Effects of daily or alternate day administration of polyethylene glycol 4000 on feed intake, digestion and health status of male goats fed on kermes oak (Quercus coccifera L.) foliage

I Ben Salem, H Ben Salem¹, M S Ben Saïd and A Ben Younes²

Ecole Nationale de Médecine Vétérinaire de Sidi Thabet, Sidi Thabet, 2020, Tunisia
bensalemimen@yahoo.fr
¹ Institution de la Recherche et de l'Enseignement Supérieur Agricoles (IRESA), 1002 Tunis, Belvédère, Tunisia
² Fondation Nationale de l’Amélioration de la Race Chevaline, Sidi Thabet, 2020, Tunisia

Abstract

This 24-day experiment aimed to determine the effects of deactivation of tannins of Quercus coccifera L. foliage with polyethylen glycol 4000 (10 g) administered daily (PEG1) or every two days (PEG2) to male goats fed Quercus coccifera foliage ad libitum. A group of 5 male goats not receiving PEG (CTL) served as control. Dry matter intake of Quercus coocifera ranged between 60.3 and 62.4 g/BW^0.75. It was not affected by the frequency of PEG supply. Compared to CTL animals, daily supply of PEG increased crude protein digestibility. This increase was not maintained when PEG was provided every 2 days. Nitrogen retention did not change with PEG supply. Goats assigned to control diet were substantially losing weight. The provision of PEG decreased the rate of weight loss. Clinical examination performed on day 24 revealed a general impairment of the health status of the animals with an increase of the cardiac frequency, while respiratory and rumen contraction frequencies decreased irrespective of the nature of the diet. Oliguria and loss of hair were also observed. In conclusion, feeding Quercus coccifera foliage alone to goats can lead to loss of weight and a degradation of the general health status. Supplying PEG as a way to neutralize the tannins of the shrub does not yield a significant improvement.

Keywords: antinutritional effects, nutritive value, microbial activity, tannin, urea

Introduction

The Mediterranean area is home to large flocks of goats that are raised in extensive production systems. Range vegetation mainly from shrublands where Quercus spp. is widespread, represents the main fodder source for these animals. Kermes oak (Quercus coccifera L.) is a dominant species in the Tunisian bushes hosting for long period of the year browsing goats. Because of their browsing behaviour, especially forage species selection, bipedal standing and higher mobility of the upper lip, goats have a greater ability to utilise woody species than cattle and sheep (Papachristou and Nastis 1992). Quercus coccifera foliage is high in condensed tannins and lignin but it is low in crude protein (Khazaal et al 1993; Ben Salem et al 2003). Moreover, the effects of tannins in reducing the nutritive value of shrub species are well documented (Ben Salem et al 1997; Landau et al 2000; Min et al 2012). Several attempts have been made to deactivate tannins in temperate and tropical forages, these include the use of a synthetic polymer polyethylene glycol (PEG) (Ben Salem et al 2002; Makkar 2003; Frutos et al 2004). PEG binds tannins irreversibly over a wide range of pH, and its presence reduces the formation of protein-tannins complex (Jones and Mangan 1977). PEG was also used to evaluate the nutritive value of some tannin-rich forage species (Waghorn et al 1994). Stress, poor welfare and imbalanced nutrition can increase susceptibility to diseases among animals, thus increasing the need for veterinary treatments, posing risks to food consumers, decreasing profitability and endangering environmental sustainability of the livestock production systems and of the associated animal food chains. However, little attention has been paid to the understanding of the linkages between animal nutrition and animal welfare. Clinical and biochemical troubles are often associated with tannins consumption and they are reflected by damages in the liver, kidneys and epithelium of the digestive tract (Filippich et al 1991; Reed 1995). Liver and kidney are involved in the process of detoxification and excretion of tannins or their degradation products (Jean-Blain 1998).

