Knowledge of Periodontal Diseases, Oral Hygiene Practices, and Self-Reported Periodontal Problems among Pregnant Women and Postnatal Mothers Attending Reproductive and Child Health Clinics in Rural Zambia

Aim To determine the level of knowledge of periodontal diseases, practices regarding oral hygiene, and self-perceived periodontal problems among pregnant and postnatal women attending reproductive and child health clinics in rural districts of Zambia. Methodology This was a quantitative, questionnaire-based, descriptive, and cross-sectional study that recruited 410 women aged 15 to 43 years. Data were analyzed using SPSS v19.0 computer program. Results Participants knowledgeable of periodontal diseases were 62%; gingivitis signs included gum swelling (87.4%) and bleeding (93.3%). Of all participants, 95.6% practiced tooth brushing: twice/day (38.5%), using plastic toothbrush (95.6%), chewing stick (12.2%), toothpick (10.7%), dental floss (2.0%), and tongue cleaning (55.4%). Self-reported periodontal problems were bleeding gums (23.2%), gums that were reddish (10.5%), swollen (11.0%), painful (15.9%), and mobile teeth (3.4%). In logistic regression analysis, painful gums, reddish gums, and toothpick use were 21.9, 4.7, and 4.3 respectively, significantly more likely to cause gum bleeding on tooth brushing. Conclusions Most studied women had general knowledge of periodontal diseases but only few knew the cause. All participants performed tooth cleaning; however, majority did not know appropriate practices, and only few had periodontal problems. Integration of oral health to general health promotion and periodontal therapy to pregnant women at high risk is recommended.


Introduction
"Periodontal problems" encompass several conditions that include gingival and periodontal diseases [1]. Periodontal diseases always start as gingivitis which denotes an inflammation of gingival tissue due to microbial challenge [2]. Epidemiological studies show that gingivitis may or may not progress to periodontal disease [3]. However, the most significant factors for gingivitis to progress to periodontal diseases include presence of periodontal pathogens in particular the red complex that includes the Porphyromonas gingivalis, Tannerella forsythensis, Treponema denticola, genetics, and poor oral hygiene in the form of accumulation of oral biofilm that is full of millions of microbes (1 gm contains more than 10 11 microorganisms) and of different types as gram positive and gram negative [4].
During pregnancy, periodontal tissues' response to biofilm challenge is reinforced as female sex hormones are necessary but not sufficient to produce gingival changes by themselves and usually plaque plays a role [5]. Pregnancy period is accompanied by an increase in the levels of both progesterone and estrogen which by the third trimester, reaches levels 10-30 times more than the one seen during typical menstrual cycle, and changes in the gingiva include an increase in gingivitis that usually starts during the second to third month of pregnancy and increases in severity through the eighth month, where it decreases along with the abrupt decrease in hormone secretion [6,7]. Pregnancy affects the severity of previously inflamed gingival tissues but does not alter healthy gingiva [8]. Pregnant women with previous chronic gingivitis which attracted no attention before pregnancy become aware of their gingival status as the previously inflamed areas become enlarged and edematous and more noticeably discolored with an increased tendency to bleeding [9].
An intensive approach to plaque removal may be effective to treat pregnancy gingivitis and all forms of gingival enlargements [10]. Improving maternal oral hygiene is important for oral health and may reduce systemic proinflammatory cytokines and improve maternal outcomes [11]. In a study involving 409 postpartum women, only half of the women brushed their teeth more than once a day for about 1-3 minutes; in addition, a substantial proportion of patients (35%) reported seeking oral care from a dentist only when they experience pain, thus making preventive strategies less possible [12].
e impact of periodontal disease on pregnancy outcome is now under scrutiny. Findings from observational studies yielded inconsistent conclusions on the relationship between periodontal disease and various pregnancy outcomes (including early pregnancy loss, preterm birth, low birth weight, and preeclampsia) [13]. A close relationship was shown to exist between lack of oral hygiene and periodontal disease in pregnant women [14]. Most of these ill-effects could be avoided by good oral hygiene practices [15]. Traditionally, tooth brushing using manual or powered toothbrush and flossing have been considered the standard for routine plaque removal and gingivitis reduction [16]. In Zambia, retrievable information on oral hygiene practices and gum/periodontal problems among females at reproductive age in particular pregnant women and mothers for young children is lacking. e aim of this study is to assess knowledge on periodontal diseases, practices regarding oral hygiene, and self-reported periodontal problems among pregnant women and postnatal mothers attending reproductive and child health clinics in rural Zambia.

