Ethnobotanical survey of medicinal plants used as anthelmintic remedies in Gabon

Author’s Accepted Manuscript Ethnobotanical survey of medicinal plants used as anthelmintic remedies in Gabon Idensi Bajin ba Ndob, Line Edwige Mengome, Henri-Paul Bourobou Bourobou, Yvon Lossangoye Banfora, Francis Bivigou www.elsevier.com/locate/jep

PII: DOI: Reference:

S0378-8741(16)30385-3 http://dx.doi.org/10.1016/j.jep.2016.06.026 JEP10228

To appear in: Journal of Ethnopharmacology Received date: 24 February 2016 Revised date: 4 June 2016 Accepted date: 8 June 2016 Cite this article as: Idensi Bajin ba Ndob, Line Edwige Mengome, Henri-Paul Bourobou Bourobou, Yvon Lossangoye Banfora and Francis Bivigou, Ethnobotanical survey of medicinal plants used as anthelmintic remedies in G a b o n , Journal of Ethnopharmacology, http://dx.doi.org/10.1016/j.jep.2016.06.026 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting galley proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

Ethnobotanical survey of medicinal plants used as anthelmintic remedies in Gabon Idensi Bajin ba Ndob1, Line Edwige Mengome1*, Henri-Paul Bourobou Bourobou1, Yvon Lossangoye Banfora1, Francis Bivigou1,2 1

Institut de Pharmacopée et Médecines Traditionnelles (IPHAMETRA), Centre National de la

Recherche Scientifique et Technique (CENAREST), BP: 12 141 Libreville/ Gabon 2

Gabon-Oregon Center (GOC), BP:23906 Libreville/Gabon

[email protected] *

[email protected]

[email protected] [email protected] [email protected]

Abstract Ethnopharmacological relevance In this article, we report on an ethnobotanical survey realized at the Peyrie market in Libreville on Gabonese medicinal plants used to treat helminthiasis. While several alerts about cases of resistance to conventional anthelmintic treatments are causing to fear a public and animal health issue, the search for new sources of active compounds becomes an urgent issue. In Gabon like in many developing countries, people regularly turn to traditional medicine in case of physical ailments and/or spiritual healing therapies. Materials and Methods To determine which medicinal plants are traditionally used by the populations of Libreville to fight against nematodes, medicinal plant traders were interviewed with standardized questionnaires. The surveys were conducted in the main market of Libreville. Ethnobotanical data such as frequency and percentage of families, species, administrations pathways, modes of preparations and parts of plants used were analyzed and summarized. Results Thirty-four (34) traders were interviewed belonging to five (5) different ethnic groups. Twenty-four 24 plants used to treat intestinal, cutaneous and ocular helminthiasis were listed. The healers mainly turned towards to ligneous species. The parts of the plant used are mostly leaves and trunk bark. Most of the traditional remedies are prepared directly in water and four (4) principal routes were used for administration namely, oral, rectal, ocular and dermal. Conclusion

This study allowed us to list anthelmintic species which will be subjected to a series of chemical and pharmacological assays. Keywords: Ethnobotanical survey - medicinal plants - anthelmintic – Gabon

1. Introduction Neglected tropical diseases (NTDs) occur mainly among the rural population in SubSaharan Africa, Asia and the Americas (Feasey et al., 2010; Lustigman et al., 2012). These diseases are considered as endemic as more than 1 billion people are affected in 149 countries worldwide (WHO, 2015). The WHO in its reports has listed 17 pathologies classified as NTDs (WHO, 2015). Helminthiases are among the most common in Africa where 85% of the NTDs results from helminths infections (Hotez & Kamath 2009). Helminths group two types of worms: nemathelmints (roundworms) and platyhelmints (flatworms). First ones are subdivided in intestinal worms (that causes soil-transmitted helminthiasis STHs) and filarial worms (that causes lymphatic filariasis and onchocerciasis). The second ones are subdivided in flukes, schistosomiases and tapeworms. According to the World Health Organization, in 2015 there were approximately 1.5 billon persons suffering from soil-transmitted helminthiasis (STHs) (WHO, 2015). STHs infections cause chronic debilitating diseases affecting human (ankylostomoses, blindness, schistosomes, filarial worms, malnourishment, anemia, retard growth, mental incapacity) and animals (canine ankylostomoses, helminthes of the cattle) (Hotez & Kamath 2009; Koné et al., 2012). Intestinal helminthiases are most commonly caused by roundworms (Ascaris lumbricoides), whipworms (Trichuris trichiura) and hookworms (Ancylostoma duodenale and Nector americanus) (WHO, 2015; Agyare et al., 2014). Although the infection is not lethal, helminthiases infections can induce symptoms such as abdominal pain, diarrhea, anemia and cognitive delays in children because of blood loss (WHO, 2015; Agyare et al., 2014). The main part of the current treatments base on six (6) essential drugs: albendazole, oxamniquine, praziquantel, ivermectin, diethylcarbamazine and mebendazole. The strategy adopted by the WHO to reduce helminthiases in developing countries consists of Mass Drug Administration (MDA) of these anthelmintic drugs (Hotez, 2008; WHO, 2015). The approach is to administer medicine to the largest number low income people thanks to public-private partnerships. However in spite of the success of the MDA, the disease is not still eradicated and the risk of appearance of resistance could be an important obstacle for this program. Indeed several cases of resistance were indicated for human and cattles (Geerts S. and Gryseels B., 2001; Wolstenholme et al., 2004; Vercruysse et al., 2011), causing to fear a public and animal health issue. Medicinal plants are a common medication for human diseases all over the world and approximately 80% of the people in Africa depend entirely on medicinal plants for their primary health care needs (Kasilo et al., 2010). In Gabon like in many developing countries (Van Andel & Carvalheiro, 2013), people regularly turns to traditional medicine for several reasons (economics, familiarity with plants, maintain of traditions) in case of physical

ailments and/or spiritual healing therapies. This article report ethnobotanical survey realized at the Peyrie market in Libreville about the Gabonese medicinal plants used to treat helminthiasis.

