Pregnant Women in Relation to Foetal Sex
Int J Clin Prev Dent 2023;19(1):7-12
Published online March 31, 2023;  https://doi.org/10.15236/ijcpd.2023.19.1.7
© 2023 International Journal of Clinical Preventive Dentistry.

Jules Julien Ndjoh1,2, Metogo Ntsama Junie Annick3, Onana Messi Marie1,2, Zilefac Brian Ngokwe1,2, Sandra Lydie Akena Ndeng1,2, René Ngoulma1,2, Lawrence Essama Eno Belinga4, Vicky Ama Moor5

1Department of Oral surgery, Maxillofacial Surgery and Periodontology, Faculty of Medicine and Biomedical Sciences, University of Yaounde, 2Laboratory of Implantology and Periodontology, University of Yaounde I, 3Department of Gynaecology and Obstetrics, Faculty of Medicine and Biomedical Sciences, University of Yaounde, 4Faculty of Medicine and Pharmaceutical Sciences, The University of Douala, 5Department of Biochemistry, Faculty of Medicine and Biomedical Sciences, University of Yaounde, Cameroon
Correspondence to: Jules Julien Ndjoh
E-mail: jules.ndjoh@fmsb-uy1.com
Received January 27, 2023; Revised March 25, 2023; Accepted March 30, 2023.
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Abstract
Objective: Periodontal disease is an inflammatory condition with a diverse aetiology that affects the gums and tooth supporting structures and, if untreated, can lead to tooth loss, dental implant loss and a reduced quality of life and self-confidence. Recent research has found that pregnant women with male foetuses experience more inflammation than those with female foetuses. Furthermore, periodontal disease has been linked to poor birth outcomes, emphasizing the significance of this research. Determine the extent of periodontal change in pregnant women in relation to foetal sex.
Methods: We conducted an analytical cross-sectional study from January 10th to May 30th 2022, recruiting participants from the YCH, the FMBS's laboratory of dental implantology and periodontology, and analysing samples at the YUTH Biochemistry laboratory. The sera samples were then used to analyse hormones (Testosterone and Progesterone) using the ELISA competitive and sandwich methods.
Results: The average age was 30 years old, and the average gestational age was 31 weeks. In both groups, we found a 58% prevalence of PD, with 30% of the 58% being in women carrying male foetuses. Testosterone levels were higher in women carrying male foetuses than in women carrying female foetuses. Between people with periodontal disease and those who did not, there was a moderately strong relationship (r=0.552) and a statistically significant difference (p=0.042) in testosterone levels.
Conclusion: Pregnancy increases the risk of periodontal disease. During pregnancy, the sex hormone progesterone had no significant association with the development of periodontal disease. Finally, women carrying male foetuses had a higher prevalence of periodontal disease than women carrying female foetuses.
Keywords : periodontal disease, pregnancy, progesterone, testosterone
Introduction

Periodontal disease (PD) is an inflammatory condition of periodontal tissues with a diverse aetiology that is one of the world's most common diseases [1]. Gingivitis is the simplest form of this disease, and if left untreated, it progresses to periodontitis, a more complex form. According to the WHO, PD affects 20-50% of adults worldwide. This prevalence varies with sex and hormonal change, with an estimated 23% of women worldwide suffering from PD, with an increase during pregnancy (56%) [2]. In Africa, the estimated prevalence of PD is 60%.

The rise in PD associated with pregnancy can be attributed to an increase in the concentration of sex hormones. These hormones are responsible for a wide range of clinical and immunological changes. According to researchers, increased female sex hormones may modulate immune cell function. Periodontal disease is thought to be caused in part by immunological changes that occur during pregnancy [3].

Several studies have been able to demonstrate the relationship between PD and pregnancy, and more specifically the role of hormones in showing that women pregnant with male foetuses have a higher rate of inflammation than women pregnant with female foetuses [4,5].

