Journal of Ethnopharmacology ∎ (∎∎∎∎) ∎∎∎–∎∎∎

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Herbs and herbal combinations used to treat suspected malaria in Bo, Sierra Leone Shamika Ranasinghe a, Rashid Ansumana b,c, Joseph M. Lamin b, Alfred S. Bockarie b, Umaru Bangura b, Jacob A.G. Buanie b, David A. Stenger d, Kathryn H. Jacobsen a,n a

George Mason University, 4400 University Drive, Fairfax, VA 22030 USA Mercy Hospital Research Laboratory, Kulanda Town, Bo, Sierra Leone c Njala University, Bo, Sierra Leone d U.S. Naval Research Laboratory, 4555 Overlook Ave. SW, Washington, DC 20375 USA b

art ic l e i nf o

a b s t r a c t

Article history: Received 19 December 2014 Received in revised form 26 February 2015 Accepted 9 March 2015

Ethnopharmacological relevance: Most adults in West Africa treat acute febrile illnesses with local herbs, but the patterns of herbs used for malaria have not been recently described in Sierra Leone. Materials and methods: We used a population-based cross-sectional approach to interview 810 randomlysampled rural and urban adult residents of Bo, Sierra Leone, in December 2013 and January 2014 about their use of herbal remedies when they suspect they have malaria. Results: In total, 55% of the participants reported taking one or more of seven herbs to treat symptoms of malaria. Among herb users, the most commonly used anti-malarial herbs were Moringa oleifera (moringa, 52%) and Sarcocephalus latifolius (yumbuyambay, 50%). The other herbs used included Senna siamea (shekutoure, 18%), Cassia sieberiana (gbangba, 18%), Uvaria afzelii (gone-botai, 14%), Morinda chrysorhiza (njasui, 14%), and Craterispermum laurinum (nyelleh, 7%). Combination herbal therapy was common, with 37% of herb users taking two or more herbs together when ill with suspected malaria. Conclusions: Indigenous medical knowledge about herbal remedies and combinations of local herbs remains an integral part of malaria case management in Sierra Leone. & 2015 Published by Elsevier Ireland Ltd.

Keywords: Cross-sectional study Herbal medicine African traditional medicine Malaria Moringa oleifera West Africa

1. Introduction Traditional medicine involving traditional healers and the use of herbs, animal parts, spiritual therapies, manual therapies, and exercises remains common in sub-Saharan Africa, where more than 80% of the people use herbs to treat their illnesses (WHO, 2002). There are thought to be more than 100 times more traditional healers than conventional medical doctors or nurses in the region, and a high proportion of the more than 300 million West Africans at risk of malaria prefer to use affordable and convenient traditional medicines when they have symptoms of malaria rather than seeking treatment from the formal healthcare system (Bodeker and Kronenberg, 2002; Soh and BenoitVical, 2007; WHO, 2002, 2013). The West African region has incredible biodiversity, and many indigenous plants are used as antimalarial

n Correspondence to: Department of Global and Community Health, George Mason University, 4400 University Drive 5B7, Fairfax VA 22030, USA. Tel.: þ 1 703 993 9168; fax: þ 1 703 993 1908. E-mail addresses: [email protected] (S. Ranasinghe), [email protected] (R. Ansumana), [email protected] (J.M. Lamin), [email protected] (A.S. Bockarie), [email protected] (U. Bangura), [email protected] (J.A.G. Buanie), [email protected] (D.A. Stenger), [email protected] (K.H. Jacobsen).

agents, even though few formal studies have examined the dosages and delivery mechanisms that are safest and most effective (Soh and Benoit-Vical, 2007). There is a need for additional research on which herbs are most widely used and which combinations of herbs are used in various populations to complement laboratory studies of antiplasmodial efficacy. Malaria remains endemic in Sierra Leone, in West Africa. Our previous research in Bo, the second largest city in Sierra Leone, found that the majority of adults in Bo presumptively self-diagnose bouts of malaria based on their symptoms and then treat their acute febrile illnesses at home (Ansumana et al., 2013). Many adults in Bo will seek professional assistance from a healthcare provider in the formal or informal sector only if they remain febrile after several days of home treatment or if they become alarmingly ill. However, our survey instrument for that study did not ask participants about the particular herbs and other local remedies that they use as home-based malaria treatment. In the follow-up study presented in this paper, we interviewed several hundred adults from both rural and urban areas in the Bo district in southern Sierra Leone about their preferred malaria treatments. We had two primary goals for this analysis. First, we sought to document the traditional medicine knowledge and practices that have been passed down through the generations and across tribal groups in Sierra Leone (Lebbie and Guries, 1995). Sierra Leone

http://dx.doi.org/10.1016/j.jep.2015.03.028 0378-8741/& 2015 Published by Elsevier Ireland Ltd.