2. Methods: 2.1. Study Area Located in Atlantic Central Africa, Gabon is a country of Guinea Gulf horseback on the Equator, between 2° and 3° north latitude and south of 14° and 9°30'' of longitude. Its area is 267,667 km2. It extends over 800 km of coastline and has a tropical climate balance, with an annual temperature rise and high rainfall reaching over 2 meters. Its forest is mentioned as the most rich in all Africa (Breteler, 1990) and covers 235 000 km2 or 82% of the land area. The population were estimated 1 534 300 inhabitants in 2010 (WHO, 2010). Gabon is divided nine provinces that are Estuaire (ES), Haut-Ogooué (HO), Moyen-Ogooué (MO), Ngounié (NG), Nyanga (NY), Ogooué-Ivindo (OI), Ogooué-Lolo (OL), Ogooué-Maritime (OM) and Woleu-Ntem (WN). Our study was conducted in the town of Libreville, administrative center of the Estuaire district, located in the north-west area. Libreville (Figure 1) is located at 0°23’24’’North and 9°27’15’’ East. Its population was estimated 850 000 inhabitants in 2014 (populationsdumonde.com). It is the most populated city in the country. All the ethnic groups of the country are represented and mixed up. We conducted our study at the “Peyrie” market of which is the principal medicinal plant market in town.

Figure 1: Map and localization of the study area. (Source: http: www.operationworld.org and www.wikimedia.org)

2.2. Market The Peyrie market is a continuation of the principal market of Libreville named «marché Mont-Bouët». The naming “marché de la Peyrie” was attributed because of the closeness with

an old zoological garden of Libreville known as «Les jardins de la Peyrie1» (The park was built in 1969 and demolished in 2008, only the name continued so far). This part of the market is dedicated to Traditional Medicine. A wide choice of healing plants, remedies and traditional liturgical objects are found there. It is a place where people can talk to and consult Traditional Medicine practitioners. Certain sellers met in the market were also practitioners of traditional medicine.

2.3. Ethnobotanical survey The present study focused on medicinal plants used to treat helminthiasis. The survey was carried out from December 2014 to August 2015. As starting point was a health problem, the investigations were based on direct questions concerning plants used traditionally by the populations to fight against nematodes infections. In Gabon, the parasitic diseases caused by helminths are grouped under the term of "worms" and used treatments are indicated "against worms". Conversations with the informants were held to build the confidence of the interviewee and in respect to local tradition. A questionnaire was filled by the investigators after obtaining oral consent from the person. The questionnaire included three parts. First part concerning "civility" in order to obtain the address and coordinates of the interviewee with his agreement in the aim of constituting a database for IPHAMETRA. The second part concerned all informations about the use of plants: vernacular name, part of the plant used, method of preparation and way of administration. The third part was reserved for the investigator to note observations and the difficulties met during the interview or during the survey. We bought a sample of every quoted plant that was available at the time of the survey. The plants were identified by botanists of the National Herbarium in Gabon (HNG). Bibliographical support “Checklist of Gabonese vascular plants, (2006)” and web sources as “theplantlist” were used to complete plants identification. The scientific names and corresponding voucher number were attributed. Bibliographical research was also made on the plants.

2.4. Data analysis Descriptive statistical methods were applied to analyze and summarize the ethnobotanical data such as frequency and percentage of families, species, administrations pathways, modes of preparations and parts of plants used.

3. Results: 3.1. Knowledge of informants and medicinal plants We interviewed 34 traders (7 men and 27 women) belonging to 5 different ethnic groups. The most represented group was Punu (41,2%) followed by Fang (29,4%), Myènè (14,7%), 1

The gardens of Peyrie

Nzébi (8,8%) and Sango (5,9%). These investigations allowed us to list 24 plants used to treat intestinal, cutaneous and ocular helminthiasis. The mentioned species belong to 18 different families and 23 genera. All species belongs to the division of magnoliopsida, subdivision of angiosperms. The majority is part of the dicotyledonous group except one specie belonging the monocotyledonous group (Cyperus articulatus). Among the 18 families the most represented are Leguminosae (3 species of Caesalpinoideae and 1 specie of Mimosoideae or 12,5% and 4,1% respectively), Asteraceae (3 species or 12,5%), Annonaceae (2 species or 8,3%) and Euphorbiaceae (2 species or 8,3%). Table 1 give indications about the family, scientific names and the corresponding voucher number at the HNG, vernacular or common names as given by the traders, the used parts, methods of preparation, way of administration and the number of case during the investigation. A Use Index (UI%) was calculated to determine the importance of the use of each medicinal plant. The Use Index formula is UI = (na/NA) x 100, where na is the number of interviewees who cite the species as useful and NA is the totally number of people interviewed [Lance et al., 1994].

Table 1: Medicinal plants used for helmithiasis in Peyrie market of Libreville in Gabon Family

Vernacular name

Repartitio n in Gabon

Used part

Method of preparation

Duguetia barteri (Benth.) Chatrou (11431)

Mululungumb e (Punu) Ebam (Fang)

OI, WN

Bark

Annickia chloranta (Oliv.) Setten & Maas (1382)

Muambebengu e (Punu)

ES, MO, NG, NY, OI, OL, OM, WN

Bark

Apocynaceae

Picralima nitida (Stapf) T. Durand & H. Durand (1383)

Dugundu (Punu)

ES, MO, NG, NY, OI, OL, OM, WN

Bark

Asteraceae

Ageratum conyzoides (L.) L. (1322) Bidens pilosa L. (6409) Vernonia amygdalina Delile (2066)

Mambi ma taba (Punu) Mekwa me kong (Fang) Matsi-mamangala (Punu) Nzong-ayol (Fang) Ndundulyè (Myènè)

ES

Leave s

Decoction or maceration. Have a drink 3 times a day and make a rectal injection every 3 days. Decoction or maceration. Drink one glass in the morning and evening. Decoction or maceration. Drink one glass (or half for children) morning, noon and evening. Make an enema by day. Decoction drink a glass twice a day

ES, HO, OI

Leave s

ES, NY, OI

Leave s

Annonaceae

Scientific name (Voucher number)

Decoction drink a glass twice a day Decoction drink a glass twice a day and wash himself with the preparation

Routes of admini s -tration oral and rectal route

Numbe r of case

Use Inde x (%)

29

85,3

oral route

28

82,3

oral route and rectal route

10

29,4

oral route

5

14,7

oral route

2

5,9

oral and dermal route

7

20,6

Enema Caricaceae

Cucurbitaceae

Carica papaya L. (136) Momordica charantia Linn. (694)

