ANIMAL FEED XIENCE AND TECHNOLOGY Animal

Feed Science and Technology55 (1995) 153-160

Adding Jerusalem artichoke (Helianthus tuberosus L.) to weanling pig diets and the effect on manure composition and characteristics
E.R. Farnworth *, H.W. Modler, D.A. Mackie
Centre for Food and Animal Research, Agriculture and Agri-Food Canada, Ottawa, Ont., KlA 0C6, Canada

Received22 June 1994; accepted 31 January 1995

Abstract Seventy-two weanling pigs, 28 days of age, were fed diets containing 0, 1%. 3% or 6% Jerusalem artichoke (JA) meal for 4 weeks. Total feed consumed and feed efficiency were significantly (P < 0.059) affected by the addition of JA to the diet. The pigs eating the diets containing JA had significantly (P < 0.05) increased concentrations of six volatile fatty acids (VFA) in their manure; animals receiving the 3% JA diet had the highest VFA levels with the exception of valeric acid. The smell of fresh (less than 4 h) manure from the pigs eating 3% or 6% JA was significantly (P < 0.005) sweeter, less sharp and pungent (P < O.Ol), and had less of a skatole smell (P < 0.001) than pigs eating the 0% control diet. The manure from pigs eating JA was also judged to be lighter in colour with significantly (P < 0.001) more brown and green but less yellow colour.
Keywords: Jerusalem artichoke; Helianthus tuberosus; Manure; Odour

1. Introduction A diet that supplies nutrients to the host animal also nourishes intestinal micro-organisms that reside in the gastrointestinal tract of the animal (Savage, 1986). Many of the compounds found in manure are produced by microbial action on the food/digests as it passes through the animal. Changes in diet composition which affect this micro-organism population may result in changes in manure composition and characteristics, such as odour, that could be beneficial to the barn environment. The tuber of the Jerusalem artichoke (Heliunthus fuberosus L.) is rich in fructans (Incoll and Bonnett, 1993). In a variety of species, including man, the addition of fructans to the * Corresponding
author.

0377-8401/95/$09.50 0 1995 Elsevier Science B.V. All rights reserved SSDIO377-8401(95)00787-3

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diet has had beneficial effects on nutrition and metabolism (Farnworth, 1993). These changes have been attributed to the fact that feeding fructans to monogastric animals alters the intestinal bifidobacteriapopulation (Yazawaet al., 1978; Hidakaet al., 1986). Evidence to support this hypothesis comes from the findings that short chain fructooligosaccharides are bifidogenic factors (Modler et al., 1990), while many other common gut micro-organisms do not use these short chain fructans (Hidaka et al., 1986). Numbers of bifidobacteria are increased in humans and animals fed fructooligosaccharides (Hidaka et al., 1986; Farnworth et al., 1992). We produced a dried meal containing macerated Jerusalem artichoke tuber and fed it to pigs to determine its feeding quality and effects on manure composition and characteristics. The aim of this study was to determine whether adding Jerusalem artichoke to the diet affected pig growth and feed efficiency and changed the amount of volatile fatty acids in fresh pig manure. The odour and colour of the manure was assessed to determine whether components of the manure odour and colour changed in pigs eating diets containing Jerusalem artichoke.

2. Materials and methods

2.1. Animal, housing and husbandry

A total of 72 (Yorkshire/Landrace) pigs were obtained from the minimum disease, barrier maintained nucleus herd at the Greenbelt Farm of Agriculture and Agri-Food Canada, Ottawa. Males were castrated at 10 days of age. At weaning (age 28 days), pigs were moved and allowed a 5day adjustment period before starting the feeding portion of the experiment. The experiment was carried out in a barn fitted with four sealed rooms similar in size, volume, temperature, humidity, air exchanges; each room had separate ventilation. Each room contained a 4 X 4 raised flat deck cage that housed three pigs. The feeding trial was replicated five times. Pigs were weighed at the start of the experiment and then weekly. Pen feed consumption was measured weekly. Room temperature and humidity were recorded daily and pigs were checked daily for general health and signs of diarrhoea. The feeding trial lasted 28 days. The experimental protocol was approved by the CFAR Animal Care Committee. 2.2. Jerusalem artichoke meal and diets A meal containing Jerusalem artichoke tuber (varieties: Sunroot, Fusil) was prepared by combining equal weights of macerated (using a Fitzmill Model M cornminuting machine, W.J. Fitzpatrick Co., Chicago) newly harvested Jerusalem artichoke tuber and corn meal. The dried mixture was incorporated (weight for weight) into the swine starter diets in place of the corn component of the diet. The diets provided all known nutrients at or above requirement levels, and contained either 0 (control), 1, 3 or 6% Jerusalem artichoke on a dry matter basis (see Table 1 for nutrient analysis of diets). The control diet contained 44.1% corn, 15% barley and 25% soybean meal.

