Background

Malaria remains one of the diseases with the highest human morbidities and mortalities in the world [1]. It is one of the greatest obstacles to socio-economic development, especially in the developing countries where it is endemic [2, 3]. In 2019, there were 229 million global malaria cases with a case incidence of 57% [1]. The African continent accounted for 95% of all global malaria cases, with Uganda accounting for 5% of these. In the same year, the global malaria mortality rate stood at 10 persons per 100,000 at risk. In 2020, there was a marked increase in global malaria incidence with about 14 million more cases and 69,000 additional deaths compared to 2019. About two-thirds of the mortalities were attributed to disruptions in malaria services during the COVID-19 pandemic, particularly in countries of the WHO African Region [1].

In East Africa, malaria remains endemic in the Lake Victoria basin, with Anopheles gambiae and Anopheles funestus being the implicated vectors perpetuating it [4, 5]. Plasmodium falciparum and Plasmodium vivax are the two deadliest malarial parasites in sub-Saharan Africa. Currently, artemisinin-based combination therapies (ACT) are the treatment of choice for malaria [6,7,8]. They are available for free but are sometimes hard to access in Ugandan government health centres and hospitals [9]. Early diagnosis and prompt treatment of malaria should occur within 24 h of the onset of symptoms to decrease the risk of severe complications and onward transmission which occurs within a few hours for P. falciparum malaria [10, 11]. Unfortunately, there are delays in seeking care, obtaining a diagnosis and receiving appropriate treatment by Ugandans which is associated with fatal malaria. While tremendous progress has been made in the fight against malaria through the improvement of health system performance and increased public knowledge about the disease, increasing resistance to commonly used treatments (including ACT) is presenting new challenges to malaria control and eradication programmes [12, 13]. Therefore, malaria cases remain high in Uganda, despite the availability of ACT [14, 15]. Due to the high risk of morbidity and mortality, the Ugandan government spends a lot of money on procuring antimalarial drugs for its citizens.

In spite of the success achieved regarding universal health coverage, traditional and complementary medicines have not remained an integral component of the health care system of Uganda. Traditional medicine is culturally accepted, readily available, free or cheap and is perceived to be safe and efficacious. The evaluation of plant materials for new drugs is justified because many modern allopathic medicines including antimalarial drugs originated from plants [16]. For example, the two main groups (artemisinin and quinine derivatives) of modern antimalarial drugs contain lead compounds derived from Cinchona species and Artemisia annua plant extracts, respectively [17]. Uganda forms part of the East African botanical plate which is rich in medicinal plants. Communities in different regions of the country use different herbs within their geographical range, although a few common herbs are used by different communities across the country [18]. However, ethnobotanical documentation of the medicinal plants used to treat malaria is far from complete among various communities in the country. Therefore, this study aimed at generating information that will contribute to the development of efficacious and safe antimalarial drugs, by documenting and prioritizing plants used for treating malaria in Tororo district, Eastern Uganda.

Methods

Study area

This was an ethnobotanical survey conducted in Tororo district (0° 41′ 34.0008″ N and 34° 10′ 51.9960″ E), Eastern Uganda (Fig. 1). Tororo borders Bugiri district to the West, Butaleja district to the North, Busia district to the South, Republic of Kenya to the East and Mbale district to the North East. It has a population of about 597,500 people distributed as 51.2% females, and 48.8% males. The majority of the people (86%) live in the rural areas. The major economic activity in the area is subsistence farming. Tororo district is one of the malaria-endemic districts with an entomological infective rate of 591, making it one of the most malaria burdened districts in Uganda [19, 20]. Despite government efforts to increase access to health services from health facilities, residents of Tororo district still rely on traditional medicine for their primary health care. This is attributed to the high level of poverty in the district, long distances travelled to access free health services and prolonged drug stockouts [21, 22].

Fig. 1
figure 1

Map showing the location of the study area. Inset is the map of Uganda showing the location of Tororo district

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Sample size and sampling procedures

A sample size of 245 respondents was calculated using the formula suggested by Krejcie and Morgan [23]. Due to COVID-19 restrictions and limited resources, we interviewed only 151 respondents (21 traditional medicine practitioners and 130 common people, i.e. local people who regularly use plants for medicinal purposes). These respondents were both females and male aged 18 years and above.

