M H M H J a b c d e f g a A R R A A K E H H T C 2 ( 0 d Journal of Ethnopharmacology 130 (2010) 43–53 Contents lists available at ScienceDirect Journal of Ethnopharmacology journa l homepage: www.e lsev ier .com/ locate / je thpharm edicinal plants used by traditional medicine practitioners for the treatment of IV/AIDS and related conditions in Uganda ohammed Lamordea,b,∗, John R.S. Tabuti c, Celestino Obuad, Collins Kukunda-Byobonae, indam Lanyerod, Pauline Byakika-Kibwikaa,b,f, Godfrey S. Bbosad, Aloysius Lubegad, asper Ogwal-Okengd, Mairin Ryanb, Paul J. Waakod, Concepta Merrya,b,f,g Infectious Diseases Institute, College of Health Sciences, Makerere University, P.O. Box 22418, Kampala, Uganda School of Medicine, University of Dublin, Trinity College, Dublin 2, Ireland Institute of Environment and Natural Resources, Makerere University, P.O. Box 7062, Kampala, Uganda Department of Pharmacology and Therapeutics, College of Health Sciences, Makerere University, P.O. Box 7072, Kampala, Uganda Department of Botany, Makerere University, Kampala, Uganda Infectious Diseases Network for Treatment and Research in Africa (INTERACT), Kampala, Uganda St James’s Hospital, Dublin 8, Ireland r t i c l e i n f o rticle history: eceived 12 February 2010 eceived in revised form 1 April 2010 ccepted 11 April 2010 vailable online 6 May 2010 eywords: thnobotany erbal medicine IV raditional knowledge a b s t r a c t Introduction and objectives: In Uganda, there are over one million people with HIV/AIDS. When advanced, this disease is characterized by life-threatening opportunistic infections. As the formal health sector struggles to confront this epidemic, new medicines from traditional sources are needed to complement control efforts. This study was conducted to document herbal medicines used in the treatment of HIV/AIDS and related opportunistic infections, and to document the existing knowledge, attitudes and practices related to HIV/AIDS recognition, control and treatment in Sembabule, Kamuli, Kabale and Gulu districts in Uganda. Methods: In this study, 25 traditional medicine practitioners (TMPs) were interviewed using structured questionnaires. Results: The TMPs could recognize important signs and symptoms of HIV/AIDS and its associated oppor- tunistic infections. The majority of practitioners treated patients who were already receiving allopathic medicines including antiretroviral drugs (ARVs) prescribed by allopathic practitioners. There were 103 species of medicinal plants identified in this survey. Priority plants identified include Aloe spp., Erythrina abyssinica, Sarcocephalus latifolius, Psorospermum febrifugum, Mangifera indica and Warburgia salutaris. There was low consensus among TMPs on the plants used. Decoctions of multiple plant species were commonly used except in Gulu where mono-preparations were common. Plant parts frequently used were leaves (33%), stem bark (23%) and root bark (18%). About 80% of preparations were administered orally in variable doses over varied time periods. The TMP had insufficient knowledge about packaging and preservation techniques. Conclusions: Numerous medicinal plants for treatment of HIV/AIDS patients were identified in the four districts surveyed and the role of these plants in the management of opportunistic infections warrants further investigation as these plants may have a role in Uganda’s public health approach to HIV/AIDS control. ∗ Corresponding author at: Research Department, Infectious Diseases Institute, ollege of Health Sciences, Makerere University, Mulago Hospital Complex, P.O. Box 2418, Kampala, Uganda. Tel.: +256 772 185590; fax: +256 41 307290. E-mail addresses: mlamorde@idi.co.ug, mohalamorde@yahoo.co.uk M. Lamorde). 378-8741/$ – see front matter © 2010 Elsevier Ireland Ltd. All rights reserved. oi:10.1016/j.jep.2010.04.004 © 2010 Elsevier Ireland Ltd. All rights reserved. 