Effects of ensiled cassava (Manihot esculenta) foliage compared to a soybean meal supplement on gastrointestinal nematode infections in goats

Seng Sokerya, Chadrawathani Phanchadcharam*, Morn Suy and J Höglund**

Center for Livestock and Agriculture Development (CelAgrid), Cambodia, P.O. Box 2423, Phnom Penh 3, Cambodia
ssokerya@celagrid.org
* Veterinary Research Institute, 59, Jalan Sultan Azlan Shah, 31400, Ipoh, Perak, Malaysia
** Department of Biomedical Sciences and Veterinary Public Health, Section for Parasitology (SWEPAR), Swedish University of Agricultural Sciences, S-750 07 Uppsala, Sweden

Abstract

Twenty four 4-6 months-old male goats weighing 15.2 ± 2.8 kg, were randomly allocated acrding to their live weight (LWt) into three treatments to investigate the effects of cassava foliage silage (CaS) on the level of gastrointestinal (GI) nematode parasites. One group of individually penned goats was fed CaS ad libitum for 10 weeks. A second group was fed grass only (CTL) and a third group given grass supplemented with 50 g urea molasses plus 200 g soybean meal/head/day (UM). At the start of the experiment, all goats were inoculated with 3,000 third-stage GI nematode larvae (L3).

There was a significant difference in cumulative live weight (LWt) among the three treatments (p < 0.001): all 8 CaS and 6 of the UM goats gained weight (average daily gain was 60.4 and 6.7 g/day, respectively), whereas goats in CTL lost weight (-6.1 g/day). The nematode faecal egg counts (FEC) in the CTL and UM groups fluctuated between 1,000 epg after three weeks of L3 infection to 2,500 epg at the end of the trial, while the FEC of the CaS goats remained below 200 epg throughout the experiment (p < 0.001). At the end of the experiment, the CaS and UM groups had 28% and 26% blood packed cell volume (PCV), respectively, which was significantly higher than the 21% in the CTL group (p £ 0.001). The majority (30-78%) of the adult worms identified at slaughter was Haemonchus contortus, followed by Trichostrongylus colubriformis (20-48%), T. axei (2-17%) and a small number of Strongyloides spp. (< 5%). compared to CTL and UM, the CaS goats had lower total worm burdens (p < 0.05) and numbers of Haemonchus contortus (p £ 0.001).

It is evident that the goats fed ensiled cassava foliage were more resilient and resistant to GI nematode parasitism, and in particular to Haemonchus contortus, compared to those only given protein supplementation.

Keywords: Anthelmintic efficacy; cassava foliage silage; protein supplementation; goats; haemonchus contortus; parasite control

Introduction

Gastrointestinal (GI) parasitism is a major problem in small ruminant production worldwide, due to its impact on animal health and productivity and the associated costs of control measures (Sykes 1994; Knox et al 2006). The problem is of particular importance in the developing world, where the nutritional resources available for ruminant livestock often are inadequate (Devendra 2000). As a consequence, acquired immunity is often compromised, resulting in lowered productivity and increased mortality (Knox and Steel 1996; Perry et al 2002). The nutritional status of the host has a significant effect on its ability to withstand parasite infection, and it has also been frequently observed that the mortality resulting from GI nematodes is more severe in malnourished animals than in well-nourished animals (Coop and Kyriazakis 1999). Manipulation of host nutrition to combat GI nematodes has been suggested as one of the promising options for sustainable control, and to reduce the dependence on conventional chemotherapy (Coop and Kyriazakis 2001; Kyriazakis and Houdijk 2006; Patra 2007 and Hoste et al 2008).

Cassava (Manihot esculenta) is a tropical crop grown for the roots, which commonly are used as a food for humans. Recently, several studies have been undertaken in the Southeast Asia on the possibility of using cassava leaves/foliages, which is a by-product after root harvesting, as a feed resource for small ruminants (Seng and Rodriguez 2001; Van et al 2001 and Nurulaini et al 2007). AFRIS (2004) reported a crude protein (CP) content of cassava leaves in the range of 22–29% of dry matter (DM), whereas Seng et al (2001) showed that the foliage contained 21–24% CP. Cassava leaves have also been reported to have a high essential amino acid content, comparable to soybean meal (Eggum 1970). For practical conditions, ensiling forage to preserve it as feed for animals is often recommended (McDonald et al 1991). An advantage of this method is that plant materials can be ensiled at any time of the year, even when weather conditions are not suitable for sun-drying. The ensiling process ensures not only increased shelf life and microbiological safety, but also makes most food resources more digestible (Caplice and Fitzgerald 1999). It has also been shown that fermentation of cassava leaf and foliage reduces toxicity levels of anti-nutritional and chemotoxic substances like hydrocyanic acid (HCN) (Chhay and Rodriguez 2001 and Sokerya et al 2009).

