Agricultural Reviews

  • Chief EditorPradeep K. Sharma

  • Print ISSN 0253-1496

  • Online ISSN 0976-0741

  • NAAS Rating 4.84

Frequency :
Quarterly (March, June, September & December)
Indexing Services :
AGRICOLA, Google Scholar, CrossRef, CAB Abstracting Journals, Chemical Abstracts, Indian Science Abstracts, EBSCO Indexing Services, Index Copernicus
Submit

Reviewer Article

Agricultural Reviews, volume 42 issue 2 (june 2021) : 156-165

Implications of Tannin Containing Plants for Productivity and Health in Small Ruminant Animals: A Review

Emmanuel M. Atiba1,2,*, Rutto K. Laban3, Sun Zewei1, Zhong Qingzhang1, Natnael D. Aschalew1
1Department of Animal Nutrition and Feed Science, College of Animal Science and Technology, Jilin Agricultural University, 2888 Xincheng Street, Changchun City, Jilin Province P.R. China.
2Department of Animal Production, College of Natural Resources and Environmental Studies, University of Juba, P.O. Box 82, Juba, South Sudan.
3Agriculture Research Station, College of Agriculture, Virginia State University, Petersburg, VA 23806, USA.
Cite article:- Atiba M. Emmanuel, Laban K. Rutto, Zewei Sun, Qingzhang Zhong, Aschalew D. Natnael (2021). Implications of Tannin Containing Plants for Productivity and Health in Small Ruminant Animals: A Review . Agricultural Reviews. 42(2): 156-165. doi: 10.18805/ag.R-173.

ABSTRACT

Infection with parasitic nematodes is a serious threat to health and production of small ruminant worldwide. It causes reduction in feed intake, weight gain and eventually death of the host. The primary control method of the nematode infection relied on frequent use of anthelmintic drugs. Unfortunately, this control strategy is no longer effective due to widespread anthelmintic resistance, which necessitates search for novel approaches to control nematodes. Condensed tannin (CT) containing forages have been used as anthelmintic to control parasitic nematodes for years. This paper reviews available information about effects of CT on productivity and health of small ruminants infected with parasitic nematodes. Many of temperate and tropical forages are nutraceutical plants (possess both nutritional and health benefits). Consumption of CT containing forages reduced negative impacts of gastrointestinal parasitism in sheep and goat by regulating establishment of worm as shown in reduced worm burdens, fecal egg count (FEC) and worm fecundity. Parasitized sheep and goats fed forages containing CT had high feed intake and body weight gain, probably due to increase in protein and amino acids supply. Condensed tannins containing feeds result in lighter meat color and tend to improve antioxidant activity. Therefore, the use of CT containing forages to control parasitic nematodes and improve production of small ruminants is one the alternatives to anthelmintic drugs.  

INTRODUCTION

Endo-parasitic nematodes represent a major threat to the health and production of small ruminant worldwide. Infection with these parasites could result in a huge economic loss for producers (Pathak et al., 2016; Atiba et al., 2016). The main clinical signs of the parasitic infection  include reduction in feed intake, poor reproduction, growth performance and eventually death (Nnadi et al., 2009). Until now, anthelmintic drugs are the basis of nematode control method in sheep and goats. However, the drugs have been rendered ineffective by widespread development of anthelmintic resistance among nematode species (Coles et al., 2006; Kaplan and Vidyashankar, 2012). Moreover, this method is not economically viable for some small scale producers due to financial challenges or availability of drugs and consumers demand for chemical free animal products (Hoste et al., 2012; Raju et al., 2015; Atiba et al., 2016). Therefore, affordable and sustainable alternative parasite control methods have been evaluated to reduce dependence on anthelmintic drugs (Arroyo-Lopez et al., 2014). Many studies have shown that feeding tannins containing plants can reduce detrimental effects of parasitic nematode infection in sheep and goats (Kahiya et al., 2003; Iqbal et al., 2007; Marume et al., 2012).
       
Tannins are complex group of polyphenolic compounds that dissolve in water and have similar physical and chemical properties (Acamovic and Brooker, 2005). Generally, tannins are classified into two distinct groups, hydrolysable and condensed. Hydrolysable tannins (HT) are esters of phenolics acids such as gallic acids in gallotannins or other phenolic acids derived from the oxidation of galloyl residues as in ellagitannins and a polyol, usually D-glucose. Condensed tannins (CT) also called proanthocyanidins are oligomers or polymers of flavan-3-ol units usually linked together by C-C bonds and occasionally by C-O-C bonds. Tannins have been the focus of many studies in fields of animal and veterinary sciences due to their anthelmintic effects on gastrointestinal nematodes. However, some of phytochemicals such as phenolic and alkaloids compounds found associated with tannins are toxins in nature. The HT are believed to be more toxic to ruminants than CT. Consumption of CT containing plants at an appropriate threshold level, neverthless can improve nutritional status of parasitized ruminants (Min and Hart, 2003; Huang et al., 2017). Moreover, tanniniferous forages are rich in nutrient particularly protein content making them potential source of animal feed. In the past two decades, the concept of using tannins containing forages as nutraceutical plants (plants combining both nutrition and health benefits) has emerged as a promising alternative to anthelmintic drugs (Kahiya et al., 2003; Marume et al., 2012; Arroyo-lopez et al., 2014; Hoste et al., 2015). Therefore, this paper reviews available information about effects of condensed tannins on productive performances and hematobiochemical as well as parasitological parameters.
       