1. Introduction About one million Ugandans are infected with HIV, a predomi- nantly sexually transmitted virus that targets the immune system (UNAIDS and WHO, 2008). The advanced stage of the disease is known as the Acquired Immune Deficiency Syndrome (AIDS). Untreated, infected individuals develop profound suppression of the immune system and become susceptible to a wide range of infections (opportunistic infections) and certain malignancies. Con- sequently, the HIV/AIDS epidemic has dramatically increased the http://www.sciencedirect.com/science/journal/03788741 http://www.elsevier.com/locate/jethpharm mailto:mlamorde@idi.co.ug mailto:mohalamorde@yahoo.co.uk dx.doi.org/10.1016/j.jep.2010.04.004 44 M. Lamorde et al. / Journal of Ethnoph h t t r a i m w a t h e i 1 u a t n w m e e f c o o 2 o K d g Twenty-four TMPs attended to male and female patients and Fig. 1. Map of survey districts in Uganda. ealth needs of the Ugandan population, placing great demands on he formal health sector. Life-long therapy with antiretroviral drugs (ARVs) is the only reatment with proven efficacy against HIV (Palella et al., 1998). In ecent years, free access to ARVs has increased in Uganda. However, s of 2008, it is estimated that less than 50% of the patients requir- ng ARVs were actually receiving treatment (UAC, 2007). Moreover, ost ARV treatment sites are located in towns and urban centres hereas access to treatment in rural areas remains disproportion- tely low. Uganda has a diverse and rich medicinal plant resource rela- ive to other parts of Africa (Davis et al., 1986). Previous studies ave identified numerous medicinal plants used for various dis- ases of public health significance such as malaria and tuberculosis n Uganda (Adjanohoun et al., 1993; Tabuti et al., 2003; Kokwaro, 993). However, traditional medicine (TM) practice remains largely nregulated and poorly integrated into the formal health sector, nd there are scarce data on medicinal plants used for HIV/AIDS reatment (Yahaya et al., 2004). Documentation of Ugandan TM is critical to safeguard indige- ous knowledge and conserve medicinal plant species, both of hich are rapidly being lost (Kingdon, 1990). Importantly, docu- entation of TM can facilitate future research on the safety and fficacy of medicinal plants in the treatment of HIV/AIDS when used ither alone or concurrently with ARVs. The objectives of this study were to collect comprehensive data rom traditional medicine practitioners (TMPs) on medicinal plants ommonly used for HIV/AIDS treatment and to document the meth- ds of preparation and administration of TM, in four rural districts f Uganda. . Methods This survey employed an ethnobotanical approach comprising f TMP interviews in four Ugandan districts, Sembabule, Kamuli, abale and Gulu (Fig. 1). The four districts are predominantly rural istricts which were selected on the basis of cultural and geo- raphic diversity. armacology 130 (2010) 43–53 Ethical approval for this study was obtained from the Uganda National Council of Science and Technology (registration number HS 410). Before interviewing any respondent, the study team mem- bers explained the objectives of the study, methods and the plans for use of the data that were to be generated from the interviews. Verbal consent to conduct the interviews was sought from every respondent before the interview and was granted in every case. In preparation for the survey, semi-structured questionnaires were developed to collect data on TMP demographics, knowledge on TM and TM treatment practices. These questionnaires were pre- tested in a pilot survey and subsequently refined. During the actual survey, one TMP in each district was identified based on their rep- utation and participation in previous ethnobotanical surveys. A snowball sampling approach was used to identify other TMPs in the respective district (Tongco, 2007; Bernard, 2002). A few TMPs were identified by chance. Only TMPs who treated HIV/AIDS patients were included in the survey. A member of the study team served as an interpreter when necessary. At the end of each interview, voucher specimens of plants mentioned by the interviewees were collected. The plants were identified by staff at Makerere University Herbarium (MHU) and named according to the Flora of Tropical East Africa (FTEA). Plant voucher specimens were processed and indexed as JRST and KCB and deposited at the MHU. The voucher specimens of commonly known plants were not indexed. Clinical conditions treated in HIV/AIDS patients were coded using the Economic Botany Data Standard (www.kew.org/tdwguses). Questionnaire and botanical data were transferred into Excel® spreadsheets for coding and pre- liminary analysis. The dataset was exported to SPSS® statistical software Version 11.0 for Windows (SPSS Inc., Chicago, IL) for statistical analysis. The data were summarized in means and frequencies. Plant prioritization was based on frequency of use among TMPs and across districts. An Informant Consensus Factor (ICF) was calculated among the four study areas to determine the probability that respondents were using almost similar medicine plants (Albuquerque et al., 2006; Heinrich, 2000). The ICF was estimated by computing the difference between the number of TMPs reporting use of TM in the treatment of HIV/AIDS (nTMP) and number of taxa (nt) mentioned per district divided by the number of TMPs (nTMP) minus one. The following expression was used to calculate the ICF. ICF = nTMP − nt nTMP − 1 A high ICF (close to 1) suggests that the community is confident in the choice of plants, whereas a low ICF (close to 0) implies that the community is still experimenting and that the treatments may not be effective. In all cases, the calculated ICF was less than 0 and is not reported on further. 