PREGNANT WOMEN USE OF TERATOGENIC PLANTS IN MOROCCO: A CROSS-SECTIONAL STUDY

DOI: https://doi.org/10.26758/15.1.23

(1) Polyvalent Team of Research and Development (PTRD), Polydisciplinary Faculty, Sultan Moulay Slimane University, 23000, Beni Mellal, Morocco; e-mail: kannane.soukaina@gmail.com

(2) ISPITS-Higher Institute of Nursing and Health Techniques, Ministry of health and Social Protection, 10000, Rabat, Morocco; e-mail: samiaboussaa@gmail.com

(3) Polyvalent Team of Research and Development (PTRD), Polydisciplinary Faculty, Sultan Moulay Slimane University, 23000, Beni Mellal, Morocco; e-mail: o.touloun@gmail.com

Address correspondence to: Soukaina Kannane, Number 17 Road 27 Ouled Ayad Beni Mellal, CP 23000, Moroco, Email address: kannane.soukaina@gmail.com, Telephone number: 0212676126097

Abstract

Objectives. Congenital malformations originate from the genetic constitution of the embryo or from an extrinsic defect during its in-utero development. The most common causes of congenital anomalies are teratogenic agents, specifically the teratogenic plants (TP). In this context, we undertook a cross-sectional study in order to assess the prevalence of TP usage by pregnant women before and during pregnancy in Morocco.

Material and methods. This study was conducted in seven health facilities providing ante-natal care in the Beni Mellal-Khenifra region, central Morocco. The study focused on a population of pregnant women (N=624) in their last trimester of pregnancy, spanning a four-months period from February 1 to May 30, 2022.

Results. In total, 13 different TP were identified. 92% of pregnant women reported that they were used with TP before pregnancy, this percentage decreased to 75% during pregnancy. For newborns after childbirth, stillbirth represents 0.7% of pregnancies. Furthermore, there were 17 newborns (2.8%) affected. The use of TP during pregnancy showed a significant association with the economic level of pregnant women (p < .05), medical insurance (p < .05), parity (p < .05), the type of pregnancy (programmed or not) (p < .05), and stillbirth (p < .05). Furthermore, a knowledge gap and dangerous practices related to TP were detected among participants.

Conclusions. This study reveals high prevalence of TP used just before and during pregnancy which present a danger to the health of mothers and their newborns, requiring an urgent action to raise public awareness of the harmful effects of these TP.

Keywords:  Pregnant women, Teratogen plants, Congenital malformations, Morocco.

Suggested citation (APA)

Kannane, S., Boussaa, S., & Touloun, O. (2025). Pregnant women use of teratogenic plants in Morocco: A cross-sectional study. Anthropological Researches and Studies, 15, 348-364. https://doi.org/10.26758/15.1.23

Introduction

Congenital malformations  refer to the structural or the functional abnormalities that arise from faulty embryogenesis (DeSilva et al., 2016). These conditions pose a significant public health challenge, contributing to the elevated rates of both mortality and morbidity. Moreover, they stand as a primary cause of disability, exerting a profound socio-economic impact.

The World Health Organization (2023) reports that approximately 3 million children are born annually with severe malformations, leading to varying prevalence rates of congenital malformations across different countries. Higher rates were observed in low-income and developing nations (Christianson, Howson, & Modell, 2006). In Morocco, a study conducted by Forci (2020) at the Souissi maternity hospital in Rabat in 2020 revealed a prevalence of malformations at 5.58 per 1000 births.

The etiology of the congenital malformations is multifactorial (WHO, 2023), arising from a combination of chromosomal abnormalities, various hereditary factors, micronutrient deficiencies, and maternal infectious diseases (such as syphilis and rubella). Furthermore, congenital malformations may be linked to exposure to the teratogenic agents like chemicals, radiation, alcohol consumption, certain drugs, and the ingestion of teratogenic plants (TP) (WHO, 2023). Indeed, the medicinal plants constitute the main pillar of traditional medicine. In most developing countries, the medicinal plants were the first choice of the population due to their low cost. According to the WHO (2005), approximately 80% of the population in developing countries depends on traditional medicine, and 90% of the remedies used in traditional medicine are based on medicinal plants.