Previous studies showed that feeding fresh cassava foliage to penned goats decreased the faecal egg counts (FEC) of GI nematode parasites (Seng and Preston 2003 and Seng et al 2007). Also the combined results of Ho and Preston (2006) and Sokerya et al (2009) suggested that ensiled cassava foliage gave better effects on growth and parasite control compared to when it was given as hay or as fresh foliage. These observations have encouraged further research on how the ensiled cassava foliage provides improved efficiency of parasite control. We hypothesized that if the effect was solely due to the improved protein content of the ensiled cassava, then similar results would be expected in goats fed on a diet containing equivalent levels of crude protein. The aim of the present study was to investigate the effects of CP in ensiled cassava foliage on GI nematode parasites in young goats by comparing live weight (LWt) gains, FEC and total worm burdens (TWB) at slaughter, in an ensiled cassava foliage fed group and in a control group supplemented with protein from soybean meal in combination with urea molasses.

Materials and methods

Experimental design

This study was carried out at the experimental farm of the Center for Livestock and Agriculture Development (CelAgrid) located in Kandal Province, 25 km southwest of Phnom Penh, the capital of Cambodia. Twenty four male goats, with an average initial weight of 15.2 ± 2.8 kg and aged between 4 and 6 months were acquired from local farmers. On arrival at the research farm, they were individually housed in pens with raised slatted floors, and adapted to pen feeding. Subsequently, each goat was treated with a subcutaneous injection of ivermectin (Ivomec® Merial, New Jersey, USA), with a dosing rate of 200 µg/kg body weight, to remove previously acquired nematode infections. A repeated dosing was given 5 weeks later for 15 goats that still had positive FECs, to ensure the complete removal of previously acquired nematode infections. After an additional 6 weeks the goats were randomly allocated in to three experimental groups based on their LWt, consisting of 8 animals each. These treatments were:

•  CTL: control – fed grass (ad libitum)

• UM: fed grass (ad libutum) + 50 g of urea molasses (UM) and 200 g of roasted soybean meal/head/day

• CaS: fed cassava foliage silage (ad libitum)

At the start of the experiment, all goats were infected with nematode larvae from faecal cultures obtained from naturally infected goats collected from nearby small-holder farms in Kandal Province. Incubating and harvesting of the infective larvae were according to established methods (Anonymous 1986). Each goat received a total of 3,000 third-stage nematode infective larvae (L3), administrated as three doses of 1,000 larvae for three consecutive days. There was a repeated dosing for three goats in the CaS group that appeared to have negative FECs 4 weeks post L3 inoculation. The experimental feeding was started after the last day of the initial L3 inoculation and was continued for further 10 weeks and 14 weeks for the three goats in CaS group.

Feeds and feeding

Feed rations were provided in a daily amount equivalent to approximately 4% DM of LWt for each goat. The daily ration was divided, and offered twice a day (at 8:30 and 15:00-h). Wheat bran (200 g/head/day) was given to all groups as an additional energy source, and was given in the afternoon. A monoculture of paragrass (Brachiaria mutica) was used as the grass source, and was collected from an area kept free from livestock grazing, or their faecal contamination, throughout the duration of the study. The cassava silage consisted of sun-wilted (3–4 hours) foliage, which was mixed with 5% of sugar palm syrup (raw sugar palm diluted in water at 1:1) and thereafter stored anaerobically (in sealed plastic bags) for at least 21 days prior to feeding to the goats. The urea molasses was comprised mainly of rice bran, sugar palm syrup and urea according to Seng et al (2001).