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2.3. Sample collection and chemical analyses Manure samples (uncontaminated by urine) were obtained from individual pigs at the end of the 4-week feeding trial while they were being weighed. Samples were kept frozen until analyzed. The fecal dry matter content was measured by freeze-drying 1 g samples for 3 days and measuring weight loss; no correction for loss of volatiles was made. The volatile fatty acid content of the manure (acetic acid, butyric acid, isobutyric acid, valeric acid and isovaleric acid) was measured using a water extraction and gas chromatographic determination using isocaproic acid as an internal standard (Erfle et al., 1979). pH of the water extract was also measured for each manure sample. 2.4. Sensory evaluation of manure Fresh manure samples were obtained from the pigs eating the control, 3% and 6% JA diets after they had consumed the diets for 4 weeks. Manure from individual pigs (within a diet) was pooled, homogenized and then divided into ten equal portions and placed in airtight containers. Odour evaluation was done immediately ( < 4 hours) after collection. Established methods of sensory analysis were applied to the sample (Poste et al., 1991). A trained panel of ten assessors evaluated the coded samples by comparison with reference standards (sweet, earthy, sour, sharp, and skatole), using a 15 cm unstructured line scale (anchored at 1.5 and 13.5 cm with slight and intense, respectively), and with one reference standard anchored at an agreed upon location. Numerical values were obtained for each sample by measuring the distance from the left end of the scale (0.0). The odour evaluation was done under red light. The panel rated the colour of the manure samples under white light in relation to colour chips designated as light, brown, green and yellow, again using a 15 cm unstructured line scale. Odour evaluation was done at the end of the five feeding replicates. 2.5. Statistical analyses Statistical tests were applied to the data to test for the effects of diet and replicate. Analyses of variance procedures were done using a statistical package available from the SAS company, Cary, NC (Statistical Analysis Systems Institute Inc., 1989). Linear and quadratic contrasts were applied because quantitative effects (level of Jerusalem artichoke in the diet) were being tested for.

3. Results and discussion The diet analysis data in Table 1 shows that dietary fiber made up approximately 17% of the diets. A detailed HPLC carbohydrate analysis indicated that sucrose was the sugar in highest concentration, followed by raffinose, fructose and glucose. However, hot water extracts of the JA diets also contained many peaks assumed to be progressively longer chained fructans (J. Mullin, unpublished data, 1995).

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Table 1 Composition of experimental diets containing Jerusalem artichoke ( JA)a Diet 0% JA Ashb Fatb Nitroge# Gross energy (ml kg- DM) Crude Sbei Acid detergent fibef Neutral detergent tibef Total dietary tibef 6.82 f 0.09 3.72 f 0.07 3.31*0.14 18.39*0.09 2.7 f 0.2 3.6f0.5 10.3 f 0.3 16.6 f 0.2 l%JA 6.2OYcO.15 3.75 f 0.08 3.35 kO.18 18.31 f0.18 2.7 f 0.2 3.4&0.2 12.1 f 1.5 _d 3% JA 7.31*0.10 3.76~0.04 3.27zbO.24 18.19*0.21 2.8 f 0.4 3.6f0.5 12.2 f 0.9 6% JA 7.15*0.04 3.61 f 0.03 3.3 1 f 0.09 18.08*0.16 2.6fO.l 3.8 kO.6 11.6* 1.8 17.4 f 0.06

Ash, fat, nitrogen and gross energy determined in lab; fibers analyzed by a commercial lab. As a percentage of dry matter (DM) Mean f standard deviation; analyses done in triplicate. d-, not determined.