Nonetheless, several studies indicated that certain medicinal plants have toxic, teratogenic, and abortive potential because of certain active principles may cross the placental barrier and reach the fetus, especially in the first trimester of pregnancy. This study has been performed with TP commonly used by the populace in Africa (Seukep, Jaures, Djeussi, & Kuete, 2014), such as Fenugreek (Trigonella foenum graecum), Tobacco (Nicotiana tabacum), Cannabis (Cannabis sativa), Lobelia (Lobelia erinus) and Veratrum californicum.

Among the most known TP, we cite Trigonella foenum gracum, known as Fenugreek, whose first alert was signaled in 2003 by the Moroccan national anti-poison and pharmacovigilance center (Skalli, 2006), which noted a co-occurrence between Trigonella foenum gracum ingestion and the occurrence of neural tube closure anomalies. Furthermore, other Moroccan studies (Forci et al., 2021; Radouani, Chahid, Benmiloud, Elammari, Lahlou, K., & Barkat, 2015; Sabiri, Kabiri, Razine, Kharbach, Berrada, & Barkat, 2013) have shown that the intake of Trigonella foenum gracum was and still is a risk factor for the occurrence of congenital malformations.

This study aims to fill the gap in data regarding the consumption of teratogenic plants by the pregnant women in Morocco. Specifically, we seek to determine the prevalence of teratogenic plant used by pregnant women before and during pregnancy. Additionally, we will assess women’s knowledge and practices concerning the use of these plants during this crucial period.

Materials and Methods

Study area

This was a cross-sectional study based on face-to-face interviews with pregnant women. The study was conducted on researches which have been done in seven health facilities providing ante-natal care in the Beni Mellal-Khenifra region, located in the central part of Morocco (Figure 1). This region covers an estimated area of 28088 Km², divided between five provinces:  Beni Mellal; Fquih Ben Saleh; Azilal; Khenifra and Khouribga (High Planning Commission, 2018). Referring to the number of deliveries, the region registered 9917 live births in its different public delivery structures in 2020 (Ministry of Health of Morocco, 2021).

Recently, a study mentioned that the prevalence of congenital malformations in Beni Mellal-Khenifra region is 5.54 per 1000 live births (Kannane et al., 2024), which exceeds the national prevalence estimated at 3.91/1000LB, the same study revealed that the prevalence of Neural Tube Defects and the prevalence of Oro-Facial clefts is respectively 1.35 and 0.56 per 1000 live births (Kannane et al., 2024).

Figure 1

Location of the study area (Beni Mellal-Khenifra) (to see Figure 1, please click here)

Population and sample:

Inclusion criteria being taken, we have been targeting all pregnant women in the third trimester of pregnancy all of them having been consulted in a health center who are physically or psychologically capable of providing the information necessary for the investigation.

The sample size was set at 624 pregnant women, calculation based on the number of live births registered in the study region (9917 live births) with a margin of error of 5% and a confidence interval of 95%.

Data collection:

A structured questionnaire was developed by the authors and validated by academics (Psychologue and epidemiologist). The questionnaire was made up of 30 items, including open and closed questions, in three sections:

– The first section was focused on the socio-demographic data of pregnant women (Residence, age, study level, economic level, occupation, etc.).

– The second section was about conditions of pregnancy (Parity, pregnancy at risk, monitoring, evolution of pregnancy, presence of congenital malformations, stillbirth, etc…).

– The third section was about Knowledge, Attitudes and Practices of participants regarding the use of teratogen plants before and after pregnancy (Type of plants, period of use, form of use, raison to use, source of information, side effects, etc.). It was noted that these teratogen plants were selected on the basis of previous studies (Kandhare et al., 2019; Ouzir et al., 2016; Seukep et al., 2014; Kristanc and Kreft, 2016) done on humans and/or animals, then presented to the women by listing the local names of the plants and also by showing a sample or photo of the plants.

Further, the questionnaire was administered directly to participants after presenting the objective of this study, and the interviews took an average of 15 minutes. A follow-up of women is done to know the status of every newborn after delivery by consulting the obstetrical registry at the level of delivery facilities.

