Introduction
The production of backyard poultry under semi-scavenging system is suitable for a large number of villagers in poorer socioeconomic countries as additional source of income and nutrient supplement (Latif, Reference LATIF2001), and there has been a marked increase in outdoor access systems in all countries due to consumer demand for animals raised under such conditions. Parasitic infestations in outdoor reared chickens can be more dangerous than other disease causing organisms because they are usually dormant and can give rise to secondary bacterial infections (Rehman et al., Reference REHMAN, JAVED, TUNIO and KUTHU2009). Increased demand for poultry and its products from deep-litter and free range production systems have been hampered by helminth infections due to heavy worm burdens (Fossum et al., Reference FOSSUM, DÉSIRÉE, PERNILLE and VÅGSHOLM2009). The most important helminth infection of poultry is Ascaridia galli, which is prevalent in a variety of production systems (Abdelqader et al., Reference ABDELQADER, GAULY, WOLLNY and ABO-SHEHDADA2008). Birds with heavy infections may present with haemorrhages, diarrhoea and listlessness (Permin and Hansen, Reference PERMIN and HANSEN1998). The invasiveness of the worm in the gut results in damage to the mucosal integrity of the intestine wall and decreased utilisation and uptake of nutrients leading to reductions in weight gain and poor FCR (Kilpinen et al., Reference KILPINEN, ROEPSTORFF, PERMIN, NØRGAARD-NIELSEN, LAWSON and SIMONSEN2005). In severe cases, consequences such as blockage of the intestine and ultimately death can result (Ikeme, Reference IKEME1971; Ramadan and Znada, Reference RAMADAN and ZNADA1991).
In addition, A. galli also has the ability to act as a vector for other disease causing organisms including Escherichia coli and Salmonella enterica, which cause economic losses from poor FCR and increased treatment cost (Chadfield et al., Reference CHADFIELD, PERMIN, NANSEN and BISGAARD2001; Martín-Pacho et al., Reference MARTÍN-PACHO, MONTOYA, ARANGUENA, TORO, MORCHON, MARCOS-ATXUTEGI and SIMON2005; Permin et al., Reference PERMIN, CHRISTENSEN and BISGAARD2006).
Conventionally, piperazine compounds have been used as the anthelmintic of choice owing to their high efficacy and low toxicity to the host for the treatment of A. galli (Soulsby, Reference SOULSBY1982). More recent drugs, such as albendazole and levamisole have been shown to be highly effective (Sharma et al., Reference SHARMA, SINGH and SAXENA1989), while others including Ivermectin, benzimidazoles and fenbendazole have attracted considerable attention because of their unique mode of action (Sharma et al., 1990; Yazwinski et al., Reference YAZWINSKI, TUCKER, WRAY, JONES and CLARK2013). Although there are many achievements in the field of developing anthelmintics against nematodes, the development of anthelmintic resistance is a major problem in the poultry industry (Stear et al., Reference STEAR, DOLIGALSKA and DONSKOW-SCHMELTER2007).
In this context, investigations on indigenous medicinal plants might be useful in the development of effective and low-cost herbal anthelmintics as alternatives to chemicals. Plants are a major part of ethno-veterinary practices which are used by rural populations in livestock and poultry sectors. Much work has been done on anthelmintic efficacy of several medicinal plants against A. galli infection but there is little information about the effect of medicinal plants and their active ingredients on the control of its eggs, and hence transmission. This review covers the studies related to screening of plant materials having in vitro and in vivo anthelmintic efficacy against A. galli around the globe.
In vitro anthelmintic activity of medicinal plants
Tribulus terrestris L. (Zygophylaceae) is a prostrate herb native to the Mediterranean region but also found in Asia, Africa, warm regions of Europe, America and Australia (Frohne, Reference FROHNE1999). Ethno-veterinary and the medicinal use of this plant is well documented for various purposes in Bulgaria and many other countries. Various biologically active ingredients are found in T. terrestris including steroids, alkaloids, flavonoids, saponins, vitamins, tannins and unsaturated fatty acids (Adaikan et al., Reference ADAIKAN, GAUTHAMAN, PRASAD and NG2000). In vitro evaluation of alcoholic extracts from the plant and a mixture of crude alkaloids from T. terrestris have demonstrated that this plant has anti-ascarid activity (Chakraborty et al., Reference CHAKRABORTY, RAY and SIKDAR1979).