3. Results 3.1. Respondents’ biographic details We interviewed 25 TMPs, 10 from Kamuli district and five each from Sembabule, Gulu and Kabale districts. Nineteen of the inter- viewed TMPs were male. The median age (inter-quartile range) of respondents was 50 (43–58) years. Ten TMPs had attained post- primary formal education. Other demographic characteristics of TMPs across districts are shown in Table 1. five TMPs treated pregnant women and children as well. TMPs esti- mated that they received on average 29 (range, 2–250) patients each year. Most TMPs (n = 18) received patients who were already on treatment with allopathic medicines and 10 respondents http://www.kew.org/tdwguses M. Lamorde et al. / Journal of Ethnopharmacology 130 (2010) 43–53 45 Table 1 Demographic characteristics of respondents. Characteristic Frequency Ethnicity Acholi 5 Mukiga 5 Muganda 5 Munyoro-Mutooro 3 Mululi 3 Musoga 3 Munyoli 1 Religion Christian 16 Muslim 8 Animist 2a Main occupationb TMP 17 Farmer 6 Tree nursery operator 1 Carpenter 1 Clergy 1 Other occupations TMP 9 r f f p o 3 O j H i m o t p t i i F Table 2 Signs and symptoms by which TMPs recognize HIV/AIDS patients. Symptom Frequency Rash 13 Diarrhea 12 Cough 8 Anorexia 6 Pallor 6 Weight loss 6 Fever 5 Headache 4 Herpes zoster 4 Reddening of the lips 4 Chronic cough 3 Weakness 4 Skin ulceration 3 Vomiting 3 Abdominal pains 2 Chills 2 Constant headache 2 Difficulty swallowing 2 Painful urination 2 Genital ulcers 2 Oral ulcers 2 Sexually transmitted infections 2 Skin lesions 2 Skin pigmentation changes 2 Othersa 15 a Each of the following symptoms was mentioned once by TMPs: joint pains, bad Farming 13 a One TMP mentioned two religions. b One TMP disclosed two main occupations. eported that they received patients who were already on ARVs rom ARV treatment sites (Fig. 2). The TMPs acquired knowledge about the treatment of HIV/AIDS rom interaction with colleagues in the practice (n = 9), from their arents (n = 5) and through experimentation (n = 5). Other sources f knowledge acquisition mentioned included books and the press. .2. Knowledge about HIV/AIDS The term commonly used to refer to HIV/AIDS is Slim (n = 19). ther local terms used include Munywenje (Runyakitara), Tuo onyo (Acholi) and Mukenenya (Luganda). TMPs commonly identify IV/AIDS by a skin rash, diarrhea and other symptoms or by review- ng patients HIV laboratory test results performed at allopathic edicine centres and laboratories (n = 8) (Table 2). The majority f the TMPs reported that HIV is infectious and caused by unpro- ected sexual intercourse and the sharing sharp instruments with ersons infected with HIV. However, two TMPs reported that HIV is ransmitted by vectors (flies) from the wounds or fecal material of nfected persons while one thought the delivery of twins resulted n HIV/AIDS. ig. 2. Proportion of TMPs treating patients already receiving antiretroviral therapy. thoughts, bleeding, bone pains, divination, bitter taste in mouth, silky hair, hyper- tension, insomnia, Kaposi sarcoma, loss of relatives, paralysis, scalp lesions, and vaginal discharge. 3.3. Treatment practices and plant species used by TMPs for HIV/AIDS patients The TMPs mentioned 145 plant species in the study (Table 3). Of these, 103 plant species belonging to 47 families were identified. The families Asteraceae (14%), Mimosaceae (9%) and Euphorbiaceae (7%) contributed the majority of the species. Five species men- tioned by more than four or more TMPs in more than one district were prioritized as shown in Table 4. One other specie, Psorosper- mum febrifugum was mentioned by five TMPs, but from one district. The parts of the plant most frequently used were the leaves, stem bark and the root bark (Fig. 3). Specific HIV/AIDS-related conditions treated by TMPs using these medicinal plants are shown in Table 5. 