Measurements of animal performance and parasitology

Individual LWt of the goats was measured, and blood and faecal samples were collected, at weekly intervals. Nematode FECs were estimated using the McMaster standard procedure (Hansen and Perry 1994) with a detection level of 50 eggs per gram faeces (epg). The red blood packed cell volume (PCV) was determined using the micro-hematocrit method. At the end of the experiment, all goats were slaughtered and the abomasum and small intestine of each goat was removed for worm recovery, identification and enumeration of GI parasites as described by Hansen and Perry (1994).

Dietary measurements

The amounts of feed offered to, and rejected by the animals were recorded daily. Representative samples were taken every two weeks for determinations of DM (Undersander et al 1993), ash, nitrogen (N) and crude fibre (CF) content (Anonymous 1990).

Data analysis

Data collections started from the latest L3 inoculation of every goat, adjusted as week 0, and lasted for 10 weeks afterward.

All data were subjected to statistical analysis using MINITAB 13.31 software (2000). Data of FECs were, according to the sensitivity of the McMaster method, transformed to log(y+50) prior to statistical analysis. The effects on the dependent variables FEC, PCV and LWt were analysed using a Generalized Linear Model (GLM) with the initial values of these factors as covariates, or the treatment and time (length of experiment) effects and their interaction as the models. Regression coefficients of LWt over time were calculated for each goat to obtain the average daily weight gain (ADG). The differences between treatments for ADG and TWB at the end of the experiment and feed intake over 10 weeks were subjected to GLM analysis with treatment as the only effect. When the differences in treatment means were significant at the probability level of p < 0.05, the means were compared by using Tukey's pair-wise test.

Results

Feed characteristics

The nutritive values of the feed components used in the experiment are shown in Table 1.

The DM contents of the residual materials were lower than that offered initially, which is a direct result of the dehydration during 24 hours before replacing the diet on the following day. Similarly, the CP contents of the residues were lower, as the goats primarily selected the young or leafy parts of both foliages (cassava and grass), which contain more protein than the stem or fibrous part.

Feed intake and growth performance

Feed intakes throughout the experiment fluctuated around 500 g/day and 600 g/day for CTL and UM goats, respectively. In most of the CaS goats the feed intake decreased from » 800 g/day to » 600 g/day during week 3-5. Both CTL and UM had lower DM and CP intake of forage than CaS. Although the CTL group consumed higher amounts of wheat bran as compared to UM, they still had the lowest total DM and CP intakes, as the UM was in addition supplemented with urea molasses and soybean meal (Table 2).

The goats in CaS consumed only a slightly higher amount of CP than the UM goats, although the difference was significant. However, they had higher LWt than the UM and CTL goats over the 10 weeks of experiment (4 kg, 1 kg and -1 kg for CaS, UM and CTL, respectively). There was a significant difference among the cumulative LWt of the three treatment groups throughout the experimental period (p < 0.001), with no significant interactions between treatments and time. Five out of 8 goats in the CTL group lost weight throughout the experimental period, while all the CaS goats steadily increased in weight after 5 weeks of the experiment.

Faecal egg counts

The FECs differed between groups already after three weeks, when both UM and CTL groups had an average of approximately 1,000 epg, whereas the count was only 200 epg in the CaS group (Figure 1).

Then there was a stable trend of increasing FECs in the UM and CTL groups between week 3 and 5, followed by a sudden rise in CTL up to a maximum of 3,000 epg between week 6 and 7. Subsequently, the FECs fluctuated from week to week, and ended with a mean of 2,000 epg at week 10. From week 7 onwards, the UM group showed a regular increase in FECs, reaching » 2,500 epg at week 8, and with about the same count as CTL at the end. In contrast, the CaS group remained consistent, with no increase in mean FEC from the commencement until the termination of the trial, at » 200 epg (p < 0.001).

Blood packed cell volume

Almost all of the goats showed decreasing PCVs throughout the experimental period, with the exception of three goats in the CaS group (p < 0.005). There was no difference in the cumulative PCVs among the three treatments; however, the slope of PCVs over time showed a difference among the groups (p < 0.05). Starting with the same level of PCV of about 35% (p > 0.05), the Cas and UM groups had final PCVs of 28.4% and 26.1%, respectively, which were higher than the PCV level in the CTL group (21.5%, p £ 0.001).