Tannins are heterogeneous polyphenolic compounds found in wide range of plants species and their concentration levels vary greatly not only between plants species but also between the parts (Table 1). They occur in every part of plant including seeds, leaves, fruits, barks, roots and wood and are present in higher concentration particularly in tropical plants (Pathak, 2013b). However, tannin content in many plant species seems to be greatly influenced by environmental factors such as season, water availability and stage of plant growth (Sampaio et al., 2011; Mcmahon et al., 2011). The HT are common in dicotyledonous plants whereas, CTs are the most abundant type of tannins found in both angiosperms and gymnosperms (Huang et al., 2017). The CT are very common in forages legumes of Fabaceae family (e.g. lespedeza spp and Onobrychis spp) , shrubs (Acacia spp) and the leaves as well as barks of other plants (Min et al., 2003). These plants are widely distributed and are suitable for feeding ruminants (Vasta et al., 2008). They have been exploited as alternative sources of feed to replace cereal concentrate in small ruminant diet and their utilization has increased in recent years. Tanniniferous plants are also believed to have positive effect on animal health as they have been shown to minimize the risk associated with parasitic nematodes infection.
 

Table 1: Concentration level of condensed tannin in some plants’ species.


       
This study focuses on the use of tanniniferous plants to combat parasitic nematode infection in small ruminants. The study applied internet search to specifically identify relevant scientific articles. The literature on the use of tanniniferous plants in sheep and goats production was systematically reviewed between December 2018 and November 2019, at Jilin Agricultural University, China. Relevant scientific papers published in English peer-reviewed journals were searched using the key words combination (tanniniferous plants or forages or legumes, parasitic nematode and small ruminants or sheep or goats). The online electronic database through Google scholar, Scopus, Web of Science and Science direct were searched to capture the latest information. The available relevant papers in the field were reviewed and summarized in the article.
 
Effect of CT on nutrition and performance of the host
 
Gastrointestinal parasites are known to be the main cause of poor performances of sheep and goats. Infestation with parasitic nematodes may reduce voluntary feed intake, weight gain, cause anemia and eventually host death. However, it has been known that consumption of tanniniferous forages could reduce negative effects of parasitic nematodes infection in small ruminants (Paolini et al., 2003; Hoste et al., 2012; Arroyo-Lopez et al., 2014). Many plant species of families Fabaceae, Fagaceae, Anacardiaceae among others have been used to improve performance of parasitized sheep and goats (Athanasiadou et al., 2001; Iqbal et al., 2007; Marume et al., 2012; Villalba et al., 2014).
 
Voluntary feed intake
 
The most significant effect of parasitism with nematodes is reduction in voluntary feed intake, which influences growth performance of small ruminants. Gastrointestinal infection in sheep and goats may result in 6-50% reduction in feed intake. It has been speculated that such effect could raise from abdominal pain or discomfort associated with gastrointestinal nematodes activities, with extend depending on the host age, breed and parasite species (Poppi et al., 1990; Knox et al., 2006).
       
The CT in forage legumes seem to be effective in suppressing gastrointestinal nematodes in sheep and goats. Sainfoin is a perennial forage legume of family Fabaceae commonly found in temperate regions. This legume has been used as pasture, conserved as hay or silage for sheep and goats. Confinement feeding trial has shown that Trichostrongylus colubriformis infected sheep consuming Sainfoin hay (S) containing 2% CT had higher feed intake compared to those on grass hay (G) containing 1% CT (Ríos-De-Álvarez et al., 2008). This could be due to nutritional modulation of host immune responses or ingestion of CT, which would regulate establishment of worm and reduce the degree of anorexia (Hoste et al., 2006; Houdijk, 2012). Moreover, tanniniferous forages are more palatable. Similarly, Romero et al., (2018) found that supplementation with perennial peanut (PEA) and Sericea lespedeza (LES) hays tended to increase feed intake (757 and 745 g/d, respectively) of nematode infected goats in confinement (Table 2).  This could be attributed to the CT content in PEA and LES which suppressed parasitic nematodes. Indeed, a large number of studies have shown that CT containing forages improved feed intake of parasitized lambs (Lisonbee et al., 2009; Merera et al., 2013) and goats (Seng et al., 2007; Moore et al., 2008; Sokerya et al., 2009; Amit et al., 2013). However, some results showed that feed intake of nematode infected sheep  (van Zyl et al., 2017) and goats (Lopes et al., 2016) were not affected by feeding tanniniferous forages (Table 2). Nevertheless, high CT concentration level has been associated with decreased diet palatability, reduced voluntary feed intake, disturbed digestibility and decreased nutrient intake (Pathak, 2013b; Addisu, 2016). Heckendorn et al., (2007) observed lower feed intake in Swiss lambs artificially infected with Haemonchus contortus consuming Chicory, Birds foot and Sainfoin containing, respectively, 3.1, 15.2 and 26.1 CT g/kg DM (Table 2). This might be due to CT concentration level or parasite species. Haemonchus contortus is the most pathogenic and prolific endoparasitic nematode. Adult female H. contortus can lay up to 5000-10000 eggs per day (Sinnathamby et al., 2018), increasing worm load and severity of the infection.
 

Table 2: Feed intake and weight gain of nematode infected sheep and goats fed plants containing CT.


 
Weight again
 
Endoparasitic nematodes found in the abomasum or small intestine cause reduction in weight gain of sheep and goats. However, consumption of CT containing forages seems to improve weight gain of the host in spite of the infection. In a feeding trial in Pakistan using H. contortus infected sheep (Iqbal et al., 2007), diet supplement was offered daily and contained low and high tannin, respectively, 2 and 3% CT. The results showed that weight gain was significantly higher (8.2 kg) in 3% CT supplemented sheep compared to 2% CT supplemented sheep (6.8 kg) and tannin-free sheep (4.8 kg). An increased in weight gain has been used as a marker of resilience in nematode infected ruminants. Additionally, a number of studies are also in agreement with these results in parasitized sheep supplemented with L. pallida (Merera et al., 2013), Sainfoin (Arroyo-Lopez et al., 2014) and Lespedeza cuneata  (Zyl et al., 2017). Most of CT containing forages are rich in protein content and are more digestible (Torres-Acosta et al., 2012).
       