In experiments conducted in Tunisia, PEG has been supplied to goats in feed blocks or with an energetic supplement (i.e. barley) to overcome the negative effects of Quercus coccifera-tannins. The main results showed an improvement of the feeding value of the diet, mainly the nitrogen value, and the health of goats fed on Quercus coccifera-based diets (Ben Salem et al 2003; Ben Salem et al 2005). Those beneficial effects would be ascribed to a balanced supply of protein and energy throughout the use of feed blocks or barley. However, it is not known whether PEG has a carryover effect when associated to shrub tannins at intermittent frequency of administration. If so, this would economise the use of this deactivating reagent, and consequently would reduce the feeding cost. To the best of our knowledge this hypothesis is not yet tested in the literature. Therefore, this study was undertaken to determine the effect of daily or alternate-day administration of PEG on diet intake and digestibility, clinical parameters and the concentrations of some plasma metabolites in male goats receiving Quercus coccifera-based diets over a short period of time.

Materials and methods

This study was carried out in the Small Ruminants Research Unit of the National Institute of Agricultural Research of Tunisia (INRAT).

Plant material, animals and treatments

Kermes oak (Quercus coccifera L.) foliage (Leaves and thin branches with a diameter less than 3 mm) was harvested three times a week from a bush in the region of Teskrya in northern Tunisia. More details on the preparation of the plant materiel are reported in our previous paper (Ben Salem et al 2003).

Fifteen Alpine x local male goats (16-month-old, body weight mean ± S.D.; 18±1.0 kg) were individually penned in an animal house. They were randomly allotted into three treatment groups of five goats each. The treatments consisted of Quercus coccifera foliage distributed ad libitum and 10 g of polyethylene glycol 4000 (PEG) mixed with 50 g of ground barley grain every day (PEG-1D) or every two days (PEG-2D). The third group of goats was supplemented with 50 g of ground barley grain without PEG serving as a control treatment (CTL).

Before the commencement of the experiment, the animals received on a daily basis oat hay ad libitum and 200 g barley grain. Fresh water was continuously available. Animals were adapted to treatments for 13 days and to metabolism cages for 3 days before the 8-days total collection period started. Goats were weighed twice, at the end of the adaptation period and at the end of the trial. Each morning of the adaptation and the collection periods, goats received first the 50 g of ground barley grain supplemented or not with PEG then the foliage of Quercus coccifera was distributed to all animals ad libitum. Goats were offered Quercus coccifera at about 20% in excess of actual intake.

During the faecal collection period, samples of each kermes oak and barley were taken every day and bulked. Refusals and total daily faecal output were collected, weighted, sampled (20%), and bulked each day of the collection period. Faeces samples of each goat were pooled for the 8 days of collection period and pooled samples were stored at –5°C. Urine was collected daily in buckets containing 100 mL of 10% sulphuric acid (urine pH < 3). A proportion (2%) of the total urine collected daily from each goat was stored at –15°C. At the end of the collection period, daily urine samples were pooled for each animal and frozen at –15°C until analysed. Dry matter contents of feed offered, individual refusals and faeces were estimated after drying samples at 80°C for 48 h. Other samples were dried in a forced air oven (50°C) and ground to pass a through 1 mm-screen and stored until needed.

Clinical examination of goats (determination of respiratory, cardiac, and rumen contraction frequencies and body temperature) was monitored one day prior to the start of the experiment and at day 24 of the experiment. Blood samples were withdrawn in heparinised vaccutainer tubes from each animal a day prior to the start and on day 17 of the experiment just before morning meal. After centrifugation, plasma was stored at –20°C until assayed.