Dilolu (Punu) Alola (Fang)

ES, OI, WN

Latex

Aboumboulou (Myènè)

ES, NG, NY, OI, OM

Stem Leave s

Cyperaceae

Cyperus articulatus L. (1125)

Andac (fang)

NY, OI, OM

Roots

Euphorbiaceae

Alchornea cordifolia (Schumach. & Thonn.) Müll. Arg. (1000) Plagiostyles africana (Müll. Arg.) Prain (223)

Nkabi (Fang) Mudèpa, Mumbundzini (Punu)

ES, HO, NG, NY, OI, OM, WN

Leave s

Mususungue (Punu)

ES,HO, MO, NG, NY, OI, OL, WN

Bark

Ocimum gratissimum L. (1282)

Madumadumb e (Nzébi)

Senna alata L. Roxb. (568)

Itsamuna (Punu)

ES, MO, OI, OL, OM

Leave s

Senna occidentalis (L.) Link 3237B

Mukemumfumbi (Punu)

ES, MO, OI, WN

Leave s

Tamarindus indica L. (721)

Tamarin , Dalè (Pygmy)

ES

Leave s

Cylicodiscus gabunensis Harms (2897)

Muduma (Punu, Sango)

ES, NG, NY, OI, OL, OM, WN

Stem

Leguminosae

Caesalpinoideae

Lamiaceae

Mimosoidea e

Leave s

a few drops diluted in water Decoction (for adults) Maceration (fo r childs) Drink in the morning, noon and evening and make a rectal injection a day. Wash with the preparation. Maceration one night. Drink on an empty stomach Eaten raw Decoction drink a glass twice a day

Decoction or maceration. Have a drink twice a day and make a rectal injection 2 days in week. Decoction with lemons. Drink a glass morning and evening. Decoction with fruits of Capsicum frutescens. Decoction. Drink and wash himself with the preparation. Decoction drink a glass twice a day wash with the preparation Decoction drink a glass in morning and wash himself with the preparation. Decoction or maceration to Drink 1 glass in the morning

oral route

2

5,9

6

17,6

oral route

3

8,8

oral route

3

8,8

oral and rectal route

30

88,2

oral route

5

14,7

oral route and dermal

2

5,9

oral route and dermal

2

5,9

oral and dermal route

2

5,9

oral and rectal route

32

94,1

oral and rectal route dermal

rectal route

Carapa klaineana Pierre (3249) Scoparia dulcis L. (5571) Drypetes gosweilleri S. Moore (3407) Brenania brieyi (De Wild.) E.M.A. Petit (8370) Zanthoxylum gilletii (De Wild.) P.G. Waterman (2219)

Égang (Fang)

ES

Bark

Duradji du bakongu (Punu) Muyungu (Nzebi)

ES

Leave s

ES, OI, WN

Bark

Oyèm (Fang)

NG, OI, OL, WN

Ndungu (Punu)

Simaroubaceae

Quassia africana (Baill) Baill. (1851)

Issintsi ighal (Punu)

Solanaceae

Solanum americanum Mill. (2282) Cissus quadrangulari s L. (125)

Iloki (Myènè) Tsari (Punu)

Meliaceae

Plantaginaceae

Putranjivaceae

Rubiaceae

Rutaceae

Vitaceae

Dyabi (Punu) Fo-ndzic (Fang)

and evening and to make a rectal injection every 2 days Decoction , drink a glass twice a day

oral route

2

5,9

Infusion. Drink morning and evening Maceration or decoction of the fresh bark.

oral route

5

14,7

oral route

1

2,9

Leave s

Decoction

rectal route

2

5,9

ES, MO, NY, OI, OL, OM

Bark

oral, rectal and ocular route

30

88,2

ES, HO, MO, NG, NY, OI, OL, OM, WN ES, OI, OL, OM, WN

Racin e

Decoction or maceration. Drink a glass twice a day and make a rectal injection every 2 days. Eye instillations of the soaked. Maceration. Drink one glass three times a day.

oral route

5

14,7

Fruits

Infusion or eaten as vegetables

oral route

4

11,8

ES

Stem

The sap is extracted from the stems

ocular route

3

8,8

The healers more resort to ligneous species to handle the intestinal worms since we distinguish at all: fifteen (15 or 62,5%) treelike sort’s species, seven (7 or 29,2%) herbaceous and two (2 or 8,3%) liana species (figure 2). The bought samples were submitted to botanists from the National Herbarium of Gabon for identification.

Repartition of plants species used as anthelmintics

70.00%

62.50%

Percentage of species

60.00% 50.00% 40.00%

29.20%

30.00% 20.00%

8.30%

10.00% 0.00% Trees and Herbaceous shrubs

Lianas

Type of plants

Figure 2: Type of plants species used for treatment of helmints in market from the peyrie. Among the medicinal plants used to treat worms, 15 are trees and shrubs (62,5%), 7 are herbaceous (29,2%) and 2 are lianas (8,30%).

3.2 Parts of plants used The parts of the plant used are (40%) leaves, (32%) trunk bark, stems, roots and fruits in equal parts (8%), and (4%) latex (figure 3). Leaves and leafed stems of the herbaceous species can be directly consumed as vegetables or prepared in infusion or decoction. In the case of liana species (Momordica charantia) the entire plant is consummate. However, only leaves for Momordica charantia can be used to treat children. The sap of the stem can also be collected for direct use (Cissus quadrangularis). For the tree like species, the bark is the most used part. It is mainly used under crushed or raw shape. In certain cases, the bark is made an incision to collect the latex (Carica papaya). The roots are used reduced to small species (Quassia africana) or crushed (Cyperus articulatus). They can also be eaten raw (Cyperus articulatus). Last, the fruits of Solanum americanum are consumed as vegetables.

Part of plants used 8%

4%

Bark

8%

Leaf 32%

8%

Stem roots

40%

Fruits Latex

Figure 3: Parts of the plant used for preparation of the remedies. As used organs, leaves were ten times quoted (or in 40%), bark eight times (or in 32%), stems, roots and fruits twice each (or in 8%), and latex one time (or in 4%).