3.4. Medicine preparation, administration and storage Commonly, decoctions of plant species were prepared using water or milk. The decoctions were mono-preparations (53.8%) or mixtures of multiple plant species (46.2%). A median of six (range, 2–20) plant species were used in the mixtures. Gulu and Kabale districts reported more mono-preparations compared to the other districts. Most medicinal preparations (80%) were orally administered in variable doses. The other routes of administration included smear- ing ointments, tying crushed herbs on wounds and bathing. About half of the TMPs (n = 13) advised their patients to take the medicinal preparations after food while others gave no advice with regard to meals. Rituals were rarely used to accompany medicinal prepara- tions for HIV/AIDS. Medicinal preparations were commonly prepared in small por- tions and prescribed for short durations (about 2–3 days). For longer storage, TMPs reported using preservation methods including mak- ing of powders, adding rock salt, Azadirachta indica extracts or honey, drying and burning to make ash. The medicines were com- monly packaged in plastic bottles (which were washed and re-used as necessary) and plastic bags. 46 M .Lam orde et al./JournalofEthnopharm acology 130 (2010) 43–53 Table 3 Medicinal plants used to manage HIV/AIDS in Kamuli, Sembabule, Kabale and Gulu districts. ID Scientific name Specimen number Family No. of TMPs No. of districts Local name (Dialect) Habitat Part useda Habit Kamuli (Soga) Sembabule (Ganda) Kabale (Kiga) Gulu (Acholi) 1 Aloe sp. KCB 29, 114, 70 Aloaceae 7 4 Kikaka, Kigagi Kigagi Rukaka Ataka-rach Homestead Garden, Pathside in Thicket L, RB Shrub 2 Erythrina abyssinica DC. KCB 55 Papilionaceae 5 3 Muyirikiti Kiko Lucoro Fallow SB Tree 3 Sarcocephalus latifolius (Sm) E.A. Bruce JRST 801, KCB 64 Rubiaceae 5 2 Mutamatama Munyu Pathside in Thicket RB, WR, TUBER Shrub/Tree 4 Psorospermum febrifugum Spach. JRST 797 Guttiferae 5 1 Kanziroziro SB, WR.RB Shrub 5 Mangifera indica L. * Anacardiaceae 4 3 Muyembe Muyembe Mango SB Tree 6 Warburgia salutaris (Bertol. f.) Chiov. JRST 752 Canellaceae 4 3 Abasi Abasi Mwiha Homestead compound SB, RB Tree 7 Albizia coriaria Oliv. KCB 11, JRST 805 Mimosaceae 3 2 Musita Omugavu Farmland SB Tree 8 Carissa edulis (Forssk.) Vahl KCB 10 Apocynaceae 3 2 Muyonza Muyonza Anthill thicket RB, SB Shrub 9 Clerodendrum myricoides (Hochst.) R.Br. ex Vatke KCB 36 Verbenaceae 3 2 Kikonge Okweru Banana plantation WR, RW Shrub 10 Eucalyptus sp. * Myrtaceae 3 2 Kalitusi Kalitusi L, SB Tree 11 Maesa lanceolata Forssk. KCB 32 Myrsinaceae 3 2 Omuwanga (omuwon- dowondo) Muhanga Banana plantation WR, L, RW Shrub 12 Maytenus senegalensis Exell JRST 799, KCB 1 Celastraceae 3 2 Muwaiswa (Ligwalimu) Nabuliko Road-side RB, RW, SB, L Shrub 13 Piliostigma thonningii (Schumach.) Milne-Redh JRST 765 Caesalpiniaceae 3 2 Kilaama Ugali Road-side RB, Tree 14 Plectranthus barbatus (Andrews) Forsk. KCB 22 Lamiaceae 3 2 Kibwankulata Kicuncu Banana plantation L Herb 15 Acalypha villicaulis Hochst. Euphorbiaceae 3 1 Mugandu WR Herb 16 Azadirachta indica A. Juss. JRST 758 Meliaceae 3 1 Neem Home garden WP Tree 17 Morella kandtiana Engl. * Myricaceae 3 1 Nkikimbo WR, SB, SW Shrub 18 Psidium guajava L. * Myrtaceae 3 1 Mupeera L, RB Tree 19 Steganotaenia araliacea Hochst. KCB 60 Apiaceae 3 1 Olwiru Thicket WR, RB Tree 20 Acacia seyal Del. KCB 12, JRST 804 Mimosaceae 2 2 kikongoito Akasana Road-side SB Tree 21 Acacia sieberiana DC. KCB 13 Mimosaceae 2 2 Mufunuwanduzi Omweramannyo Road-side SB Tree 22 Capparis tomentosa Lam. KCB 5, 52 Capparaceae 2 2 Kirobo omumyufu Okuma Banana plantation, Thicket WR, RB Shrub M .Lam orde et al./JournalofEthnopharm acology 130 (2010) 43–53 47 23 Citrus limon (L.) Burm. f. * Rutaceae 2 2 Eniimu Endiimu L, F Tree 24 Securidaca longipedunculata Fres. JRST 715 Polygalaceae 2 2 Mukondwa Mukondwe RB Tree 25 Spathodea campanulata Beauv. * Bignoniaceae 2 2 Kinalisa Mwatashare/Kifabakazi SB Tree 26 Acacia gerrardii Benth. KCB 25 Mimosaceae 2 1 Muwawa, Munyinya Thicket SB Tree 27 Bidens pilosa L. * Asteraceae 2 1 Nyabarashana L Herb 28 Capparis erythrocarpos Isert. KCB 26 Capparaceae 2 1 Kirobo omwelu Thicket WR, SB Shrub 29 Dracaena steudneri Engl. * Dracaenaceaea 2 1 Kajolyenjovu SB Shrub 30 Flueggea virosa Voigt KCB 4 Euphorbiaceae 2 1 Lukandwa Banana plantation SB, WR Shrub 31 Leonotis nepetifolia (L.) W.T. Aiton KCB 116 Lamiaceae 2 1 Kicumucumu Homestead compound L Shrub 32 Sesbania sesban (L.) Merr. KCB 15 Mimosaceae 2 1 Ntatembwa, Muwoganyanja Homestead garden L, SW Shrub 33 Venonia amygadalina Del. * Asteraceae 2 1 Mubirizi L, RW Shrub 34 Zehneria scabra (L.f.) Sond. KCB 113 