Regarding the length of elaborating the study period, this study was carried out over a period of four months, from February 1 to May 30, 2022.

Ethical considerations: 

The authors were authorized by Morocco’s Ministry of Health and Social Protection and the ethical committee to collect the data (Ref. N°482/2021). Before conducting the survey, all interviewers were informed of the aims of the study, a written consent was obtained and the principle of confidentiality was respected and maintained throughout the survey.

Statistical analysis:

Data were entered and analyzed by SPSS software version 21.0. Descriptive analyses were used with the aim to describe the socio-demographic variables in relation to conditions of pregnancy and the knowledge, attitude and practice of participants regarding the use of teratogen herbs. A KH2 test was carried out to examine the association between the qualitative variables. Only those variables identified as significant in univariate analyses were included in multivariate analyses. The results have been considered significant at p < .05.

The ethnobotanical data were analyzed based on two indexes. Firstly, we employed the use value (UV) which is a quantitative index reflecting the relative importance of the locally known species (Philips et al., 1994). This index was calculated according to Phillips and Gentry (Philips et al., 1994) using the following formula: UV = ∑/N. where “∑” designates the number of uses reported by respondents, indicating fewer reports of use cited by respondents. If a plant obtains a high UV score, this indicates that there are many reports of use for this plant, while a low score indicates a few reports of use cited by respondents, indicating fewer reports of use cited by respondents.

Beside the UV index, we used the relative frequency of quotation (RFC) in order to identify which species were well-known and most used by the women. This is obtained by dividing the number of respondents mentioning a useful species (citation frequency (CF)) by the total number of respondents in the study (N) (Philips et al., 1994). This index was calculated using the following formula: RFC = FC/N (0 < RFC < 1). The value of the index varies from 0 (no one mentioned the plant) and 1 if the respondent mentioned it.

Results

Among the 624 pregnant women invited to the survey, a total of 611 pregnant women have participated (participation rate 97.9%). The majority of them (30.4%) have an age between 20 and 25 years, with a median age of 27.8 years. 21.8% of them were illiterate, 39.3% of participants had a primary education level, and the majority of them were housewives (95.6%). The majority were married (98.4%), and 65.3% of interviews were conducted in rural areas. Concerning for their economic level, it was noticed that the half of the participants (52.4%) had an average level, while 28.3% had a low level and 11.3% had a very low level. Only 56.8% of women had a medical insurance (Table 1).

Regarding pregnancy, 69.9% of women were multiparous, 27.8% of pregnancies were not programmed, and 85.6% of them were monitored. Pregnancy at risk represented 12.8% of the survey respondents.

Table 1

Characteristics of pregnant women participating in the study (to see Table 1, please click here)

For the outcome of newborns after delivery, stillbirth presents 0.7% of pregnancy. Besides, a number of 17 newborns (2.8%) present congenital anomalies: spina bifida (5 cases), anencephaly (2 cases), club feet (3 cases), trisomy 21 (3 cases), and others (5 cases) (Table 1). In total, 92% of pregnant women use TP before pregnancy, this percentage decreases to 75% throughout pregnancy. During pregnancy, the frequency of use is 32% in the 1st trimester (TR1), 17% in the 2nd trimester (TR2) and 51% in the 3rd trimester (TR3) (Figure 2). Among the TP used by participants, 13 different TP were identified (Table 2) from which 8 TP were used before and during the pregnancy, 3 TP were only consumed before pregnancy and 2TP were only taken during the pregnancy.

The most commonly used TP taken just before pregnancy were Camellia sinensis (UV= 0.840), Coffea (UV= 0.771), Trigonella foenum graecum (UV= 0.426) and Foeniculum vulgare (UV= 0.200). It’s noted that the use value decreased during pregnancy with Camellia sinensis (UV= 0.678), Coffea (UV= 0.524), Trigonella foenum graecum (UV= 0.165) in contrast, the used value of Foeniculum vulgare (UV= 0.640) has increased during pregnancy.

