Assessment of Undergraduate Nursing Students’ Understanding of Herbal Medicines and Herb–Drug Interactions in Riyadh, Saudi Arabia

Introduction

Around the world, people are using herbal medicine (HM) more frequently in their everyday routines. This is due to the high cost of, or some other dissatisfaction with, allopathic or conventional medication [1–4], or because people believe that HMs are safe since they are made from natural ingredients; however, earlier research has shown that this is not always the case [5]. HMs are products containing active ingredients from plants or plant materials [6,7]. The prevalence of HM differs in different study populations in the literature, in different countries and within the same country [8,9]. For example, it was 75.6% in 2019 in the Saudi population [6], while it was 62.7% among Saudi university undergraduates in 2022 [3]. The prevalence of Saudi pharmacy students taking dietary supplements was 46.8% [9]. It was estimated that 80% of individuals in developing countries rely on HM for the prevention of various ailments [10–12].

The use of HM in conjunction with conventional medicine can alter the effects of the conventional medicine, or can result in an unexpected event, potential interactions, or a change in the target drug’s clearance or systemic exposure caused by the herbal product’s inhibition or activation of drug-metabolizing enzymes and transporters. Such interactions are collectively known as herb–drug interactions (HDIs) [10–13]. For instance, the use of ginseng along with warfarin results in a decrease in international normalized ratio of 1.5. Similarly, ginger (Zingiber officinale) interacts with nonsteroidal anti-inflammatory drugs (NSAIDs) to causes declined pain relief [13]. In this regard, HDIs may enhance or inhibit drug absorption, distribution, metabolism, and excretion, or alter their clinical or physiological effects in the body, resulting in unexpected adverse effects [14,15]. Furthermore, studies have documented that HMs may cause adverse effects like headaches, dizziness, agitation, dry mouth, seizures, exhaustion, tachycardia, rashes, nausea, vomiting, and diarrhea [16]. Furthermore, when taken with conventional medicine, HMs can cause severe adverse effects [16,17].

Monitoring of a drug’s effect after ingestion is crucial in healthcare, to prevent interactions of the administered drug with other HMs or foods [16,17]. The use of HM among individuals differs according to their disease status [18–20]. For instance, 68% of patients with chronic diseases reported using herbal products, alongside allopathic medicine [18], while 32% of diabetic patients used HM, and most of the HMs used were honey and herbs such as black seeds (Nigella sativa), fenugreek, and myrrh [19]. Similarly, 32% of patients with liver problems used herbal products to treat their disease [20]. This raises the potential for HDIs [21,22]. The outcomes of HDIs can lead patients to suffer from severe toxicity and increased hospitalization and medical costs [21,22].

A previous study by Stanojević-Ristić et al aimed to assess the knowledge and behaviors of healthcare professionals (HCPs), including nurses, regarding the risk of potential drug-herb interactions [23]. The findings revealed that HCPs were mostly familiar with the interaction of doxycycline with magnesium, while they were least familiar with the interaction between warfarin and glucosamine [23]. Furthermore, the findings showed that knowledge of drug-herb interactions was significantly lower among nurses, compared with other HCPs [23]. On the other hand, another study by Badke et al, among nursing students, indicated that undergraduate nurses have been noted to be uncertain about using medicinal herbs, indicating the need for advancements in nursing education [24]. Additionally, another systematic evaluation of 26 studies of herbal and complementary medicine practice among nursing students found a positive opinion of herbal and complementary medicine therapies, despite their inadequate knowledge [25]. Similarly, studies from developed countries reported that most of the students knew that herbs could interact with conventional drugs when administered concurrently, but students failed to provide specific examples of such interactions [26,27]. In Saudi Arabia, the HDI initiative was started by the Saudi Food and Drug Authority to identify and evaluate possible HDIs and guarantee patients’ safety [28]. HDIs can alter the pharmacokinetic and pharmacodynamic properties of medications, leading to toxicities [28–30]. Moreover, a plant may intensify or lessen the effects of medications taken concurrently [29,30].

The nurse’s role in various aspects of health care is well documented, including patient counseling and education [31]. Nurses play an important role in the safe and effective use of medications, and they are frequently involved in delivering medications to their patients [26,27,31]. From the viewpoint that nursing undergraduates are future practicing HCPs, possessing adequate knowledge about HDIs in their undergraduate education not only helps in achieving excellent grades but also helps in their future practice. As per our knowledge, no research has been conducted so far among Saudi undergraduate nursing students to examine their knowledge about HMs and HDIs. Hence, this questionnaire-based study aimed to evaluate the knowledge of HMs and HDIs in 147 undergraduate nursing students in Riyadh, Saudi Arabia, between March 2022 to June 2022.