Laboratory analysis

Samples of feeds and individual refusals and faeces were analysed for dry matter (DM, Id 7.007), ash (ID 7.009) and crude protein (CP, ID 7.015) as per AOAC (2005). Neutral detergent fibre (NDF), in feed offered and refused and in faeces was determined according to Van Soest et al (1991). Acid detergent fibre (ADF) and acid detergent lignin (ADL, only in feed offered, were analysed as described by Robertson and Van Soest (1981) and Van Soest et al (1991). Minerals (Ca, K, Na, Mg, Fe, Zn, Mn and Cu) in feed were measured after ignition at 550°C for 6 h and absorbance was measured on atomic absorption spectrophotometer (Unicam 919). Phosphorus (P, ID 7.128) in feed was analysed by a calorimetric method, following ashing at 550 °C and HCl digestion (AOAC 2005). Total extractable phenols and tannins and condensed tannins (butanol procedure) in Quercus coccifera foliage were determined in aqueous acetone (70:30, acetone: distilled water) extracts as described by Makkar (2000). Total nitrogen (ID 7.015) in urine samples was determined by Kjeldahl procedure (AOAC 2005). Urinary allantoin was used as an indicator of microbial nitrogen synthesis (Chen et al 1992).

Plasma samples collected after blood centrifugation were analysed for urea and creatinine using Vitalab Flexor auto-analyser and kits.

Statistical analysis

Data on feed intake, digestibility, nitrogen balance and blood metabolite profile were subjected to analysis of variance using the following general linear model (GLM) of SAS (2013, Version 9.4).

Yi = µ + Di + ei

Where Yi is the individual observations, µ the overall mean, D the average effect of dietary treatment and e the unexplained variation assumed normally and independently distributed. Where the F-test was significant, treatment means were compared using Duncan’s Multiple Range Test.

Results

Composition of feed

The fibre content (NDF and ADF) of Quercus coccifera L. foliage was high, while crude protein content was low (Table 1). Total phenols, total tannins and condensed tannins are relatively high in the foliage of this shrub species averaging 66.0 and 60.2 g eq tannic acid/kg DM and 75.1 g eq leucocyanidin/kg DM, respectively. The ratio of calcium to phosphorus was 0.82.

Feed intake and diet digestibility

Feed intake and apparent digestibility of diets are reported in Table 2. Daily DM intake of Quercus coccifera ranged between 60.3 and 62.4 g/BW ^0.75. It was not affected by the frequency of PEG supply. Referring to the control diet, daily supply of PEG was associated with the highest crude protein digestibility. It is important to note that this increase was not maintained when PEG was provided at 2 day-intervals. The effect of PEG supply on digestible crude protein intake was similar to that noted for CP digestibility (Table 2).

Nitrogen balance, microbial activity and growth rate

Goats in each dietary treatment consumed similar amounts of nitrogen (Table 3). The nitrogen balance indicates a trend for increased N retention in goats given 10 g of PEG daily. The same level and frequency of PEG supply led to a decrease in faecal N.

Daily provision of 10 g of PEG tended (p=??) to increase allantoin excretion in urine when compared to the control diet. Over the 24 days of this experiment, all goats lost weight. The greatest weight loss was recorded in those animals maintained on control diet (Table 3).

Plasma urea and creatinine and clinical parameters

Referring to initial measurements done the day before the start of this experiment; the concentrations of urea and creatinine in goat plasma increased after 17 days of the beginning of the experiment (Table 4). There were no differences between animals fed the three experimental diets with regards to the above mentioned blood metabolites. Conversely, plasma urea concentration had doubled with the daily administration of 10 g PEG in goat diets.

Clinical examination performed on day 24; at the end of the experiment; showed that respiratory frequency ranged between 14 and 16 cycles/min. Cardiac frequency was in the range of 95-111 beats/min. The rate of rumen contractions varied between 3 and 4 cycles / 5 min (Table 4). When compared to clinical parameters obtained before the start of the trial, we noted an increase of the cardiac frequency, while respiratory and rumen contraction frequencies decreased irrespective of the nature of the diet.

There was no consistent effect of PEG on the level of plasma creatinine. However, 17 days after the start of the trial, urea plasma concentrations of goats fed the PEG-1D experimental diet increased noticeably when compared to the control diet.