This difference in inflammation was observed at the placental level and was later traced back to the secretion and action of the hormone testosterone [4,6], which is present in higher concentrations in women pregnant with male foetuses, and thus women with male foetuses are at a higher risk of developing PD.

Pregnancy PD has been linked to negative birth outcomes such as low birth weight, preterm birth, and miscarriage [7].

With the aforementioned negative effects of PD, we aimed to determine the prevalence of periodontal disease in pregnant women, the role of sex hormones in PD, and finally to establish a relationship between a male foetus and increased inflammation at the periodontal level.

1. General Objective

Determine the extent of periodontal disease in pregnant women in relation to foetal sex.

Materials and Methods

We conducted an analytical cross-sectional study that lasted 8 months, from November 1st to May 30th, 2022.

Our target population included healthy pregnant women in their second and third trimesters who visited the Yaoundé Central Hospital (YCH) gynaecological unit and the Laboratory of Dental implantology and Periodontology of the Faculty of Medicine and Biomedical Sciences (FMBS) University of Yaoundé I.

Participants in our study were recruited from the YCH's principal maternity and the Laboratory of Dental Implantology and Periodontology at the University of Yaoundé I's Faculty of Medicine and Biomedical Sciences. The blood samples were analysed at the Yaoundé University Teaching Hospital (YUTH) Laboratory of Biochemistry.

This study included pregnant women who visited the principal maternity YCH and the laboratory of Dental Implantology and Periodontology and gave their consent to participate.

Participants in the second and third trimesters of pregnancy who had not had an echography performed by a certified radiologist to confirm the foetal sex, women on hormonal therapy, women with systemic conditions such as Diabetes, HIV, and women on medications such as phenytoin were excluded from our study.

1. Data Collection and Analysis

The data collected using a pre-designed questionnaire was entered into the software CsPro version 7.5 and a Microsoft Excel 2016 spreadsheet. The software IBM-SPSS version 23.0 was used for the analysis.

A significant threshold of 0.05 was established, which meant that all p-values less than 0.05 were considered statistically significant.

To conduct this study, ethical approval was obtained from the Ethical Committee of the Faculty of Medicine and Bio-medical Sciences of the University of Yaoundé I (N°196/ UY1/FMSB/VDRC/DAASR/CSD).

Administrative authorities from the various hospitals provided ethical clearances.

2. Variables of interest:

Clinical: Gingival inflammation, presence of dental plaque, clinical attachment loss, pocket depth and tooth mobility.

Paraclinical: Testosterone and progesterone dosage.

RESULTS

Our study included 60 patients, of which 12 were excluded and 48 were retained.

1. Demographic information

The mean age in our study was 30.25±4.41, and the major age group represented was 26-30 with a frequency of n=21 (43.8%), followed by 30-35 with a frequency of n=15 (31.3%).

According to our observations, 45.8% of our participants were married, while the other 54.2% were single. In terms of residence and educational qualifications, 97.9% of our participants were from Yaoundé, and 54.2% were university graduates.

2. Social habits

A majority of our participants (62.5%) stated that they did not consume alcohol, while 37.5% stated that they did consume alcohol on occasion and in various quantities, with those consuming at least a glass of alcohol per week accounting for a higher percentage (27.1%) and those consuming at least a bottle per week accounting for 10.4%. 100% of our participants stated that they do not use tobacco in any form.

3. Obstetric background

We had a mean gestational age of 31 weeks, and 62.5% of our participants were expecting their second child. We had a 50-50% distribution of foetal sex (24 males and 24 females), with a higher percentage being pregnant for the second time (62.5%). Out of all our participants, 25% confirmed having had a miscarriage at some point in their lives, while 75% had not. A percentage of 43.7% also reported health issues associated with their current pregnancy, such as excessive body fatigue, despite the fact that they were not currently receiving treatment for it.