Material and Methods

ETHICAL APPROVAL, DESIGN, SETTINGS, AND POPULATION:

The study was permitted to proceed (E-22-7368) by the King Saud University College of Medicine ethical committee after they had examined the study protocol and questionnaires. Before data collection, the students gave their informed consent. A cross-sectional, web-based study was conducted among undergraduates at King Saud University, College of Nursing in Riyadh, Saudi Arabia over 4 months, between March and June 2022. The data were collected using a structured, self-administered online questionnaire prepared and distributed using Google Forms among undergraduate second- to fourth-year nursing students. We excluded nursing students who had just recently joined the program, and undergraduates from other disciplines, since students who had just recently joined the course had yet to complete a preparatory course where they learn the basics of the nursing curriculum. The concept of drugs and their interactions begins in the second year of study, which is the reason for the exclusion of the first-year students.

SAMPLE SIZE ESTIMATION:

The sample required for this study was calculated similarly to previous studies [3,22,32–35]; namely, by using an electronic calculator, Raosoft, with a confidence interval of 95% and a margin of error of 5% (http://www.raosoft.com/samplesize.html). A sample size of 137 was calculated by referring to the total number of registered senior undergraduates in the College of Nursing records, which was 200 in 2022. However, we decided to survey a maximum number of undergraduates in an attempt to ensure higher reliability.

QUESTIONNAIRE DESIGN AND PROCEDURE:

The questionnaire was adopted from the existing literature [26,27] and was evaluated by a senior colleague with extensive survey design experience. The questionnaire consisted of 3 sets. The first set covered demographic characteristics, such as age and gender, year of study, nationality, and history and frequency of HM usage, as well as the students’ opinions on recommending HM and whether any members of their family have used it (8 items). The second set consisted of HM knowledge-related questions, such as whether HMs have any adverse effects, the availability of numerous HM preparations, and whether HM is an integral part of traditional medicine, with a total of 5 items. All these knowledge items were assessed on a binary scale (Yes/No) except the third item, which was assessed on a 5-point Likert scale (strongly agree to strongly disagree). The last set of questionnaires was related to the assessment of knowledge of HDIs. These included questions such as: “Do you think you know enough about HDIs?”, “Can herbs and conventional drugs interact when taken together?”, and questions on whether the students understood that pharmacokinetic and pharmacodynamic pathways mediate HDIs, that transporters and drug-metabolizing enzymes are important components of HDIs, and examples of particular HDIs. This section had a total of 6 items; 5 of the items were measured on a binary scale (Yes/No) and 1 item had the multiple-choice Likert scale option. The knowledge score was computed for the 5 knowledge items (Yes/No) by assigning a score of 1 for the correct answer and a score of 0 for the wrong answer. Similarly, all the knowledge items were combined to obtain the overall knowledge score, which was further classified into 2 groups, adequate (scored >50% of the total possible score) and inadequate (<50% of the total possible score).

Following the completion of the initial draft of the questionnaire, it was subjected to a translation technique using forward-backward translation [36]. Firstly, the questionnaires were translated from English to the local language (Arabic) using forward translation with the assistance of a bilingual English speaker. A committee of 2 professors from the College of Nursing then evaluated the translated version and then the Arabic-translated version was then translated back into English. Before distributing the Arabic questionnaires, a pilot study of a randomly selected sample of undergraduates (n=30) was done to assess the questionnaire’s readability and ease. The results of the pilot study were not incorporated into the main investigation. The Cronbach’s alpha values for the general knowledge and knowledge of HDIs questions were 0.71 and 0.79, respectively, indicating that the questionnaires were valid and reliable for conducting the study.

Similar to previous findings [3,22,32–35], data on undergraduate nursing students were collected using a convenience sampling technique using electronically created Google Forms. Before proceeding to the questionnaire, there was a statement regarding the purpose of the study and verbal informed consent. Undergraduates who agreed and completed the survey were included in the study. Furthermore, undergraduates were given sufficient time to complete the questionnaire. To collect data, a researcher from the College of Nursing was assigned to contact undergraduates. Nursing students were assured that the data would only be used for research and that confidentiality would be maintained throughout the study

STATISTICAL ANALYSIS:

The acquired data were analyzed with IBM SPSS Statistics 26 (IBM Inc., Chicago, IL, USA) software. The data were checked for accuracy and completeness; those with missing responses (>3 variables) were excluded from the study. The use of descriptive statistics, frequencies (n), and percentages (%) were utilized to summarize the information. The continuous data were represented by mean and standard deviation (SD) values, presented in the form of mean(SD). To assess the association between the variables, chi-square and Fisher exact tests were applied, with a P-value of <0.05 considered to be statistically significant.