Discussion

Composition of feed

The CP content of Quercus coccifera foliage was relatively low (75 g / kg DM). Data reported by Ben Salem et al (2003; 2005) indicate that CP content varied from 62 to 81 g / kg DM depending on the season during which the kermes oak is harvested (i.e June vs March-April). Tsiouvaras (1987) reported that the crude protein content of this shrub specie varied over the four seasons between 71 and 78 g / kg DM while Khazaal et al (1993) reported a decrease in crude protein content of Quercus coccifera foliage associated with an increase in total extractable condensed tannins from summer to autumn. In this experiment, condensed tannins concentrations were comparable to those reported by Ben Salem et al (2003) and Khazal et al (1987).

Feed intake and diet digestibility

PEG had no effect on the intake of Quercus coccifera by goats. Similar trends were observed with other tanniniferous fodder shrubs like foliage of Acacia cyanophylla (Ben Salem et al 1999) and fruits of Acacia nilotica (Tshabalala et al 2013). Conversely, Silanikove et al (1997) demonstrated that a PEG to tannins ratio ranging between 1/4.0 and 1/8.0 tended to improve the ingestion of diets composed of tannin-rich forage species.

In agreement with Ben Salem et al (2003; 2005) the main effect of PEG was an increase of the availability of nitrogen in Quercus coccifera-based diet. Daily provision of 10 g PEG to goats substantially increased the digestible CP intake and digestibility. It would appear that condensed tannins had interacted with PEG, thus releasing protein from the tannin-protein complex and rendering them available for ruminal microorganisms (Reed 1995). None of these effects was maintained when PEG was given to goats at 2-day interval instead of daily administration. Our results contrast with the findings of Ben Salem et al (2005) who demonstrated that the slight increase of the nitrogen value of the diet obtained on goats supplemented daily with PEG persisted with the discontinuous supply of PEG at 2-day interval. These differences may be ascribed to different levels of PEG used (i.e. 10 vs. 20 g). Condensed tannins were a causative factor of the poor utilisation of the nitrogen of this woody species by goats. Since the positive effect of PEG resulted in an improvement of nitrogen value of the experimental diets but it didn’t affect neither OM nor NDF digestibility of the diet, we can hypothesise that Quercus coccifera-tannins don’t bind to a high degree to carbohydrate and cell walls. Barry et al (1986) demonstrated that PEG supply didn’t affect digestibility of cellulose and hemicellulose in sheep given a tanniniferous forage species, i.e. Lotus pedunculatus, while Nastis and Malechek (1981) reported that Quercus gambelli -tannins affected negatively NDF digestibility of the diet. However, all these effects would depend mainly upon the level and biological activity of tannins and the degree of maturity of the plant species (Makkar et al 1991).

Nitrogen balance, microbial activity and growth

When expressed as percentage of N intake, positive N balance was obtained only when 10 g PEG was provided daily. Other data seem to indicate that excessive consumption of condensed tannins in shrub species reduced considerably the whole tract apparent digestibility and increased faecal nitrogen losses by sheep but reduced urinary nitrogen losses (Barry et al 1986). Similar increase of the diet CP digestibility recorded in the current experiment was obtained when PEG was added to tannin-rich diets (Kebede et al 2014; Yisehak, et al 2016). Obviously in this experiment, clear conclusions are not possible since trends in decreasing faecal N losses obtained by a daily supply of 10 g PEG didn’t reach statistical significance and urinary losses were similar for the three experimental diets.

Allantoin is a major component among purine derivatives and its concentration in urine had been used to predict the microbial N supply (Ben Salem et al 2000). Ben Salem et al (2005) noted an increase of urinary excretion of allantoin following PEG supply to goats fed on Quercus coccifera-based diets, indicating an increased availability of nitrogen in the rumen. In the current experiment, daily provision of 10 g PEG tended to increase the urinary excretion of allantoin.

