Use of Medicinal Plants during Pregnancy, Childbirth and Postpartum in Southern Morocco

Southern Morocco, particularly the Guelmim-Oued Noun region, is rich in a wide diversity of plant species. Pregnant women in this region use medicinal plants during pregnancy and childbirth for various purposes; however, the use of these plants has never been documented. The objectives of this study are threefold: to estimate the prevalence of medicinal plant uses by pregnant women in the province of Guelmim, Morocco, to describe the traditional practices of self-medication and to determine the associated factors. This is a multicenter cross-sectional study with descriptive and analytical approaches. Data were collected using an interview questionnaire, which was administered to pregnant women at health care centers and hospitals in the province of Guelmim. A total of 560 women participated in this study. The prevalence of medicinal plant use was 66.96%. Artemisia herba-alba Asso, Thymus maroccanus Ball., Trigonella foenum-graecum L., Aloysia citriodora Palau, Lepidium sativum L. and Cuminum cyminum L. were the plants with the highest UV. Pain, the induction and facilitation of childbirth, flu syndrome and anemia were the most listed reasons for use. The use of medicinal plants was significantly associated with the level of education (chi-square = 15.651; p = 0.004), and pregnancy monitoring (chi-square = 5.283; p = 0.028). In the province of Guelmim, the prevalence of the use of medicinal plants by women during pregnancy and childbirth is high. Further research is necessary in order to explore potential associated risks and complications.


Introduction
The concept of traditional Arabic herbal medicine has increasingly attracted interest among traditional herbalists and the scientific community worldwide. According to the World Health Organization (WHO), 80% of the world's population, especially in developing countries, uses a variety of traditional medicines for their primary health care [1]. In the Arab world, traditional medicine has always been practiced despite advances in modern medicine.
In Morocco, the number of medicinal plants is estimated to be about 600 species [2,3], and more than half of them (360 species) are used for the treatment of a wide variety of diseases [4,5]. Traditional medicine is a very important form of health care for many rural populations, especially in the mountainous regions of the Atlas [6,7]. It has been estimated that 50% to 75% of the Moroccan population depends on the use of medicinal plants for their remedies [8].
Pregnancy is accompanied by physical and physiological changes in the female's body leading to many pregnancy-related problems, including nausea, vomiting, constipation and heartburn [9]. Pregnant women tend to turn to natural medicinal plants (MPs) rather than prescription drugs to deal with these changes, especially because they are concerned about the safety of the fetus [10].

The Study Area
The Province of Guelmim is part of the Gulemim-Oued Noun region; it covers an area of 10,783 Km 2 , which account for 18% of the territory of the region ( Figure 1). It is bordered to the north by the provinces of Tiznit and Sidi Ifni, to the south by the provinces of Tan-Tan and Assa-Zag, to the east by the provinces of Tata and Assa-Zag and to the west by the Atlantic Ocean. Administratively, the province of Guelmim is made up of two territories and 20 municipalities, 2 of which are urban. The province of Guelmim constitutes a buffer zone between the Moroccan Sahara and the Souss plain. The proximity of the Atlantic Ocean attenuates the effects of the Sahara Desert close to the ocean. The climate is marked by a variability in precipitation. The average annual rainfall varies between 90 and 120 mm. The maximum and minimum temperatures are 45 • C and 0.1 • C, respectively. The average annual temperature is around 20.5 • C. The winds are very frequent causing sand accumulations of different forms. Map of the province of Guelmim and boundaries of the study area; High commission for planning-Guelmim regional directorate. (https://www.hcp.ma/region-guelmim/Presentation-dela-region_a1.html (accessed on 1 April 2021)) .

Type of Study
This is a cross-sectional, descriptive and analytical study conducted in the province of Gulemim.

Study Population
The study opted for a comprehensive sampling by including all the pregnant women who presented themselves for the prenatal consultation (PNC) at the level of all structures within the primary health care facilities network in the province of Guelmim, namely: 05 s-level rural health centers with a delivery unit (127 pregnant women monitored), 04 firstlevel rural health centers (28 pregnant women monitored) and 09 first-level urban health centers (305 pregnant women monitored). For women who had given birth, the study exhaustively recruited all women who admitted themselves to the hospital maternity ward during the study period in order to collect as much information as possible on the therapeutic uses of the medicinal plants used during pregnancy and childbirth.
Inclusion criteria: All pregnant women who presented themselves for prenatal consultation at all structures of the network of primary health care facilities and women admitted for childbirth at the maternity hospital in the province of Guelmim.
Exclusion criteria: Women who refused to participate in the study. Map of the province of Guelmim and boundaries of the study area; High commission for planning-Guelmim regional directorate. (https://www.hcp.ma/region-guelmim/Presentation-dela-region_a1.html (accessed on 1 April 2021)).