3.3 Methods of preparation and administration Most of the traditional remedies are prepared directly in water. The major methods of preparation were at 55,2% decoctions, 31% macerations and 6,9% infusions (figure 4). But the drugs can also be cooked and eaten as Solanum americanum or directly eaten without any preparation as Cyperus articulatus. For administration, four (4) principal routes were used (figure 5): oral, rectal, ocular and dermal. Oral and rectal route are indicated for intestinal helminthiasis. The oral route is the most frequent method (61,6%), the flavor of the beverage can be bitter or very bitter. The second is the rectal route (19,4%) where administration is made by enema with an enema syringe. The rectal injections are sometimes associated to the oral route (Picralima nitida, Plagiostyles africana, etc.). The preparation used for the enema is identical to that administered by oral route and that association allows maximizing the eviction of worms. The dermal (13,8%) is indicated in the cases of lymphatic filariasis. The ocular route (5,5%) is used for ocular filariasis.

Method of preparation 6,9%

6,9% Decoction Maceration

31%

55,2%

Infusion Other

Figure 4: Various methods of preparation of the anthelmintic remedies. Several methods of preparation were indicated. They are decoctions in sixteen cases (corresponding to a 55,2% frequency), macerations in nine cases (31% frequency), infusions in two cases (6,9%), and others in two cases (6,9%). For the other methods the drugs can be cooked and eaten or directly eaten without any preparation.

Routes of administration 5,5% 13,8% Oral route Rectal route 19,4%

61,1%

Dermal Ocular route

Figure 5: Different routes of administration of the remedies. The routes of administration are oral route in twenty two cases (about 61,1%), rectal route in seven cases (about 19,4%), dermal in five cases ( about 13,8%) and ocular in two cases (about 5,5%).

3.4. Bibliographical information Bibliographical research on the plants collected led us to list other traditional uses, anthelmintic, antiparasitic and other screening. The results of biological activities are reported in Table 2.

Table 2: Literature review citing other traditional uses and previous anthelmintic or parasitic screening Family

Annonaceae

Scientific name Anthelmintic (Voucher screening number) Duguetia barteri (Benth.) Chatrou (11431) Annickia chloranta (Oliv.) Setten & Maas (1382)

Apocynaceae

Picralima nitida (Stapf) T. Durand & H. Durand (1383)

Asteraceae

Ageratum conyzoides (L.) L. (1322)

Parasitic and other screening

- Kamboj & Saluja 2008 (review, T. solium , P. posthuma, Meloidogyne

- Antiplasmodial : Ngbolua et al., 2013 - Antimycobacterial and Cytotoxicity (human lung fibroblast MRC5 cells) : Doneng Donfack et al., 2014 )

- Antimalarial : Iwu & Klayman, 1992 ;François et al., 1996 ; Okokon et al., 2007 ; Dibua et al., 2013 - Tripanocidal : Wosu & Ibe, 1989 - Antileishmanial : Iwu et al., 1992 - Antimicrobial : Obasi et al., 2012 - Hypoglycaemic activity Aguwa et al., 2001 ; Nguessan et al., 2013 - Antidiarrhoeal : Kouitcheu et al., 2006 - Cytotoxic : Osayemwenre et al., 2011 - Toxicity : Mabeku et al., 2008 ; Fakeye et al., 2004 ; Ilodigwe et al., 2012 - Antiplasmodial : Ukwe Chinwe et al., 2010; Arya et al., 2011 ; Owuor et al., 2012 ;

Chemical composition (major components)

- alkaloids : palmatine, jatrorrhizine, columbamine and pseudocolumbamine (Bourdat-Deschamps et al., 2004) - oxygenated sesquiterpenoids : 7,8dihydro-8hydroxypalmatine (Wafo et al., 1999) - alkaloids : akuammine, pseudoakuammine, akuammigine, picraline, (Henry & Sharp 1972 ; Okunji et al., 2005 ; Erharuyi et al., 2014) - Polyphenols : coumestan glycosides (Kouam et al., 2011)

incognita) - Wabo Poné et al., 2011 (Heligmosomoides bakeri) - Parveen et al., 2014 (Rhipicephalus microplus) - Mbogning Tayo et al., 2014 (Haemonchus contortus)

- Antiulcerogenic Aulprakash et al., 2012 - Toxicity Diallo et al., 2010 - Antibacterial Gbadamosi, 2012

Vernonia amygdalina Delile (2066)

- Agyare et al., 2014 (Caenorhabditis elegans) -Siamba et al., 2007 (Ascaridia galli) - Danquah et al., 2012 (Lumbricus terretris). - Iqbal et al., 2006 (mixed nemathodes) - Oluwafemi, 2010 (Haemoncus contortus)

- Antiplasmodial : Ngbolua et al., 2013; Iwalokun , 2008 ; Njan et al., 2008 -Antioxydative and chemopreventive : Farombi & Owoeye, 2011 - Toxicity : Njan et al., 2008

Caricaceae

Carica papaya L. (136)

- Kermanshai et al., 2001: (benzyisothiocyanate) - Stepek et al, 2005 (Heligmosomoides polygyrus) - Krishna et al., 2008

- Antimalarial, antimicrobial, antifungal, : Krishna et al., 2008

Cucurbitaceae

Momordica charantia Linn. (694)

- Lal et al., 1976 (Ascaridia galli)

- many pharmacological studies : Grover & Yadav 2004 - Antimicrobial : Bracca et al., 2008; Mahmood et al., 2011

Bidens pilosa L. (6409)

- Sujon et al., 2008 - Shahadat et al., 2008

- Antimalarial : AndradeNeto et al., 2004 ; Brandao et al., 1997 - Antimicrobial Geissberger et al., 1991 - Leishmanicidal : Garcia et al., 2008