A study investigating the anthelmintic activity of Bassia latifolia showed that an aqueous extract of dried seeds was more effective against adult A. galli than alcoholic extract in vitro. In a comparative study, water extract of B. latifolia proved to be more effective than piperazine hexadihydrate (Asadullah and Sabir, Reference ASADULLAH and SABIR1980).
Piper betle L. (Piperaceae) is a dioecious perennial climber with swollen nodes on its stems and leaves which have a yellowish to bright green colour. P. betle has been shown to have antimicrobial (Tewari and Nayak, Reference TEWARI and NAYAK1991), hepatoprotective and antioxidant (Choudhary and Kale, Reference CHOUDHARY and KALE2002; Santhakumari et al., Reference SANTHAKUMARI, PRAKASAM and PUGALENDI2003) activities. The active ingredients in this plant include alkaloids, flavonoids, polyphenols and terpenes which may be responsible for its anthelmintic activity (Bate-Smith, Reference BATE-SMITH1962). The essential oil from leaves of P. betle, when given at the dose rate of 200 mg/kg body weight at 24 hourly interval s in poultry, reduced the worm burden by 13.9% after the first dose and 51.4% after second dose of treatment, demonstrating its anthelmintic potential against A. galli infection (Shilaskar and Parashar, Reference SHILASKAR and PARASHAR1985).
Morinda citrifolia L. (Rubiaceae) is an important medicinal plant used in ethno-veterinary medicines, and is usually called Indian mulberry. It has been referred to in a medical context for over 2000 years in Polynesia (Zhu and Woerdenbag, Reference ZHU and WOERDENBAG1995). It has been reported to possess a vast range of nutritional and therapeutic values (Whistler, Reference WHISTLER1985) and the fruit of M. citrifolia has been shown to have some in vitro anthelmintic activity against A. galli (Priyanto, Reference PRIYANTO1995).
Thespesia lampas Cav. (Malvaceae) grows on slopes of hills in forests and its leaves have shown activity against ring worm, skin diseases and inflammation, while the roots can be used as a general tonic (Kirtikar et al., 1999). This plant possesses kaemferol and its glycosides, quercetin, gossypol, herbacetin, rutin, ß-sitosterol and lupeol as active ingredients (Anonymous, 1995). In a bio-assay, extracts were used with different concentrations (10-50 mg/ml) and piperazine citrate at 10 mg/ml was used as reference drug with distilled water as control. The results revealed better activity of the extract at a lower concentration (10 mg/ml) against A. galli (Kosalge and Ravindra, Reference KOSALGE and RAVINDRA2009).
Mentha logifolia L. (Lamiaceae) grows along stream sides, verges, bogs, irrigation channels and the borders of paddy fields throughout the Kashmir Valley (Kaul, Reference KAUL1997). The active components are diverse and stable natural compounds with low molecular weight which have been shown to prevent the onset of anthelmintic resistance (Tariq et al., Reference TARIQ, CHISHTI, AHMAD and SHAWL2009). A worm motility inhibition (WMI) assay was used in vitro to evaluate the anthelmintic potential of crude hydroalcoholic extract (CHE) and crude aqueous extract (CAE) of M. longifolia at concentrations of 25 and 50 mg/ml on live worms of A. galli to check the paralysis and/or death after exposure of six hours. The CHE and CAE of M. longifolia at a concentration of 50 mg/ml showed the highest worm mortality of 82% and 46%, respectively. Both CHE and CAE of M. longifolia exhibited time-dependent anthelmintic activity against A. galli in chickens. The leaves of M. longifolia possess significant potential as an anthelmintic and could be a future alternative to treat worm infestations in chickens (Javid et al., Reference JAVID, SYED and BILAL2013).
Sesbania grandiflora L. (Fabaceae) leaves have traditionally been associated with anthelmintic activity against selected helminthes (Vaidhyaratnum, Reference VAIDHYARATNUM1996). Trial results suggested that flavonoid, phenol, tannin, alkaloid, saponin and acid in aqueous extracts of S. grandiflora can serve as an alternate, effective helminthicide replacing synthetic drugs. Aqueous extracts from leaves of S. grandiflora at concentrations of 10-100 mg/100 ml of medium per 10 parasites, showed that an increased concentration of the extracts decreased the survival of A. galli (Karumari et al., Reference KARUMARI, SUMATHI, VIJAYALAKSHMI and EZHILARASI2014).