Results

CHARACTERISTICS AND FREQUENCY OF USE OF HERBAL MEDICINE AMONG NURSING STUDENTS:

A total of 200 undergraduates were approached for this study. Of these, 160 of the respondents completed the questionnaires and returned them, of which 13 were excluded due to incomplete or missing responses, leaving 147 valid questionnaires and a 73.5% response rate. Of the respondents, the majority were males [136 respondents (92.5%)]. The most common age range was between the ages of 21–25 years old [68 respondents (46.3%)]. Most of the undergraduates [59 (40.1%)] belonged to the third-year class, followed by second-year [49 (33.3%)] and fourth-year [39 (26.5%)] students (Table 1). The findings indicated that the majority of the nursing undergraduates used HM (74.8%) as a treatment. Among the users of HM, 6.1% of them used some type of HM every day, while 19.7% of them had used HM within the past month, and 8.2% of them used HM within the past 2 days. Furthermore, most of the participants agreed that they would advise the use of HM to others (70.1%). A detailed description of participant characteristics is presented in Table 1.

KNOWLEDGE AND COMMON SOURCES FOR HERBAL MEDICINE:

The participants demonstrated high knowledge of some individual question areas regarding HM. For instance, the knowledge of the adverse effects of using HM was 79.6%, and the students revealed that they understood that the use of HM can be associated with adverse effects. Furthermore, most of the participants (78.9%) agreed that HMs are an integral part of traditional medicine. With regard to the availability of the different HM preparations, only 46.3% of the students agreed that HMs are available in different forms, while more than half of them disagreed about this point. Similarly, when we asked about the majority of the people in developing countries using HM for their treatment, 93 participants (63.2%) agreed or strongly agreed that this was true (Table 2). Regarding the most common source of HM knowledge, 31.3% of nursing undergraduates (n=46) revealed that personal experience or the experience of friends and relatives in the family was their most common source, followed by lectures [40 students (27.2%)], social media or the internet [26 students (17.7%)] and the scientific/medical literature [21 students (14.3%)] (Figure 1).

BELIEFS ABOUT HDIS AND COMMONLY IDENTIFIED HDIS:

The majority of the students, 76.9% (n=113), believed that herbs can interact with conventional medicine, but only a third of the students, 29.9% (n=44), said they knew enough about HM. Additionally, participants had a high understanding of the fact that pharmacokinetic and pharmacodynamic pathways mediate HDIs; 79.6% of the students (n=117) agreed with this statement. The most commonly identified HDI by undergraduates in this study was gingko biloba (20.4%) with warfarin and ibuprofen. This was followed by: warfarin interactions (13.6%) with herbs like green tea, ginger, and chamomile tea; antibiotics with herbs (13.6%); St. John’s wort (1.3%) (Hypericum perforatum) interactions with drugs like antidepressants and antiplatelet drugs; and interactions between garlic and anticoagulants (1.3%) and antiplatelet drugs (1.3%) (Table 3). The results revealed that 41.7% (n=60) of the students had poor knowledge of HM, while 58.3% of them (n=84) had good knowledge of HM (Figure 2).

DIFFERENCES IN KNOWLEDGE OF HERBAL MEDICINE AND NURSING STUDENTS’ CHARACTERISTICS:

Table 4 describes the differences between knowledge scores and participant characteristics. According to the findings, the mean score of HM knowledge was found to be 3.40 (SD=1.30, Range 0–5). Previous history of HM use in the family significantly affected the mean knowledge scores of the undergraduates (t=4.635; P≤0.0001). Similarly, a history of recommending herbal remedies to others significantly affected the mean knowledge scores (t=3.800; P≤0.0001). The participant’s gender (t=0.582; P=0.290), age (F=0.538; P=0.657), year of study (F=1.320; P=0.270), nationality (t=2.353; P=0.150), and whether they had ever used HM (t=1.516; P=0.188) were found to have no impact on the knowledge score of HMs, as shown in Table 4.

Discussion

In the present study, 79.6% of the nursing undergraduates agreed that HM use can be associated with adverse effects. However, with regard to knowledge of HDIs, only 29.9% of them thought that they had sufficient knowledge about HDIs. In addition, 76.9% of the undergraduates agreed that herbs can interact with a conventional drug when taken together. These findings were consistent with previous findings by Amaeze et al in 2020 among nursing and medical undergraduates at the University of Lagos, Nigeria, who reported that approximately 97% of them knew that herbs can interact with allopathic medicine [26]. However, another study by Sekhri et al reported that 67% of undergraduate students at their university were lacking in safety concerns associated with the use of herbal products and HDIs [37]. Similarly, another study by Boparai et al in 2017 conducted to identify the knowledge and awareness of medical undergraduates regarding the use of HMs and HDIs, to improve the teaching skills and curriculum development for medical undergraduates, reported that only 44.4% of the medical students were aware of the fact that HM can interact with conventional medicine [27]. This is supported by studies by Xu et al and Sekhri et al, who reported that medical residents and undergraduates felt that they had very little exposure to the topic of HMs in their formal education [37,38]. Possessing enough knowledge and awareness of the possible drug interactions before administering drugs to patients may help in preventing adverse events associated with the combinations. Therefore, it is crucial to assess HDI knowledge among undergraduates to create awareness of the importance of HDIs among HCPs and the public.