Study Design, Place of Study, and Participants.
is was a quantitative, descriptive, cross-sectional health facility-based study. It was conducted in Chibombo and Chisamba rural districts located in the Central Province in Zambia. Five different health facilities participated including four rural health centres (RHC) and one district hospital. ese health facilities were readily accessible and thus conveniently selected. Specific health facilities that participated were Chibombo RHC, Twalumba RHC, and Mwachisompola RHC from Chibombo district together with Malombe RHC and Liteta District Hospital from Chisamba district. Recruitment of study participants involved all pregnant women (PW) who were routinely attending 2nd visit antenatal clinic and all postnatal mothers (PM) who were routinely attending postnatal services provided that they were willing and thus gave their consent.

Sampling.
e single stage cluster sampling was utilized to select the five RHC clinics for the study, and the recruitment of study participants was done by registering consecutively every consenting pregnant woman and postnatal mother in the selected health facilities until achieving the required sample size. No random sampling was undertaken rather a convenience sampling approach was used within the clinic setting.

Data Sources and Collection Procedure.
A pretested and validated questionnaire which was prepared in English and translated in Bemba and Lenje, the local languages of the study participants, was used to interview 90% of the participants who could not read and write, and the rest undertook a self-administered questionnaire. e data collection tool consisted of questions on sociodemographic factors (age, level of education, and marital status), knowledge of periodontal diseases (17 items), oral hygiene practices (9 items), and self-reported periodontal problems (5 items). Correct responses/answers in each section were summed up and divided over the total items for calculation of percentages out of 100% as regards to knowledge of periodontal diseases, oral hygiene practices, and self-reported periodontal problems. e respondents who scored above 50% were graded as "good" and those who scored below 50% were graded as "poor."

Data Analysis.
Data were entered into a computer and analyzed using Statistical Package for Social Sciences (SPSS) version 19.0. Frequency tables were generated. Data transformation was undertaken in particular dichotomization of some variables that had more than two options for example, age (15-24 years versus 25 years and above) and level of education (primary education and lower versus secondary, college, and university education). Furthermore, the type of occupation of the study participants was dichotomized and recoded as informal (none and self-employed) versus formal (employed and business persons), and health facility was dichotomized as hospital versus health centres. e responses to specific oral hygiene practices and self-reported periodontal problems were dichotomized into presence (Yes) or absence (No) of the specific condition. Cross tabulations were processed between dichotomized categorical variables that generated two-by-two contingency tables. e chi-square test or Fisher's exact test (in cross tabulation cases where one or more of the cells had a value of "5" or less) was used to detect statistically significant differences between two groups of any categorical variables under consideration. In all analyses, the statistical significance level was set at "<0.05." For binary logistic regression analyses, the dichotomized variables were recoded into zero (0) for a code that was assigned to an advantageous or nonproblematic aspect, and a code number of one (1) was given to any previous code number that meant to be in a disadvantageous or problematic aspect. For example, someone who is brushing the teeth twice a day in line with the international recommendation (thus being on an advantageous aspect) were given a code number of zero (0), and anyone who was not brushing according to this recommendation did put him/herself into disadvantageous aspect and thus was given a new code number of one (1). Also, anyone having a sign of a disease or condition under study was given a code number of one (1), whereas a study participant without any sign of that disease or condition was given a code number of zero (0). All those variables that were recoded for the binary logistic regression analyses were subjected to descriptive statistics in particular cross tabulation. Variables with a significant probability (P) value (P < 0.05) during cross tabulation were selected and entered into the logistic regression analysis. In addition, all variables that were thought to be important as predisposing factors for the dependent variable (gum bleeding) provided that P value was less than 0.3 (arbitrarily chosen) and were included in the logistic regression analyses. e characteristic of maternal status, meaning that the study participant was either "pregnant" or a "postnatal" woman, was deliberately included in the model although the probability value was far above the selected cutoff point because it was strongly felt that this factor is associated with bleeding gums. e backward stepwise (Wald) logistic regression method was chosen for analysis. e dependent variable was the self-reported condition as experienced "gum bleeding"' and the rest of the variables on oral hygiene practices, knowledge, and other predisposing conditions were considered as categorical "covariates" whereby the contrast was the "indicator" and reference category was set as the "first" category. e options were set at the 95% confidence interval (95% CI) for the exponential (B) whereby the probability for the backward stepwise (Wald) model was set at entry value of 0.05 and removal at value 0.10. e final iteration of the backward stepwise (Wald) model was included as final results.