Table 2 shows the body daily weight gain, feed consumption and feed efficiency of pigs fed the control and Jerusalem artichoke meal diets. The pigs did not show any aversion to the diets containing the Jerusalem artichoke meal; there were no health problems with any of the pigs, and the incidence of diarrhoea was similar in all groups. The largest average daily weight gain was recorded for the group eating the diet containing the 3% JA, although no statistical differences (P > 0.05) due to diet were found. The group fed the diet containing 6% JA had the lowest feed intake, and the best value for feed efficiency. Total feed consumed (on a pen basis) and feed efficiency had a significant (P < 0.05) quadratic relationship with
Table 2 Mean body weights, feed consumption and feed efficiencies of pigs eating experimental diets containing Jerusalem artichoke (JA) Diet Mean initial pig body Mean average daily weight (kg) weight gain (kg day- ) 0.522 f 0.06 0.514~0.08 0.533 kO.08 0.504 f 0.05 NS NS NS Total feed consumedb per pen (kg) Feed efficiencyC

0% JA 8.33 f 0.97 l%JA 8.07 f 1.60 3% JA 8.75 f 1.69 6% JA 8.2OkO.94 Significance of effects (P values)e Effect of diet NS Linear contrast Quadratic contrast

70.7*5.1 70.8 f 12.5 74.8 f 11.O 65.3f6.1 I NS *

0.62 f0.02 0.61 f0.03 0.60 f 0.02 0.65 f 0.05 NS NS

??

&Datafrom five replicates. 28 day feeding trial. Feed efficiency = individual pig body weight gain/ (pen feed consumption/3). dMean f standard deviation. NS, not significant,P>0.05; *, P<O.O5; **, P<O.Ol.

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Table 3 Volatile fatty acid content of manure from pigs fed experimental diets containing Jerusalem artichoke (JA) Volatile fatty acid Acetic Diet ( pmole g- I DM) O%JA(n=18) 148f 63 1% JA (n= 13) 173*34 3% JA (n= 17) 218+ 110 6% JA (n= 18) 182+60 Significance of effects (P values) ** Diet Linear NS If Quadratic Mean f standard deviation. NS,notsignificant,P>0.05; Propionic Butyric Isobutyric Valerie Isovaleric

56*20 72+21 92+53 63k23 1.1 NS *.*

60+19 72*31 93*45 69*29 ** NS ***

4.9 * 2.2 5.9k3.6 7.2 * 3.9 5.2 f 3.4

7.1 k3.9 10.2+4.8 11.9f6.2 15.1 * 10.9

9.3 +4.2 11.2k6.4 13.2k6.9 9.8 + 6.2

*
NS **

I
*** NS

I
NS **

*,P<O.l;

* ,P<O.Ol;

*,P<O.OOl.

diet. These results are consistent with those of Farnworth ( 1994) and reports in the Japanese literature on the beneficial effects of fructans (Neosugar) in swine diets (Nakamura, 1986; Fukuyasu and Oshida, 1986). Table 3 contains the manure volatile fatty acid data. As has been reported previously (Friend et al., 1962; Kass et al., 1980; Giusi-Perier et al., 1989), acetic acid was the most abundant volatile fatty acid in the digestaimanure samples. Acetic acid and lactic acid have been shown to be characteristic fermentation products of Bifidobacteria (Bezkorovainy, 1989). In our samples, butyric and propionic acids were the next most abundant after acetic; isobutyric acid was found in the lowest concentrations. Lactic acid was not measured. The pattern was similar for the six volatiles that were measured (with only one exception, valeric acid), namely, the concentration of the individual volatile fatty acids was greatest for the group eating the 3% JA diet. It is evident from the data in Table 3 that the diets containing the Jerusalem artichoke meal had a significant (diet) effect (PI 0.05) on the concentrations of all of the VFAs that were measured. It is known that volatile fatty acids are major fermentation products of plant polysaccharides (Roustan et al., 1977; Titus and Ahearn, 1992). In a diet, the polysaccharide component is often referred to as fiber. However, the definition of fiber and methodology to measure fiber can vary from study to study. We have recently published detailed carbohydrate data for Jerusalem artichoke tuber, where we showed that soluble sugars, insoluble and soluble fiber can account for over 70% of the tuber (Mullin et al., 1994). The Jerusalem artichoke is unique in the plant world because this carbohydrate is almost entirely fructan (Bacon and Edelman, 195 1). It appears that the diets used in this study containing JA were supplying fermentable carbohydrates and this resulted in increased VFA production. Numerous literature references can be quoted that show the quantity and proportion of VFAs in digesta and manure are affected by the fiber component in the diet (Friend et al., 1962; Sambrook, 1979; Stanogias and Pearce, 1985; Fleming et al., 1992). It is not possible at this time to say what organism and substrate was the cause of the increase in individual VFAs in this study.