Please cite this article as: Ranasinghe, S., et al., Herbs and herbal combinations used to treat suspected malaria in Bo, Sierra Leone. Journal of Ethnopharmacology (2015), http://dx.doi.org/10.1016/j.jep.2015.03.028i

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is a biodiverse country, and documentation of that diversity is an important part of preserving the cultural heritage of the nation's many ethnic populations as well as promoting environmental conservation (Macfoy, 2013; Turay, 1997). Older studies of herbs used for malaria treatment in Sierra Leone are useful resources (Macfoy and Sama, 1983; Marshall et al., 2000), but the diversity of current-day Bo provides a unique opportunity to explore how herbal remedies are being used today. Second, we wanted to explore whether herbs were being used singly or in combination in Bo. Artemisin-based combination therapy (ACT) is the malaria treatment recommended by the World Health Organization, because it helps to combat the development of drug resistance (WHO, 2013), and our conversations with respected local herbalists had indicated that herbal mixtures rather than single herbs were increasingly being recommended to Bo residents seeking traditional remedies.

2. Materials and methods 2.1. Sampling/Recruiting We collected data in Bo city and the surrounding rural areas of Bo district during December 2013 and January 2014. Households were randomly sampled for this study using a geographic information system (GIS) database created and maintained by the Mercy Hospital Research Laboratory (MHRL) in Bo (Ansumana et al., 2010). A twostage cluster sampling strategy was used for urban residents. In the first stage, seven of 68 municipal sections (neighborhoods) in the city were randomly sampled. In the second stage, 30 households from each of those seven sections were randomly sampled for participation. Thirty households were also recruited from each of 23 villages randomly sampled from a list of all 1266 villages in Bo district. When a sampled community was home to fewer than 30 households, interviewers visited households near the sampled village until the 30 households had been contacted. Interviewers alternated between requesting to interview a female household member and requesting to interview a male household member. Adults febrile at the time of household contact were preferentially recruited, as long as they were healthy enough to consent to and complete an interview. In total, an adult representative from 824 (91.6%) of the 900 sampled households participated in the study. Of these 824 participants, 810 answered the questions about the use of herbs for malaria treatment. 2.2. Questionnaire The questionnaire asked a series of questions about sociodemographics, health status, and malaria diagnosis and treatment practices. In particular, we asked “When you think you have malaria, do you usually take a local herb?” and we asked those who reported usually taking an herbal treatment for malaria an open-ended follow-up question about which herb or herbs were usually taken. We did not use a pre-selected list of antimalarial herbs; this was an open-ended question for each participant. We also asked what kind of medication those with current fevers were taking. Of the 33 febrile participants who said they were taking anti-malaria herbs at the time of the survey, eight listed only one herb and the remaining 25 named herbal combinations. Most of these 33 participants provided the same response to both the question about current herbs (asked only to those with fevers at the time of the survey) and the question about usual herbs (asked of all participants), but when there were discrepancies the lists of herbal combinations were merged. 2.3. Plant identification The scientific names for local herbs were acquired and validated by: (1) consulting with respected local herbalists in Sierra

Leone about the products they collect, process, and sell, (2) using two books about medicinal herbs in Sierra Leone, Medicinal Plants and Traditional Medicine in Sierra Leone (Macfoy, 2013) and Medicinal Plants of Sierra Leone: A Compendium (Turay, 1997), to confirm the scientific names provided by local experts, (3) consulting with a botany professor who specializes in African plant biology about the current classification and naming of the herbs, and (4) confirming the accepted scientific names, families, and botanical authorities in the African Plant Database (2015) and The Plant List (2013).

2.4. Ethical considerations The research protocol was approved by the institutional review boards of Njala University, George Mason University, the Liverpool School of Tropical Medicine, the U.S. Naval Research Laboratory, and the Office of the Sierra Leone Ethics and Scientific Review Committee (SLESRC). No compensation or incentives were provided to participants, and their involvement was voluntary. All participants provided written documentation of informed consent.

2.5. Analysis The study population for this analysis consisted of the 810 participants who answered the question about whether they usually take herbs when they have malaria. We used 2-sided Pearson's Chi-squared tests with a significance level of α ¼0.05 to compare characteristics of those who do and do not use herbal anti-malarial remedies. All analyses were conducted using IBM SPSS version 21.