Distribution of Study Participants.
A total of 410 study participants comprising 270 pregnant women and 140 postnatal mothers were recruited ( Table 1) with age ranging from 15 to 43 years (Mean age ± standard deviation: 25.72 ± 6.88 years). e median age was 24 years. Majority of the study participants were at 15-24 years of age (65.7%). e ever married women were the majority (83%). Most of the study participants had primary education or less, and generally the employed group was 56%. Health centres had higher number of study participants (75%) as compared to the hospital.

Oral Hygiene Practices.
e prevalence of oral hygiene practices and self-reported periodontal problems among pregnant women and postnatal mothers is shown in Table 2. All participants claimed to practice regular tooth brushing, but frequency of tooth brushing varied among individuals. Tooth brushing once per day was 24.9% and brushing twice per day was 38.5%. ose who brushed three times per day were 36.3%. Duration of tooth brushing was estimated to take about 1-3 minutes (57.1%). Chewing stick users were at 12.2%. Use of a plastic toothbrush to clean teeth (Table 2) was significantly higher among postnatal mothers (100%) than in pregnant women (93.3%, P � 0.001, χ 2 � 9.672).
Replacement of tooth brushes once/month was done by 25.4% while 39.3% replaced their toothbrushes after every three months. Slightly more than half of the study participants (55.4%) had the habit of cleaning the tongue regularly. Regular use of toothpaste during tooth brushing was reported by 91.7%, and there were no significant differences between pregnant women and postnatal mothers ( Table 2).
e level of knowledge of oral hygiene practices when categorized as "good" or "poor" in relation to different demographic factors among women attending the RHC clinics in rural Zambia is shown in Table 3.
Of all the participants in the category of good knowledge, there were more married women than singles, more of the low level of education, and more from the health centres than their respective counterparts. However, the level of knowledge of oral hygiene practices (good versus poor) did International Journal of Dentistry not statistically differ significantly between age groups, marital status, level of education, employment, and type of health facility attended. ere was a significantly higher proportion of pregnant women (Table 3) in the category of poor knowledge (69.8%) as compared to that of good knowledge of oral hygiene practices (59.2%) (χ 2 � 4.741, P � 0.029) ( Table 3). e level of knowledge of gum and periodontal diseases in relation to different demographic factors among women attending the RHC clinics in rural Zambia is shown in Table 4. e level of knowledge of gum and periodontal diseases as categorized as "good" or "poor" in various demographic factors including pregnant women and postnatal mothers, low and high education, singles and married women, and employment status was homogeneous in that the difference was not statistically significant ( Table 4).
Results of the bivariate analysis regarding self-reported gum bleeding in relation to maternal status (pregnant woman or postnatal mother), sociodemographic factors, lack   International Journal of Dentistry of knowledge on periodontal diseases, oral hygiene practices, and self-reported periodontal problems are shown in Table 5. Prevalence of self-reported gum bleeding was significantly associated with being of older age 25-45 years (χ 2 � 4.04, P � 0.036) and lack of knowledge that eating balanced diet can prevent gum and periodontal diseases (χ 2 � 5.527, P � 0.019). Other significant factors were as follows: not changing the toothbrush after a period of 1-3 months (χ 2 � 10.766, P � 0.001), self-reported presence of swollen gums (χ 2 � 97.703, P < 0.001), reddish gums (χ 2 � 70.871, P < 0.001), painful gums (χ 2 � 98.310, P < 0.001), and shaky (mobile) teeth (χ 2 � 18.812, P < 0.001). e final model of the binary logistic regression analyses (backward stepwise, Wald) for occurrence of self-reported gum bleeding in relation to selected demographic factors and periodontal problems among pregnant women and postnatal mothers is shown in Table 6.
Factors that more likely and significantly associated with self-reported gum bleeding were being a pregnant woman (odds ratio (OR): 6.198