Albizia, a genus of Fabaceae family comprises of more than 150 species, widely distributed in tropical regions in Africa and in South Central America. Albizia anthelmintica is believed to be rich in CT and other bioactive compounds rendering it potential drug for many diseases of animals. Administrating trials with Albizia anthelmintica capsules (Gradé et al., 2008) were carried out using parasitized sheep to address some of the shortcomings from feeding experiments. The results showed that CT drenched increased weight gain of the sheep (Table 2). This could be due to increase in amount of protein by-pass ruminal degradation. Moreover, converting the CT containing forages into hay seems to increase protein bound and possibly covalently linked between CT and protein (Mueller-Harvey et al., 2019). Some results from study under temperate condition showed that supplementation with sun-dried Sericea lespedeza increased weight gain of goats naturally infected with nematodes (Moore et al., 2008). Similar observations were made by Sokerya et al., (2009) in Cambodian goats infected with nematodes fed cassava foliage and Marume et al., (2012) in Xhosa lop-eared goats of South Africa fed Acacia karroo. Contrary, Seng et al., (2007) and Osoro et al., (2007) reported that feeding nematode infected goats tanniniferous plants did not increase weight gain (Table 2). This could be due to low total feed intake and availability of nutrient in the feed.
 
Effect of CT on hematobiochemical parameters of the host
 
Gastrointestinal parasitism in sheep and goats is directly associated with anemia and hypoproteinaemia resulting from endogenous protein and blood losses. Studies show that supplementation with CT containing forages alleviate impacts of parasitism in sheep and goats (Arroyo-Lopez et al., 2014; Singh et al., 2016). A pasture trial conducted by Merera et al., (2013) showed that supplementation with Leucaene pallida significantly increased packed cell volume (PCV) of nematode infected Horro lambs compared to those assigned grazing alone. In the United States, Moore et al., (2008) evaluated the anthelmintic effects of S. lespedeza (SL) on H. contortus infected goat kids randomly assigned to two dietary treatments consisting of 75% SL hay (CT) or Bermuda grass (no CT) and 25% concentrate. At the end of experimental period, a significant increase in PCV was recorded in goats in the SL group relative to those in no CT group. Similar results have been obtained by Merera et al., (2013) and Arroyo-Lopez et al., (2014) from infected lambs fed sainfoin. The increased in PCV could be due to reduce number of blood sucking parasites in abomasum and small intestine by CT or improved protein nutrition allowing the host to replace lost protein more rapidly. Further, Villalba et al., (2013) reported increased in MCHb of H. contortus infected sheep fed sainfoin (Onobrychis viciifolia) but no effect was observed on MCV.  In contrast, Sokerya et al., (2009) reported that feeding Manihot esculenta to nematode infected goats for long-term reduced PCV from 30% to 25% (Table 3). Contrary, Seng et al., (2007) have shown that CT had no effect on PCV of nematode infected goats of Cambodia fed fresh Manihot esculenta foliage for short-term.
 

Table 3: Effect of CT on blood and biochemical parameters of nematode infected sheep and goats.


       
A number of studies have examined the effects of CT on different biochemical variables (hemoglobin, Protein, urea, mast cells, pan cells, mean corpuscular cells, globulin, eosinophil) in parasitized sheep (Azuhnwi et al., 2013; Rios-De-Álvarez et al., 2014) and goats (Singh et al., 2016) receiving different tanniniferous forages. Azuhnwi et al., (2013) reported increased in plasma essential and semi-essential amino acids (AA) concentration in lambs artificially infected with H. contortus fed sainfoin. This increased in essential and semi-essential amino acids concentration could be due to increase in amino acids supply and absorption in small intestine. In addition to improve protein nutrition, CT can also modulate activity of host immune cells. Eosinophil cells are the most important elements in the response to nematode infection and are often associated with the expression of host resistance against the parasites (Terefe et al., 2005; Alba-Hurtado and Muñoz-Guzmán, 2013). Contrary, study carried out by Marume et al., (2012) showed that supplementation of Xhosa lop-eared goats of South Africa with Acacia karroo did  not affect eosinophil cell count. Similar results have been observed by Joshi et al., (2011) in H. contortus infected goats consuming Sericea lespedeza (Table 3). The lack of effect here is difficult to explain; probably, the goat breeds are naturally resistant to nematode infection.
 
Effect of CT on parasite
 
The CT have demonstrated good anthelmintic effects in both in vitro and in vivo studies on endoparasitic nematodes. These effects include reduction in egg excretion, worm number, lower fertility, lower worm establishment as well as impairing hatching and development of egg into third-stage larvae (Hoste et al., 2015).
       