The positive effect of PEG on the nitrogen retention did not impact on goat growth. Goats were losing weight throughout the experiment irrespectively of the diet. Conversely, Yisehak et al (2016) showed that addition of PEG as a tannin binder improved digestion and growth performance in goat fed tannins-rich diets.

As suggested by previous studies, it appears that tannins may not be the unique constraint to an optimal valorisation of the foliage of Quercus coccifera by animals (Ben Salem et al 2003; 2005). Low contents of nitrogen and high content of lignin act in concert with tannin content to limit efficient ruminal activity and optimal digestion of Quercus coccifera by goats. It was suggested that the positive response of the animal to tannin-rich diets could be explained by the higher CP and lower NDF contents combined with a lower protein-precipitation capacity of the tannins (Stewart et al 2000).

Concentration of urea, creatinine and clinical measurements

The increase of urea concentration in goat plasma could be attributed to the administration of PEG. Indeed, PEG binds strongly to tannins and this allows the release of proteins from tannin-protein complexes, hence becoming more available for ruminal microflora (Hagerman et al 1981). Ben Salem et al (2005) found an increase of urea levels in the serum of goats given Quercus coccifera and PEG-containing concentrate. Urea concentrations in goats receiving daily PEG exceeded the normal values (73.9 versus 11-17 mg/mL) (Jaziri 1985). Urea concentrations depend to a large extent on protein digestion (Ostrowski et al 1989). Finco and Duncun (1976) suggested that the increased urea concentration in blood reflects a high protein catabolism rather than a decrease of its clearance via rumen and kidneys. Plasma concentrations of creatinine of goats used in the current experiment were within the normal range reported by Jaziri (1985) for local goats (0.3 to 1.42 mg/100 ml). Based on creatinine concentrations obtained in our experiment, we can postulate that kidney function was not seriously hampered by tannin rich-diets or at least that loss of glomerular function didn’t exceed 75% of the total nephrons. Such finding provides further evidence that the tannins in Quercus coccifera affect urea metabolism in goats through their interactions with proteins rather than their nephrotoxic properties. The probable renal damage caused by the consumption of tannins may be partial and further specific studies to investigate the effects on kidneys are needed (Ben Salem et al 2003).

The general health status of goats before the start of this experiment was good but their condition was impaired seriously during the experimental period. Goats showed a decrease of ruminal activity, heart and respiratory rates and rectal temperature. Such impairments were reported when Quercus coccifera foliage was given as sole diet to goats by Ben Salem et al (2003). In another experiment reported in the literature, goats consuming diets rich in condensed tannins, did not show clinical signs of ill health or signs of tannin toxicity (Olafadehan 2011).

In the current experiment, we noticed an oliguria that might be attributed to a decrease in glomerular filtration rate caused by ischemia and the nephrotoxic nature of tannins and their metabolites (Shi 1988). A loss of hair was also observed in this experiment. These results are in line with previously reported data, which revealed that the growth of wool on sheep is impaired by tannin-rich diets (Barry 1985). It would appear that this is linked to a deficit of methionine excessively used to detoxify tannins through the hepatic methylation process (Ben Salem et al 2005).

Conclusions

• It is concluded that the nutritive value of Quercus coccifera foliage is low and cannot even provide the maintenance requirements of male goats.
  
  
• PEG supplied either on daily basis or at 2-day interval failed to overcome the body weight losses and the observed general impairment of the goats’ health.
  
  
• This would support our hypothesis that tannins in this shrub cannot be pinpointed as the unique factor associated with the reported adverse effects on body weight and health of the animals.
  
  
• Other factors e.g. low true protein provision and a low energy intake could be the causes of the poor performance of goats used in this experiment.
  
  
• Such findings should be integrated in the design of improved management systems for extensive goat farming in the shrubby woodlands of Northern Tunisia and other similar ecosystems in the Mediterranean.
  
  
• It also raises original queries on the interactions between nutrition and health in systems where animals thrive on naturally occurring shrubs.

Conflict of interest

The authors declare that they have no conflict of interest.

