A Descriptive Observational Survey on Italian Women’s Awareness of the Association Between Periodontal Disease and Pregnancy

Abstract

The literature has identified several common acute and chronic complications associated with periodontal health during pregnancy, such as gingivitis, recession, periodontitis, and changes in systemic health, such as gestational diabetes, which may act as additional risk factors for chronic periodontal disease. Are the general public and health care providers aware of the potential risks of systemic and intrauterine inflammation caused by bacteria from the oral microbiota entering the bloodstream through inflamed gingival tissue and affecting the fetoplacental unit, leading to complications, such as preterm birth and reduced prenatal growth? A questionnaire-based survey, conducted between January 2023 and June 2023, aimed to assess patients’ personal oral hygiene practices and their understanding of the link between pregnancy and periodontal health. A total of 826 people completed a questionnaire for this study. The majority of women surveyed (86.9%) were not pregnant, but 77.7% had at least one child. The majority of women believed in good oral hygiene during pregnancy but lacked knowledge about how oral care can affect pregnancy outcomes.

1. Introduction

Pregnancy is defined as a physiological state, lasting between 37 and 42 weeks (average 40 weeks), in which the female body undergoes multiple changes in metabolic, psychological, vascular, and hormonal status, leading to the growth of the embryo/fetus in the uterus after fertilization by male gametes [1,2].

Several studies in different fields have reported a bidirectional relationship between pregnancy and periodontal disease and a possible triadic relationship including metabolic disorders. A local infection usually presents pathogenic bacteria in the mouth, particularly in periodontal pockets, and can travel through the bloodstream to the placenta, triggering inflammatory molecules that contribute to intrauterine and systemic inflammation, leading to a higher likelihood of poor fetal growth and preterm birth [2,3,4].

During pregnancy, there is a normal increase in secreted female sex hormones: estrogen increases tenfold, while progesterone increases about thirtyfold [1,2]. For these reasons, several physiological changes occur in such a short time, affecting the cardiovascular system; the hematological, vascular, and endocrine apparatus; the respiratory, renal, and gastrointestinal organs, etc. [1,2,3,4]. To ensure proper healthcare for pregnant women and to protect the health of the future baby, it is essential to prioritize oral health during pregnancy to reduce risk factors for both individuals [3,4].

The literature extensively describes physiological changes in the oral cavity during pregnancy, including vascular modifications due to high levels of estrogen and progesterone receptors in soft tissue. These changes increase blood supply, vessel permeability, exudation, and exfoliation of non-keratinized oral epithelium [3,4,5,6].

These local changes improve the inflammatory response of periodontal tissues and increase the risk to develop gingivitis, periodontitis, edema, tooth sensitivity, pocket bleeding, dental caries, dry mouth, and other local inflammation, and for these reasons, oral hygiene before and during pregnancy could be a good way to help prevent and reduce these risks [3,4,5,6].

Moreover, changes in collagen production may slow down wound healing and allow certain bacteria to enter the bloodstream. These bacteria are typically gram-negative and can enhance inflammation through endotoxins and lipopolysaccharides. As a result, levels of inflammatory substances like prostaglandins (PGE2) and cytokines (IL-1) rise locally in the gum crevices and possibly throughout the body. The biological explanation for the increased risk of preterm birth in pregnant women with periodontal disease may involve gram-negative bacteria, dysbiosis, and inflammatory mediators, which are absent in individuals with periodontal health [6,7].

In general, during pregnancy, there is a temporary suppression of humoral and cell-mediated immunological functions and a more susceptible response to every local infection; in particular, there is a suppression of T-helper (Th) 1 and T-cytotoxic (Tc) and a consequent down regulation of some cytokines [6,7].

There is also an up-regulation of Th-2 cells and IgA, IgG, and IL-1ß levels.

It appears that these mediators might have a primary function in the pro-inflammatory response of expecting mothers to common oral infections [8].

Periodontal disease is one of the most common infectious diseases in the world and the sixth most widespread chronic disease. It affects more than 60% of the population in Italy, especially in patients older than 35 years old, and 10% of these cases could be severe forms [9,10,11].

The occurrence of periodontal disease tends to rise steadily as individuals age, with a noticeable spike between the third and fourth decades, peaking at approximately 38 years old. The likelihood of developing periodontitis is higher in smokers and as people get older but appears to level off around 50 years of age [12,13].