Early evidence of CT effect on nematodes causing reduction in egg excretion and worm number has been reported under both temperate (Heckendorn et al., 2007; Moore et al., 2008; Joshi et al., 2011;  Marume et al., 2012;) and tropical conditions  (Kahiya et al., 2003; Seng et al., 2007; Iqbal et al., 2007; Max et al., 2007; Gradé et al., 2008; Sokerya et al., 2009; Minho et al., 2010; Merera et al., 2013). Recent results obtained from H. contortus and T. colubriformis infected sheep (Ríos-De Álvarez et al., 2008; Azuhnwi et al., 2013; Villalba et al., 2013; Arroyo-lopez et al., 2014; Zyl et al., 2017) showed significant reductions in egg excretion and adult worm number in the presence of tanniniferous forages (Table 4). Counting of worm egg excreted with feces is a practical and cost effective diagnostic tool for determining parasitism in small ruminants (Rinaldi et al., 2019). This method is used to estimate worm burden in sheep and goats.  Few tanniniferous forages have been extensively investigated through in vitro assays and controlled in vivo studies. For instance, the results from in vitro assays that evaluated inhibitory capacity of Ziziphus nummularia and Acacia nilotica extracts against egg hatching and development of larvae were somehow discouraging (Bachaya et al., 2009), however, the results of in vivo studies on sheep naturally infected nematodes were much more encouraging. Moreover, goats fed heather (Calluna vulgaris) (Moreno-Gonzalo et al., 2012) and perennial peanut or Sericea lespedeza (Romero et al., 2018) had lower egg excretion, adult worm number and worm fecundity. Similar results were reported by Brito et al., (2018) who observed 57.7% and 66.9% reduction, respectively, in adult H. contortus and egg excretion in sheep consuming Mimosa caesalpiniifolia (Table 4). It is generally assumed that CT could reduce adult worm number, egg excretion, egg hatching and larvae development through direct or indirect effects. Direct effects of CT could be mediated through CT-parasite interactions, thereby affecting physiological functions of the worms and causing their death (Hoste et al., 2006; Arroyo-Lopez et al., 2014).  The CT can also bind to the free proteins, resulting in reduced nutrient availability and hence larvae starvation and death (Athanasiadou et al., 2001; Iqbal et al., 2007). Indirectly, CT can improve host protein nutrition by increasing amount of by-pass protein, thereby improving host resistance to parasites. However, in goats grazed B. pulchella in tropical area of Brazil, Lopes et al., (2016) found no effect of CT on egg excretion but CT significantly reduced egg hatching percentage (Table 4). The lack of effect could be due to repeated and heavy mixed infection which overwhelmed the effect of CT.
 

Table 4: Parasitological parameters of nematode infected sheep and goats fed plants containing CT.


 
Effect of CT on meat
 
Little work has be done to investigate effects of CT on carcass characteristics and meat quality of nematodes infected lambs (Pathak et al., 2013a; Zhong et al., 2015) and goats (Min et al., 2015) consuming different tanniniferous forages. Parasites infestation causes extensive protein losses leading to poor growth, meat production and meat quality of ruminants. The most convincing evidence to support the effect is that some results indicating an improved meat color (significant increased in redness and antioxidant activity) (Zhong et al., 2015) has been exhibited when lambs consumed green tea polyphenol (4g GTP). The mechanism by which CT effects meat color is unclear but can partly be explained by reducing biohydrogenation and thus exerting positive effects on the oxidative stability of the meat (García et al., 2019). Skatole and indole are the main meat volatiles that strongly affect flavor. According to Priolo et al., (2009), skatole and indole were lower in fat of lambs supplemented with tannin compared to non-supplemented animals. In tropical regions of Asia, several trees of Myrtaceace and Moraceace families have been identified and explored for their tannins contain (Pathak et al., 2013a). Parasitized sheep consuming Ficus infectoria and Psidium guajava had significantly high carcass dressing percentage (Pathak et al., 2013a). However, fresh carcass weight and gastrointestinal weight were not affected in this experiment. Further researches in this area are needed to fully understand the mechanism through which CT affects meat color.
 
Effect of CT on milk
 
Up to now, effect of CT on milk yield and composition of nematodes infected sheep and goats has not been intensively investigated. However, milk production and composition of ruminants fed tanniniferous forages have been documented (Vasta et al., 2008; Kushwaha et al., 2011; Priolo, 2014; Morales and Ungerfeld, 2015). Recently, Abo-donia et al., (2017) reported that increased in dietary tannin increased concentration of cis-14 C18:1, cis-9, cis-12 C18:2 n-6 LA, total cis monounsaturated fatty acids (MUFA), polyunsaturated fatty acids (PUFA), n-3 and n-6 polyunsaturated fatty acids but reduced fat content in goat milk. Similar observations were made by Keles et al., (2017) who noted that increased in tannin level increased in C18:0 and total protein of goat milk. Further ewe receiving Hazelnut skin had greater milk MUFA and 18:1 trans than ewe fed no hazelnut (Campione et al., 2020). Tanniferous forages/tannin-containing diet could be used as effective means to increase unsaturated fatty acids content in ruminant milk.

CONCLUSION

Consumption of CT containing forages enhanced host resistance to endoparasitic infection as depicted in reduced adult worm number, egg excretion and increased PCV, albumin and total protein. Tanniniferous forages can also improve host resilience to nematode infections by reducing detrimental impacts and increasing feed intake and weight gain. The effect of CT containing forages on meat quality of nematode infected ruminants has been less studied so far. However, tanniniferous forages can improve meat color and antioxidant activity as well as increase unsaturated fatty acids in the milk. Therefore, CT containing forages have great potential to improve production of sheep and goats and potential anthelmintic properties to reduce reliance on anthelmintic drugs to combat endoparasites. Further researches to determine applicable CT doses and develop effective tools as well as methods of extraction are crucial.

CONFLICT OF INTEREST

No potential conflicts of interest.

REFERENCES


  1. Abo-donia, F., Yang, L.Y., Hristov, A.N., Wang, M., Tang, S.X., Zhou, C.S., Han., X.F., Kang, J.H., Tan, Z.L., He, Z.X. (2017). Effects of tannins on the fatty acid profiles of rumen fluids and milk from lactating goats fed a total mixed ration containing rapeseed oil. Livestock Science. 204: 16-24. doi: 10.1016/j.livsci.2017.08.002.

  2. Acamovic, T. Brooker, J. D. (2005). Biochemistry of plant secondary metabolites and their effects in animals. Proceedings of the Nutrition Society. 64(03): pp. 403-412. doi: 10.1079/PNS2005449.

  3. Addisu, S. (2016). Effect of Dietary Tannin Source Feeds on Ruminal Fermentation and Production of Cattle; a Review: Online Journal of Animal and Feed Research. 6(2): 45-56. http://www.science-line.com/indexCn http://www.ojafr.ir.

  4. Alba-Hurtado, F., Muñoz-Guzmán, M.A. (2013). Immune responses associated with resistance to haemonchosis in sheep. BioMed Research International. 2013. doi: 10.1155/2013/162158.