4. Oral hygiene practices and oral health changes during pregnancy

We discovered that a majority of n=30 (62.5%) brushed only once per day, while a minority of n=18 (37.5%) brushed twice per day. A larger proportion of our participants, n=28 (58.3%), had never visited a dentist in their lives.

Additionally, it was found that 39 women (81.3%) reported experiencing changes in their oral cavity at some point throughout their current pregnancy, whereas the remaining 18.7% reported no differences in their oral cavity before or after becoming pregnant. The two symptoms with the highest frequency, n=37 and n=18, were halitosis and bleeding gums during brushing, respectively, of the 81.3% of women who noticed discomfort during pregnancy. With a frequency of n=12, tooth mobility came in third.

In both male and female pregnancies, the plaque index and pocket depth were 2 and 3, respectively. However, no statistically significant difference was found (p=0.867 and p=0.984). Gingival and CAL indices were also found to be statistically insignificant (p=0.894 and p=1) (Table 1).

Table 1 . Comparison of oral hygiene indices

Variable (mean±SD)Women with maleWomen with femalep-value
Plaque index2±1.22±10.867
Gingival bleeding index2±11±10.894
Pocket depth3.1±1.33±2.30.984
Clinical attachment loss1±11±11


Oral discomfort was reported by all 24 (100) women with male children, compared to 15 (88.2) of women with female children. However, no statistical significance (p>0.05) was found between the groups. Both groups had halitosis, tooth mobility, and gingival abscesses, but there was no statistical significance (p>0.05) (Table 2).

Table 2 . Group comparison of oral symptoms

VariableCategoryWomen with male foetuses Women with female foetuses p-value


n (%)
Symptoms during pregnancyBleeding during brushing24 (100)15 (88.2)0.099
Halitosis11 (50)7 (41.2)0.748
Tooth mobility8 (36.4)4 (23.5)0.389
Gingival abscesses7 (31.8)2 (11.8)0.141


Dental caries were the most common pathologies, accounting for 70% of pathologies in the first group and 72.7% in the second. Gingivitis and periodontitis were also present, albeit to a lesser degree. There was no statistically significant difference between groups (Table 3).

Table 3 . Comparison of different oral pathologies

VariableCategoryMothers with maleMothers with femalep-value


n (%)
Dental and oral pathologiesDental caries7 (70)8 (72.7)0.89
Gingivitis6 (60)3 (27.3)0.13
Periodontitis2 (20)1 (9.1)0.47
Cellulitis0 (0)1 (9.1)0.32
Dental abscesses---


Testosterone levels were higher in women with male children than those with women Pregnant with female children. The difference was statically significant at p≤0.001 (Table 4).

Table 4 . Testosterone concentrations in both sexes

Variable (mean±SD)Women with maleWomen with femalep-value
Testosterone1.21±0.750.43±0.17<0.001
Progesterone45.6±4.844.44±4.010.658


The difference in progesterone levels was not statistically significant.

There was a moderately strong relationship (r=0.552) and a statistically significant difference (p=0.042) in testosterone levels between persons with periodontal diseases and those without (Figure 1).

Figure 1. Testosterone concentrations in both sexes. Group 1: women with male foetuses, Group 2: women with female foetuses.

There was a weak and negative correlation (r=−0.327) in progesterone levels between those with and without periodontal disease. There was no statistically significant difference (p>0.05) between groups (Figure 2).

Figure 2. Correlation of progesterone levels between those with periodontal disease.
Discussion

There were 48 pregnant women in our study, with an equal distribution of foetal sex (24 males and 24 females), a mean age of 30.25±4.41 and a mean gestational age of 31 weeks.

According to our findings, the majority of participants (58.3%) had never visited a dentist in their entire lives, and 81% had experienced oral discomfort at some point during their current pregnancy.

Most of our participants, regardless of foetus gender, had periodontal disease, with a prevalence of 58%, and these participants had no knowledge of this condition.