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Table 4 Sensory evaluation of the smell of manure of pigs fed experimental diets containing Jerusalem artichoke ( JA)b Characteristic Diet 0% JA 3%JA 4.3 2.4 2.9 4.3 4.0 6% JA 5.0 2.4 3.3 4.1 3.9 0.34 0.22 0.34 0.46 0.49 Standard error of mean Effect of dietC

sweet
Earthy Sour Sharp, pungent Skatole

3.9 2.5 2.9 5.4 6.0

.
NS NS ** .**

A minimum of 43 values per characteristic. ?3amples were evaluated at the end of each of five replicates. *,P<O.Ol; ,P<O.OOl. CNS,notsigniticant,P>0.05; ,P<O.O5; ??

The pH measurements of the extracts used for the volatile fatty acid analysis showed no diet effect. pH values ranged from 5.78 to 6.95; but on average, manure samples from all treatments averaged 6.3-6.4. Changes in the pH of manure of pigs fed fructans have not been as dramatic as reported in other species (Hidaka et al., 1986; Mitsuoka et al., 1987; Farnworth et al., 1992; Farnworth, 1994), and the reason for this difference is not known. The results of the sensory evaluation panel are shown in Table 4 Table 5. During the training sessions the panel members were able to agree upon five odours (sweet, earthy, sour, sharp-pungent, skatole) that could be distinguished in the manure samples, and that could be represented by known standards. Using these reference standards, the panel of ten assessors were able to conclude that the fresh manure obtained from pigs that had eaten the diets containing Jerusalem artichoke had a sweeter smell, was less sharp and pungent, and had less of a skatole smell compared with that of pigs that had eaten the control diet. Skatole is of particular interest; first, because it is very odiferous and has a characteristic pig smell; second, because it is found in high concentrations in pig faeces compared to other species (Dehnhard et al., 199 1) ; third, because it is one of the compounds responsible for boar taint in boar carcasses (Lundstrom et al., 1980; Lundstrom et al., 1984). It should be emphasized that only fresh manure samples free from contamination by urine were analyzed. Once manure mixes with urine and is exposed to air, its composition and characteristics change
Table 5 Sensory evaluation of the colour of manure of pigs fed experimental diets containing Jerusalem artichoke ( JA)ab Characteristic Diet 0% JA Light Brown Green Yellow 4.3 3.0 3.0 5.5 3% JA 1.9 6.3 8.2 3.1 6% JA 9.1 8.5 10.5 2.0 0.34 0.43 0.54 0.29 *.* *** ..* .** Standard error of mean Effect of diete

aA minimum of 43 values per characteristic. Samples were evaluated at the end of each of five replicates. eNS,notsignificant,P>0.05; ,P<O.O5; **,P<O.Ol: ,P<O.OOl.

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and become more complex. The panel s evaluation of the colour of the manure samples was even more conclusive. The manure from control pigs was significantly (P<O.OOl) darker, less brown, less green and more yellow than the manure from pigs eating the Jerusalem artichoke meal. An earlier report indicated that the intensity of the odour of manure from pigs fed Jerusalem artichoke was less (but not significantly less) than manure from pigs fed a control diet (Farnworth et al., 1993). Fresh manure was characterized in both studies and therefore any conclusions may not apply to current swine husbandry facilities where manure mixes with urine and may sit for several days within the barn. Yasuhara et al. (1984) reported many changes in the number and concentration of compounds isolated from fresh and anaerobically digested pig manure. Long lists of compounds, many odiferous, that have been isolated and identified in pig digests/manure, have been published (Yasuhara and Fuwa, 1983; Yasuhara et al., 1984). The digesta, as it passes through the pig, is subject to metabolism by the intestinal microorganisms. This microbial action contributes to the large number of compounds that are found in digesta/faeces. If the population of micro-organisms is changed as a result of a change in the diet (addition of fructans for example), changes in manure odour and colour may result. Fructans that can be extracted from the tuber of Jerusalem artichoke have been shown to be bifidogenic (Modler et al., 1990). Adding Jerusalem artichoke to the diet changes the manure; this may be due to bifidobacteria (Modler et al., 1990). Differences in response that have been seen in feeding trials involving Jerusalem artichoke or other fructan sources may be due to differences in the fructan content of the diets. We have seen large differences in the fructan spectrum of different varieties of Jerusalem artichoke and differences in tubers harvested in different years (E. Farnworth, unpublished data, 1995); storage and processing can also bring about compositional changes.

Acknowledgements The financial support of Ralston Purina Canada is gratefully acknowledged. CFAR swine area staff cared for the animals. Technical assistance was provided by S. Winter. Sensory analysis was carried out with the assistance of Joanne Elsaesser, and R. Williams aided in the VFA analysis. CFAR contribution number 2236.

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