Study design, selection of study sites and participants

Field survey for this study was conducted from February 2020 to September 2020 using a cross-sectional study design. Three sub-counties of Tororo district (Fig. 1) namely Eastern division, Kirewa, and Paya were randomly selected. Two parishes were randomly selected from each division and eventually, two villages were considered. This gave a total of 12 villages. In each village, herbalists were purposively sampled based on their reputation in the community to treat symptoms of malaria. As the key informants, herbalists were identified using snow balling method based on the principle of saturation [24]. Using this method, once an herbalist was identified and interviewed, they were asked to refer the research team to another herbalist within their networks. The subsequent herbalist then referred us to the next herbalist in their networks until saturation was reached. From each village, 10–15 respondents were interviewed altogether. Experienced non-herbalists were randomly selected to participate in the study after obtaining their prior informed consent.

Ethnobotanical data collection

A pilot study was undertaken in February 2020 to introduce the study to the local area administration, seek their permission to conduct the study and pre-test the study tool. Data were collected from the respondents following guidelines of conducting research during the COVID-19 pandemic established by the Uganda National Council of Science and Technology [25]. Data were collected using a semi-structured questionnaire which was translated into Japadhola, the principal language spoken in Tororo district. The questionnaire included questions on the respondent’s biodata, knowledge on signs and symptoms of malaria, harvesting, preparation, administration and dosage of malaria herbal medicines (Additional file 1: S1). Questions on the existing knowledge, attitudes and practices related to malaria recognition, control and treatment in Tororo district were also included. Three focus group discussions were held with community members (one per sub-county) to complement the questionnaire survey. Plants mentioned by respondents were identified during guided field walks with the informants [26]. Voucher specimen of each plant species were prepared for correct botanical identification and deposited at the Makerere University Herbarium. Species nomenclature follows the flora for tropical East Africa and was verified using the Plants of the World Online (POWO) database (https://powo.science.kew.org).

Data analysis

Numerical data were entered into Microsoft Excel spread sheet, coded, and exported to SPSS software (version 26, SPSS Inc.) for analysis. Descriptive statistics such as percentages and frequencies were used to summarize ethnobotanical and respondents’ socio-demographic data. Further, ethnobotanical data were used to calculate informant consensus factor as well as perform paired comparison and preference ranking.

Informant consensus factor

To determine the homogeneity of the ethnobotanical information collected from the respondents, the Informant Consensus Factor (ICF) was computed using formula 1 [27]:

$$\mathrm{ICF}=\frac{\mathrm{Nur}-\mathrm{Nt}}{\mathrm{Nur}-1},$$
(1)

where “\(\mathrm{Nur}\)” refers to the total number of use reports for each disease cluster and “\(\mathrm{Nt}\)” refers the total number of species in each use category. The ICF values range from 0 to 1. High ICF values (close to 1) are obtained when only a few plant species are reported to be used by a high proportion of informants to treat a particular disease and this implies that there is a well-defined mechanism in the community of sharing information between informants. Low ICF values (close to 0) are obtained when many plant species are reported to be used by a high proportion of informants to treat a particular disease and this implies that there is no well-defined mechanism in the community of sharing information between informants.

Preference ranking

Preference ranking was performed as reported by Martin [28]. When a variety of plant species are utilized to treat the same health problem, individuals prefer one over the other. Key informants were given the task of comparing the given medicinal plants based on their values, with the highest number (5) given to medicinal plants which they preferred to be the most effective in treating malaria and the lowest number (1) given to those plants that they preferred to be the least effective in treating malaria [29].

Paired comparison of medicinal plants

A paired comparison was made for five medicinal plants used to treat malaria in the study area. Ten reputable herbalists were requested to rank the species based on their efficiency in management of malaria as follows: 1 = least, 2 = good, 3 = very good and 4 = excellent [29].

Results

Sociodemographic characteristics

The respondents were distributed by gender with 41.1% females and 58.9% males. The majority of these (94%) were married. The major occupation was subsistence farming (61.6%), followed by casual labour for wages (22.5%). The respondents had a median age of 46.0 years, and a significant percentage (65%) had attained only primary education (Table 1).