  5. Amin, M.R., Mostofa, M., Islam, M.N., Asgar, M.A. (2011). Effects of neem, betel leaf, devil’s tree, jute and turmeric against gastrointestinal nematodes in sheep. Journal of the Bangladesh Agricultural University. 8(2): 259-263. doi: 10.3329/jbau.v8i2.7935.

  6. Amit, M., Cohen, I., Marcovics, A., Muklada, H., Glasser, T.A., Ungar, E.D., Landau, S.Y. (2013). Self-medication with tannin-rich browse in goats infected with gastro-intestinal nematodes. Veterinary Parasitology. Elsevier B.V., 198(3-4), pp. 305-311. doi: 10.1016/j.vetpar.2013.09.019.

  7. Arroyo-Lopez, C., Manolaraki, F., Saratsis, A., Saratsi, K., Stefanakis, A., Skampardonis, V., Voutzourakis, N. (2014). Anthelmintic effect of carob pods and sainfoin hay when fed to lambs after experimental trickle infections with Haemonchus contortus and Trichostrongylus colubriformis. Parasite. 21(71): 1-9. doi: 10.1051/parasite/2014074.

  8. Athanasiadou, S., Kyriazakis, I., Jackson, F., Coop, R.L. (2001). Direct anthelmintic effects of condensed tannins towards different gastrointestinal nematodes of sheep: in vitro and in vivo studies. Veterinary Parasitology. 99: 205-219.

  9. Atiba, E.M., Sayre, B., Temu, V.W. (2016). Effects of dietary protein supplementation on the performance and non-carcass components of goats artificially infected with Haemonchus contortus. Science Letter. 4(2): 124-130.

  10. Azuhnwi, B.N., Hertzberg, H., Arrigo, Y., Gutzwiller, A., Hess, H.D., Mueller-Harvey, I., Torgerson, P.R., Kreuzer, M., Dohme-Meier, F. (2013). Investigation of sainfoin (Onobrychis viciifolia) cultivar differences on nitrogen balance and fecal egg count in artificially infected lambs1. Journal of Animal Science. 91(5): 2343-2354. doi: 10.2527/jas.2012-5351.

  11. Bachaya, H. A., Iqbal, Z., Khan, M.N., Sindhu, Z., Jabbar, A. (2009). Anthelmintic activity of Ziziphus nummularia (bark) and Acacia nilotica (fruit) against Trichostrongylid nematodes of sheep. Journal of Ethnopharmacology. 123(2): 325-329. doi: 10.1016/j.jep.2009.02.043.

  12. Brito, D.R.B., Costa-Júnior, L.M., Gracia, J.L., Torres-Acosta, J.F.J., Louvandini, H., Cutrim-Júnior, J.A.A., Araújo, J.F.M., Soares, E.D.S. (2018). Supplementation with dry Mimosa caesalpiniifolia leaves can reduce the Haemonchus contortus worm burden of goats. Veterinary Parasitology. Elsevier, 252: 47-51. doi: 10.1016/j.vetpar.2018.01.014.

  13. Campione, A., Natalehho, A., Valenti, B., Luciano, G., Rufino-Moya, P.J., Avondo, M., Morbidini, L., Pomente, C., Krol, B., Wilk, M., Migdal, P., Pauselli, M. (2020). Effect of feeding hazelnut skin on animal performance, milk quality and rumen fatty acids in lactating ewes. Animals. 10(4): 1-16. doi: 10.3390/ani10040588.

  14. Coles, G.C., Jackson, F., Pomroy, W.E., Prichard, R.K., vonSamson- Himmelstjerna, G., Silvestre, A., Taylor, M.A., Vercruysse, J. (2006). The detection of anthelmintic resistance in nematodes of veterinary importance. Veterinary Parasitology. 136: 167-185. doi: 10.1016/j.vetpar.2005.11.019.

  15. García, E.M., López, A., Zimerman, M., Hernández, O., Arroguy, J.I. (2019). Enhanced oxidative stability of meat by including tannin-rich leaves of woody plants in goat diet. Asian-Australasian Journal of Animal Sciences. 32(9): 1439-1447. doi: 10.5713/ajas.18.0537.

  16. Gradé, J.T., Arble, B.L., Weladji, R.B., Van Damme, P. (2008). Anthelmintic efficacy and dose determination of Albizia anthelmintica against gastrointestinal nematodes in naturally infected Ugandan sheep. Veterinary Parasitology. 157(3-4): 267-274. doi: 10.1016/j.vetpar.2008.07.021.

  17. Heckendorn, F., Häring, D. A., Maurer, V., Senn, M., Hertzberg, H. (2007). Individual administration of three tanniferous forage plants to lambs artificially infected with Haemonchus contortus and Cooperia curticei. Veterinary Parasitoloy. 146: 123-134. doi: 10.1016/j.vetpar.2007.01.009.

  18. Hoste, H., Jackson, F., Athanasiadou, S., Thamsborg, S.M., Hoskin, S.O. (2006). The effects of tannin-rich plants on parasitic nematodes in ruminants. Trends in Parasitology. 22(6): 253-261. doi: 10.1016/j.pt.2006.04.004.

  19. Hoste, H., Martinez-Ortiz-De-Montellano, C., Manolaraki, F., Brunet, S., Ojeda-Robertos, N., Fourquaux, I., Torres-Acosta, J.F.J., Sandoval-Castro, C.A. (2012). Direct and indirect effects of bioactive tannin-rich tropical and temperate legumes against nematode infections. Veterinary Parasitology. Elsevier B.V. 186(1-2): 18-27. doi: 10.1016/j.vetpar. 2011.11.042.

  20. Hoste, H., Torres-Acosta, J.F.J., Sandoval-Castro, C.A., Mueller-Harvey, I., Sotiraki, S., Louvandini, H., Thamsborg, S.M., Terrill, T.T. (2015). Tannin containing legumes as a model for nutraceuticals against digestive parasites in livestock. Veterinary Parasitology. Elsevier B.V. 212(1-2): 5-17. doi: 10.1016/j.vetpar.2015.06.026.