Type of Study
This is a cross-sectional, descriptive and analytical study conducted in the province of Gulemim.

Study Population
The study opted for a comprehensive sampling by including all the pregnant women who presented themselves for the prenatal consultation (PNC) at the level of all structures within the primary health care facilities network in the province of Guelmim, namely: 05 s-level rural health centers with a delivery unit (127 pregnant women monitored), 04 first-level rural health centers (28 pregnant women monitored) and 09 first-level urban health centers (305 pregnant women monitored). For women who had given birth, the study exhaustively recruited all women who admitted themselves to the hospital maternity ward during the study period in order to collect as much information as possible on the therapeutic uses of the medicinal plants used during pregnancy and childbirth.
Inclusion criteria: All pregnant women who presented themselves for prenatal consultation at all structures of the network of primary health care facilities and women admitted for childbirth at the maternity hospital in the province of Guelmim.
Exclusion criteria: Women who refused to participate in the study.

Questionnaire
A researcher-administered questionnaire was used for data collection. The first part of the questionnaire was devoted to the socio-demographic characteristics of the women surveyed (age, level of education, marital status, language spoken, height, weight, place of residence, professional occupation and income). The second part included questions related to pregnancy (reason for consultation, parity, gestation, pregnancy monitoring, medical, surgical and gynecological-obstetrics history, pregnancy at risk, type of pregnancy at risk by using prenatal consultation follow-up sheets as part of the pregnancy and childbirth followup program (PCFP)). The last part of the questionnaire covered information related to the use of MPs (vernacular name of each species, mode of preparation and administration, period of use and reasons for use).
First, a list of the vernacular names of the medicinal plants used by the respondents was prepared by referring to the taxonomy of Fennane et al. (1999Fennane et al. ( , 2007 and 2014) on the flora of Morocco [30][31][32]. The scientific names of the plant species were determined based on the list of plants presented on the site (http://www.theplantlist.org (accessed on 1 May 2021). Validation of the concordance between the vernacular names, the botanical names and the names in French were carried out at the Laboratory of Biotechnology and Valorization of Natural Resources of the Faculty of Sciences, University Ibn Zohr, Agadir, Morocco.

Ethical Considerations
The present study was approved by the ethics committee for biomedical research at the Faculty of Medicine and Pharmacy of Rabat, Morocco, under the number 29/19. The consent for participation in the study was obtained before each interview by proving to the participants all the information related to the nature of the study and its objective. The women included in the study were identified by an anonymous study number corresponding to each participant. In addition, the confidentiality of the data collected was rigorously respected.

Statistical Analysis
Quantitative variables were presented as the median ± interquartile range. Qualitative variables were described using frequencies and percentages. A test of association between categorical variables was carried out using chi-square test or Fischer's exact test in the case where the conditions of the chi-square test were not met. The significance level was set at 5%. The data collected were coded, entered, processed and analyzed using SPSS version 24.0 software.
Ethnobotanical data were analyzed using the use value (UV) and relative frequency citation (RFC) to determine which species were well known and most used by the women in this study. UV is a quantitative index that demonstrates the relative importance of locally known species [33,34].
RFC shows the local importance of each species and is obtained by dividing the number of informants mentioning a useful species (frequency citation (FC)) by the total number of informants in the survey (N) [35]. This index was calculated using the following formula: RFC = FC/N (0 < RFC < 1).
Use value (UV) was calculated according to Phillips and Gentry et al. 1994 [33] using the following formula: where "∑ "refers to the number of uses mentioned by the informants for a given species and "N" refers to the total number of informants interviewed. If a plant secures a high UV score, that indicates that there are many use reports for that plant, while a low score indicates fewer use reports cited by the respondents.

General Characteristics of the Population Surveyed
A total of 560 pregnant and postpartum women were interviewed, 305 pregnant women were interviewed at the first-level urban health centers, 127 pregnant women were interviewed at the second-level rural health centers with delivery unit, 28 pregnant women were interviewed at the first-level rural health centers and 100 women delivered their interviews at the maternity hospital (Table 1). Table 1. Distribution of pregnant women interviewed by health structures.