Only Lathyrus sp (UV= 0.002), Indigofera sp (UV= 0.002), and Peumus boldus Molina (UV= 0.002) were used before pregnancy. While, Lobelia erinus (UV=0.005) and Lupinus sp (UV= 0.002) were taken throughout pregnancy.

These TP genera and species were confirmed by botanists according to decription and origin.

According to the Table 2, for the relative frequency of quotation (RFC) four species have the highest RFC value were: Camellia sinensis (RFC = 0.840), Coffea (RFC= 0.771), T. foenum-graecum L (RFC= 0.245), Foeniculum vulgare (RFC=0.164).

Figure 2

Prevalence of TP usage just before pregnancy and throughout pregnancy (Trimester 1, 2 and 3) (to see Figure 2, please click here)

Table 2

List of teratogen plants used by pregnant women just before and during the pregnancy (to see Table 2, please click here)

Before pregnancy, 28.5% of women were exposed to Nicotiana tabacum among them, 27.9 % were passive smokers, and only 0.6% were active smokers. During pregnancy, 27.3% of participants were exposed to Nicotiana tabacum with 26.8% being passive smokers and 0.5% being active smokers (Table 3).

Table 3

Nicotiana tabacum use among pregnant women interviewed before and during the pregnancy N(%) (to see Table 3, please click here)

According to knowledge among pregnant women about TP, 75.6% have never heard about TP, of which 62.16% indicated that family and friends were the source of the information, and 24.32% have received information from a health professional (Table 4).

Only 18% of participants were familiar with some types of TP. Among them, 70.9% mentioned Trigonella foenum gracum just 5.45% indicated Coffee; and 1.82% indicated Ceratonia siliqua. It’s noted that no women mentioned Camellia sinensis, Nicotiana tabacum, Cannabis sativa and others TP. Will, 11.82% of them mentioned cannel which is not TP.

The most common reasons for the use of TP were nourishing (27.33%), reducing gastritis and burning sensations (6.07%), and reducing colopathy and dysmenorrhea (0.87%). Weight gain, and to manage tooth pain (0.65%), and finally, to induce abortion (0.43%).

The majority of women using TP did not report experiencing any side effects except vertigo and urticaria when using Cannabis sativa and Trigonella foenum graecum. 96.07% of participants ignored the existence of a national poison control center to report any toxicity or an undesirable reaction to a plant consumption.

The infusion is the most used form for the intake of TP among the participants (96.3%), followed by decoction (13.23%), inhalation (5.21%), mouthwash (0.65%), Cataplasm (0.43%), Gargarism (0.22%). During antenatal care, 95.09% of participants claimed not to receive advice or information from a health professional in relation to TP.

Use of TP during pregnancy was significantly associated with the economic level of the pregnant women (p < .05), the medical insurance (p < .05), the Parity (p < .05), the type of pregnancy (programmed pregnancy or not) (p < .05) and the stillbirth (p < .05).

Table 4

Pregnant women’s knowledge regarding the consumption of teratogen plants (to see Table 4, please click here)

Discussion

One of the public health problems threatening the reproductive health is represented by the congenital malformations, leading to high rates of morbidity and infant mortality. It also results in disability, placing a heavy burden on the individual, the family and society. Among the risk factors implicated in the appearance of the congenital malformations is the consumption of TP during pregnancy. According to the World Health Organization (WHO) 80% of the world’s population, especially in developing countries, relies on a variety of traditional medicines for their primary health care (WHO, 2005).

The Moroccan Kingdom is one of the countries where medicinal plants are widely used for medication and/or nutrition. There is a large variety of plants, accordingly to the estimated number of medicinal plants there are about 600 species which grow natively or those which were cultivated in Morocco (Kamel et al., 2022 ; Kharchoufa et al., 2018) of which more than half (360 species) are used to cure a huge variety of diseases (Fennane & Rejdali, 2016). More importantly, the MP sector is not standardized, structured, regulated or recognized by the national health system (Fakchich & Elachouri, 2014). Even so, the use of plants during pregnancy is not always safe; it may have a harmful effect on both women and their fetus (Illamola et al., 2019). Among other effects, there is a potential teratogen effect on offspring. Until now, no database is available about the use of TP among pregnant women in Morocco; however, previous studies revealed the large use of MP among pregnant women (Kamel et al., 2022).