  21. Houdijk, J.G.M. (2012). Differential effects of protein and energy scarcity on resistance to nematode parasites. Small Ruminant Research. Elsevier B.V. 103(1): 41-49. doi: 10.1016/j.smallrumres.2011.10.017.

  22. Huang, Q., Liu, X., Zhao, G., Hu, T., Wang, Y. (2017). Potential and challenges of tannins as an alternative to in-feed antibiotics for farm animal production. Animal Nutrition. Elsevier Taiwan, xxx: 1-14. LLC. doi: 10.1016/j.aninu.2017.09.004.

  23. Iqbal, Z., Sarwar, M., Jabbar, A., Ahmed, S., Nisa, M., Sajid, M.S., Khan, M.N., Mutfi, K.A., Yaseen, M. (2007). Direct and indirect anthelmintic effects of condensed tannins in sheep. Veterinary Parasitology. 144(1-2): 125-131. doi: 10.1016/j.vetpar.2006.09.035.

  24. Joshi, B. R., Kommuru, D.S., Terrill, T.H., Mosjidis, J.A., Burke, J.M., Shakya, K.P., Miller, J.E. (2011). Effect of feeding Sericea lespedeza leaf meal in goats experimentally infected with Haemonchus contortus. Veterinary Parasitology. Elsevier B.V., 178(1-2): 192-197. doi: 10.1016/j.vetpar. 2010.12.017.

  25. Kahiya, C., Mukaratirwa, S., Thamsborg, S.M. (2003). Effects of Acacia nilotica and Acacia karoo diets on Haemonchus contortus infection in goats. Veterinary Parasitology. 115(3): 265-274. doi: 10.1016/S0304-4017(03)00213-9.

  26. Kaplan, R.M., Vidyashankar, A.N. (2012). An inconvenient truth/ : Global worming and anthelmintic resistance. Veterinary Parasitology. Elsevier B.V. 186(1-2): 70-78. doi: 10.1016/j.vetpar.2011.11.048.

  27. Keles, G., Yildiz-akgul, F., Kocaman, V. (2017). Performance and milk composition of dairy goats as affected by the dietary level of stoned olive cake silages. Asian-Australian Journal of Animal Science. 30(3): 363-369.

  28. Knox, M. R., Torres-Acosta, J. F. J., Aguilar-Caballero, A.J. (2006). Exploiting the effect of dietary supplementation of small ruminants on resilience and resistance against gastrointestinal nematodes. Veterinary Parasitology. 139(4): 385-393. doi: 10.1016/j.vetpar.2006.04.026.

  29. Kushwaha, R., Rai, S.N., Singh, A.K., Chandra, G., Vaidya, M.M., Sharma, V.K., Pathan, M.M., Kumar, S. (2011). Tanninerous feed resources in dairy: Review. Agricultural Reviews. 32(4): 267-275.

  30. Lisonbee, L. D., Villalba, J.J., Provenza, F.D., Hall, J.O. (2009). Tannins and self-medication: Implications for sustainable parasite control in herbivores. Behavioural Processes. 82(2): 184-189. doi: 10.1016/j.beproc.2009.06.009.

  31. Lopes, S.G., Barros, L.B.G., Louvandini, H., Abdalla, A.L., Costa Junoir, L.M. (2016). Effect of tanniniferous food from Bauhinia pulchella on pasture contamination with gastrointestinal nematodes from goats. Parasites and Vectors. 9(1): 3-9. doi: 10.1186/s13071-016-1370-3.

  32. Marume, U., Chimonyo, M., Dzama, K. (2012). Influence of dietary supplementation with Acacia karroo on experimental haemonchosis in indigenous Xhosa lop-eared goats of South Africa. Livestock Science. Elsevier B.V. 144(1-2): 132-139. doi: 10.1016/j.livsci.2011.11.007.

  33. Max, R.A., Kimambo, A.E., Kassuku, A.A., Mtenga, L.A., Buttery, P.J. (2007). Effect of tanniniferous browse meal on nematode faecal egg counts and internal parasite burdens in sheep and goats. South African Journal of Animal Sciences. 37(2): 97-106. doi: 10.4314/sajas.v37i2.4033.

  34. Mcmahon, L.R., McAllister, T.A., Berg, B.P., Majak, W., Acharya, S.N., Popp, J.D., Coulman, B.E., Wang, Y., Chang, K.J. (2011). A review of the effects of forage condensed tannins on ruminal fermentation and bloat in grazing cattle. Canadian Journal of Plant Science. 80(3): 469-485. doi: 10.4141/p99-050.

  35. Merera, C., Ayana, T., Gudeta, T. (2013). Effect of feeding Leucaena pallida with concentrate and antihelmentic treatment on growth performance and nematode parasite infestation of Horro ewe lambs in Ethiopia. International Journal of Livestock Production. 4(10): 155-160. doi: 10.5897/IJLP2013.0176.

  36. Min, B.R., Barry, T.N., Attwood, G.T., McNabb, W.C. (2003). The effect of condensed tannins on the nutrition and health of ruminants fed fresh temperate forages: A review. Animal Feed Science and Technology. 106(1-4): 3-19. doi: 10.1016/S0377-8401(03)00041-5.

  37. Min, B.R., Hart, S.P. (2003). Tannins for suppression of internal parasites. Journal of Animal Science. 81(2): 102-109. doi: /2003.8114_suppl_2E102x.

  38. Min, B.R., Wilson, E.A., Solaiman, S., Miller, J. (2015). Effects of condensed tannin-rich pine bark diet on experimentally infected with Haemonchus contortus in meat goats. International Journal of Veterinary Health Science and Research. 3(3): 49-57. doi: 10.19070/2332-2748-1500013.