Acknowledgements

This study was supported by the International Atomic Energy Agency as part of the research contract IAEA-INRA Tunisia (TUN11672 - Tannins levels in local feed sources and development of strategies to reduce their negative effects and valorisation).

References

AOAC 2005 Official methods of analysis. Association of Analytical Chemists, 18th edition. Washington, DC,USA.

Barry T N 1985 The role of condensed tannins in the nutritional value of Lotus pedunculatus for sheep 3-Rates of body and wool growth. British Journal of Nutrition 54: 211-217. https://www.cambridge.org/core/services/aop-cambridge-core/content/view/A890B2B44B1CDE52657D87ED439B6C4E/S0007114585000253a.pdf/role_of_condensed_tannins_in_the_nutritional_value_of_lotus_pedunculatus_for_sheep.pdf

Barry T N Manley T R and Duncan S J 1986 The role of condensed tannins in the nutritional value of Lotus pedunculatus for sheep 4-Sites of carbohydrate and protein digestion as influenced by dietary reactive tannin concentration. British Journal of Nutrition 55: 123-137. https://www.cambridge.org/core/services/aop-cambridge-core/content/view/6C0C9373D06ABA14B0ED48400EB75140/S000711458600017Xa.pdf/role_of_condensed_tannins_in_the_nutritional_value_of_lotus_pedunculatus_for_sheep.pdf

Ben Salem H, Nefzaoui A, Ben Salem L and Tisserand J L 1997 Effects of Acacia cyanophylla Lindl. Foliage supply on intake and digestion by sheep fed lucerne hay-based diets. Animal Feed Science And Technology 68: 101-113. https://ac.els-cdn.com/S0377840197000151/1-s2.0-S0377840197000151-main.pdf?_tid=034984c8-239c-4295-bea6-8dc65ff6eda3&acdnat=1539088863_d1667788edf55be740e440193c9fedc7

Ben Salem H, Nefzaoui A, Ben Salem L and Tisserand J L 1999 Different means of administrating polyethylene glycol to sheep: effect on the nutritive value of Acacia cyanophylla Lindl. foliage. Animal Science 68: 809-818.

Ben Salem H, Nefzaoui A, Ben Salem L and Tisserand J L 2000 Deactivation of condensed tannins in Acacia cyanophylla Lindl. foliage by polyethylene glycol in feed blocks. Effects on feed intake, diet digestibility, nitrogen balance, microbial synthesis and growth by sheep. Livestock Production Science 64: 51–60.

Ben Salem H, Atti N, Priolo A and Nefzaoui A 2002 Polyethylene glycol in concentrate or feed blocks to deactivate condensed tannins in Acacia cyanophylla Lindl. foliage. 1. Effects on intake, digestion and growth by Barbarine lambs. Animal Science 75: 127-135.

Ben Salem H, Ben Salem I, Nefzaoui A and Ben Said M S 2003 Effects of PEG and olive cake feed blocks supply on feed intake, digestion, and health of goats given kermes oak (Quercus coccifera L.) foliage. Animal Feed Science and Technology 110: 45 -59. https://ac.els-cdn.com/S0377840103002153/1-s2.0-S0377840103002153-main.pdf?_tid=a5e4f1a0-07f7-4791-a25f-804f90cae680&acdnat=1539088995_d02bcfbf6489fd9ff4288304d10cb8a8

Ben Salem H, Ben Salem I and Ben Said M S 2005 Effect of the level and frequency of PEG supply on intake, digestion, biochemical and clinical parameters by goats given kermes oak ( Quercus coccifera L) based diets. Small Ruminant Research 56: 127-137. https://ac.els-cdn.com/S0921448804001178/1-s2.0-S0921448804001178-main.pdf?_tid=bedd2d93-7696-4c5d-bfb2-18612fa38b95&acdnat=1539089039_af735021e26ff66c465d5482a8a2e68b

Chen X B and Gomes H J 1992 Estimation of microbial protein supply to sheep and cattle based on urinary excretion of purine derivatives- an overview of the technical details. International Feed Resources Unit. Rowett Research Institute, Aberdeen, Occasional publication, 1-20.