In vivo anthelmintic activity of medicinal plants
Anacardium occidentale L. (Anacardiaceae) is a plant largely used in Africa for the treatment of various diseases (Tédong et al., Reference TÉDONG, DZEUFIET, DIMO, ASONGALEM, SOKENG, FLEJOU, CALLARD and KAMTCHOUING2007) and has been reported to have anthelmintic activity. Preliminary phytochemical screening of its alcoholic extract revealed the presence of tannins, glycosides, steroids, phenolics and triterpenoids while aqueous extracts contained flavonoids, steroids, carbohydrates, saponins and glycosides. Of these compounds, tannins were shown to produce anthelminthic activities (Niezen et al., Reference NIEZEN, WAGHORN, CHARLESTON and WAGHORN1995) due to interference with energy generation in helminth parasites by uncoupling parasite specific fumarate reductase-mediated oxidative phosphorylation reactions. Other possible pathway of the anthelminthic effect of tannins is that they bind to free proteins in gastrointestinal tract of host animal (Athnasiadou et al., Reference ATHNASIADOU, KYRIAZAKIS, JACKSON and COOP2001) or glycoprotein on the cuticle of the parasite (Thompson and Geary, Reference THOMPSON and GEARY1995) which causes death. The alcoholic and aqueous extract (250 and 500 mg/ml) from the false fruit of A. occidentale displayed significant anthelminthic properties at higher concentrations. Both extracts showed anthelmintic activities in dose-dependent manner, with the shortest time of paralysis and death seen at 500 mg/ml concentration (Varghese et al., Reference VARGHESE, JACOBO, GEORGEKULTY and PETER1971; Aiswarya et al., Reference AISWARYA, REZA, RADHIKA and RAHUL2011).
Piliostigma thonningii Schum is grows abundantly as a wild uncultivated small tree in many parts of Nigeria, such as Minna, Zaria, Bauchi, Ilorin, Plateau, Lagos and Abeokuta (Keay, Reference KEAY1989). It is a leguminous plant that belongs to a family of shrubs and trees called Caesalpinaceae. This plant has received attention due to claims for its application as an ethno-medicinal plant to cure diseases including common malaria, dysentery, fever, infectious respiratory ailments, snake bite, hookworm, hepatobiliary ailments, hydropsy, sterility, rachitis and skin diseases in humans (Tira-Picos et al., Reference TIRA-PICOS, NOGUEIRA and GBOLADE2010). Ethanol bark extracts, at concentrations of 1000, 2000 and 4000 mg/kg of the plant, showed a dose dependent reduction of 39%, 53% and 56%, respectively against A. galli infected chickens by stimulating neuromuscular junctions principally and ganglions to a lesser degree (Asuzu and Onu, Reference ASUZU and ONU1994).
Caesalpinia Crista L. (Fabaceae) is a prickly shrub or woody vine containing carbohydrates, alkaloids, glycosides, tannins, flavonoids and coumarins as active ingredients. Powdered C. crista at dose rates of 30, 40 and 50 mg/kg body weight, sourced from water and methanolic extracts was used to study chickens injected with artificial infection of A. galli. Methanolic extract as well as the whole plant in a crude form at dose rates of 40 and 50 mg/kg showed significant (P<0.001) effects on worm burden at days 10 and 15 post-treatment, whereas the dose rate of 30 mg/kg was effective (P<0.05) on day 15 only. The aqueous extract failed to show any significant results. Treatment of birds with the seeds of C. crista as a powder or methanolic extract compared against piperazine at the dose rate of 200 mg/kg showed reduction in worm burden as 94±3, 98±1 and 100±0% respectively after 15 days of treatment. The results of this study suggested that these treatments had equal effect against infections caused by ascarids in poultry. A study further suggested that the crude powder of C. crista was better compared to methanolic extract in terms of any side effects (Javed et al., Reference JAVED, AKHTAR, RAHMAN, KHALIQ and AHMAD1994).