Since the 1980s, Miller and co-workers have stated that oral infections, such as periodontal disease, may be an indication of bacteria increasing inflammatory response, involving also pregnancy complications [14].

Animal studies confirmed clinical observations. In pregnant hamsters, it has been reported that gum infections, induced with Porphyromonas gingivalis, lead to a smaller fetus (approximately 20% less weight than normal) and to an up-regulation of inflammatory mediators (TNF alpha, PGE2, and other cytokines) both at the site of infection and in amniotic fluid [15].

This evidence, highlighting a strong association between periodontal disease and adverse pregnancy outcomes, has encouraged clinicians and researchers to focus on this topic [16].

Most of the well-performed, randomized clinical trials in the literature has reported that nonsurgical periodontal therapy during the second trimester of pregnancy does not improve pregnancy outcomes, probably because this can be partially too late to prevent placental colonization by periodontal bacteria, inducing potential injury at the fetoplacental unit. Thus, oral hygiene and professional prevention during the period before conception may be more effective to prevent periodontal disease and adverse pregnancy outcomes [16].

Some studies have delved further into the awareness of women regarding the connection with periodontal health. Aiuto et al. conducted a study involving a sample of 763 women from the north, central, and south regions of Italy with at least one child (52.7%). Of this sample, 40% were above 35 years old, and 52% were between 25 and 35 years of age, and the authors found that young patients often downplay the significance of oral care before, during, and after pregnancy [17]. Based on the results of this observational epidemiological study, nowadays, many women have limited knowledge of the impact of oral health on pregnancy, particularly younger women, so surveys should be updated with information based on the periodontitis–pregnancy relationship. For this reason, the aim of the present questionnaire-based survey is to evaluate the domiciliary oral hygiene of Italian women and their awareness/ literacy about the relationship between periodontal disease, oral hygiene, and negative pregnancy outcomes in women coming from several regions of Italy.

The hypothesis of this study is that women who are not currently pregnant or have never been pregnant have a lower awareness of the importance of oral hygiene and its impact on pregnancy, particularly regarding the risks associated with periodontal disease and adverse pregnancy outcomes.

2. Materials and Methods

The survey was carried out by administering an anonymous questionnaire in the Italian language, generated with Google form, to women registered in the database of patients of the Dental Clinic of the Tuscan Stomatologic Institute (Camaiore, Italy) between December 2022 and December 2023 and including all female volunteers available, because the questionnaire was published online and was distributed through social networks, such as Whatsapp, Facebook, Instagram, and Tele-gram, related to the clinic. The inclusion criteria were the following:

-

Female gender;

-

Aged 18 years or older.

The exclusion criterion was the inability to complete the questionnaire for any reason.

The procedures followed were in accordance with the ethical standards proposed by the committee responsible for human experimentation, the Declaration of Helsinki, and the ethical recommendations of the Saint Camillus International University of Health Sciences for the following principles:

-

Informed consent (participants must be fully informed about the purpose of the survey);

-

Confidentiality and anonymity;

-

Avoiding bias and leading questions;

-

Respecting diversity;

-

Data security;

-

Transparent communication;

-

Building trust and credibility for replies;

-

Aged 75 years or older;

-

Obtaining reliable information.

In fact, the questionnaire, which was translated into English in order to publish these data, respected the following principles: anonymity, in order to increase the veracity of the data collected; brevity, in order to be more accessible and easier to complete; simplicity of language, in order to be better understood, regardless of the level of education and nationality of the participants. It received ethical approval, and it was validated from a psychological point of view (R.L.), taking into account a previous publication [17]. The first part of the questionnaire focused on personal information, such as age and geographical location. Participants then answered questions about pregnancy, children, gynecological visits, dental recommendations, the importance of dental care, and perceptions. The second section aimed at collecting data on the importance of oral hygiene during pregnancy and the association between periodontal disease and adverse pregnancy outcomes. The complete questionnaire is shown in

Table 1. Questionnaire about pregnancy and periodontal health, translated from Italian to English.