The present study is the first of its kind in Morocco aiming to determine the prevalence of the use of teratogen plants by pregnant women before and during pregnancy, and to assess women’s knowledge and practices regarding the use of these plants during this crucial period. In this study, we report that pregnant women in the center of Morocco use TP just before and during their pregnancy. The prevalence decreases between these two periods; it’s about 92% just before pregnancy, and it’s around 75% during pregnancy. This prevalence is significantly higher compared with other similar research conducted in other countries, such as the study done in southern Morocco by Kamel (Kamel et al., 2022), which revealed that the prevalence of the medicinal plants used among pregnant women was 66.96% in 2022.

Another study (Nega et al., 2019) showed the prevalence of MP use during pregnancy in Addis Ababa in 2018 was 60%, and 93.9% of them 93.9% did not disclose their use of MP to their health care providers. In addition, an African systematic review (El Hajj & Holst, 2020) published in 2020 reported that the prevalence of MP used during pregnancy ranges among different African regions from 32% in Central Africa to 45% in East Africa depending on the geographic location, ethnicity, cultural traditions, socioeconomic status and religious and spiritual values of the people who use it.

In Italy, a research (Cuzzolin et al., 2010) identified the prevalence of 27.8% of women who have been taking one or more herbal products during pregnancy, and the prevalence of pregnant women using MP was 30.9% in Northeastern Brazil in 2016 (de Araújo et al., 2016); this prevalence was very low in USA (Broussard et al., 2010); it was 10.9% among 3 months before or during pregnancy, and it was 9.4% during pregnancy.

The high prevalence of TP among surveyed women in this research may be explained by the low level of education. It can also be caused by a low or very low economic level, with the majority of them being housewives with no financial income and nearly half having no medical insurance. The high rate of TP among interviewed women may also be explained by the dominance of the rural residence, which constitutes a favorable environment where plants are available free of charge, to which must be added the lack of geographical accessibility to healthcare services in rural areas. Another study done in Morocco (Fakchich & Elachouri, 2014) in 2014 showed that rural participants are the main consumers of MP (83.1%). Also, the unplanned nature of 27.8% of pregnancies may increase the prevalence of TP use during pregnancy, especially in the first trimester.

The number of users is still very high, even though this study’s prenatal coverage rate (85.6%) was relatively high compared to the World Health Organization’s (WHO) recommendations on prenatal coverage. WHO recommends that 98% of pregnant women in developed countries should be covered. This finding raises the questions about the quality of prenatal consultations in Morocco, where especially about 95% of participants didn’t receive any information or advice on TP during prenatal consultations.

Despite the experience of pregnancy among participants (69.9% of women were multiparous), a gap in knowledge on TP was detected, with 75.6% of them having never heard TP. The source of their knowledge was essentially their families, which is similar to the finding of an Ethiopian study that revealed that 75.2% of pregnant women were recommended to use MP by their family members (Ahmed et al., 2021), the same result was found in the USA, where it was mentioned that the information on the efficacy and safety of MP generally comes from the experience of past generations (Broussard et al., 2010). Moreover, another study (de Araújo et al., 2016) indicated that relatives were most responsible for the use of plants among pregnant women (81.8%), whereas health professionals were the source of only 2.6% of advice. Besides, a study (Illamola et al. 2019) found that Healthcare providers rarely question pregnant women about the use of medical plants, even though little is known about the safety of plants and their interactions with drugs during pregnancy.

In this survey, no more than 18% of surveyed women knew some kind of TP; the most known TP was Trigonella foenum gracum, few women noted Coffea and Ceratonia siliqua. Whereas pregnant women are completely unaware of the teratogenic effect of plants such as Camellia sinensis, Nicotiana tabacum, Cannabis sativa e.g. In addition, there is wrong information like that 11.82 % of them mentioned Cinnamon (Cinnamomum verum) which is not a TP. Besides, almost all of those interviewed women were ignorant of the existence of a national poison control center to report any toxicity or undesirable reaction to a plant.