Discussion
e study was a quantitative, descriptive, cross-sectional investigation that took place among pregnant women and postnatal mothers in Chibombo and Chisamba rural districts in Zambia. e sample size and age ranges were almost similar to a study done in Nigeria [9]. is could be due to the fact that this is the reproductive age (15-49 years) in sub-Saharan Africa [17].
In the current study, it showed that majority of the women did not go to school or went up to primary level. is could be due to poverty and early marriages which stands at 31.4% in Zambia [18], especially in rural areas where this study was conducted as well as long distances to a few available schools [19] which led many to drop out of school and end up getting married. e proportion of study participants that had primary education was similar to a study done in Pakistan [20], where more than half of the participants ended at primary school level (Asia levels at 64% versus sub-Saharan Africa with 65% [21]). e current study found that more than three quarters were married (83%) than the singles. is is different from the study done in south-west Sydney [22], where more than half of the participants were single, and it is speculated that the possible reason might be the difference in culture and lifestyles. Health centres had more RHC clinic attendances than the hospital. is can be attributed to the number of rural health centres included in the study (four) versus one rural hospital as is typical of levels and referral health system in Zambia. Another study done in Nigeria [9] reported that women do not seek professional help if they perceive that their gingival status is normal and that women were more likely to use dental services in pregnancy if married, educated, and had dental insurance. However, for comparability, retrievable reports on oral health among pregnant women in Zambia were scarce.
In the current study, almost all the respondents were brushing their teeth at least once per day and the finding is consistent with what was reported elsewhere in Tanzania [23]. e use of chewing sticks (twigs or roots of certain plants that are chewed until one end is frayed and used to clean teeth) in the current study was slightly more than one  to ten (1 : 10), and the possible explanation might be due to difficult affordability within the rural constraint economy and these results are consistent with the studies done in Nigeria and Tanzania, respectively [2,23]. In the present study, a minority of the subjects use dental floss, unlike the study done in Australia [6] where the majority were using dental floss with an understanding that it would help prevent gum disease. is shows that the participants in the current study in rural Zambia had insufficient knowledge on interdental space cleaning and were limited to toothbrushes as cleaning aids [24]. Most of the study participants pointed out that plaque can be controlled by maintaining good oral hygiene, and this is achieved by brushing the teeth at least twice daily and this is in line with what is recommended worldwide [21]. Serious attention to this important preliminary understanding emphasis on oral hygiene instruction, for example, systematic tooth brushing for two minutes [25] and interdental cleaning might be a good area to begin with when launching customized oral health program in Zambia. e most used tooth cleaning aids were plastic toothbrush, followed by chewing stick, whereby the latter is believed to be an effective oral hygiene aid by which different cultures have attached functional value since ancient times [26]. It happened that about one percent of the pregnant women used a finger for cleaning teeth whereas their level of education was above primary school. is could be due to extreme poverty as most of them were unemployed. Also, the issue of beliefs cannot be underestimated because   International Journal of Dentistry these participants, for example, could have used chewing sticks that were readily available in rural areas. e proportion of knowledge of periodontal diseases displayed by women in the age group less than 30 years was moderately higher compared to those above 30 years, and further, it was higher among the singles as compared to the married; however, the differences did not reach a statistically significant level. e study participants who had attained secondary education were more knowledgeable than the ones who were primary school leavers or below. is simply shows that education plays a part in terms of knowledge and exposure [27]; however, the difference was statistically insignificant.
e proportion of pregnant women that had knowledge of periodontal disease was moderately higher than the postnatal mothers. e reason could be that pregnant women were able to identify themselves with the features of periodontal diseases that are modified by the presence of high levels of circulating hormones during pregnancy; however, the differences did not reach a statistically significant level. Even though the pregnant women and the postnatal mothers were knowledgeable about periodontal diseases, only a minority were aware of the causative factor and dental plaque.
is may point to a serious need for proper oral health education to the pregnant women and postnatal mothers in the studied rural population. Slightly less than three quarters of the participants knew what plaque was and how it could be removed, and this is consistent with the Saudi Arabia study [28], but inconsistent with the findings from elsewhere [6] where the majority knew about dental plaque and did not know about periodontal disease. e possible explanation for this might be the differences in the availability of oral health education and health promotion programs in these populations [29]. e majority of the pregnant women and postnatal mothers knew the presentation of periodontal disease as well as the prevention. Proper nutrition and healthy lifestyle also play a key role in the general well-being of the mother to be, and this includes periodontal health [30].
Regarding self-reported gum and periodontal problems, a minority of the study participants reported having bleeding gums, and the findings are similar to those reported by women attending a tertiary health institution in Nigeria [31]. On the other hand, our findings differ from the ones reported in Nigerian women [32] and Ghanaian women [33] where bleeding of gums was much higher than what was found in our study, and the most probable explanation is the difference in methodology.
e current study has a low proportion of women reporting painful gums, swollen gums, and bleeding gums as compared to other studies which revealed that hormonal changes in pregnancy combined with neglected oral hygiene tend to increase the gingivitis which is characterized by increased redness, edema, and higher tendency toward bleeding [34,35].
Use of plastic toothbrush in our study was significantly higher among pregnant mothers than postnatal women, and this difference might be accounted by possible exposure to oral health education session during antenatal visits.
e results in the current study are similar to the study done in Nigeria [36] where most of the participants used plastic toothbrushes and paste.
Likewise, there were no statistically significant differences on the level of knowledge of gum and periodontal diseases in relation to different demographic factors between pregnant women and postnatal mothers in our study, thus showing a similar experience between the groups. ese results are in agreement with Bangalore report where awareness of gum disease among pregnant women was not associated with age and educational qualifications [37].
Lack of knowledge that eating balanced diet can prevent gum and periodontal diseases was in the bivariate analysis found to be a significant factor as regards to the self-reported gum bleeding on tooth brushing. Lack of knowledge on the importance of balanced diet was higher in our study than in Bilaspur, India [38], and the possible reason among others was that our study was done in rural area alone while the latter was in both urban and rural. In comparison with postnatal mothers, pregnant women were significantly more likely to experience gum bleeding on tooth brushing, and this might be explained by the inflammatory reaction of the gingival due to hormonal changes coupled with presence of poor oral hygiene [34,35]. Findings from a similar study in India revealed that less than one third of the studied pregnant women had experienced bleeding from gums during pregnancy, and that, slightly less than a quarter did not brush their teeth when they experienced bleeding, instead, they cleaned using fingers [39]. e results of this study must be viewed in the light of certain limitations. Due to constraint in resources especially time and funds to collect data for this elective study, the rural area was selected for convenience. is approach limits the inference of the findings to be much more applicable to the rural districts studied population and not to the whole RHC clinic attendees in the country. is study relied on selfreported information and therefore the data are subject to some form of bias. Furthermore, the face-to-face interview with most of the study participants might have provoked "socially desirable responses" instead of what was the real practice in daily life [40,41].