Total worm burden

The worm species comprised of 30-78% Haemonchus contortus and about 10% Trichostrongylus axei in the abomasum. The main species in the small intestine was Trichostrongylus colubriformis (20-48%), with a low number of Strongyloides spp. (< 5%). The Haemonchus contortus population was significantly lower (p £ 0.001) in the CaS compared to the CTL and UM groups. However, there were no differences between the remaining worm species (Table 3).

The mean total worm count (TWC) was also somewhat lower in the CaS group (388 adult worms) commpared to UM (728) and CTL (820). However, the difference in TWC was mainly due to the variation in Haemonchus contortus, which constituted a large proportion of the total worm population.

Discussion

In this study we evaluated the antiparasitic effects of different crude CP supplements in pen-fed goats experimentally infected with GI nematode parasites, by measuring their performance together with parasitological responses. The animals were either fed on grass supplemented with soybean meal and urea molasses (UM) or were given a high-protein diet of ensiled cassava foliage (CaS). A third group fed on grass alone was included as an additional non-supplemented low-protein control group.

Effect of protein supplement on GI nematode infected goats

Although the voluntary protein intake from the supplementation of 200 g/day of soybean meal and 50 g urea molasses in the UM goats failed to reach the CP intake in the CaS group, it was almost twice as high as in the CTL goats. It seemed that the additional protein for the UM goats was just enough to maintain body growth, at the same time as this feed ration also compensated for the parasite-induced blood losses. These finding are basically in agreement with those of Wallace et al (1995), who showed that the PCVs in Haemonchus contortus challenged Hampshire Down lambs were improved if they were supplemented with soybean for 10 weeks. The goats that were supplemented with soybean meal in the present study gained weight, and they were also less anaemic than the animals that only received a basal diet of grass. However, no significant effect was observed in either mean worm burdens nor in FECs. Blackburn et al (1991) also found that a high plane of nutrition in growing kids had a positive effect on the resilience of growing goats to Haemonchus contortus. However, kids that were kept on a low plane of nutrition tended to carry larger numbers of worms, and they also achieved higher establishment rates. Similarly, Bricarello et al (2005) described the increased ability of lambs to withstand the pathophysiological effects of Haemonchus contortus on a high-protein diet that contained 240 g soybean meal per kg of diet. Although the increased levels of metabolised proteins in that study resulted in reduced FECs and TWCs, this was only observed in one (Santa Ines) of the two breeds that were tested. It is notable that the goats in the present study only received half the amount of urea molasses and soybean meal as in the study by Bricarello et al (2005). Even if the supplementation in the UM group failed to reduce the FECs and TWCs, the UM goats were still able to withstand the pathophysiological effects of nematode infection, indicated by their weight maintenance and improvement of PCV value by the end of experiment. This indicates that the resilience was affected in the UM goats. Also, Torres-Acosta et al (2004) demonstrated beneficial effects following supplementation with 100 g of soybean meal (26%) and sorghum meal (74%) in Criollo kids naturally infected with GI nematodes. It was shown that protein supplementation enhanced the resilience to parasite infection indicated only through increased weight gains and PCVs compared to the unsupplemented-control animals. However, as was observed in the UM group in the present study, no effect on host resistance was found. Similarly, in another follow up study, no difference in FECs among the supplemented and unsupplemented groups was found in infected kids (Torres-Acosta et al 2006).

To date there is increasing evidence to support the view that protein supplementation can reduce the level of gastrointestinal nematodes in growing small ruminants, particularly if given to otherwise malnourished animals during the later stages of infection at the phase of expression of immunity (Coop and Kyriazakis 1999). Irrespective of this we could not demonstrate any significant effect in the present study, either on FECs or TWCs between the UM and CTL groups. However, in most situations where the beneficial effect of protein supplementation has been demonstrated, the effect has not appeared earlier than 12-weeks following primary infection, whereas the current trial lasted for only 10 weeks. For example, Knox and Steel (1999) found that infected sheep supplied with urea showed reduced Haemonchus contortus FECs from week 10 onwards, whereas Trichostrongylus colubriformis was unaffected until week 19. Thus, in this experiment it is possible that the effect on parasites in the protein supplemented group would have been detected if the experiment had been extended for some additional weeks.