According to participants, the mode of administration, the most common one is the oral mode more, the infusion is the most used form for the intake of TP in the participants (96.3%), followed by decoction (13.23%).

In a review (Illamola et al., 2019), pregnant women use MP to improve their well-being or to treat pregnancy-related problems. It is known that the physiological changes during pregnancy may result in a number of ailments, such as notably nausea, vomiting, headaches and cramps in the lower abdomen, all of which may cause discomfort (Erhirhie, et al. 2020). Consequently, the pregnant women prefer to use plants rather than drugs to treat pregnancy-related complaints, especially with the evidence that plants are safe because they are natural (Bernstein et al., 2021; Illamola et al., 2019).

The results of this research found that the most common reasons for the use of TP were   nourishing (27.33%), to reduce   pregnancy ailments like gastritis, burning sensation, colopathy, weight gain, tooth pain and finally, to induce abortion. Compared to a study done in southern Morocco in 2022 (Kamel et al., 2022), pain, the induction and facilitation of childbirth, flu syndrome and anemia were the most common reasons for using MP among pregnant women.

Another study (Ahmed et al., 2021) done in Addis Ababa mentioned colds and headaches as the most common reasons for the use of MP during pregnancy. In the USA (Broussard et al., 2010), MP were used to improve the wellbeing of the mother and/or baby or for other reasons like to help decrease nausea and vomiting, treat infection, ease gastrointestinal problems, prepare for labor, induce labor and ease labor pains.

In this study, the prevalence of use was maximal in the 3rd trimester (51%), constituting the 2nd trimester as the fetogenesis stage where growth and functional maturation occur and teratogens affect growth and functional aspects such as intelligence and reproduction (Bruno et al., 2018). So, it was admitted that 32% of participants have used TP in the 1st trimester, considered a high-risk period during which organogenesis occurs and embryonic differentiation occurs and during which malformations may arise from brief exposure (Kristanc & Kreft 2016; Seukep et al., 2014). In the same line of the finding of this study, a study showed that the prevalence was maximal in the first trimester in the USA (Broussard et al, 2010).

In Brazil, 21.9% of pregnant women used MP in the first trimester of pregnancy; researchers have also claimed other toxic effects of plants in the second and third trimesters as affecting growth and functional development (de Araújo et al., 2016; Bernstein et al., 2021).

In the study context, there were 13 different plants identified, meaning that these plants are bioavailable. Allgaier & Franz mentioned in 2015 that worldwide, more than 350 plant species in up to 13 families contain pyrrolidine alkaloids, which, at higher doses, exert foetotoxic and teratogenic effects.

Notably, Camellia sinensis is the most commonly used TP before and throughout pregnancy (UV = 0.840; UV = 0.678); it is also used as food and not as a medicinal plant. Moroccan mint tea is very popular and isn’t just a drink in Morocco; it is a sign of friendship, hospitality and tradition. Previous studies (Kharchoufa et al., 2018; Kamel et al., 2022) mentioned that Camellia sinensis was used by the population in Morocco. In the same line, Coffea is widely used by participants before and during pregnancy (UV = 0.771; UV = 0.524), Coffea is commonly used as a stimulant drink because this species contains more Caffeine involved in a teratogenic effect (da Silva Costa et al., 2012; Seukep et al., 2014). In the United States, 75% of pregnant women consume drinks containing Caffeine, including those from plants such as black tea (Camellia sinensis), green tea, cola and guarana (Seukep et al, 2014).

Trigonella foenum-graecum L, known as Fenugreek, is used as a seasoning plant and as a medicinal widely used in Moroccan, Mediterranean and Asian cuisine. Its teratogenic effect is due to its contain in Alkaloids, such as trigonelline (Kristanc & Kreft, 2016; Ouzir et al., 2016; Seukep et al., 2014). In this survey, this plant was among the most frequently used (UV = 0.426; UV = 0.165) before and during pregnancy. Recently, the highest UV was accorded to this plant among pregnant women   in southern Morocco (Kamel et al., 2022), the same observation has been made for the general population in the Oriental Moroccan (Fakchich & Elachouri, 2014). Also, Trigonella foenum-graecum L, was cited as a toxic plant used by the people of the North Eastern Kingdom (Kharchoufa et al., 2018).