Conclusions
In this study, most pregnant women and postnatal mothers had general knowledge of periodontal diseases but only few knew the cause and their prevention. All participants were engaged in tooth cleaning procedures; however, the majority did not know the appropriate practices. Self-reported signs of gingival and periodontal diseases were experienced by the minority.

Recommendations
In view of the ever growing evidence that periodontal diseases are associated with various systemic conditions including adverse pregnancy outcomes, it is recommended that oral health be integrated into general health care of pregnant women in all reproductive and child health clinics in the country.

Data Availability
Quantitative data were used. Data used to support the findings of this study are available from the corresponding author upon request.

Ethical Approval
Ethical clearance was granted by the Research and Publication Committee of the School of Dentistry empowered by MUHAS Ethical Committee.

Disclosure
is work was an elective research study which was part of the requirement for the Doctor of Dental Surgery (DDS) undergraduate training at Muhimbili University of Health and Allied Sciences (MUHAS).

Conflicts of Interest
e authors declare that there are no conflicts of interest regarding the publication of this article.

Authors' Contributions
T. M. Kabali participated in developing the proposal and data collection tool, performed all the data collection, data entry into the computer, and some data analysis under guidance, and was responsible for interpretation, write-up, and submission of the manuscript. E. G. Mumghamba conceived the study, supervised the development of proposal and data collection tool, performed data entry into the computer, data cleaning, guided data analysis, and logistic regression analyses, was responsible for interpretation and write-up, and gave final approval to submission of the manuscript.