They were also completely unaware of the risks and consequences of periodontal disease on their overall health, particularly the health of the foetus.

We also discovered that, while periodontal disease was present in 58% of our participants, the vast majority of those 58% were already nearing the end of their gestational period. This was similar to a study conducted by Taani, who discovered that the severity of gingival inflammation increased during pregnancy, peaking just before parturition [8].

Inflammation-induced swelling and loosening of the gingival tissues around the teeth may be a contributing factor to the higher periodontal pocket depth by allowing the probe to pierce deeper into the tissues [8,9].

We discovered that 25% of our patients had suffered a miscarriage, this unfortunate birth outcome could be attributable to the high prevalence of periodontal disease in our study and this association has been described previously [7,10,11].

We observed dental plaque and eventually periodontal disease. We also noticed that the presence of periodontal disease was dependent on but unrelated to the amount of dental plaque accumulated, as the degree of clinical attachment loss and periodontal pocket depth were not directly proportional to the amount of plaque. This was consistent with research conducted by Wu et al in 2015 [1,12], even though some claimed to maintain good and consistent oral hygiene.

Similar studies found that 89% of pregnant women in Ghana, 86.2% in Thailand, and 47% in Brazil had gingivitis [13-15].

There was no direct relationship between hormonal concentrations and periodontal disease in our study. We noted that women with higher levels of progesterone had similar levels of periodontal disease as their counterparts with lower hormone concentrations.

Our findings agreed with those of Lundgren and Lindhe [16], who found that daily injections of oestrogen and progesterone, separately or in combination, for three months did not affect the degree of alveolar bone resorption induced by a periodontitis-accelerating diet. Knight and Wade (1974) [17] found that women on oral contraceptives for more than 1.5 years had more periodontal destruction than women of comparable age in the control group in their study of 89 women aged 17-23 years. As a result, the duration of hormonal therapy, rather than a short-term increase, appears to affect periodontal attachment levels [18].

Our findings contradicted the findings of Mealey et al, [19] who discovered that increased circulating levels of progesterone during pregnancy cause gingival capillary dilation, increased capillary permeability, and gingival exudate. They described how progesterone affects the gingival vasculature and causes increased exudation.

Progesterone levels between those with periodontal disease and those without it showed a marginally negative connection (r=−0.327). There was no statistically significant difference between the two groups (p>0.05).

There was no significant difference in plaque index between the two groups, as both women with periodontal high progesterone levels appeared to have the same plaque index as those with lower concentrations of progesterone. This was consistent with the findings of Bloomquist, pregnant women showed no increase in plaque score during pregnancy, but there was a shift in the predominant types of bacterial flora. Specifically, there was an increase in Prevotella intermedia populations in the plaque obtained from these women [20].

Several authors have illustrated a mechanism by which increased progesterone levels in pregnancy magnify the clinical features of plaque-induced gingivitis without directly magnifying the plaque quantity, via prostaglandin synthesis stimulation [21-23].

It was also discovered that the sex hormone profile influences subgingival microbiology. This profile has been shown to promote the growth of periodontopathogenic bacteria like Porphyromonas gingivalis, subgingival anaerobic-aerobic bacteria, prevotella melaninogenica, and Prevotella intermedia.

We discovered that the plaque index and pocket depth were 2 and 3 in both male and female pregnancies, respectively. However, no statistically significant difference was found (p=0.867 and p=0.984). Gingival and CAL indices were also found to be statistically insignificant (p=0.894 and p=1). There was no statistical significance (p>0.05) between the groups because all women pregnant with male foetuses had experienced bleeding during brushing at some point during their current pregnancy, giving us a percentage of 100% as opposed to 82% of those pregnant with female foetuses, giving us a p-value of 0.009.

Both groups had halitosis, tooth mobility, and gingival abscesses, but there was no statistical significance (p>0.05).