In the present study, 79.6% of the nursing students reported that HDIs are mediated by pharmacokinetic and pharmacodynamic mechanisms, while 78.9% of them reported that drug-metabolizing enzymes and transporters play significant roles in HDIs. These results were similar to an earlier study by Amaeze et al (2020), in which the author reported that 98.2% of the undergraduates knew that HDIs are mediated by pharmacokinetic and pharmacodynamics mechanisms and that drug-metabolizing enzymes and transporters play significant roles in HDIs [26]. This might be a result of their exposure to pharmacognosy themes on medicinal plants and other related subjects that are all part of the nursing curriculum. In the present study, most of the nursing students [46 (31.3%)] revealed that advice from family and friends is the most common source of HM knowledge, followed by lectures [40 (27.2%)], internet or social media [26 (17.7%)], and textbooks [21 (14.3%)]. These findings were consistent with previous findings among university undergraduates [27], revealing that the internet (55.6%) medical journals (16.8%), and pharmacopeias (14.7%) are potential sources for advice on the use of HM among participants [27]. This finding that advice from elders in the family regarding HM use is the highest source of HM-related knowledge among participants shows a lack of scientific attitudes or beliefs [27].

With regard to knowledge of specific HDIs, the majority of the undergraduates lacked it. Only 10.2% of the undergraduates identified specific examples of HDIs. The most commonly reported HDI in the present study was ginkgo biloba with warfarin and ibuprofen, followed by warfarin interactions with green tea, ginger, and chamomile tea; and St. John’s wort interactions with antidepressants and antiplatelet drugs. It was known that St. John’s wort can lower the plasma concentration of many drugs [39]. Furthermore, St. John’s wort also increases or alters the therapeutic activity of several drugs, especially indinavir, digoxin, and cyclosporine. The interactions between warfarin and certain herbs can lead to spontaneous postoperative bleeding, hematomas, haematemesis, melena, subarachnoid hemorrhage, and thrombosis [40]. The limited knowledge on specific HDIs among undergraduates in this study has also been observed in previous studies in Nigeria [26], Canada [38], and Ireland [41]. The possible reason for this knowledge deficiency among undergraduates might be the lower content of information on HDIs in curricula. This can be the cause of the undergraduates’ limited understanding of particular HDIs. The number of adverse effects associated with supplements and HDIs is increasing along with the global increase in the usage of herbal medications and other supplements [42]. To avoid these negative effects, and the likelihood of any HDIs, strict regulations should be adopted in the approval process for herbal medications, and their production and marketing should be standardized and made to comply with higher standards for patient safety [22,26,27].

The current study has several limitations. First, the data presented here were limited to nursing students. Second, because the results of this study were drawn from a single university in Saudi Arabia’s Riyadh region, they may not fully reflect the knowledge of all nursing undergraduates in Saudi Arabia. Due to the self-administered nature of the online questionnaire used to gather the data, recall or social desirability bias may have been present. Thus, in future research, we propose an alternate technique for gathering data that might reduce this issue. Third, because male and female colleges in Saudi Arabia have separate campuses and women are still not permitted to study alongside men, responses from the female student population were limited. Future research with a larger sample size and nursing undergraduates from other nursing-related schools is needed to better corroborate the findings.

Conclusions

To summarize, nursing students have a lack of understanding and knowledge of HDIs. The vast majority of students agreed that they needed to learn more about HM and its interactions. The knowledge of HDIs was found to be inadequate in identifying specific HDIs. For example, only 20.4% of them identified ginkgo biloba interactions with warfarin and ibuprofen, and 13.6% of them identified warfarin interactions with green tea, ginger, and chamomile tea. Students with a previous history of using HMs had a higher mean knowledge score (3.75), compared with those without a family history of using HM (2.76), suggesting a statistically significant correlation. In a similar vein, people who suggested HMs to others had a mean knowledge score (3.65) that was greater than those who did not (2.78), revealing a significant effect on the mean knowledge scores of HMs. There is a need to educate and teach undergraduates about HMs and HDIs, and this can be achieved by introducing courses on HM and HDIs in the academic curriculum. This could help graduates to overcome obstacles during practice.