Cucurbitaceae 2 1 Kabindizi Road-side L Herb 35 Acacia campylacantha Hochst. ex A. Rich. * Mimosaceae 1 1 Kibere SB Tree 36 Acacia mearnsii De Willd. * Mimosaceae 1 1 Burikoti SB Tree 7 Adenia cissampeloides Harms JRST 798 Passifloraceae 1 1 Lugelogelo RB, SB, L Shrub (woody climber) 38 Ageratum conyzoides L. KCB 115 Asteraceae 1 1 Bukabuka Homestead compound L Herb 39 Alstonia boonei De Wild. * Apocynaceae 1 1 Mubadangalabi SB Tree 40 Ananas sativa Schult. f. * Bromeliaceae 1 1 Enanansi F Herb 41 Aspilia kotschyi (Sch. Bip.) Oliv. KCB 106 Asteraceae 1 1 kiterankuba homestead garden L Herb 42 Bartsia sp. KCB 108 Scrophulariaceae 1 1 Kanisampato homestead garden L Herb 43 Bidens sp. (not pilosa) * Asteraceae 1 1 Mugosoola (Mukazi) WR Herb 44 Bridelia micrantha (Hochst.) Baill. KCB 9 Euphorbiaceae 1 1 Katazimiti fallow WR Shrub 45 Carica papaya L. * Caricaceae 1 1 Papali L Tree 46 Cassia nigricans Vahl. KCB 53 Caesalpiniaceae 1 1 Aban ceng pathside L Herb 47 Centella asiatica (L.) Urban KCB 97 Apiaceae 1 1 Kutukumwe Class 1 homestead garden L Herb 48 M .Lam orde et al./JournalofEthnopharm acology 130 (2010) 43–53 Table 3(Continued ) ID Scientific name Specimen number Family No. of TMPs No. of districts Local name (Dialect) Habitat Part useda Habit Kamuli (Soga) Sembabule (Ganda) Kabale (Kiga) Gulu (Acholi) 48 Chenopodium opulifolium Koch. & Ziz KCB 118 Chenopodiaceae 1 1 Mujuma L Herb 49 Coffea arabica L. * Rubiaceae 1 1 Mwani L Shrub 50 Combretum molle R. Br. Ex. G. Don. * Combretaceae 1 1 Ndagi SB Tree 51 Commelina benghalensis L. * Commelinaceae 1 1 Etiija WP Herb 52 C. bonariensis (L.) Cronquist KCB 96 Asteraceae 1 1 Wambuba homestead garden L Herb 53 Crassocephalum crepidioides (Benth.) S. Moore KCB 99 Asteraceae 1 1 Sununu homestead garden L Herb 54 Solanecio mannii (Hook. f) C. Jeffrey KCB 62 Asteraceae 1 1 Ta-lyech RW Shrub 55 Crotalaria glauca Willd. KCB 54 Papilionaceae 1 1 Abora garden RB Shrub 56 Echinops amplexicaulis Oliv. KCB 67 Asteraceae 1 1 Lutikwang elephant grass WR Herb 57 Entada abyssinica Steud. ex A. Rich. * Mimosaceae 1 1 Mwolola L, SB Tree 58 Erythrococca bongensis Pax. KCB 16 Euphorbiaceae 1 1 Musonji sonji homestead L Shrub 59 Euphorbia stapfii Berger KCB 2 Euphorbiaceae 1 1 Lubowa banana plantation SAP Shrub 60 Ficus mucuso Ficalho KCB 69 Moraceae 1 1 Olam fallow Tree 61 Ficus natalensis Hochst. * Moraceae 1 1 Kitoma L Tree 62 Grewia pubescens Beauv. JRST 806 Tiliaceae 1 1 Mukomakoma RB Shrub/Tree 63 Guizotia scabra (Vis) Chiov. KCB 58 Asteraceae 1 1 Unknown spear grass L, SB, FL, F Herb 64 Helichrysum nudifolium (L.) Less. var. oxyphyllum (DC.) Beentje KCB 65 Asteraceae 1 1 Abongo-nyar elehpant grass WR Herb 65 Hydrocotyle mannii Hook.f. KCB 98 Apiaceae 1 1 Kutukumwe Class 3 homestead garden WP Herb 66 Hygrophila auriculata Heine * Acanthaceae 1 1 Unknown L Herb 67 Hymenocardia acida Tul. * Euphorbiaceae 1 1 Mbaluka SB Shrub/Tree 68 Ipomoea hidebrandtii Vatke KCB 103 Convolvulaceae 1 1 Unknown homestead garden L Shrub 69 Ipomoea wightii Choisy KCB 18 Convolvulaceae 1 1 Lubowa homestead garden SAP Herb 0 Justicia betonica Linn. KCB 17 Acanthaceae 1 1 Nnalongo homestead garden L Herb 1 Justicia flava Vahl KCB 23 Acanthaceae 1 1 Kalaza pond bank L Herb M .Lam orde et al./JournalofEthnopharm acology 130 (2010) 43–53 49 72 Bryophylllum pinnatum (Lam.) Oken * Crassulaceae 1 1 Kisanasana L Herb 73 Kigelia africana (Lam.) Benth. * Bignoniaceae 1 1 Naizongwe RB Shrub/Tree 74 Lonchocarpus laxiflorus Guill. & Perr. JRST 803 Papilionaceae 1 1 Muzugangoma RB Tree 75 Markhamia lutea K. Schum. * Bignoniaceae 1 1 Musambya RB Tree 76 Mentha sp. (close to Mentha × piperata) KCB 24 Lamiaceae 1 1 Nabugira banana plantation L Herb 77 Microglossa pyrifolia (Lam.) O. Kuntze KCB 3 Asteraceae 1 1 Kafuga Nkande banana plantation WR Shrub 78 Moringa oleifera Lam. KCB 59 Moringaceae 1 1 Kakwalu garden L, F Tree 79 Musa paradisiaca L. * Musaceae 1 1 Gonja L Tree 80 Ocimum sauve Willd. * Lamiaceae 1 1 Mujaja L Shrub 81 Olea europaea L. * Oleaceae 1 1 Olive oil Tree 82 Parsea americana Mill. * Lauraceae 1 1 Vacado SEEDS Tree 83 Piptadeniastrum africanum (Hook.f.) Brenan * Mimosaceae 1 1 Mpewere SB Tree 84 Plumbago zeylanica L. KCB 35 Plumbaginaceae 1 1 Musajja abanda banana plantation WR Herb/Shrub 85 Polyscias fulva Harms. KCB 31 Araliaceae 1 1 Setaala banana plantation SB Tree 86 Prunus africana (Hook.f.) Kalkman. KCB 109 Rosaceae 1 1 Muba homestead RB, RW Tree 87 Pseudocedrela kotschyi (Schweinf.) Harms. KCB 68 Meliaceae 1 1 Oputu spear grassland Tree 88 Rauvolfia vomitoria Afzel * Apocynaceae 1 1 Kawule WR Shrub/Tree 89 Rhus natalensis Bernh. KCB 34 Anacardiaceae 1 1 Musese banana plantation SB Shrub 90 Rhus vulgaris Meikle KCB 7 Anacardiaceae 1 1 Tebuda (akak- wasokwanso) homestead garden L Shrub 91 Sapium ellipticum (Hochst.) Pax * Euphorbiaceae 1 1 Musaasa RB Shrub/Tree 92 Senna occidentalis (L.) Link. KCB 63 Caesalpiniaceae 1 1 Yat-Akwota (Tulala) stream bank L, WR Herb 93 Sida cuneifolia Gray * Malvaceae 1 1 Keyeeyo (Kaku- mukumu) L Shrub 94 Sigesbeckia orientalis L. KCB 33 Asteraceae 1 1 Seziwundu banana plantation L Herb 50 M .Lam orde et al./JournalofEthnopharm acology 130 (2010) 43–53 Table 3(Continued ) ID Scientific name Specimen number Family No. of TMPs No. of districts Local name (Dialect) Habitat Part useda Habit Kamuli (Soga) Sembabule (Ganda) Kabale (Kiga) Gulu (Acholi) 95 Solanum incanum L. * Solanaceae 1 1 Ntengotengo RB Shrub 96 Terminalia glaucescens Benth. * Combretaceae 1 1 Musasa RB Tree 97 Tetradenia urticifolia (Baker) Phillipson KCB 111 Apiaceae 1 1 Muravunga homestead garden L Shrub 98 Tropaeolum majus L. KCB 101 Tropaeolaceae 1 1 Unknown homestead garden L Herb 99 Vernonia adoensis Walp. * Asteraceae 1 1 Bijumero L Herb/Shrub 100 Vitex ferruginea Schumach. & Thonn. KCB 61 Verbenaceae 1 1 Ana-lyech stream bank RB Shrub/Tree 101 Zanthoxylum chalybeum Engl. * Rutaceae 1 1 Ntala ya irungu SB, WR, RB, SW, RW Shrub/Tree 102 Zanthoxylum gillettii (De Wild) Waterm. * Rutaceae 1 1 Muyenye SB Tree 103 Zanthoxylum leprieurii Guill. & Perr. * Rutaceae 1 1 Ntala ya irungu SB, WR, RB, SW, RW Tree *Commonly known plant. a Part used: L, leaves; RB, root bark; RW, root wood; SB, stem bark; WR, whole root. M. Lamorde et al. / Journal of Ethnopharmacology 130 (2010) 43–53 51 Table 4 The most frequently used herbal medicine plant species in the management of HIV/AIDS in Sembabule, Kamuli, Kabale and Gulu Districts of Uganda. Scientific name Family Voucher number Part useda Habitb No. of TMPs No. of districts Condition treated Aloe sp. Aloaceae [JT1] KCB 70 L, RB H 7 4 Fever, hepatitis Erythrina abyssinica DC Papilionaceae KCB 55 RW, SB, RB T 5 3 Cough Sarcocephalus latifolius (Sm) E.A. Bruce Rubiaceae JRST 801, KCB 64 RB, WR S 5 2 Diarrhea, sexually transmitted diseases Psorospermum febrifugum Spach. Guttiferae JRST 797 SB, RB, WR, S 5 1 Skin sores Mangifera indica L. Anacardiaceae JRST 785 SB, RB T 4 3 Diarrhea, cough SB ot. A c H i T 4 4 i d t t p t a t e p s t 4 i t a i p t t E Warburgia salutaris (Bertol.f.) Chiov. Canellaceae JRST 752, 780 a Part used: L, leaves; RB, root bark; RW, root wood; SB, stem bark; WR, whole ro b Habit: H, herb; T, tree; S, shrub. The TMPs assessed patient recovery by patient feedback. ccording to TMPs, 84% of their patients confirmed that their ondition improved following the use of medicinal preparations. owever, only 48% of the TMPs interviewed kept records indicat- ng whether or not their patients had recovered and none of the MPs used hospital laboratory tests to confirm recovery. . Discussion .1. Traditional knowledge of HIV/AIDS treatment HIV/AIDS is a relatively new disease—first described in Uganda n 1985 (Serwadda et al., 1985), and the practice of TM for HIV/AIDS oes not appear to be well developed. Knowledge about HIV/AIDS reatment was acquired mainly from colleagues and by experimen- ation and there has been no opportunity for refinement of this rocess over generations. In contrast to allopathic medicine—which makes the distinc- ion between the treatment of HIV infection and the treatment of ssociated opportunistic infections, TMPs appeared to focus on the reatment of AIDS symptoms and opportunistic infections. This is xpected because HIV infection may be asymptomatic for extended eriods and patients are likely to seek treatment only at the later tages of the disease when AIDS-related symptoms and opportunis- ic infections occur. .2. Treatment practices and medicinal plants Many plant species identified in this survey belonged to the fam- lies Asteraceae and Euphorbiaceae, which are well recognized for heir medicinal value in Uganda (Hamill et al., 2000). These plants re widely distributed in nature and chances of TMPs experiment- ng with them are high. The disagreement (or the very low ICF) in lants reported by different TMPs may be explained by the fact hat TMPs treated the AIDS conditions and opportunistic infec- ions rather than HIV infection per se. For example, Mangifera indica, rythrina abyssinica, Warburgia salutaris and Eucalyptus sp.