Health Structures Number of Pregnant Women Interviewed
First-level urban health centers 305 Second-level rural health centers with delivery unit 127 First-level rural health centers 28 Maternity hospital 100 Total 560 The characteristics of the population surveyed are presented in Table 2. The median age of the women surveyed was 30 years with an interquartile range (IQR) of 10.14 years. Almost all (98.9%) of the respondents were married. Women with no level of education represented 24.5% of the respondents, and those with a university level represented 13.1%. Women from urban areas made up 66% of the respondents. Women covered by health insurance represented 23.8%, and those covered by beneficiaries of the medical assistance scheme for the economically underprivileged persons (RAMED) represented 50.5%. Half of the participants had very low income, while 10.6% were rich. As for the occupation of the husbands, 96.6% of the spouses worked intermittently. Women with previous gynecologicalobstetrics, medical and surgical history represented 27%, 19% and 6%, respectively. In terms of gestation, 29% were first-timers and 27% second-timers. Nulliparous women represented 11% of the respondents, second parents 26.5% and third parents 17.7% Pregnant women under medical control (pregnancy follow-up) represented 93.7% of the respondents, and 34.3% of them were diagnosed with high-risk pregnancies.

Prevalence and Risk Factors Linked to the Use of MPs
This study showed that 67.45% of the respondents used MPs during pregnancy, 26.82% during childbirth and 5.73% at postpartum (Figure 2). With regard to the period during which MPs were used, 48.89% of women used MPs during the first trimester, 24.07% in the second trimester and 27.04% in the third trimester ( Figure 2). In addition, data analysis showed that the use of MPs by pregnant women is related to the level of education (p = 0.004) and also with the pregnancy follow-up (p = 0.028) ( Table 2). pertension and 3.97% with pre-eclampsia (Table 2).

Prevalence and Risk Factors Linked to the Use of MPs
This study showed that 67.45% of the respondents used MPs during pregnanc 26.82% during childbirth and 5.73% at postpartum (Figure 2). With regard to the perio during which MPs were used, 48.89% of women used MPs during the first trimeste 24.07% in the second trimester and 27.04% in the third trimester ( Figure 2). In addition data analysis showed that the use of MPs by pregnant women is related to the level o education (p = 0.004) and also with the pregnancy follow-up (p = 0.028) ( Table 2).

Monograph of Medicinal Plants Used by Pregnant Women and Reasons for Use
A list of the plants identified during this study is presented in Table 3. They are presented according to families, scientific names and vernacular names, the modes of preparation, the use value (UV) and the relative frequency of citation (RFC). Data analysis revealed the presence of 43 different MPs used by pregnant women. They belong to 23 botanical families, the most represented ones were Apiaceae (seven species), Lamiaceae (five species), Asteraceae and Fabaceae (four species), while other families were represented by either one or two species.
The use value (UV) of the species (Table 3)

Mode of Preparation and Route of Administration
The present study revealed that various routes are used for the administration of herbal preparations. The oral route was the predominant one (73.21%), followed by

Mode of Preparation and Route of Administration
The present study revealed that various routes are used for the administration of herbal preparations. The oral route was the predominant one (73.21%), followed by vaginal (20.53%) and then the nasal route (3.84%) ( Table 4). With regard to the mode of preparation, decoction was the preferred mode (34.86%) followed by infusion (31.27%) ( Table 5).

Source of Information
This survey showed that 46% of the pregnant women interviewed refer to family members for information related to MP use, while 34% refer to neighbors and friends ( Table 6). Table 6. Top sources of herbal medicine recommendations.