The first event was a complaint by the national Poison control and pharmacovigilance center in 2006 (Skalli, 2006), which reported the occurrence of congenital malformations such as hydrocephalus and spina bifida after ingestion of Trigonella foenum-graecum during pregnancy. Further, other Moroccan studies revealed   that the consumption of fenugreek was a risk factor for congenital malformations in general (Es Seddiki, Messaouidi, & Amrani, 2017; Sabiri et al., 2013) and also for neural tube defects (Radouani et al., 2015; Forci et al., 2021). In addition, in Morocco, the terratogen effect of Trigonella foenum-graecum has also been documented in animals (Khalki et al., 2010, 2012, 2013; Ouzir et al., 2016).

Many reasons for the use of these plants were mentioned by participants in line; another study done in Ethiopia (Ahmed et al., 2021) reported that 7.5% of pregnant women used them for many reasons, including to prepare for labor, induce labor, gastric ulcers or burning sensation, while it’s also used for anemia in the USA (Illamola et al., 2019).

This research revealed that 28.5% of women were exposed to Nicotiana tabacum just before their pregnancy, and 27.3% of participants were exposed to it throughout pregnancy. The majority of them were passive smokers; fortunately, only about 0.6% were active smokers. Nicotiana tabacum contains alkaloids, which are potentially teratogenic and cause cleft palates and skeletal malformations in the fetus (Kristanc and Kreft, 2016). This research found that parental smoking during pregnancy increased the risk of club feet (Dickinson et al., 2008).

Luckily, in this study context, few women consume Cannabis sativa (UV = 0.010); it’s cited as used by the population in this oriental Moroccan areas (Fakchich and Elachouri, 2014) such in North Eastern Morocco (Kharchoufa et al., 2018), where those plants causes brain defects in the fetus (Kristanc and Kreft, 2016; Seukep et al., 2014).

Concerning foeniculum vulgare more of respondents admitted that it was also consumed by participants before and during pregnancy (UV = 0.200; UV = 0.640) and that the use of this plant has increased during pregnancy. It’s cited as a toxic plant frequently used in north-eastern Morocco (Kharchoufa et al. 2018). In Italy, Foeniculum vulgare was the most used MP among pregnant women (Cuzzolin, et al., 2010). It’s consumed throughout pregnancy for several benefits, such as gastralgia and other types of pain, flatulence, constipation, and a gastrointestinal disorder.

While Lupinus was taken only in the first trimester of pregnancy (UV = 0.002), it contains alkaloids that are potentially teratogenic, which generate cleft palates and congenital contracture-type skeletal in foetuses (Kristanc & Kreft, 2016; Seukep et al., 2014).

Also it was noted that both Lathyrus (UV= 0.002), Indigofera (UV = 0.002), and Peumus boldus Molina (UV= 0.002) were used only before pregnancy. It’s known that Lathyrus causes congenital skeletal malformations in cows and sheep (Kristanc & Kreft, 2016) and Indigofera contains indospicine which is teratogenic (Seukep et al., 2014). Furthermore, Peumus boldus has a teratogenic and abortifacient effect but is still used by pregnant women in Brazil (de Araújo et al., 2016; da Silva Costa et al., 2012).

It was noted that no participants have mentioned the use of Crocus sativus known as saffron, just before and during pregnancy, which is a plant frequently used in Moroccan foods, and it’s also used as a medical plant; however, a study (Ouzir et al., 2016) done in 2016 revealed teratogen effects in mice . The non-use of this plant may be explained by its high price.

According to the interviewed women, four TP were effective with the highest relative frequency of quotation (RFC): (Camellia sinensis (RFC = 0.840), Coffea (RFC = 0.771), T. foenum-graecum L (RFC= 0.245), Foeniculum vulgare (RFC=0.164)). A review(Bernstein et al. 2021)  reported that a high proportion of pregnant women in developing countries consider MP as effective for their ailments.