—which Fig. 3. Distribution of plant pa T 4 3 Cough were identified in this survey, are medicinal plants recognized for treatment of coughs and some opportunistic infections in HIV/AIDS present with cough (Gautam et al., 2007; Hamill et al., 2000; Tabuti et al., 2010). Alternative plants were used for treating patients presenting with other symptoms. Other factors which could have contributed to the low consensus include imperfect transfer of TM knowledge, diversity in cultural backgrounds of TMPs, high plant diversity in the study areas and declining knowledge of medicinal plants (Thomas et al., 2009). The underlying cause of the clinical disorders seen in HIV/AIDS patients is the progressive loss of CD4 positive T-cell lympho- cytes in blood. These cells are important because they mediate immune responses and their depletion is associated with oppor- tunistic infections (Kaslow et al., 1987). In a pre-clinical study in Cuba, a stem bark extract of Mangifera indica was shown to pro- long survival of T-cell lymphocytes by opposing T-cell activation—a significant mechanism for T-cell depletion in HIV/AIDS patients (Hernandez et al., 2006). This finding suggests that Mangifera indica may have beneficial effects on the immune system of HIV/AIDS patients however, its role in actual patients remains to be estab- lished. Knowledge on the efficacy and safety of the other priority plants is derived mainly from a few in vitro studies. A sequiterpenoid isolated from the extract of Warburgia salutaris has demonstrated antibacterial activity (Rabe and van Staden, 2000) and this charac- teristic may be useful for bacterial infections in HIV/AIDS patients. In contrast, the extract of Erythrina abyssinica lacks antibacterial activity, it however may be useful in the treatment of malaria which is co-endemic with HIV/AIDS in Uganda (Wagate et al., 2010; Yenesew et al., 2003). The extract of Erythrina abyssinica should however be used with caution because it contains chalcones which are toxic to intestinal cells (Cui et al., 2008). This survey provides a first view of the wide range of medic- inal plants used for treatment of HIV/AIDS patients in the study districts. Conservation of these medicinal plants is critical. Medic- inal plants may yield novel compounds that may be of interest for drug development and some African medicinal plants have recently rts used for medicines. 52 M. Lamorde et al. / Journal of Ethnoph Table 5 AIDS conditions and opportunistic infections treated by TMPs. Conditions treated Frequency Category Diarrhea 16 Digestive system disorders Cough 8 Respiratory system disorders Sores 8 Skin/subcutaneous cellular tissue disorders Venereal diseases (non-specified) 5 Infections/infestations Colic 4 Digestive system disorders Carbuncles 4 Skin/subcutaneous cellular tissue disorders Rashes 4 Skin/subcutaneous cellular tissue disorders Appetite stimulant 3 Nutritional disorders Chest pain 3 Pain Dysuria 3 Genitourinary system disorders Bleeding 3 Blood system disorders Bloat 3 Digestive system disorders Helminth worm infestations 2 Digestive system disorders Malaria 2 Infections/infestations Other pain 2 Pain Sore throat 2 Respiratory system disorders Tuberculosis 2 Infections/infestations Candidiasis 2 Infections/infestations Oedema 2 Abnormalities Arthritis 1 Muscular–skeletal system disorders Malignant neoplasms 1 Neoplasms Breathlessness 1 Respiratory system disorders Epigastric pain 1 Pain Fever 1 Infections/infestations Hepatitis 1 Infections/infestations Lactation stimulant 1 Pregnancy/birth/puerperium disorders Nasal discharge 1 Respiratory system disorders Anaemia 1 Blood system disorders Vomiting 1 Digestive system b t o a i t p T A e e b p i T m fi disorders Malaise/fatigue 1 Ill-defined symptoms een shown to have anti-HIV activity (Klos et al., 2009). Although he medicinal plants identified in this survey appeared to target pportunistic infections, the presence or absence of specific activity gainst HIV can only be established after appropriate in vitro stud- es. Record keeping among TMPs should also be improved upon o facilitate the verification of claims of the effectiveness of their reparations. We observed that TMPs frequently advised their patients to take M with food. Food may reduce stomach irritations caused by TM. lso, food may increase absorption of TM (and potentially increase fficacy) or decrease absorption of TM (possibly to reduce side- ffects of potent agents). In addition, food may be given to increase lood glucose levels which may be reduced by some medicinal lants (Ojewole, 2004). While food intake may be