Filippich L J, Zhu J and Alsalami M T 1991 Hepatotoxic and nephrotoxic principles in Terminalia oblongata. Research in Veterinary Science 50: 170-177. https://ac.els-cdn.com/003452889190101S/1-s2.0-003452889190101S-main.pdf?_tid=ff0b6f9c-2fdd-4480-b07b-9294d6f82a4b&acdnat=1539089089_6638530a7c62e3d01ac917e2f45961b3

Finco D R and Duncun J R 1976 Evaluation of blood urea nitrogen and serum creatinine concentrations as indicators of renal dysfonction: a study of 111 cases and a review of related literature. Journal of the American Veterinary Medical Association 234: 3014-3016.

Frutos P, Hervás G, Giráldez F J and Mantecón A R 2004 Review. Tannins and ruminant nutrition. Spanish Journal of Agricultural Research 2: 191-202.

Hagerman A E and Butler L G 1981 The specificity of proanthocyanidin-protein interactions. Journal of Biological Chemistry 256: 4494–4497.

Jaziri F 1985 Contribution à l’étude de quelques paramètres biochimiques chez la chèvre de race locale en Tunisie. Thèse Doctorat Médecine Vétérinaire. Ecole Nationale de Médecine Vétérinaire de Sidi Thabet.

Jean-Blain C 1998 Aspect nutritionnels et toxicologiques des tanins. Revue de Médecine Vétérinaire 149: 6911-920.

Jones W T and Mangan J L 1977 Complexes of condensed tannins of sainfoin (Onobrychis viciifolia Scop.) with fration –1 leaf proteine and with submaxillary muccoprotein, and their reversal by polyethylene glycol and pH. The Journal of the Science of Food and Agriculture 28: 126-136.

Kebede B, Kechero Y and Beyene A 2014 Polyethylene glycol improves the utilization of a high tannin forage in sheep. Livestock Research for Rural Development. Volume 26, Article #214. Retrieved October 9, 2018, from http://www.lrrd.org/lrrd26/12/kebe26214.html

Khazaal K, Markantonatos X, Nastis A and Ørskov E R 1993 Changes with maturity in fibre composition and levels of extractable polyphenols in Geek browse: effects on in vitro gas production and in sacco dry matter degradation. Journal of the Science of Food and Agriculture 63: 237-244.

Landau S, Silanikove N, Nitsan Z, Barkai D, Baram H, Provenza F D and Perevolotsky A 2000 Short-term changes in eating patterns explain the effects of condensed tannins on feed intake in heifers. Applied Animal Behaviour Science 69: 199-213.

Makkar H P S 2000 Quantification of tannins in tree foliage. A laboratory manual for the FAO/IAEA co-ordinated research project on the use of nuclear and related techniques to develop simple tannin assays for predicting and improving the safety and efficiency of feeding ruminants on tanniniferous tree foliage. FAO/IAEA Working Document, IAEA, Vienna, p. 38.

Makkar H P S 2003 Effects and fate tannins in ruminant animals, adaptation to tannins, and strategies to overcome detrimental effects of feeding tannin-rich feeds. Small Ruminant Research 49: 241-256. https://ac.els-cdn.com/S0921448803001421/1-s2.0-S0921448803001421-main.pdf?_tid=658bcf22-a28c-40ba-ade1-b4ac4c2cda1f&acdnat=1539089220_17894faf3bb842de0354b3d24b648e2c

Makkar H P S, Dawra R K and Singh B 1991 Tannin levels in leaves of some oak species at different stages of maturity. Journal of the Science of Food and Agriculture 54: 513–519.