Table 1 Socio-demographic characteristics of respondents from Tororo district
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Knowledge on malaria, its symptoms and treatment-seeking behaviour of patients

Malaria appeared to be prevalent and well understood by the respondents in Tororo district. Most respondents (90%) had suffered from malaria in the last six months before the date of the interview. The respondents also mentioned the correct signs and symptoms of malaria (Fig. 2). Fever (33%) was the main sign of malaria reported by the respondents, followed by vomiting (13%) and body weakness (11%). Other signs and symptoms of malaria reported were headache (13%), diarrhoea (7%), convulsions (6%), loss of appetite (6%) and body chills (11%).

Fig. 2
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Reported signs and symptoms of malaria by respondents in Tororo district, Eastern Uganda

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On developing malaria, most respondents (76%) reported that they used traditional medicine (TM) alone as the first line of treatment compared to 17.2% who used modern medicine (MM) alone. When they failed to improve, they switched to MM. Thus, on re-treatment, the number of people that used TM alone decreased to 51%, while 41% used MM (Fig. 3). In clinical practice, a first-line treatment/first-line therapy is the treatment that is accepted as best for the initial treatment of a condition or disease. In the context of our study, malaria patients tend to use herbal remedies (TM) as the first treatment for malaria before attempting to use MM. In case it fails, the second treatment sought after is MM.

Fig. 3
figure 3

Treatment options used by malaria patients in the studied communities of Tororo district, Eastern Uganda. TM: traditional medicine; MM: modern medicine

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Plant species used in preparation of herbal remedies for malaria treatment in Tororo district

Forty-five plant species were mentioned by respondents in this study to be used in preparation of herbal remedies for management of symptoms of malaria (Table 2). Of the inventoried species, nine were mentioned by six or more people. These are; Vernonia amygdalina Delile (58), Chamaecrista nigricans (Vahl.) Greene (14), Aloe nobilis (L.) Burman. (13), Warburgia ugandensis Sprague (12), Abrus precatorius L. (11), Kedrostis foetidissima Cogn. (10), Senna occidentalis L., Azadirachta indica (7 each), and Mangifera indica L. (6). The species were distributed as trees (37.7%), shrubs (26.7%) and herbs (35.6%) by growth habit. These species were from 26 families and 44 genera. Fabaceae (17.8%), Asteraceae (8.9%), Lamiaceae and Rutaceae (6.7% each) were the most represented families (Fig. 4). The ICF for malaria calculated was 0.76, implying that there is considerable agreement among the community members in the medicinal plants used in management of malaria. For preference ranking, Vernonia amygdalina Delile, Chamaecrista nigricans (Vahl.) Greene and Aloe nobilis (L.) Burman. were ranked first, second and third, respectively (Table 3). The results of paired comparison test for the five frequently mentioned plant species, respondents (10) selected Vernonia amygdalina Delile first, followed by Chamaecrista nigricans (Vahl.) Greene, Warburgia ugandensis Sprague, Aloe nobilis (L.) Burman. and Abrus precatorius L. (Table 4).

Table 2 Medicinal plants used in Eastern Division, Kirewa, and Paya sub-counties of Tororo district, Uganda, for treating malaria (n = 45)
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Fig. 4
figure 4

Distribution of medicinal plant species for management of malaria in Tororo district by families

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Table 3 Preference ranking of medicinal plants used for treating malaria in Tororo District, Eastern Uganda
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Table 4 Paired comparison on five commonly used medicinal plants used for treating malaria in Tororo District, Eastern Uganda
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Preparation and administration of herbal medicine for management of malaria

Leaves (67.3%) were the most commonly used plant part, followed by roots (13.5%), root bark (5.8%) and fruits (5.8%) (Fig. 5). The herbal remedies are prepared through maceration (56%) and as decoctions (34%). However, they can also be powdered (6%) or prepared as infusions (4%).

Fig. 5
figure 5

Plant parts used in the treatment of malaria in Tororo district, Uganda

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The herbal medicines were majorly administered orally (86.7%). Other routes of administration were topical baths (11.1%) and steam baths (2.2%). The medicaments were mostly processed and used when needed, and were rarely preserved. The most used packaging materials for liquid forms were plastic bottles (0.5–1L) and small jerricans (1–3L), whereas solids and powders were packed in polyethene bags. The plant materials were collected from the wild (46%), gardens (30%), compounds (14%) and other places (11%) such as roadsides and swamps. Most respondents (78.8%) reported that they grow the plants while others (10%) said that they purchase the herbs.