1. How old are you?	2. Where do you live in Italy?
- 18–30 years	- South (Calabria, Basilicata, Puglia, Campania, Molise, Abruzzo)
- 30–45 years	- Centre (Tuscany, Marche, Lazio, Umbria)
- 46–60 years	- Islands (Sicily, Sardinia)
- Over 60 years old	- North (other regions)
3. Are you pregnant?	4. If you are not pregnant, have you already had children?
- Yes	- Yes
- No	- No
- I do not know
5. How many children do you have?	6. During gynecological professional check-up do you have received any suggestions to go to the dentist or dental hygienist?
- 1	- Yes
- 2	- No
- 3	- I do not know
- 4 or more
7. Even if you did not receive any recommendations, do you consider important to go for a dental examination before or during pregnancy?	8. May you receive a professional oral hygiene treatment during pregnancy?
- Yes	- Yes always
- No	- Yes, in the first and second trimester of pregnancy
	- Yes, in the third trimester of pregnancy
	- No, it is too dangerous for the fetus
9. Do you think that the domiciliary oral health can have effect on the pregnancy and fetus?	10. If you notice bleeding gums during pregnancy, do you think you should go to the dentist or dental hygienist?
- Yes	- Yes
- No	- Yes but only if it continues for then 3 days
	- No, it is normal if there was bleeding even before the pregnancy
	- No, it is a physiological response of gums to the hormonal stimulus of the pregnancy
11. If you had bleeding gums during pregnancy, who did you ask information to?	12. Which information did you received?
- Dentist or Dental Hygienist
- Gynecologist or Obstetrics	- Free answer
- General Doctor or Family Doctor
- Pharmacist
13. Do you think pregnancy could make you lose teeth?	14. Do you know what periodontal disease is?
- Yes	- Yes
- No	- No
15. Do you think you are affected by periodontal disease?	16. Do you know there is a strong association between periodontal diseases and adverse pregnancy events?
- Yes	- Yes
- No	- No
- I do not know
17. If you replied yes to the previous questions, which are your fount of this information?	18. Knowing that there are bacteria in the mouth that can have positive or negative effects on the entire organism, do you think these bacteria can be transmitted to the fetus during pregnancy?
- Dentist or Dental Hygienist	- No, the placenta protects the foetus
- Gynecologist, Family Doctor, Pharmacist and other medical professionals	- Yes, through the blood stream
- TV and social media (Instagram, Facebook, TikTok)
- Parents, Family and friends - Books, School, University, Journals
- Other

.

This questionnaire has been approved by the internal ethical board of the Unit of Orthodontics and Paediatric Dentistry, University of Pavia, with the following protocol number: “2022-0629-Questionario Gravidanza”.

Statistical Analysis

The analysis explored, as primary endpoints, the recorded questionnaire replies. The numeric data of patient-generated responses, as a percentage, were analyzed using the Stata 12.0 statistical software (Copyright 1985–2011 StataCorp LP Statistics/Data Analysis StataCorp, 4905 Lakeway Drive, College Station, TX, USA), and the significant level was set at p < 0.05. Data analyses also included descriptive statistics for the total patient sample and were according to age. Means with standard deviation scores for each domain were computed. Age, lower/upper jaw, and failing implants were analyzed on disparities. After testing the explanatory variables for normality (Shapiro–Wilk test) and homoscedasticity (Chi-square test), comparisons between subgroups were made using independent Student t-tests.

3. Results

For the present study, a total of 826 interviewed individuals completed the questionnaire. The recruitment lasted approximately 6 months (January–June 2023).

From the analysis of the first part of the questionnaire, it appears that the women who participated in the survey were mostly aged between 30 and 45 years (52,3%), only 6.1% were aged between 46 and 60 years, more than one third were aged less than 30 years (41.6%), and no one was older than 60 years. Half of this sample was from the northern regions of Italy (50.4%), one third (29.1%) were from the south, 14% were from the center, and 6.5% were from islands.

Most of the women who participated in this survey (86.9%) were not pregnant; however, 77.7% of the participants have at least one child. The questionnaire then inquired about the necessity of a dental examination during a gynecological check-up: 94.9% declined, yet 92.4% still believe an initial dentist visit is crucial. With respect to information on the women’s perception of oral hygiene during pregnancy, the following data emerged: 82.6% believe that professional hygiene can always be performed during pregnancy regardless of the month of gestation and 8.5% that it is possible just in the third trimester. Approximately the same percentage believe that a healthy mouth can have effects on the fetus, but only 47% of them believe it is necessary to visit the dentist and/or a dental hygienist in case of gum bleeding during pregnancy for professional oral hygiene.

In

Table 2. Questionnaire about pregnancy and periodontal health with queries and answers from number 9 to number 18 (% of participants who have replied with that option).