- acetylene and phenolic compounds : 1-phenyl-1,3-dyin-5-en-7ol-acetate (Deba et al., 2008 ; Brandão et al., 1997; Lima Silva et al., 2011) ; quercetin-3,3dimethoxy-7-0rhamnoglucopyranose (Brandão et al., 1998 ; Oliveira et al., 2004 ; Lima Silva et al., 2011) - terpenoids : βcaryophyllene, scadinene, α-pinene, limonene, βtrans-ocimene, αcaryophyllene, caryophyllene oxide (Lima Silva et al., 2011) - sterols, hydrocarbons (Lima Silva et al., 2011) . -sesquiterpene lactones , vernolide, vernodalol, epivernodalol, vernodalin (Erasto et al., 2006 ; Yeap et al., 2010 ; Farombi et al., 2011 ) - flavonoids : luteolin, luteoli-7-O-βglucuronoside, luteolin-7O-β-glucoside (Igile et al., 1994) - steroid glycosides and vernonioside A, B, A1, A2, A3, B2, B3, A4, D and E (Igile et al., 1995 ; Farombi et al., 2011) - carbohydrates, lipids, minerals, proteolytic enzymes : papaine, chemopapaine (Krishna et al., 2008) - alkaloids : carpaine, pseudocarpaine, dehydrocarpaine (Krishna et al., 2008) - terpenoid : linalol (Flat & Forrey, 1977) ; benzylisothiocyanate (Tang, 1971 ; Flat & Forrey, 1977 ; Krishna et al., 2008) -terpenoids : trans-nerolidol, apiole, cis-dihydrocarveol and germacrene D (Braca et al., 2008). cucurbitanetype triterpenoids

- Antimalarial : Amorim et al., 1991

Cyperaceae

Cyperus articulatus L. (1125)

Euphorbiaceae

Alchornea cordifolia (Schumach. & Thonn.) Müll. Arg. (1000)

Caesalpinoideae

Leguminosae

Lamiaceae

- Antiamoebic : Kabbashi et al., 2015a - Antimalarial : Rukunga et al., 2008 ; Muthaura et al., 2011 - Antimicrobial : Kabbashi et al., 2015b ; Oladosu et al., 2011 - Anti-Candida : Duarte et al., 2005

- Opekon et al., 2004 (Rabditis pseudoelongata)

- Antimalarial, tripanocidal, leishmanicidal : Okpekon et al., 2004 - antiprotozoal (antiplasmodial and tripanocidal) : Mesia et al., 2008 -Antibacterial : Magassouba et al., 2007

Plagiostyles africana (Müll. Arg.) Prain (223) Ocimum gratissimum L. (1282)

- Pessoa et al., 2002 - Bihari et al., 2010 (Pheretima posthuma)

- Antiparasitic : Barreira Cavalcanti et al., 2004 - Antileishmanial : Ueda Nakamura et al., 2006 - Antifungal : Faria et al., 2006 ; Koba et al., 2009

Senna alata L. Roxb. (568)

- Agyare et al., 2014 (Caenorhabditis elegans)

(Nakamura et al., 2006 ; Hsu, 2011) - alkaloid : momordicin (Grover & Yadav, 2004 ; Singh et al, 2011). -cucurbitane glycosides : momordicosides Q, R, S, and T, and karaviloside XI. (Tan, 2008) - monoterpenes : cyperene, rotundene, cypera-2,4-diene, patchoulenone, cyperotundone, αcyperone, cyperene, (Azzaz et al, 2014, Zoghbi, et al, 2006, Nyasse et al., 1988). - sesquiterpenes : articulone, copaene, αcorymbolol, βcorymbolone, mandassidione and mustakone, ledol and caryophyllene oxide - fatty acids : 3-ethylhexane, 2nonanone , mandassidione, himachalene γ-dihydrone , cis-calamine. - anthocyanidines : 5-methyl-4’-propenoxy anthocyanidines 7-O-β-Ddiglucopyranoside ; 5’methyl 4’, 3, 5, 7 tetrahydroxy anthocyanidine (Mavar-Manga et al., 2008 ; Okwu & Ukanwa, 2010), - steroids : sitosterol, daucosterol (MavarManga et al., 2008)

- essential oil : terpenoids : monoterpenes : β-pinene, α-pinene and sabinene ; sesquiterpenes α- and βselinene, and trans-βcaryophyllene ; phenylpropanoids: eugenol, 1,8-cineole, selinene. (Sahouo et al., 2003 ; Sartoratto et al., 2004, Benitez et al., 2009) - anthraquinones : Rhein, chrysophanic acid, aloe-emodin chrysophanol, physcion (Hauptmann & LacerdaNazáriô, 1950 ; Dave & Ledwani, 2012)

Senna occidentalis (L.) Link (3237B)

Tamarindus indica L. (721)

Mimosoideae

Meliaceae

Plantaginaceae

Putranjivaceae

Cylicodiscus gabunensis Harms (2897)

Carapa klaineana Pierre (3249) Scoparia dulcis L. (5571)

Drypetes gossweileri S. Moore (3407)

Antiplasmodial Ngbolua et al., 2013

- Mute et al., 2009 (Pheretima posthuma) - Das et al., 2011 (Pheretima posthuma, Tubifex tubifex) - Badhoriya et al., 2011 (Eisonia fatida, Taenia solium)

:

- Antiplasmodial : Koudouvo et al., 2011 ; El Tahir et al., 1999 - Antileishmanial : El Tahir et al., 1998 - Antibacterial : Khotari & Seshadri, 2010

- antimicrobial : Kouitcheu et al., 2007 ; - antidiarrhoeal : Kouitcheu et al., 2006 - antiplasmodial : Okokon et al., 2006

- Trypanocidal, antiplasmodial, anti Chagas disease and leishmanicidal : Calderon et al., 2010

- Antifungal : Ngouana et al., 2011; Tabopda et al., 2015 - Antiprotozoal, cytotoxicity : Mesia et al., 2008 ; Muganza et al., 2012

-anthraquinones : achrosin, aloe-emodin, chrysophanol, emodin, 1,8 dihydroxy anthraquinone, physicon, rhein, bianthraquinones (Chukwujekwu et al., 2006 ; Yadav et al., 2010; Dave & Ledwani, 2012) -sterols: campesterol, sitosterols; -phenolics: kaempferol, quercetin, -fatty acids : linoleic acid, linolenic acid, oleic acid, physcion ; carbohydrates : rhamnosides (Yadav et al., 2010) - fatty acids : palmitic acid, oleic acid, linoleic acid, and eicosanoic acid. - polyphenolics : apigenin, catechin, procyanidin B2, with taxifolin, eriodictyol and naringenin (Khanzada et al, 2008 ; Meher et al., 2014) - terpenoids and sterols : limonene, benzyl benzoate, eicosanoic acid, β-sitosterol, (+)-pinitol, campesterol, β-sitosterol. (Khanzada et al, 2008 ; Meher et al., 2014) - triterpene saponnins: cylicodiscoside, gabunoside (Pambou et al., 1990-1991; Tene et al., 2011) - coumestan glycosides : coumestoside C and coumestoside D (Nchancho et al., 2009)