Discussion

Malaria is still a disease of public health importance in Tororo district. Our results indicate that people are familiar with malaria, and can correctly recognize it basing on the signs and symptoms. Majority of the people used TM (as opposed to MM) to treat malaria. A study on treatment-seeking behaviour and practices among caregivers of children aged 5 years with presumed malaria in rural Namutumba district (a nearby district in Eastern Uganda) showed that only 36.1% of the patients took herbal medicines. Most of them sought MM with nearly all the patients who used TM also taking modern antimalarials [30]. Further, 79.2% of the patients who used herbal medicines to treat malaria also received artemether–lumefantrine in in the same study area [30]. Hasabo et al. [31] in their study in South Sudan reported that when people fell sick from malaria, 78% of the patients sought treatment from the nearby primary health centre (MM). Although we could not ascertain the real drivers of the high use of TM in this study area, we think that apart from poverty that makes the conventional drugs unaffordable [32], the high travel restrictions instituted during the COVID-19 pandemic especially on border districts like Tororo could have forced patients to find alternative therapies of which herbal medicines are the most readily available and affordable. Additionally, they were also perceived to be efficacious and safe. The form of treatment chosen for malaria depended on its perceived severity. For the most part, uncomplicated malaria is often treated using a mixture of traditional and modern methods, and this is a common practice throughout Africa [33, 34].

This study identified 45 plant species used in Tororo district, Eastern Uganda for managing malaria. Most of the species identified has been cited for treatment of malaria in other parts of Uganda as well as other countries. For example, Albizia coriaria, Momordica foetida and Carica papaya are used elsewhere in Uganda [18, 30, 35, 36], Cameroon [37] and Zimbabwe [38]. Harrisonia abyssinica is used in Tanzania [39] and South Africa [40], while Tamarindus indica, Carica papaya and Ocimum basilicum are used in Indonesia [41]. With the exception of a few species such as Kedrostis foetidissima, Mangifera indica and Carissa spinarum, most of the plants indicated by the respondents in Tororo are used in the management of malaria and its symptoms in the neighbouring Kenya [5]. The high ICF (0.76) implies that there is sharing of indigenous knowledge related to medicinal plants use in malaria management among the community members. Hence, it is likely that the same plant species are used in the preparation of herbal medicines for malaria by majority of the people in Tororo. The dominant source of collection of medicinal plants from the wild highlights the dependence of the traditional healers on wild crafted materials. However, they are also interested in conserving the species as some collect them from gardens and the compound. The species mentioned by most people could be considered to be efficacious for the treatment of malaria and were prioritized on this basis for further analysis. A review of the available literature revealed that of the 45 plant species used in the traditional treatment of malaria in Tororo, 17 species have been evaluated for the antimalarial/antiplasmodial activity using different assays. These species possess acceptable preclinical safety and efficacy (Table 5). This confirms that indeed the reported medicinal plants possess antimalarial properties which can be further investigated for development of new antimalarial drugs.

Table 5 Literature on antiplasmodial/antimalarial activities and toxicity of extracts and isolated compounds of the plants identified in Tororo District, Eastern Uganda
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The oral route was the most used mode of drug administration. This could partly be attributed to the fact that oral dosage forms are easy to prepare and administer [5]. Like in other communities, appropriate dose determination was a challenge as many herbalists just gave estimates using cups and spoons. The preparation and packaging procedures were also prone to contamination and there was no evidence of consistency in the preparation procedures used. Hence, there is a need to sensitize the respondents about standardization procedures and good manufacturing practices so as to enhance the quality of their traditional medicine.

Conclusion

This study identified 45 medicinal plants majorly from family Fabaceae and Asteraceae used in preparation of traditional medicines for management of symptoms of malaria in Tororo district. The phytochemical constituents, antiplasmodial and antimalarial activity as well as toxicity profiles of the unstudied species with high percentage use values should be investigated to validate their uses in the management of malaria in an effort to discover novel antimalarial drugs.