Ocimum gratissimum L. (Lamiaceae) has various medicinal properties including as a treatment for diarrhoea using its leaf extracts, while haemorrhoids and stomach pain are relieved by the use of cold leaf infusions. Thymol-riched leaves of O. gratissimum have shown antimicrobial properties (Olowokudejo and Pereira-Sheteolu, Reference OLOWOKUDEJO and PEREIRA-SHETEOLU1998) while terpenoids (oleanolic acid) anthelmintic activity. Plant extract of O. gratissimum at a dose rate of 1500 mg/kg caused a 55.8% reduction in A. galli infection in cockerels and this effect was significant (P<0.01) compared to control group (Njoku, Reference NJOKU1997).
Cassia occidentalis L. (Leguminosae) is an important plant which is found in tropical areas of South America including the Amazon region of Brazil. This plant is locally called Manjerioba or Fedegoso and is well known for its medicinal properties in many countries. Traditionally, many parts of C. occidentalis (seeds, leaves, roots, and stems) are used widely as a laxative, febrifuge, analgesic, hepatoprotective, diuretic and vermifuge. The plant is used to treat various diseases including tuberculosis, dysmenorrhoea, gonorrhoea, flu, anaemia, liver and urinary tract infections in humans (Coimbra, Reference COIMBRA1994; Di Stasi and Hiruma-Lima, Reference DI STASI and HIRUMA-LIMA2002). Helminth infections of poultry can be treated with C. Occidentalis, which contains carbohydrates, saponins, flavonoids, terpenes, sterols, alkaloids, anthraquinones and tannins (Muyibi et al., Reference MUYIBI, OLORODE, ONYEYILI and OSUNKWO2000). The plant extract showed a higher reduction in worm burden of A. galli at 24 mg/ml (P<0.01) as compared with 16 and 20 mg/ml concentrations (P<0.05). Activity against H. gallinarum did not show any significant (P>0.05) difference in effect compared to Ivermectin. The EC50 of the extract was 17.78 mg/ml for H. gallinarum and 11.78 mg/ml for A. galli. Trials suggested that the extract of C. occidentalis is safe because there was no observation of toxicity even at 25,000 mg/kg (Kateregga et al., Reference KATEREGGA, MARIA, PATRICK and JAMES2003).
Allium sativum L. (Amaryllidaceae) was reported to have anthelmintic activity against A. galli in chicken due to its allicin component (the main active component of garlic) but did not represent as an alternative to flubendazole (Velkers et al., Reference VELKERS, DIEHO, PECHER, VERNOOIJ, VAN ECK and LANDMAN2011). Das and Thakuria (Reference DAS and THAKURIA1977) stated that 2, 4 and 6% garlic oil caused mortality in A. galli after exposure of 12, 10 and 8 hours respectively, and in Heterakis gallinarum after 10, 8 and 6 hours respectively. Garlic extract significantly reduced the glucose uptake, glycogen content and oxygen consumption in both parasites (Singh and Shalini, Reference SINGH and SHALINI2000).
Ananas comosus L. (Bromeliaceae) i.e. pineapple, is found in tropical areas and the fruit of this plant contains coalesced berries. An experiment was carried out to determine the comparative anthelmintic efficacy of pineapple leaf extracts, piperazine citrate and levamisole against ascariasis in poultry. Although the leaf extract showed less effectiveness in reducing parasite count in post-mortem examinations than piperazine citrate and levamisole, it may be useful due to less adverse side-effects. In all treated groups, haemoglobin (Hb) estimation, packed cell volume (PCV) and total erythrocyte count (TEC) significantly increased (P<0.01) while total leukocyte count (TLC) and erythrocyte sedimentation rate (ESR) decreased significantly (P<0.01). Body weight was increased following administration of pineapple leaves extract, piperazine citrate and levamisole (Hoque et al., Reference HOQUE, MOSTOFA, AWAL, CHOUDHURY, HOSSAIN and ALAM2006).
In vitro and in vivo anthelmintic activity of leaf extracts of Tephrosia vogelli and Vernonia amygdalina has been reported against A. galli infections. From in vitro studies, modifications were seen in larval migration assays. For this purpose, pre-incubation of larval suspension (750 μl) was done using plant extracts for a period of four hours at room temperature and then by Pasteur pipette, and were then transferred to larval migration inhibition (LMI) tubes. In vivo screening of birds was done 14 days after infection and birds in different groups were quantified and isolated for necropsy. The main chemical constituents in plant extracts were identified as rotenoids, lactones, sesquiterpene, glycosides, tannins and anthracenes, which all showed significant anthelmintic activity (P<0.05) in vitro and in vivo against A. galli. Results of in vitro study were supported by a 74.7% and 63.7% larval migration inhibition and a reduction in faecal egg counts by 77.4% and 76.9% for extracts of T. vogelli and V. amygdalina respectively (Siamba et al., Reference SIAMBA, OKITOI, WATAI, WACHIRA, LUKIBISI and MUKISIRA2007).