Dental caries were the most common pathologies, accounting for 70% of pathologies in the first group (male foetuses) and 72.7% in the second group. A decrease in salivary pH is observed in pregnant women and may lead to an increased incidence of dental caries during pregnancy [24].

Following hormone analysis, we discovered that Testo-sterone levels were higher in women carrying male foetuses than in women carrying female foetuses. At p=0.001, the difference was statistically significant.

There was no statistically significant difference in progesterone levels. There was a moderately strong relationship (r=0.552) and a statistically significant difference (p=0.042) in testosterone levels between people with periodontal disease and those who did not.

This could be because in pregnancies with a male foetus, there is more possibility for increased expression of pro-inflammatory cytokine such as Tumour necrosis factor-alpha (TNF-α) and less output of anti-inflammatory cytokine [4].

Women carrying a male foetus may have a reduced ability to counteract an inflammatory response [5].

Because the gum is extremely protective during and after pregnancy, we must be cautious with implants and monitor the periodontal condition.

The gingiva is such an important component of implant longevity, the patient's rehabilitation will be jeopardized in the long run if there is a risk of mucositis and peri-implantitis.

Even though these incidents will not always occur, this information can be used to avoid them.

Pregnant women are more susceptible to periodontal infections due to hormonal imbalance, and multiparous women are more likely to lose dental and implant implants due to weakened periodontal support.

Conclusion

According to our findings, there is an increase in the prevalence of periodontal disease during pregnancy.

Furthermore, the hormone progesterone was not significantly associated with the initiation and progression of periodontal disease.

Finally, women with male foetuses had a higher prevalence of periodontal disease than women with female foetuses, which was consistent with previous studies that found women with male foetuses to be more likely to have periodontal disease than women with female foetuses.

Periodontal disease and peri-implantitis are nearly identical in that, just as one can lose a natural tooth, one can also lose a dental implant due to this inflammation, which is exacerbated during pregnancy and is related to foetal sex.

Conflict of Interest

No potential conflict of interest relevant to this article was reported.