In this study, our research discovered that the majority of women using TP did not report experiencing any side effects except for vertigo and urticaria when using Cannabis sativa and Trigonella foenum graecum. It appears that there is a paucity of research on TP in general, except for studies specifically focused on Trigonella foenum graecum.

The high prevalence of TP consumption by women just before and during the pregnancy and also other dangerous practices that we described in this survey may be explained by a lack of knowledge about TP. The World Health Organization attributes the pattern of MP practice to the weakness of the national drug regulatory authorities (WHO, 2005). Suffering from and lack of knowledge about herbal medicine, lack of assessment of safety, quality control and efficacy should be reglemented by new laws.

Concerning the outcome of the newborns after delivery we took into consideration, in this study, that the birth of stillbabies accounted for 0.7% of pregnancy. Additionally, 2.8% of newborns presented congenital anomalies including spina bifida, anencephaly, club feet, trisomy 21 and others. It was also noted that no association was detected in this study between the use of TP and the occurrence of birth defects (p ˃ .05).

This study revealed that use of TP during pregnancy was significantly associated with the economic level of the pregnant women (p < .05), the medical insurance (p < .05), the Parity (p < .05), the type of pregnancy programmed pregnancy or not (p < .05), stillbirth (p < .05). Another Moroccan study done in southern Morocco (Kamel et al., 2022) showed that the use of MP among pregnant women was significantly associated with the level of their education (p < .05), and pregnancy monitoring (p < .05). While an African study (Nega et al., 2019) mentioned that the age and the marital status were significantly associated with the use of medicinal plants. In addition, a systematic review (El Hajj & Holst, 2020) found that MP use during pregnancy was statistically significantly associated (p < .05) with numerous factors such as increasing age, lower educational level of women, lower educational level of the spouse, being married, large family size, low socioeconomic status, poor pregnancy outcomes, herbal medicine use in prior pregnancies, perception that MP are effective, self-employment, unemployment, and rural residence. A review (Illamola et al. 2019) of the literature has shown that the use of MP by pregnant women may vary depending on region, cultural traditions, age, and education. However, in Brazil, a study (de Araújo et al., 2016) found that no statistically significant correlation was detected between the social class and the use of medicinal.

The present study is the first to do so in a Moroccan context, assessing the use of TP before and during the pregnancy among pregnant women and evaluate their knowledge, attitude and practice, as well as assessing the outcome of their newborns. The high prevalence of TP use by women may be explained by the likes of KAP among women or /and by lack of advice from healthcare providers, while certain limitations should be taken into consideration when interpreting the results, such as the lack of TP quantification and frequency of use, which were difficult to determine from surveyed women.

Conclusion

Morocco is known for its rich biodiversity. In fact, the medicinal plants are widely used by women. However, many medicinal plant species are poorly studied, and their teratogenic effects on the fetus are still unclear. This study reveals that the use of TP just before and during pregnancy in the center of Morocco could be more then a threat to the health of mothers and their newborns. The prevalence is still very high, and a gap of knowledge and dangerous practices was founded. The Consumption of these plants among pregnant women was associated with various risk factors including parity, unplanned pregnancy, stillbirth, economic level of pregnant women and medical insurance. These findings hold significance for healthcare personnel, researchers, policy-makers and pregnant women themselves.

There is an urgent need to raise the awareness of TP among women of childbearing age so that they abandon the idea that MP are safe and to educate the healthcare professionals about the dangers of TP. Additionally, more studies are needed to evaluate the plant’s toxicity and teratogenicity and to evaluate the concomitant use of TP with the drugs used before and during pregnancy.

Acknowledgements

The current study’s authors are grateful to all pregnant women and health workers who contributed and to the Moroccan Ministry of Health and Social Protection for their assistance.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Declaration

The authors have no conflicts of interest relevant to this article.

Consent to participate

Informed written consent was obtained from each participant at the time of recruitment. The subjects were informed that they could withdraw from the study at any stage, and they were assured of confidentiality.

Author Contributions

Kannane S: Conceptualization, Methodology, Formal Analysis, Investigation, Writing – Original Draft Preparation,

Boussaa S: Data Curation, Methodology, Validation, Review & Editing

Touloun O: Resources, Formal Analysis, Validation, Review & Editing.

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