- diterpenoids : Scopadulin (Hayashi et al., 1990), scoparinol; dulcinol (Ahmed & Jakupovic, 1990), copadulcic acid (Phan et al, 2005), scoparic acid (Latha et al., 2009) - lignans : nirtetralin and niranthin (Phan et al, 2005) - essential oil : benzyl isothiocyanate (56–94%), benzyl cyanide and benzaldehyde (Mvé-Mba et al., 2012), - alkaloids : gossweilerine, (Tabopda

- Antibacterial : Tabopda et al., 2015

Brenania brieyi (De Wild.) E.M.A. Petit (8370) Zanthoxylum gilletii (De Wild.) P.G. Waterman (2219)

- Estrogenic effect : Magne Ndé et al., 2007 - Antibacterial : Iwu, 2002

Simaroubaceae

Quassia africana (Baill) Baill. (1851)

- Antiviral : Apers et al., 2002 - Antiplasmodial : Mbatchi et al., 2006 - Antiprotozoal and Cytotoxicity : Muganza et al., 2012

Solanaceae

Solanum americanum Mill. (2282) Cissus quadrangularis L. (125)

- Antileishmanial and antifungal : Braga et al., 2007 - Anti-inflammatory and antimicrobial : Lin et al., 1999; Luseba et al., 2007 - Managemant of weight loss : Oben et al., 2008

Rubiaceae

Rutaceae

Vitaceae

- Antitrypanosomal : Atindehou et al., 2004 -Antiplasmodial : Zirihi et al., 2005, 2010 - Cytotoxicity : Zirihi et al., 2005 - Toxicity : Ngogang et al., 2008 - Antimicrobial : Dzoyem et al., 2014

et al., 2015). - triterpenoids and steroids : gossweilone, friedelin, 3,7-dioxofriedelan, and 3oxo-16βhydroxypachysonol (Ngouela et al., 2003 ; Tabopda et al., 2015).

- mono and sesquiterpenes : terpinene, myrcene, sabineneocimene, camphene, caryophyllene, cariophylene oxide, cadinene (Japheth et al, 2014) - alkaloids : benzophenanthridine, benzylisoquinoline, aporphine, protoberberine and berberine and quinolines (Krane et al. 1984; Waterman & Grundon, 1983; Cordell, 1981 ; Patiño, 2012) - quassinoids : quassin and simalikalactone D (Lumonadio & Vanhaelin, 1986; Apers et al., 2002; Sama et al., 2014) - alkaloids : 4-methylthiocanthin-6-one and 5-methoxycantin-6one (Ayafor, 1993), canthin-6-one, 4,5dimethoxycanthin-6-one and beta-carboline-1propionic acid (Lumonadio & Vanhaelin, 1986) - Steroidal glycosides (Ando et al., 1999), Triterpenoids : tetracyclic triterpenoid : 7oxoonocer-8-ene-3β,21αdiol, (Gupta & Verma 1990) sterols : δ- amyrone, δamyrin, β-sitosterol, Taraxeryl acetate, friedelan-3-one, taraxerol (Bhutani et al, 1984; Gupta & Verma, 1991; Thakur et al., 2009) phenolics : flavonoids : kaempferol, quercetin and resveratrol (Thakur et al, 2009) stilbene derivatives :

quadrangularins A, B, and C, resveratrol, piceatannol, pallidol, and parthenocissine A (Saburi A. Adesanya 1999,) stilbene glucoside : transresveratrol-3-O-glucoside (Thakur et al., 2009)

4.

Discussion:

In this study, 24 medicinal plants used to treat helminthiases were surveyed in the Peyrie market in Libreville district. The most used species, according to their Use Index (Table1), were Cylicodiscus gabunensis (94,1%), Plagiostyles africana (88,2%), Zanthoxyllum giletti (88,2%), Duguetia barteri (85,3%) and Annickia chlorantha (82,3%). All of these were timber species and the used parts were the bark or stem bark. As a general rule, rural people use plants that are in their surroundings, and the choice of leaves, barks, stems, roots, fruits and collected latex can be attributed to their ease of collection by local people (Dibong et al., 2011). The use of herbal or leaves, stem, bark in the preparation of remedies is also common (Akendengué & Louis, 1994; Mengome et al., 2010; 2014). Most treatments were decoction and maceration in 55% and 31% of cases respectively. The preparation of indicated remedies uses water in most time, such as the case in most of the traditional medicines in Central Africa. The remedies were prepared in water in most time and immediately after harvest. The shelf life never exceed seven (7) days, after this deadline the medicine degrades and become unfit for consumption. Therefore the frequent use of freshly prepared remedies could indicate the availability of plant material in the surroundings. High oral administration (61.1%) was observed afterwards rectal route (19,4%). The posology of medicine administered by oral route is the object of a particular attention: the weekly dose is regularly conditioned in bottles of 150 cl, the glass from 20 to 25 cl approximately is the basic measure for the adults and the soup spoon is preferentially used for the children. Outcomes of the survey were confronted with previous studies realized in Gabon and abroad. In Gabon, among the collected plants, seventeen (17) were described as vermicide or anthelmintic plants: Annickia chloranta, Carica papaya, Bidens pilosa, Cyperus articulatus, Plagiostyles africana, Senna alata, Tamarindus indica, Cylicodiscus gabunensis, Drypetes gosweilleri, Brenania brieyi , Quassia africana, Solanum americanum, Cissus quadrangularis (Walker & Sillans, 1961), Picralima nitida (Walker & Sillans, 1961; Adjanohoun et al., 1984), Vernonia amygdalina (Akendengué & Louis, 1994), Cararpa klaineana (Walker & Sillans, 1961; Sima Obiang et al., 2015) and Scoparia dulcis (Walker & Sillans, 1961; Akendengué, 1992). In spite of organ plants used seem to be different for few plants, for most of them; the informations were similar to those whom we registered concerning the used part, the method of preparation and the route of administration. For example the used organs and the mode of use of Picralima nitida and Quassia africana differ according to sources: Walker & Sillans (1961), attributes the vermicide properties of Picralima nitida to the root, whereas the instructions for use described by Adjanohoun et al. (1984) are identical to the information