Momordica charantia L. (Cucurbitaceae) (i.e. the korolla fruit) is a tendril-bearing and herbaceous vine that can grow up to five meters and is used for treatment of diabetes and cancer prevention in human and animal studies (Wang et al., Reference WANG, ZHANG, ZHAO, WANG, FAN, WU and HU2011). Ivermectin Pour-on and an extract of whole M. charantia were compared in vitro and in vivo for their anthelmintic efficacy against adult A. galli infected chickens. There was an increase in body weights for groups treated with Ivermectin Pour-on at 500 μg/kg body weight and for those receiving the 3% aqueous extract of M. charantia after treatment but decreased body weight was seen in the control group. Hb, TEC and PCV were increased significantly (P<0.05) in chickens of treated groups whereas ESR was increased in the control group (Shahadat et al., Reference SHAHADAT, MOSTOFA, MAMUN, HOQUE and AWAL2008).
Aloe secundiflora L. (Asphodelaceae) is primarily used for its exudates and leaf gel as the main active components, which are derived from inner epidermal layers and parenchytomous cells respectively. The exudates possess a mixture of phenolic compounds, including phenyl pyrones, athrones, chromonesand, tannins, polysaccharides, phenolic compounds and terpenoids while the gel mainly consists of polysaccharides. Active components of the leaves of Aloe spp. are credited to possess anthelmintic, antibacterial, antiviral and antifungal properties. In vitro efficacy of A. secundiflora extracts was assessed on A. galli and the results demonstrated that different extracts including hexane, acetone, ethylacetate, chloroform and methanol showed anthelmintic activity by reduction of A. galli egg shedding. The lowest concentration of five different extracts was 5 mg/ml which resulted in an inhibition percent (IP) of 75.52, 87.21, 79.60, 43.6 and 86.13% respectively. A maximum of 50 mg/ml was used as the highest concentration for these extracts and resulted in an IP of 91.84, 100, 97.55, 91.29 and 99.46% respectively. The researchers concluded that different extracts of A. secundiflora have many active ingredients which possess in vitro anthelmintic efficacy against the larvae of A. galli (Kaingu et al., Reference KAINGU, ALFRED, REBECCA, ROBERT and LEWIS2013).
The plant Azadirachta indica L. (Meliaceae) leaves has major medicinal importance. The chemical constituents of this plant contain many biologically active compounds including alkaloids, lavonoids, triterpenoids, phenolic compounds, carotenoids, steroids and ketones (Verkerk et al., 1993). Aqueous extracts of A. indica leaves and a rage of piperazine concentrations were screened for their anthelmintic effects against A. galli in indigenous chickens. Data revealed that aqueous extract of A. indica leaves showed significant (P<0.05) anthelmintic efficacy at dose rates 1, 2, 4 and 20 mg/ml against chicken ascariasis and the shortest time to achieve parasitic paralysis was observed at 20 mg/ml dose. From post-mortem worm counts, A. indica leaves showed considerable efficacy against worm burden. The aqueous extract of A. indica did not show any adverse effects on haematological parameters and the physiological condition of treated birds (Khokon et al., Reference KHOKON, SHARIF, EMRAN, MOHAMMAD, JAMES and MAHBUB2014).
Conclusions
The use of plant extracts against A. galli has considerable advantages, including lower meat and egg contamination, and may substitute for conventionally used synthetic drugs which can present various health hazards including drug resistance in endemic pathogen populations and drug residues in poultry meat. However, there are many obstacles for using plants in the field, even though they have shown efficacy in vitro. For anthelmintic purpose, the accurate dose rate of active ingredients of these plants need to be carefully determined and this information should be made widely available for the best treatments and outcomes. Furthermore, the efficacy of these plants should also be registered and verified at government level to facilitate and train farmers about their potential usage.