3. Results In total, 442 (54.6%) of the 810 participants reported taking local herbs when suspected that they had malaria (Table 1), usually by drinking a tea made from the leaves or other parts of the plant, depending on the species. Herbal remedy use did not vary significantly by age, years of formal education, or functional literacy. Males and rural residents were more likely than females and urban residents to take antimalarial herbs. Although those who were febrile and those who were without fever at the time of the interview reported similar rates of herbs when they had malaria, those who reported average or poor quality of life and satisfaction with health over the past four weeks were much more likely than more satisfied persons to report usually using antimalarial herbs for malaria treatment. Participants who reported interacting less often with the formal healthcare system —not seeking confirmatory laboratory tests or consulting with a doctor —were more likely than others to use herbs. Seven herbs were named by participants as ones that they usually use when they have malaria. The scientific names, local names, and families for all seven are listed in Table 2. Of the 442 participants who take herbs for malaria, 424 provided the name of at least one antimalarial herb they take regularly for symptoms of malaria. The most commonly named herbs were Moringa oleifera and Sarcocephalus latifolius. In total, 267 (63.0%) of the 424 reported taking only one antimalarial herb when ill. The most common herbs used alone were M. oleifera (n¼101), S. latifolius (n¼ 79), and Cassia sieberiana (n¼46). Combination herbal therapy was popular (Table 3), with 66 (15.6%) of the herb-taking participants using 2 herbs together, 41 (9.7%) taking 3 herbs, 42 (9.9%) taking 4 herbs, and 8 (1.9%) taking 5 or 6 herbs. The most common combinations were M. oleifera and S. latifolius (n¼27); M. oleifera, S. latifolius, Senna siamea, and Uvaria afzelii (n¼18); Morinda chrysorhiza, M. oleifera, and S. latifolius (n¼10); M. oleifera, S. latifolius, and S. siamea (n¼ 9); and M. chrysorhiza and M. oleifera (n¼8).

Please cite this article as: Ranasinghe, S., et al., Herbs and herbal combinations used to treat suspected malaria in Bo, Sierra Leone. Journal of Ethnopharmacology (2015), http://dx.doi.org/10.1016/j.jep.2015.03.028i

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Table 1 Characteristics of participants who usually take a local herb when they suspect they have malaria in Bo, Sierra Leone. Characteristic

Response

All participants Sex

Male Female Age 18–29 30–49 50–115 Years of formal education No formal school 1–7 years 8–11 years Z 12 years Comfortable reading newspaper Yes No Location Rural Urban Health status at the time of the survey Febrile Afebrile Quality of life over the past four weeks Good or very good Average Poor or very poor Satisfaction with health over the past four Satisfied or weeks very satisfied Average Dissatisfied or very dissatisfied Comparison of health status to the average More healthy person of the same age About the same Less healthy Belief about how often adult fevers in the Always community are due to malaria Most of the time Sometimes Rarely or never Had a laboratory test to determine the cause Yes of most recent febrile illness No Yes Usually consults with a doctor (or other No health professional) about suspected malaria Usually takes a laboratory test to confirm Yes suspected malaria No Yes Usually buys medicines to treat malaria without first consulting a doctor (or other No health professional)

Percentage of study participants Percentage of participants within each row who use by demographics and other antimalarial drugs characteristics

p-values comparing the rate of antimalarial herb use by demographics and other characteristics

100 (n ¼810) 50.5 49.5 29.4 41.2 29.4 64.2

54.6 (n¼ 442) 59.4 49.6 50.6 54.7 58.4 53.3

– 0.005

14.4 10.5 10.9 30.3 69.7 81.0 19.0 50.5 49.5 31.8

65.8 52.9 48.9 50.6 55.1 56.9 44.8 55.7 53.4 45.1

39.1 29.2

58.2 59.7

46.8

48.0

25.7 27.5

61.1 59.6

28.5 29.9

50.6 54.1

41.6 25.4 36.0

57.6 62.6 55.1

32.7 5.8

46.8 59.6

40.5 59.5 53.5 46.5

51.7 56.3 51.1 57.5

40.9 59.1 79.7 20.3

48.8 57.9 56.5 46.9

0.245

0.056

0.318 0.007 0.497 0.001

0.002

0.263

0.015

0.192 0.071

0.011 0.028

Table 2 Species of plants used for malaria treatment in Bo, Sierra Leone, among the 424 participants who named one or more herbs they use for malaria treatment. Scientific name

Plant family

Local Name

Number of participants who take this herb when they suspect they have malaria

Moringa oleifera Lam. Sarcocephalus latifolius (Sm.) E.A. Bruce Senna siamea (Lam.) H.S. Irwin and Banerby Cassia sieberiana DC. Uvaria afzelii G.F. Scott-Elliot Morinda chrysorhiza DC. Craterispermum laurinum (Poir.) Benth.