McNeill D M, Komolong M K, Gobius N and Berber D 1999 Influence of dietary condensed tannin on microbial crude protein supply in sheep. In “Proceedings of the International Workshop on Tannins in Livestock and Human Nutrition”. (Ed. Brooker JD) pp. 57–61, Adelaide, Australia, 31 May–2 June. ACIAR Proceedings No. 92171, Canberra.

Min B R, Solaiman S, Gurung N, Behrends J, Eun J S, Taha E and Rose J 2012 Effects of pine bark supplementation on performance, rumen fermentation, and carcass characteristics of Kiko crossbred male goats. Journal of Animal Science 90: 3556-3567.

Nastis A S and Malechek J C 1981 Digestion and utilisation of nutriments in oak browse by goats. Journal of Animal Science, 53: 283-289.

Olafadehan O A 2011 Changes in haematological and biochemical diagnostic parameters of Red Sokoto goats fed tannin-rich Pterocarpus erinaceus forage diets. Veterinarski arhiv 81, 471-483.

Ostrowski S R, Smith B P, Spier S J, Norman B B and Oliver M N 1989 Compensatory weight gain in steers recovered from oak bud toxicosis. Journal of the American Veterinary Medical Association 195: 481-484.

PapachristouT G and Nastis V P 1992 Feeding behaviour of goats in relation to shrub density and season of grazing in Greece. World Review of Animal Production 27: 68-71.

Reed J D 1995 Nutritional toxicology of tannins and related polyphenols in forage legumes. Journal of Animal Science 73: 1516-1528.

Robertson J B and Van Soest P J 1981 The detergent system of analysis. In “The Analysis of Dietary Fibre in Food”. (Eds James WPT, Theander O) pp. 123–158 Marcel Dekker, New York.

Shi Z C 1988 Identification of the phenolic substances in bovine urine associated with oak leaf poisoning. Research in Veterinary Science 45: 152-155.

Silanikove N, Gilboa N and Nitsan Z 1997 Interaction among tannins, supplementation and polyethylene glycol in goats given oak leaves: effects on digestion and food intake. Animal Science 64: 479-483.

Statistical Analysis System (SAS) 2005 Users Guide: Statistics Version 9.4 5th Edition. Cary, N.C: SAS Institute. Inc.

Stewart J L, Mould F and Mueller-Harvey I 2000 The effect of drying treatment on the fodder quality and tannin content of two provenances of Calliandra calothyrsus Meissner. Journal of the Science of Food and Agriculture 80: 1461-1468.

Tshabalala T, Sikosana J L and Chivandi I E 2013 Nutrient intake, digestibility and nitrogen retention in indigenous goats fed on Acacia nilotica fruits treated for condensed tannins. The South African Journal of Animal Science 43, 457-463

Tsiouvaras C N 1987 Ecology and management of kermes oak (Quercus coccifera L.) shrublands in Greece: a review. Journal of Range Management 40: 542–546.

Van Soest P J, Robertson J B and Lewis B A 1991 Methods for dietary fibre, neutral detergent fibre, and nonstarch carbohydrates in relation to animal nutrition. Journal of Dairy Science 74: 3583–3597. https://ac.els-cdn.com/S0889157515000216/1-s2.0-S0889157515000216-main.pdf?_tid=3db70a51-8fcb-4887-9d5b-daf1e2388d1e&acdnat=1539091282_993b242a1f99974e349c5e6fc0b2376f

Waghorn G C, Shelton I D and McNabb W C 1994 Effects of condensed tannins and the nutritive value of herbage. Proc. N. Z. Grasslands Assoc 51: 171-179.

Yisehak K, Kibreab Y, Taye T,Lourenço M R A and Janssens GPJ 2016 Response to dietary tannin challenges in view of the browser/grazer dichotomy in an Ethiopian setting: Bonga sheep versus Kaffa goats. Tropical Animal Health and Production 48: 125–131. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4710639/pdf/11250_2015_Article_931.pdf

Received 10 October 2018; Accepted 16 October 2018; Published 1 November 2018

Go to top