Effect of ensiled cassava foliage on GI nematode infected goats

Nutrient supplementation is a frequently recommended strategy that has been used to mitigate the negative consequences of pasture borne parasite infection in grazing sheep (Torres-Acosta and Hoste 2008). Although the exact mechanism has not been resolved, it is believed that the positive effect comes from an increased protein value in the diet acting on the host immune responses, which in turn will improve the resistance against the gastrointestinal nematodes. There is now increasing evidence showing that during periods of protein scarcity an increased supply of protein, from a wide range of sources, can indeed reduce gastrointestinal nematode parasitism in both growing and periparturient small ruminants (Kyriazakis and Houdijk 2006).

In this experiment, goats fed ensiled cassava foliage (CaS) had the highest DM and CP intake and the highest weight gains and PCVs, at the same time as their FECs and Haemonchus contortus numbers were significantly lower than the levels in the other groups. These results are in agreement with previous findings by Sokerya et al (2009), who showed that if goats are fed ensiled cassava foliage for 10 weeks this will improve the resilience and resistance to GI nematode parasites. The FECs reduction is supported by several other studies, as has been reported previously by Sokerya et al 2009. However, the “Haemonchus specific” effect indicated by the reduction of the actual worm count could not be just have been the result of protein consumption level, as it was not seen in the UM group. There is no simple explanation for this, but it may be related to the protein composition of cassava foliage in combination with the ensiling process, which possibly makes it different from the proteins in the supplement that was used in the UM group. Cassava leaves have a high CP content and almost 85% of the CP fraction is true protein (Ravindran 1993). Evidence for “bypass” protein characteristics in cassava leaves was reported by Ffoulkes and Preston (1978) who showed that fresh cassava leaves could completely replace soybean meal. Wanapat (2001) suggested that the condensed tannins contained in cassava leaves could have a potential role in forming tannin-protein complexes that escape rumen degradation to reach duodenal digestion. Alternatively, if ensiled cassava foliage contains any direct antiparasitic compound, as was suggested by the reduction of FECs and Haemonchus contortus population, this will allow the protein in the CaS treatment to be fully used for growth.

Feed intake and growth performance

Both CTL and UM goats had a lower forage intake than the CaS goats. This was most likely due to the high fiber content in grass (21%), which probably bulked the space of the rumen and thus reduced the total DM intake, compared to what was found in cassava foliage (13%). The DM and CP intakes, as well as the ADG of goats in both the CTL and CaS groups, were found to be more or less consistent with a previous experiment by Sokerya et al (2009). Goats on diet CaS had the highest DM, CP and ADG as compared to the other groups. The increase in feed intake and hence the growth of goats was reported when cassava hay (Dung et al 2005), fresh cassava (Seng and Preston 2003 and Ho et al 2003), wilted cassava (Phengvichith and Ledin 2007) and ensiled cassava foliage (Ho and Preston 2006), were supplemented to low quality feeds. Apart from the possible antiparasitic activity in cassava, it has also been reported that the CP intake stimulates the bacterial population in the rumen, thereby increasing the availability of fermentable nitrogen, and later contributing to an improved digestion of fibre in the rumen (Khang and Wiktorsson 2004).

Conclusions

• There are several factors that affect the nutrient utilization in parasitised host animals, which in turn will influence the resources allocated for animal productivity. In this study, ensiled cassava leaves feeding for 10 weeks resulted in lower FECs and Haemonchus contortus burdens in goats that were experimentally inoculated with mixed infections of gastrointestinal parasites. Although it seems likely that the effect was partly a result of a high nutrition level that most likely improved host immunity, there must have been other additional-unknown factors in the ensiling process of cassava foliage that acted in combination with the secondary metabolites to reduce the level of parasitism. Therefore, making silage to preserve the foliage produced as residue during cassava root harvesting would be worthwhile as a natural low-cost deworming agent alternative to the chemical anthelmintics used by small ruminant producers in the region. Accordingly, studies should be carried further to investigate the silage of other forages, and their effect on nematode parasite in comparison with cassava foliage.

Acknowledgments

The study was financed by the Swedish International Development cooperation Agency, Department for Research cooperation (Sida/SAREC), through the regional program Mekong Basin Animal Research Network (MEKARN). Research facilities were provided by the Center for Livestock and Agriculture Development (CelAgrid). We also acknowledge Ms Anna Rydzik, who helped us with the worm counting in this experiment.

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Received 4 April 2010; Accepted 18 April 2010; Published 10 June 2010

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