9. Do you think that oral health can have effect on the pregnancy and fetus?	10.  If there is gums bleeding during pregnancy, do you think you should go to the dentist or dental hygienist?
- Yes (82.8%)	- Yes (47.0%)
- No (17.2%)	- Yes, but only if it continues for then 3 days (27.4%)
	- No, it is normal if there was bleeding even before pregnancy (9.6%)
	- No, it is a physiological response of gums to the hormonal stimulus of the pregnancy (16.0%)
11.  If you had bleeding gums during pregnancy, who did you ask information to?	12.  Which information did you received?
- Dentist or Dental Hygienist (76%)	“That they could not receive any professional dental care during the pregnancy, just Paracetamol for the pain”. “It is normal to have gums bleeding during pregnancy” “Periodontitis often occurs during pregnancy, especially if you had gingivitis” “It is due to problems before” “It is due to hormonal factor” “Go for a dental examination”
- Gynecologist or Obstetrics (8.3%)
- General Doctor or Family Doctor (8.3%)
- Pharmacist (7.4%)
13.  Do you think pregnancy could make you lose teeth?	14.  Do you know what periodontal diseases are?
- Yes (46.0%)	- Yes (60.0%)
- No (54.0%)	- No (40.0%)
15.  Do you think you are affected by periodontal disease?	16.  Do you know there is a strong association between periodontal diseases and adverse pregnancy events?
- Yes (52.3%)	- Yes (26.4%)
- No (38.5%)	- No (73.6%)
- I do not know (9.2%)
17.  If you replied yes to the previous questions, which are your fount of this information?	18.  Knowing that there are bacteria in the mouth that can have positive or negative effects on the entire organism, do you think these bacteria can be transmitted to the fetus during pregnancy?
- Dentist or Dental Hygienist (59.8%)	- No, the placenta protects the fetus (15.5%)
- Gynecologist, Family Doctor, Pharmacist and other medical professionals (3.9%)	- Yes, through the bloodstream (84.5%)
- TV and social media (Instagram, Facebook, TikTok) (16.9%)
- Parents, Family and friends (7.4%) - Books, School, University, Journals (8.3%)
- Other (3.7%)

, Questionnaire about pregnancy and periodontal health with queries and answers from number 9 to number 18 (% of participants who have replied with that option).

4. Discussion

This manuscript explores Italian women’s awareness of the possible association between periodontal disease and pregnancy outcomes through a survey study. While most participants acknowledged the importance of oral hygiene, many have limited knowledge of its impact on pregnancy, particularly the risks associated with periodontal issues.

In recent years, three possible mechanisms have been proposed and identified by which periodontal infection and adverse periodontal outcomes may be related:

• Translocation and transmigration of periodontal pathogens from periodontal pockets to the fetoplacental unit;
• Actions on the fetoplacental unit of periodontal virulence factors of some bacteria in case of dysbiosis such as lipopolysaccharides;
• Actions on the fetoplacental unit of inflammatory mediators up-regulated during local infection (IL-1, IL-6, TNF alpha, and PGE2) [18,19].

All these mechanisms are discussed in literature and among clinicians, but the prevalent fact is that this correlation is underestimated and unknown by professionals and by mothers.

Among these processes, periodontitis can lead to adverse/negative pregnancy outcomes, such as preterm birth, low birth weight, pre-eclampsia, fetal growth restriction, miscarriage, stillbirth, and gestational diabetes mellitus, but many researchers have pointed out a lack of knowledge in the community about this association [17,20,21].

The present anonymous questionnaire, consisting of 18 questions of the present survey, highlighted some curious aspects of society, reporting a lack of information in young women who do not have proper literacy, and this may be due to a lack of a multidisciplinary approach and confrontations between professionals in a specific phase of life for a woman who also needs psychological help and support from health professionals.

Half of the women who experience gingivitis during pregnancy consult a dental hygienist or dentist, while a small proportion consult a gynecologist or obstetrician, a family doctor, or a pharmacist. The most trusted professionals in this situation are those in the dental field, despite many recommendations involving misinformation about periodontal disease and gingivitis during pregnancy. In addition, the final section of the survey revealed that almost half of the participants said that pregnancy could cause teeth to loosen (46%), while 40% were unaware of periodontal disease and gum bleeding. Almost 40% were unsure if they had periodontitis, and only 26.4% recognized the negative impact of periodontal disease on pregnancy. Most learned about the link from dental professionals, with 16.9% obtaining information from television and social media. Surprisingly, only 3.9% heard about it from other healthcare providers [22]. These findings may indicate that young women’s health information is heavily influenced by TV and social media, leading to the development of apps and other programs aimed at improving professional and home oral hygiene compliance among adolescents and other groups [22,23,24,25,26,27,28,29].