  39. Minhoi, A.P., Filippsen, L.F., do Amarante, A.F.T., Abdalla, A.L. (2010). Efficacy of condensed tannin presents in acacia extract on the control of Trichostrongylus colubriformis in sheep. Ciencia Rural, Santa Maria. 40(6): 1360-1365. doi: 10.1590/S0103-84782010005000088.

  40. Moore, D.A., Terrill, T.H., Kouakou, B., Shaik, S.A., Mosjidis, J.A., Miller, J.E., Vanguru, M., Kannan, G., Burke, J.M. (2008). The effects of feeding Sericea lespedeza hay on growth rate of goats naturally infected with gastrointestinal nematodes. Journal of Animal Science. 86(9): 2328-2337. doi: 10.2527/jas.2007-0411.

  41. Morales, R., Ungerfeld, E.M. (2015). Use of tannins to improve fatty acids profile of meat and milk quality in ruminants: A review: Chilean Journal of Agricultural Research. 75: 239-248. doi: 10.4067/S0718-58392015000200014.

  42. Moreno-Gonzalo, J., Ferre, I., Celaya, R., Frutos, P., Ferreira, L.M.M., Hervás, G., Gracía, U., Ortega-Mora, L.M., Osoro, K. (2012). Potential use of heather to control gastrointestinal nematodes in goats. Small Ruminant Research. 103(1): 60-68. doi: 10.1016/j.smallrumres.2011.10.019.

  43. Mueller-Harvey, I., Bee, G., Dohme-Meier, F., Hoste, H., Karonen, M., Kölliker, R., Lüscher, A., Niderkorn, V., et al. (2019). Benefits of condensed tannins in forage legumes fed to ruminants: Importance of structure, concentration and diet composition. Crop Science. 59(3): 861-885. doi: 10.2135/cropsci2017.06.0369.

  44. Nnadi, P. A., Kamalu, T. N., Onah, D. N. (2009). The effect of dietary protein on the productivity of West African Dwarf (WAD) goats infected with Haemonchus contortus. Veterinary Parasitology. 161(3-4): 232-238. doi: 10.1016/j.vetpar. 2009.01.014.

  45. Osoro, K., Benit-Peña, A., Frutos, P., Garc, U., Ortega-Mora, L.M., Celaya, R., Ferre, I. (2007). The effect of heather supplementation on gastrointestinal nematode infections and performance in Cashmere and local Celtiberic goats on pasture. Small Ruminant Research. 67: 184-191. doi: 10.1016/j.smallrumres.2005.09.032.

  46. Paolini, V., Bergeaud, J.P., Grisez, C., Prevot, F., Dorchies, Ph., Hoste, H. (2003). Effects of condensed tannins on goats experimentally infected with Haemonchus contortus. Veterinary Parasitology. 113(3-4): 253-261. doi: 10.1016/S0304-4017(03)00064-5.

  47. Paswan, J.K., Kumar, K., Kumar, S., Chandramoni, Kumar A., Kumar, D., Kumar, A. (2016). Effect of feeding Acacia nilotica pod meal on hematobiochemical profile and fecal egg count in goats. Veterianry World. 1400-1406. doi: 10.14202/vetworld.2016.1400-1406.

  48. Pathak, A.K. (2013a). Potential of using condensed tannins to control gastrointestinal nematodes and improve small ruminant performance. International Journal of Molecular Veterinary Research. 3(8): 36-50. doi: 10.5376/ijmvr. 2013.03.0008.

  49. Pathak, A.K., Dutta, N., Banerjee, P.S., Pattanaik, A.K., Sharma, K. (2013b). Influence of dietary supplementation of condensed tannins through leaf meal mixture on intake, nutrient utilization and performance of Haemonchus contortus infected sheep. Asian-Australasian Journal of Animal Sciences. 26(10): 1446-1458. doi: 10.5713/ajas. 2013.13066.

  50. Pathak, A. K., Dutta, N., Banerjee, P.S., Goswami, T.K., Sharma, K. (2016). Effect of condensed tannins supplementation through leaf meal mixture on voluntary feed intake, immune response and worm burden in Haemonchus contortus infected sheep. Journal of Parasitic Diseases. Springer India. 40(1): 100-105. doi: 10.1007/s12639-014-0455-1.

  51. Poppi, D.P., Sykes, A.R., Dynes, R.A. (1990). The effect of endoparasitism on host nutrition - the implications for nutrient manipulation. Proceedings of the New Zealand Society of Animal Production. 50: 237-243. doi: 10.1079/BJN19660078.

  52. Priolo, A., Vasta, V., Fasone, V., Lanza, C.M., Scerra, M., Biondi, L., Bella, M., Whittington, F.M. (2009). Meat odour and flavour and indoles concentration in ruminal fluid and adipose tissue of lambs fed green herbage or concentrates with or without tannins. Animal. 3(3): 454-460. doi: 10.1017/S1751731108003662.

  53. Raju, J., Sahoo, B., Chandrakar, A., Sankar, M., Garg, A.K., Sharma, A.K., Pandey, A.B. (2015). Effect of feeding oak leaves (Quercus semecarpifolia vs Quercus leucotricophora) on nutrient utilization, growth performance and gastrointestinal nematodes of goats in temperate sub Himalayas. Small Ruminant Research. Elsevier B.V., 125: 1-9. doi: 10.1016/j.smallrumres.2014.12.013.

  54. Rinaldi, L., Amadesi, A., Dufourd, E., Bosco, A., Gadanho, M., Lehebel, A., Maurelli, M.P., Chauvin, A., Charlier, J., Cringoli, G., Ravinet, N., Chartier, C. (2019). Rapid assessment of faecal egg count and faecal egg count reduction through composite sampling in cattle. Parasites and Vectors. BioMed Central. 12(1): 1-8. doi: 10.1186/s13071-019-3601-x.