Moringaceae Moringa 221 Rubiaceae Yumbuyambay 210

52.1 49.5

Fabaceae

Shekutoure

76

17.9

Fabaceae Annonaceae Rubiaceae Rubiaceae

Gbangba Gone-botai Njasui Nyelleh (alum bark)

74 60 60 30

17.5 14.2 14.2 7.3

4. Discussion More than half of the Sierra Leonean adults participating in this study said that they take one or more local herbs as treatment

Percentage of those who take local herbs for malaria who use this herb

when they think they have malaria. A previous study of child health in Sierra Leone found that 22% of caregivers give their children herbs when the children have fevers (Bakshi et al., 2013). Both the adult and child health studies noted that participants

Please cite this article as: Ranasinghe, S., et al., Herbs and herbal combinations used to treat suspected malaria in Bo, Sierra Leone. Journal of Ethnopharmacology (2015), http://dx.doi.org/10.1016/j.jep.2015.03.028i

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Table 3 Number of participants in Bo, Sierra Leone who indicated using one herb or combinations of herbs to treat malaria. 1 Herb (n¼ 267)

Mo (101) Sl (79) Cs (46) Ss (16) Mc (12) Ua (8) Cl (5)

2 Herbs (n¼ 66)

3 Herbs (n¼ 41)

4 Herbs (n ¼42)

Mo|Sl (27) Mc|Mo (8) Cs|Sl (6) Sl|Ua (6) Mc|Sl (4) Cl|Sl (3) Mo|Ss (3) Cl|Mo (2) Mo|Ua (2) Cl|Mc (1) Sl|Ss (1) Cl|Ua (1) Cs|Mo (1) Cs|Ua (1)

Mc|Mo|Sl (10) Mo|Sl|Ss (9) Cs|Mo|Sl (5) Sl|Ss|Ua (4) Mo|Sl|Ua (3) Cl|Cs|Mc (1) Cl|Cs|Mo (1) Cl|Mo|Sl (1) Cl|Sl|Ua (1) Cl|Ss|Ua (1) Cs|Mo|Ss (1) Cs|Mo|Ua (1) Cs|Sl|Ss (1) Mc|Sl|Ua (1) Mo|Ss|Ua (1)

Mo|Sl|Ss|Ua (18) Cl|Mo|Sl|Ss (5) Mc|Mo|Sl|Ss (5) Cs|Mc|Mo|Sl (4) Mc|Mo|Sl|Ua (4) Cl|Mc|Mo|Sl (1) Cl|Mc|Sl|Ss (1) Cl|Sl|Ss|Ua (1) Cs|Mc|Mo|Ss (1) Cs|Sl|Ss|Ua (1) Mc|Sl|Ss|Ua (1)

5 or 6 Herbs (n¼ 8)

Cl|Mc|Mo|Sl|Ss (2) Mc|Mo|Sl|Ss|Ua (2) Cl|Cs|Mc|Mo|Sl|Ua (1) Cl|Cs|Mo|Sl|Ua (1) Cl|Cs|Sl|Ss|Ua (1) Cs|Mc|Mo|Sl|Ss (1)

Cs: Cassia sieberiana; Cl: Craterispermium laurinum; Mc: Morinda chrysorhiza; Mo: Moringa oleifera; Sl: Sarcocephalus latifolius; Ss: Senna siamea; Ua: Uvaria afzelii.