we collected (bark). Likewhise, the vermicide properties of Quassia africana are attributed to the bark (Walker & Sillans, 1961) while our interlocutors have appointed the roots. On another hand, all of the reported plants have been previously described in literature for many other traditional uses. The most frequently cited were Annickia chlorantha, Picralima nitida and Senna alata. The stem bark of Annickia chlorantha are used in the treatment of malaria (Betti et al., 2013a), female fertility (Aboughe Angone et al., 2009), for the management of hypertension (Madingou et al., 2012) and for dyeing (Madiele et al., 2013). The roots are crunched in case of lumbago (Betti et al., 2013b) or prepared (maceration or decoction) in association with stem bark of Picralima nitida or roots of Schumagnophyton magnificum in the treatment of male sexual dysfunction (Betti et al., 2013b). The stem bark of Picralima nitida were also reported for the treatment of malaria (Betti et al., 2013a and b), hernia and lumbago (Betti et al., 2013b) while the leaf and fruits were employed for the treatment of high blood pressure (Madingou et al., 2012). Finally, the leaves of Senna alata were reported to be used against malaria (Betti et al., 2013a), in the treatment of HIV/AIDS opportunistic diseases as skin rashes, stomach ache and venereal diseases (Feuya Tchouya et al., 2015) and as dyeing agent (Madiele et al., 2013). The ethnobotanical studies conducted out of Gabon were examinated for each plant (Table 2). Only 14 species were also described as vermicide plants (Picralima nitida, Carica papaya, Ageratum conyzoides, Bidens pilosa, Vernonia amygdalina, Momordica charantia, Cyperus articulatus, Alchornea cordifolia, Ocimum gratissimum, Senna alata, Senna occidentalis, Tamarindus indica, Scoparia dulcis, Drypetes gossweileri, and Cissus quadrangularis). Among them the most cited were Carica papaya, Tamarindus indica and Senna occidentalis (Krishna et al., 2008; Havinga et al., 2010; Yeap et al., 2010). Carica papaya is specie widely described as anthelmintic plant around the world (Krishna et al., 2008). Although the part of plant differs from a country to another: seeds (Koné & Kamanzi, 2006; Agyare et al., 2014; Nalumansi et al., 2014), leaves (Teklehaymanot et al., 2007; Agyare et al., 2014; Arif Khan et al., 2015), latex (Walker & Sillans, 1961; Arif Khan et al., 2015), fruits (Arif Khan et al., 2015) all organs (Diehl et al., 2004), bark (Nalumansi et al., 2014). The anthelmintic properties of Carica papaya appeared to be fully investigated pharmacologically (Stepek et al., 2005; Krishna et al, 2008). For Tamarindus indica, many ethnobotanical surveys exhibited the vermifuges properties of leaves (Boiteau & Allorge-Boiteau, 1993; Diarra et al., 2015), stem bark and fruits (Okulo et al., 2014), and other organs like bark and seeds (Havinga et al., 2009; Deepak et al., 2014). Other properties like antimalarial, antihypertensive, treatment of stomachache, diarrhea, and purgative properties are claimed (Havinga et al., 2009; Deepak et al., 2014). The vermifuges properties were pharmacologically assessed on nematode strains like Pheretima posthuma (Mute et al., 2009; Das et al., 2011), Tubifex tubifex (Das et al., 2011) Eisona fatida and Taenia solium (Badhoriya et al., 2011). Vernonia amygdalina is a woody shrub or small tree present in Africa and Asia. The leaves are consumed as vegetables and are efficient remedies in gastrointestinal disorders (Iwu, 1993). The use of V. amygdalina has been reported (Iwu, 1993; Teklehaymanot et al., 2007; Yeap et al., 2010; Agyare et al., 2014). Yeap et al., (2010) recorded the ethnomedicinal usages of the plant in 16 countries for the treatment of many ailments like parasitic diseases, gastrointestinal disorders, diabete and more. The anthelmintic property were assessed by pharmacological studies against several nematode strains infecting

vegetables, animal and humans: Ascaridia galli (Siamba et al., 2007), Caenorhabditis elegans (Agyare et al., 2014); Lumbricus terretris (Danquah et al., 2012), Haemoncus contortus (Oluwafemi, 2010). Many other activities like antiplasmodial (Yeap et al., 2010; Idowu et al., 2010; Ngbolua et al., 2013), antioxydative and chemopreventive (Farombi & Owoeye, 2011), toxicity (Njan et al., 2008) and antiamoebic (Longanga et al., 2000) were also reported. All these observations confirmed the efficiency of informations we collected and are in the favor of the use of these plants as anthelmintic remedies as long as they exhibited several uses in traditional medicine in sub-Saharan Africa, Asia and Central and South America. Only three (3) species: Duguetia barteri, Plagiostyles africana and Carapa klaineana were not found in our bibliographical research for any use in other countries. Althought, in Gabon, Duguetia barteri has pedicullicide properties (Walker & Sillans, 1961), Plagiostyles africana is reported to be used against helmints (Walker & Sillans, 1961), constipation (Akendengué & Louis, 1994), and venereal diseases (Feuya Tchouya et al., 2015) and Carapa klaineana has anthelmintic properties (Walker & Sillans, 1961; Sima Obiang et al., 2015). Duguetia barteri is the only specie described for the first time as anthelmintic properties with a high Use Index. Anthelmintic properties were assessed by pharmacological studies against several nematode strains infecting vegetables, animals and humans. Ten (10) of our species were studied for their anthelmintic activity: Carica papaya, Ageratum conyzoides, Bidens pilosa, Vernonia amygdalina, Alchornea cordifolia, Ocimum gratissimum, Senna alata, Senna occidentalis and Tamarindus indica (table 2). All species were also reported for antiparasitic and many biological activities (table 2). To the best of our knowledge, no biological screenings were founded for Duguetia barteri, Plagiostyles africana, and Carapa klaineana. These results are in favour with the use of the “collected plants” as medicinal plants and allow us to trust the indications formulated by the healers. More biological screenings will be able to confirm the results and complete the lack of information about the plant for which no anthelmintic activities were published. The chemical compositions of 21 species were already investigated and are presented in table 2. All of the species which have been submitted to anthelmintic screenings (table 2) were fully studied and presented a wide variety of metabolic compounds. To the best of our knowledge, the active principles were clearly identified only for Carica papaya. This specie presented a large amount of various compounds revealed in fruit, juice, seeds, leaves, bark and latex (Krishna et al., 2008). Thus, many proteolitic enzymes (papaine, chemopapain, chymopapain) were present in latex, and alkaloid compounds (carpaine, pseudocarpain, and dehydrocarpaine I and II) were located in leaves. Anthelmintic properties of the specie were investigated and attributed to five different chemical constituents identified as carpaine, carpasemine (benzylthiourea), benzylisothiocyanate and also papain and chymopapain (Stepek et al., 2005; Krishna et al., 2008). Among the most investigated plants which have been studied for in vitro anthelmintic activities, A. conyzoides possess many compounds reported from various parts of the plant. Constituents inclues among others terpenoids and sterols (like β-sitosterol and stigmasterol); pyrrolizidine alkaloids (lycopsamine, echinatine); polyphenolic flavonoids (like ageconyflavone A, B and C, and eupalestin), and chromenes (precocene I and II), (Kamboj and Saluja, 2008; Kaur & Dogra, 2014). Cyperus articulatus rhizome and stem essentials oils compositions were reported by many studies (Nyasse et al., 1988; Zogbi et al., 2006; Nabil AE Azzaz et al., 2014; Metuge et al., 2014). The main