References
  1. Wu M, Chen S-W, Jiang S-Y: Relationship between Gingival Inflammation and Pregnancy. Mediators Inflamm. 2015: 1-11, 2015.
    Pubmed KoreaMed CrossRef
  2. Löe H, Silness J: Periodontal Disease in Pregnancy I. Prevalence and Severity. Acta Odontol Scand. Taylor & Francis;. 21(6): 533-51, 1963.
    Pubmed CrossRef
  3. Basic books for the operating room: Supplement V. AORN J. 10(4): 181-9, 1969.
    Pubmed CrossRef
  4. Challis J, Newnham J, Petraglia F, Yeganegi M, Bocking A: Fetal sex and preterm birth. Placenta. 34(2): 95-9, 2013.
    Pubmed CrossRef
  5. Ramiro-Cortijo D, de la Calle M, Böger R, Hannemann J, Lüneburg N, López-Giménez MR, Rodríguez-Rodríguez P, Martín-Cabrejas MÁ, Benítez V, de Pablo ÁLL, González MDC, Arribas SM: Male fetal sex is associated with low maternal plasma anti-inflammatory cytokine profile in the first trimester of healthy pregnancies. Cytokine. 136: 155290, 2020.
    Pubmed CrossRef
  6. Arnold AP, Lusis AJ: Understanding the sexome: measuring and reporting sex differences in gene systems. Endocrinology. 153(6): 2551-5, 2012.
    Pubmed KoreaMed CrossRef
  7. Davenport E: Does periodontal disease affect pregnancy outcome? Br Dent J 197: 247, 2004.
    CrossRef
  8. Taani DQ, Habashneh R, Hammad MM, Batieha A: The periodontal status of pregnant women and its relationship with socio-demographic and clinical variables. J Oral Rehabil. 30(4): 440-5, 2003.
    Pubmed CrossRef
  9. Kinnby B, Matsson L, Astedt B: Aggravation of gingival inflammatory symptoms during pregnancy associated with the concentration of plasminogen activator inhibitor type 2 (PAI-2) in gingival fluid. J Periodontal Res. 31(4): 271-7, 1996.
    Pubmed CrossRef
  10. Farrell S, Ide M, Wilson RF: The relationship between maternal periodontitis, adverse pregnancy outcome and miscarriage in never smokers. J Clin Periodontol. 33(2): 115-20, 2006.
    Pubmed CrossRef
  11. Chanomethaporn A, Chayasadom A, Wara-Aswapati N, Kongwattanakul K, Suwannarong W, Tangwanichgapong K, Sumanonta G, Matangkasombut O, Dasanayake AP, Pitiphat W: Association between periodontitis and spontaneous abortion: A case-control study. J Periodontol. 90(4): 381-390, 2019.
    Pubmed CrossRef
  12. Armitage GC: Development of a classification system for periodontal diseases and conditions. Ann Periodontol. 4(1): 1-6, 1999.
    doi: 10.1902/annals.1999.4.1.1. PMID: 10863370.
    Pubmed CrossRef
  13. Vogt M, Sallum AW, Cecatti JG, Morais SS: Factors associated with the prevalence of periodontal disease in low-risk pregnant women. Reprod Health. 9: 3, 2012.
    Pubmed KoreaMed CrossRef
  14. Nuamah I, Annan BD: Periodontal status and oral hygiene practices of pregnant and non-pregnant women. East Afr Med J. 75(12): 712-4, 1998.
    Pubmed
  15. Rakchanok N, Amporn D, Yoshida Y, Harun-Or-Rashid M, Sakamoto J: Dental caries and gingivitis among pregnant and non-pregnant women in Chiang Mai, Thailand. Nagoya J Med Sci. 72(1-2): 43-50, 2010.
    Pubmed
  16. Lundgren D, Lindhe J: Lack of influence of female sex hormones on alveolar bone loss in hamsters. Scand J Dent Res. 79(2): 113-8, 1971.
    Pubmed CrossRef
  17. Knight GM, Wade AB: The effects of hormonal contraceptives on the human periodontium. J Periodontal Res. 9(1): 18-22, 1974.
    Pubmed CrossRef
  18. Laine MA: Effect of pregnancy on periodontal and dental health. Acta Odontol Scand. 60(5): 257-64, 2002.
    Pubmed CrossRef
  19. Mealey BL, Moritz AJ: Hormonal influences: effects of diabetes mellitus and endogenous female sex steroid hormones on the periodontium. Periodontol 2000 32: 59-81, 2003.
    Pubmed CrossRef
  20. Jensen J, Liljemark W, Bloomquist C: The effect of female sex hormones on subgingival plaque. J Periodontol. 52(10): 599-602, 1981.
    Pubmed CrossRef
  21. Goodson JM, Haffajee AD, Socransky SS: The relationship between attachment level loss and alveolar bone loss. J Clin Periodontol. 11(5): 348-59, 1984.
    Pubmed CrossRef
  22. Morishita M, Miyagi M, Iwamoto Y: Effects of sex hormones on production of prostaglandin E2 by human peripheral mono-cytes. Journal of Periodontology. 64(11): 1075-1078, 1993.
    Pubmed CrossRef
  23. Morishita M, Miyagi M, Iwamoto Y: Effects of sex hormones on production of interleukin-1 by human peripheral monocytes. Journal of Periodontology. 70(7): 757-760, 1999.
    doi: 10.1902/ jop.1999.70.7.757.
    Pubmed CrossRef
  24. Silva de Araujo Figueiredo C, Gonçalves Carvalho Rosalem C, Costa Cantanhede AL, Abreu Fonseca Thomaz ÉB, Fontoura Nogueira da Cruz MC: Systemic alterations and their oral manifestations in pregnant women. J Obstet Gynaecol Res. 43(1): 16-22, 2017.
    Pubmed CrossRef


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