desired, it is mportant to note that food may not always be available to patients. he chronic debilitating nature of HIV/AIDS is such that patients ay be unable to work for extended periods, leading to food insuf- ciency. In order to minimize risks arising from non-compliance armacology 130 (2010) 43–53 to food recommendations, clarification of the role of food during administration of the different TM preparations is needed. Unfortunately, TM packaging and storage methods do not comply with the proposed standards of the Ugandan regulatory authorities. Re-used plastic containers and plastic bags were used, raising concerns of possible contamination of the TM preparations. In order to improve on this practice, TMP sensitization and educa- tion on safe packaging and storage of TM preparations is needed. 4.3. Role of TM in Uganda’s HIV/AIDS response With increasing access to ARVs in Uganda, an important con- sideration is the potential for interactions between TM and ARVs when they are administered concurrently. Some classes of ARVs have great potential for unwanted herbal–drug interactions (Lee et al., 2006; Piscitelli et al., 2002) and some African medicinal plants have shown potential for unfavorable drug–herbal interac- tions with ARVs in laboratory studies (Brown et al., 2008; Mills et al., 2005). Although it is recommended that clinicians collect information on TMs used by patients on ARVs (MOH, Jun 2009), patients may not know the actual medicinal plants being used or may underreport the use of TM during their ARV clinic visits. Eth- nobotanical studies are therefore crucial to identify the panel of medicinal plants being used in order to facilitate pharmacologic studies to characterize the potential of these agents to affect the metabolism and activity of ARVs. Nevertheless, positive roles have been identified for TM in Uganda’s HIV/AIDS response. The Ugandan government highlights TM as a key resource for the expansion of prevention and treatment services for opportunistic infections (UAC, 2007). This is because TMPs cater to health needs of the general community and are well positioned to provide primary health care services relevant to HIV/AIDS. In order to prevent the spread of HIV/AIDS to the commu- nity, public health officials should engage TMPs in order to equip the TMPs with the skills for disseminating prevention messages to their patients. Also, improved referral systems between TMPs and ARV clinics can increase HIV/AIDS testing and treatment efforts. Furthermore, research collaborations between TMPs may promote research and development of new treatments from medicinal plant sources. In order to take advantage of these opportunities, TMPs must be reassured that their intellectual property rights will be pro- tected during collaborations with other stakeholders. An ongoing dialogue between the Ugandan government and TMP associations is therefore needed to share information on the safety of TM, poten- tial for interactions with ARVs and to delineate the role of TMPs in the HIV/AIDS response. 5. Conclusion Based on the findings of this survey, TM may have a role in Uganda’s public health approach to HIV/AIDS control. Many medic- inal plants identified in this survey that are used to manage the numerous ailments occurring in HIV/AIDS patients, need to have their value in the therapeutic management of HIV/AIDS-related opportunistic infections investigated. Acknowledgements We wish to thank the TMPs for providing information about their practice. We thank Mulindwa Daniel of Makerere University and Charles Odongo of Gulu University for their assistance with data collection. We thank members of staff of Makerere Herbarium for their assistance in specimen identification. We acknowledge logistic support from JCRC clinics in Kabale and Gulu, Sembabule Health Centre and Kamuli Health Centre. This survey was funded hnoph b R N A T c R A A B B C D G H H H K K K M. Lamorde et al. / Journal of Et y the Health Research Board of Ireland/Irish AID Global Health esearch Awards grant awarded to Dr. Concepta Merry to study eglected translational research to improve HIV outcomes in rural frica (GHRA07/09). The Uganda national Council for Science and echnology (UNCST) is acknowledged for granting permission to onduct this study. eferences djanohoun, J.E., Ahyi, M.R.A., Ake Assi, L., Alia, A.M., Amai, C.A., Gbile, Z.O., Johnson, C.L.A., Kakooko, Z.O., Lutakome, H.K., Morakinyo, O., Mubiru, N.K., Ogwal-Okeng, J.W., Sofowora, E.A., 1993. 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