Discussion
This is the first study on traditional self-medication practices related to pregnancy and childbirth in the province of Guelmim, Morocco. The aim of this study was to estimate the prevalence of the use of medicinal plants by pregnant women and to determine the associated factors. Many reports have documented the use of herbs by pregnant women for medical treatments [28,[36][37][38][39][40]. In this study, we show that pregnant women in the province of Guelmim also use MPs during pregnancy. The prevalence of medical plant use differs from one country to another [28,39,[41][42][43][44][45][46]. In the province of Guelmim, 66.96% of women use herbal medicine during pregnancy. This rate is significantly high compared with other similar studies conducted in other countries, such as Kenya, India, Oman, Palestine, Egypt and Taiwan [16,36,38,47,48]. These variations in prevalence could be associated with differences in the study design and/or sample dynamics [49], and also to the existence and enforcement of laws governing the marketing of medicinal plants, which also varies between countries [42,50]. The difference in socio-demographic and cultural factors also play a role in the number of women who use MPs [49]; many studies have revealed a strong belief among women in the safety of MPs during pregnancy [51][52][53], although little scientific evidence exists on their safety [50,54,55].
In a recent survey carried out in Brazil, 60% of the women who participated in the study did not believe in the existence of toxic effects of MPs, and around 39% were unaware of the potential adverse effects of MPs [56]. In addition, pregnant women tend to turn to MPs to ease complications associated with pregnancy because many medical prescriptions are contradicted by pregnant women [57].
In this study, women used herbal medicine especially during the first trimester and the labor period. This can be explained by the increase in pregnancy-related problems during these periods [58]. Herbal medicine use during the first trimester has been reported previously [40,43,55,[58][59][60][61][62]. Other studies have reported that the use of medicinal plants is more common in the second trimester [63], third trimester [64] or throughout pregnancy [49].
The timing of MP usage depends on the reasons behind using herbs and varies geographically from one region to another [19,43,55,58,65,66]. This study showed that the most common reasons for using MPs by pregnant women were pain, the facilitation of childbirth, flu syndrome, anemia and the induction of labor. These results are in accordance with previous studies [17,40,61,63,64,67,68]. According to El Hajj and Holst (2020), medicinal plants can sometimes be used in the context of maternal care to treat pregnancy-related problems and often to improve the well-being of the mother and/or the unborn child [69]. For instance, ginger has been used for nausea and vomiting in the first trimester of pregnancy [37,55] and peppermint, thyme, chamomile and green tea for bloating, upset stomach and maintaining health during pregnancy [42,55,70]. Other studies have reported various other reasons for using MPs during pregnancy, such as improving the beauty and health of the fetus, and even the intelligence of the future child [16,20,49,58,59,62,71,72], enhancing fetal growth [17,68,73], as nutritional supplements, to treat skin problems and urinary tract infections [74] and to increase milk production during lactation [63]. It has also been show that MPs can ease pregnancy, improve the course of pregnancy [63], prevent/treat malaria and prevent miscarriages [17,40,73,75]. Medicinal plants are also used to fight against sleep disorders, anxiety and fatigue, to control blood sugar and cholesterol levels [76,77], maintain pregnancy, induce labor and facilitate childbirth and delivery, and for postpartum hemostasis [67].
The socio-demographic characteristics of the respondents differ from one country to another [53,60,78,79]. In this study, the median age of women who use medicinal plants was 30 years. Similar results were reported in other studies [74,80].
The present study showed that the use of medicinal plants is related to the level of education (p = 0.004) and to the follow-up of pregnancy (p = 0.028). Women with a high-level school of education make less use of MPs with a proportion of only 14%. Similar results were reported in previous studies [63,81].
The level of education is an important factor in terms of reproduction and health; the higher the level of education of women, the more it contributes to and facilitates their access to information and allows them to consult and be followed by medical specialists and to respect their instructions [82]. Illiteracy has been shown to be an important determinant associated with the use of herbal medicines [28]. In a review of 50 studies published by [83], it was reported that the use of MPs during pregnancy was significantly (p < 0.05) higher among women with a low level of education, higher age, married status, low socio-economic status, a low level of education of the spouse and a previous history of MP use during previous pregnancies. Other studies have revealed statistically significant differences according to age, place of residence and education of husbands, marital status, multiparity/nulliparity and many other variables [10,14,18,28,37,49,80]. This study has limitations such as not taking into consideration the psychological factors related to the use of MPs by pregnant women during pregnancy and childbirth.