Other researchers have suggested that maternal health during pregnancy may influence not just systemic health but also dental formation and health in children, such as tooth decay and weak enamel, and patients should also be informed about this aspect [23,24]. Despite advances in the understanding of nutrition and health among medical professionals and mothers, the importance of maintaining good home oral hygiene and the link between gum disease and pregnancy complications is often overlooked [17,25,26,27,28,29].

One limitation of this study is its evaluation of women without any standardization or randomization of the sample. This group of women was heterogeneous, because there were old women who had already been pregnant and young women who had not, and this group was not controlled, and it followed only the database of the dental clinic and its related online social media. Furthermore, the sample was quite small compared to the population of all of Italy or the entire world. Another bias could be related to the average age of the cohort of subjects: it was very young. This was probably only due to the casual online distribution of the questionnaire through Google and not because the older patients are not interested in dental hygiene and oral preventive care. Also, the statistical analysis was only descriptive, and future studies with larger sample sizes should include more elaborated data information, including participants’ age range, medical history, and other biases. The questionnaire’s translation was not validated.

Participants from different social classes or educational backgrounds may have given different answers and results due to different cultural backgrounds. In addition, the medical information of these patients was not recorded, but it could be useful to analyze these elements as confounding factors. Patients who are aware of their general health and prevention could be better informed, such as patients with a particular medical history and numerous hospital visits. This is a pilot project of the survey, and monitoring the awareness and literacy of women and professionals in this field should be recommended in future retrospective studies, surveys, and clinical projects to inform patients and doctors.

In the context of this research, the analysis of the questionnaire showed that the majority of women who responded to the questionnaire had a good perception of oral hygiene during pregnancy but did not have adequate knowledge of the subject. In fact, 53% of them believed that bleeding of the gums during home oral hygiene was quite normal during pregnancy. Unfortunately, the survey also revealed some misunderstandings or even incorrect information about oral health prevention, and this information was often given to young women by health professionals, such as gynecologists and/or obstetricians, family doctors, and even dentists, showing a disorganized and inadequate heterogeneous prevention plan even in such a small area of Italy, despite the clinical studies and systematic reviews available in the literature on the subject, recalling that almost half of the cohort came from the northern regions and one third from the southern regions [30,31]. The analysis of the survey also showed that a good portion of the sample does not have sufficient information on periodontal disease and therefore also has an incorrect perception of the effects of oral health or inflammation on pregnancy, and it is still normal to lose teeth during pregnancy as if it were a physiological process.

Nowadays, the national health system should invest more in dental hygienists, decisive figures in the prevention of oral pathologies, including periodontitis, during pregnancy, with the possibility of reducing the negative effects of pregnancy, such as underweight children or premature births, which also entail costs of public care (e.g., incubators), and also the negative effects on the periodontal health of future mothers, with important psychological impairments related to the loss of teeth and a worsening of oral aesthetics [32,33]. Greater cooperation and exchange of information between dentists, dental hygienists, gynecologists, psychologists, midwifes, general practitioners, and pharmacists could also be useful in preventing and controlling the periodontal changes that often occur during pregnancy [34,35,36,37,38].

5. Conclusions

This survey study revealed a lack of knowledge about the relationship between oral infections and periodontal disease and adverse pregnancy outcomes, not only among the general population of women who participated in this survey but also among health professionals, such as gynecologists, obstetricians, pharmacists, family doctors, and dental professionals. Full information on the relationship between pregnancy and periodontitis is essential and should be given to adolescent women to promote good oral hygiene habits from an early age. Dental hygienists should also be involved in antenatal classes to raise awareness among pregnant women.

A multidisciplinary approach is essential, involving dentists and other health professionals, to provide the best and most comprehensive care and to encourage women to maintain good oral health during pregnancy.

This study revealed a notable gap in the awareness and understanding of the connection between oral health and maternal–fetal well-being, emphasizing the need for improved education and literacy to enhance dental care practices among pregnant women.

Larger observational studies and clinical trials are needed to clarify This issue and to standardize the results according to confounding factors, such as the socio-economic status of the participants.