constituents were monoterpenoids (α-pinene, β-pinene, pinocarvone), sesquiterpenoids (articulone, copaene, muskatone), hydrocarbons, fatty acids and derivatives. Zoghbi et al., (2006) highlighted typical constituents of the Cypearceae like cyperene, rotundene, cypera2,4-diene, patchoulenone, cyperotundone and α-cyperone. Ocimum gratissimum essential oils were also fully studied. The chemical composition exhibited the presence of phenylpropanoids, monoterpenoids and sesquiterpenoids (Sahouo et al., 2003; Sartoratto et al., 2004; Benitez et al., 2009). Essential oils of both Ageratum conyzoides, Cyperus articulatus and Ocimum gratissimum showed anthelmintic activity (Pessoa et al., 2002; Kamboj & Saluja, 2008; Metuge et al., 2014). Quassia africana chemical composition exhibited quassinoids (quassin and simalikalactone D), alkaloids (canthin-6-one, 4methylthiocanthin-6-one, 5-methoxycanthin-6-one) and hydrocarbons (Luminadio & Vanhaelin, 1986; Foyere Ayafor et al., 1993; Apers et al., 2002; Sama et al., 2014). The methanolic extract of the root bark of Quassia africana showed a significant activity against Onchocerca volvulus and the bio-assay guided fractionation of this extract lead to the isolation of the 4-methylthiocanthin-6-one (Foyere Ayafor et al., 1993). However, these compounds were weakly active. Beyond the anthelmintic activity, Quassia africana conducted to the isolation of simalikalactone D a quassinoid that showed antimalarial activity (Apers et al., 2002). As far as Quassinoids are chemical compounds responsible of many biological activities such as antiparasitic, antimicrobial or antitumoral (Alves et al., 2014), evaluation of anthelmintic activity of simalikalactone D could be considered. Differently, the essential oil of Ocimum gratissimum exhibited interesting antiparasitic and antifungal activities, and one constituent identified as eugenol were raised as the active principle. These results show that chemical studies of these plants could lead to potent anthelmintic metabolites that can be helpful for the development of new drugs. A large spectrum of secondary metabolites could be of interest in the search of new anthelmintic compounds. Usually, the sold medicinal plants are used by the traders themselves and the strong presence of certain species at the market shows the control of medicinal use by traders. In Gabon, knowledge transfer about medicinal plants does not take place appropriately due to lack of interest among young people generation to learn and practice, which could be assigned as the growing influence of modernism. In the study area, only two (2) suppliers had a level of end of primary literacy study, this minority does not contain much information that the illiterate group as also revealed by studies conducted elsewhere (Apema et al., 2010). Creating a database on medicinal plants in general is needed in Gabon. The development of tree nurseries and the creation of botanical gardens or gardens dedicated to medicinal plants will be helpful for safeguard biodiversity.

5. Conclusion This survey allowed us to list 24 anthelmintic species. One (1) specy (Duguetia barteri) is described for the first time as medicinal plant. The uses as vermifuges are confirmed for at least twenty (20) of them by the literature even if the mode of administration, the posology or the used parts can differ. After the harvests on the market, plants were dried and crushed, then subjected to a series of extractions for future pharmacological and phytochemical studies.

Several organs of every plant should be tested to increase the possibilities of obtaining bioactive molecules.

Competing interest The authors declare that they have no competing interests. Author’s contributions Idensi Bajin ba Ndob, designed the study, performed the ethnobotanical survey, contribute to the writing of the manuscript and drawing of graphics. Line Edwige Mengome, designed the study, contribute to the writing of the manuscript and drawing of graphics. Henri-Paul Bourobou Bourobou, designed the study, contribute to the botanical identification and the writing of the manuscript. Yvon Lossangoye Banfora, designed the study, performed the ethnobotanical survey and contribute to the botanical identification. Francis Bivigou, designed the study, contribute to the writing of the manuscript.

Author’s information IBN, Phytochemistry, Ph.D.; LEM, Health Science, Ph.D., Chargée de Recherche CAMES; HPBB, Botanique, Ph.D., Maître de Recherche CAMES; YLB, Agro-forester, Engineer; FB, Biomedical, Engineer. IBN, LEM, HPBB, YLB and FB are all researchers at the Pharmacopeia and Traditional Medicine Institute (Institut de Pharmacopée et de Médecine Traditionnelles/ IPHAMETRA) were their work is focused on medicinal plants used in Gabonese and African Traditionnal Medicines. The objectives of the Institute is identifying plants of interest by ethnobotanical surveys, evaluating their pharmacological activity and isolating active molecules in the aim of providing new active principles for the production of new medicines. The main aimed pathologies are parasitosis, diabetes and high blood pressure.

Aknowledgments We wish to express our sincere appreciation to Mr. Nick Koumba who helped us in conducting the survey and to sirs Raoul Gnangadouma, Thomas Nzabi, and Mayombo for the identification of plants. We also want to thank all the sellers who agreed to participate in this study and the Gabon Oregon Center (GOC) which had supported the survey. References

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Graphical abstract

Map and localization of the study area