frequently treated fevers at home with local herbs and only sought outside assistance if the condition did not resolve after several days or became worse (Bakshi et al., 2013). While some studies in West Africa have found that medicinal herbs are preferred to other pharmaceutical agents because the herbs are cheaper, cultural and religious preferences also influence this decision (Jusu and Sanchez, 2013). The most popular anti-malarial herbs described in recent studies from other countries in West Africa are similar to those from this study in Sierra Leone. In Burkina Faso, C. sieberiana, S. latifolius, and S. siamea are used (Nadembega et al., 2011). In Ghana, M. oleifera and S. latifolius are used (Asase et al., 2010). In neighboring Guinea, S. latifolius is the most popular antimalarial herb, and C. sieberiana, Craterispermum laurinum, M. chrysorhiza, and S. siamea are also used (Traore et al., 2013). In Nigeria, C. sieberiana, M. oleifera, S. latifolius, and S. siamea are used (Adebayo and Krettli, 2011). U. afzelii is used by traditional healers from Cote d'Ivoire (Ménan et al., 2006; Okpekon et al., 2004). The use of combinations of herbs has been previously reported from Sierra Leone. In 1994, herbalists from the Mende population reported recommending a combination of C. sieberiana and C. laurinum or, less often, a combination of C. laurinum and M. chrysorhiza (Lebbie and Guries, 1995). M. oleifera was not commonly used at that time, at least not among the Mende, who remains the largest ethnic group in Bo today, although M. oleifera is widely used across the tropics, especially in South Asia, as a remedy for a diverse set of health conditions (Anwar et al., 2007). Similarly, S. siamea was not common in the study area 20 years ago, even though it is widely used for medicinal purposes in Southeast Asia (Kamagaté et al., 2014). But the use of multiple antimalarial herbs—often three or more herbs at one time—may have become more common since then. A recent qualitative study of herbalists from Ghana found that herbal combination therapy had become the standard recommendation, and that herbalists believed that the use of multiple herbs was more effective for treating malaria than the use of just one species (Asase et al., 2012). In Guinea, a survey of traditional healers found that combinations of plants were more common than the use of single herbs, with a third of the traditional healers reporting recommending the use of three or more herbs (Traore et al., 2013). A systematic review of antimalarial herbs from Nigeria reported that single herbs were most commonly used but some multiple herb combinations were identified as well (Adebayo and Krettli, 2011). Although laboratory tests of C. sieberiana, M. chrysorhiza, and S. siamea previously conducted in Sierra Leone did not find significant antiplasmodial activity (Marshall et al., 2000), some studies conducted

in Africa on herbs such as S. latifolius and S. siamea have suggested otherwise (Adebajo et al., 2014; Sanon et al., 2003). The level of antiplasmodial activity observed in laboratory studies may depend on which part of the plant is tested. For example, the stems and roots of S. latifolius have different efficacies but are usually prescribed together (Benoit-Vical et al., 1998). Laboratory tests may not capture the combined effect of multiple plant parts in humans. The demand for new antiparasitic agents requires more of these common local herbs to be investigated in laboratory studies, and for subsequent clinical trials to be considered when the results of preliminary examinations are favorable. Besides evaluating the safety, efficacy, and optimal dosage of single herbs and herb combinations for use in malaria treatment, it will be important to examine possible interactions between herbs used in combination and between herbs and other malarial medications such as ACT. This study had several limitations: we asked community members to self-report medication use, we did not confirm that participants could correctly identify various samples of herbal specimens (though we did confirm the identities of local herbs through consultation with local experts in herbal medicine), and we did not use methods that allowed for the computation of plant use indices such as the salience value, use value, or fidelity value (Hoffman and Gallaher, 2007). Even so, this large population-based cross-sectional survey of herbal remedies for malaria in rural and urban Sierra Leone highlights the popularity of traditional medicines for home-based acute febrile illness treatment.

5. Conclusions Several species of herbs are used to treat malaria in Bo, Sierra Leone. Among them, M. oleifera and S. latifolius are frequently used, as they are in other West African countries. Combinations of several herbs are often used, with some local residents drinking five or six different herbs together when they suspect malaria. Traditional herbal therapies remain an integral part of the health environment in Bo. Future studies should document current (and perhaps changing) patterns in which herbs and herbal combinations are being used for medical purposes in various communities. These studies would contribute to ecological conservation efforts, preservation of cultural knowledge, and the promotion of public health.

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Please cite this article as: Ranasinghe, S., et al., Herbs and herbal combinations used to treat suspected malaria in Bo, Sierra Leone. Journal of Ethnopharmacology (2015), http://dx.doi.org/10.1016/j.jep.2015.03.028i

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Please cite this article as: Ranasinghe, S., et al., Herbs and herbal combinations used to treat suspected malaria in Bo, Sierra Leone. Journal of Ethnopharmacology (2015), http://dx.doi.org/10.1016/j.jep.2015.03.028i

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Herbs and herbal combinations used to treat suspected malaria in Bo, Sierra Leone.

Most adults in West Africa treat acute febrile illnesses with local herbs, but the patterns of herbs used for malaria have not been recently described...
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