The plants listed in this study have a very important place in traditional herbal medicine in Morocco, in Mediterranean countries and in the Middle East [28,40,[84][85][86][87][88], indicating the therapeutic importance of these plant species in the cultural heritage of populations, their abundance and their ease of acquisition. Indeed, the south of Morocco, in particular the Guelmim-Oued Noun region, is known to have a great diversity of plant species [29]. In this study, we found that the most common plants used were A. herba-alba Asso, T. maroccanus Ball., A. citriodora Palau and T. foenum-graecum L. In other parts of Africa, the four species of MPs used mostly by pregnant women are Zingiber officinale (ginger), Allium sativum L. (garlic), Cucurbita pepo L. (pumpkin) and Ricinus communis L. (castor oil) [83], while in the Middle East, peppermint, ginger, thyme, chamomile, sage, anise, fenugreek and green tea were among the most common herbs used during pregnancy [40]. At the international level, ginger, cranberry, valerian and raspberry were among the most used plants [43]. The choice of plants is related to the culture and the season [49].
During this survey, the highest UVs were attributed to the following MPs: -A. herba-alba Asso (UV = 0.059); it is one of the most used plants in the Mediterranean region to treat various diseases including diabetes, hypertension, spasmodic dysphonia and certain bacterial infections [89]. In this study, A. herba-alba was cited for the treatment of gestational diabetes, hypertension, problems of the digestive tract, certain genital infections and to facilitate childbirth. It has been reported that the aqueous extract of A. herba-alba has hypoglycemic properties [90], antihypertensive activity [91] and antimicrobial and antifungal activities [92]. T. maroccanus Ball. (UV = 0.045); it is a perennial aromatic shrub widely used to treat digestive, respiratory and nervous system diseases, rheumatism, bronchitis, fever, cough, wounds and many infections [93][94][95][96][97][98][99]. Pregnant women in the region of Guelmim use T. maroccanus Ball to treat problems related to pregnancy, namely, digestive disorders (constipation, vomiting, indigestion, etc.), genital infections, coughs, colds, the induction and acceleration of labor and also for good development of the fetus. The antiviral and analgesic activities of T. maroccanus oil have been documented previously [100]. In addition, a study by Belaqziz et al. (2013) [101] showed that the essential oil of T. maroccanus possesses antibacterial potential. -T. foenum-graecum L. (UV = 0.037); it is used by women in the Gulemim region to treat anemia, facilitate childbirth, promote the production of breast milk, induce labor and prevent and treat genital infections. According to Ulbricht et al. (2008), this herb has been used to treat a range of ailments ranging from labor induction to digestion to cough [102]. Additionally, previous studies have shown that fenugreek seeds increase milk production in lactating women [103]. According to Orief et al. (2014), fenugreek should be consumed with caution during pregnancy as the seeds have the ability to lower blood sugar levels and stimulate uterine contractions [16]. According to Vu (2019), fenugreek is well tolerated without serious side effects. However, it was reported by the same authors that when fenugreek is taken with certain pharmaceutical drugs, it can exacerbate the effect of the drugs [104].
The modes of preparation of MPs, as well as the dosage, are extremely important. Pregnant women and women who have gone through childbirth in the province of Guelmim prepare MPs by different methods, especially decoction and infusion. This is consistent with other studies conducted in Morocco and elsewhere in the world [28,[105][106][107]. While in other studies, medicinal plants were consumed in raw form [108], in the form of maceration [109] or even pressed and chewed [67].
In this study, the most common route of herbal administration among pregnant women was oral (73.21%). Similar findings were reported in other studies [67,83,107].
However, in other places, such as in the Ivory-cost, only 28.7% of women surveyed reported taking MPs orally [17].
With regard to the source of information or recommendation for the use of medicinal plants, family recommendation was the main source (46%), followed by recommendations from experienced people in the entourage (34%). This is in accordance with previous studies [10,16,17,40,80,83,[110][111][112]. In other studies, it had been reported that 80% to 90% of the pregnant women surveyed received their information on the use of MPs from people other than health care providers [58,74,112]. However, in other places such as Russia, physician recommendations were most often cited [43].

Conclusions
The prevalence of the use of medicinal plants during pregnancy and childbirth seems high in the province of Guelmim; the level of education is one of the important determinants associated with it. The use of herbs by women must be taken into consideration during prenatal consultations in order to offer an integrated prenatal follow-up and avoid any possible complications and risks for the mother or the fetus. The results of this investigation could serve as a basis for the design and development of strategies, education and awareness programs focused on the safer use of medicinal plants that are intended, more particularly, for pregnant women and women who have given birth with a low level of education. Moreover, in-depth research seems necessary on the effects and risks associated with the use of plants during pregnancy and childbirth. Informed Consent Statement: Informed consent was obtained from all subjects involved in the study.