  55. Ríos-De-Álvarez, L.ÿ Greer, A.W., Jackson, F., Athanasiadou, S., Kyriazakis, I., Huntley, J.F. (2008). The effect of dietary sainfoin (Onobrychis viciifolia) on local cellular responses to Trichostrongylus colubriformis in sheep. Parasitoloy. 135: 1117-1124. doi: 10.1017/S0031182008004563.

  56. Romero, J.J., Zarate, M.A., Ogunade, I.M., Arriola, K.G., Adesogan, A.T. (2018). Tropical plant supplementation effects on the performance and parasite burden of goats. Asian-Australian Journal of Animal Science. 31(2): 208-217.

  57. Sampaio, B.L., Bara, M.T.F., Ferri, P.H., da Costa Santa, S., de Paula, J.R. (2011). Influence of environmental factors on the concentration of phenolic compounds in leaves of Lafoensia pacari. Brazilian Journal of Pharmacognosy. 21(6): 1127-1137. doi: 10.1590/S0102-695X2011005000177.

  58. Saric, T., Rogosic, J., Zupan, I., Beck, R., Bosnic, R., Sikic, Z., Skobic, D., Tkalcic, S. (2015). Anthelmintic effect of three tannin-rich Mediterranean shrubs in naturally infected sheep. Small Ruminant Research. Elsevier B.V. 123(1): 179-182. doi: 10.1016/j.smallrumres.2014.11.012.

  59. Seng, S., Waller, P.J., Ledin, I., Höglund, J. (2007). The effects of short-term feeding of fresh cassava (Manihot esculenta) foliage on gastrointestinal nematode parasite infections in goats in Cambodia. Tropical Biomedicine. 24(1): 47-54.

  60. Singh, S., Pathak, A.K., Khan, M., Sharma, R.K. (2016). Effect of tanniferous leaf meal mixture based multi nutrient blocks on nutrient utilization and biochemical profile of Haemonchus contortus infected goats. Indian Journal of Animal Research. 50(5): 725-732. doi: 10.18805/ijar.5716.

  61. Sinnathamby, G., Henderson, G., Umair, S., Janssen, P., Bland, R., Simpson, H. (2018). The bacterial community associated with the sheep gastrointestinal nematode parasite Haemonchus contortus. PLoS ONE. 13(2): e0192164. https://doi.org/10.1371/journal.pone.0192164.

  62. Sokerya, S., Waller, P.J., Try, P., Höglund, J. (2009). The effect of long-term feeding of fresh and ensiled cassava (Manihot esculenta) foliage on gastrointestinal nematode infections in goats. Tropical Animal Health and Production. 41(2): 251-258. doi: 10.1007/s11250-008-9182-x.

  63. Terefe, G., Yacob, H.T., Grisez, C., Prevot, F., Dumas, E., Bergeaud, J.P., Dorchies. Ph., Hoste, H., Jacquiet, P. (2005). Haemonchus contortus egg excretion and female length reduction in sheep previously infected with Oestrus ovis (Diptera: Oestridae) larvae. Veterinary Parasitology. 128(3-4): 271-283. doi: 10.1016/j.vetpar.2004.11.036.

  64. Torres-Acosta, J.F.J., Sandoval-Castro, C.A., Hoste, H., Aguilar-Caballero, A.J., Cámara-Sarmiento, R., Alonso-Díaz, M.A. (2012). Nutritional manipulation of sheep and goats for the control of gastrointestinal nematodes under hot humid and subhumid tropical conditions. Small Ruminant Research. Elsevier B.V. 103(1): 28-40. doi: 10.1016/j.smallrumres.2011.10.016.

  65. van Zyl, E.A., Botha, F.S., Eloff, K.J.N., Msuntsha, P.P., Oosthuizen, P.A., Stevens, C. (2017). The use of Lespedeza cuneata for natural control of gastrointestinal nematodes in Merino sheep. Onderstepoort Journal of Veterinary Research. 84(1): 1-7. doi: 10.4102/ojvr.v84i1.1259.

  66. Vasta, V., Nudda, A., Cannas, A., Lanza, M., Priolo, A. (2008). Alternative feed resources and their effects on the quality of meat and milk from small ruminants. Animal Feed Science and Technology. 147: 223-246. doi: 10.1016/j.anifeedsci.2007.09.020.

  67. Villalba, J.J., Miller, J., Hall, J.O., Clemensen, A.K., Stott, R., Snyder, D., Provenza, F.D. (2013). Preference for tanniferous (Onobrychis viciifolia) and non-tanniferous (Astragalus cicer) forage plants by sheep in response to challenge infection with Haemonchus contortus. Small Ruminant Research. Elsevier B.V., 112(1-3): 199-207. doi: 10.1016/j.smallrumres.2012.11.033.

  68. Villalba, J.J., Miller, J., Ungar, E.D., Landau, S.Y., Glendinning, J. (2014). Ruminant self-medication against gastrointestinal nematodes/ : evidence, mechanism and origins. Parasite. 21(31). doi: 10.1051/parasite/2014032.

  69. Zabré, G., Kabore, A., Bayala, B., Katiki, L.M., Costa-Júnior, L.M., Tamboura, H.H., Belem, A.M.G., Abdalla, A.L., Niderkorn, V., Hoste, H., Louvandini, H. (2017). Comparison of the in vitro anthelmintic effects of Acacia nilotica and Acacia raddiana. Parasite. 24 (44). doi: 10.1051/parasite/2017044.

  70. Zhong, R.Z., Li, H.Y., Fang, Y., Sun, H.X., Zhou, D.W. (2015). Effects of dietary supplementation with green tea polyphenols on digestion and meat quality in lambs infected with Haemonchus contortus. Meat Science. 105: 1-7. doi: 10.1016/j.meatsci.2015.02.003. 
Reviewed By

Download Article
In this Article
    Contact us
    Follow us

    Editorial Board

    View all (0)