Experimental infections with Hyostrongylus rubidus and the effects on performance of growing pigs

Veterinary Parasitology, 17 (1984/85) 2 1 9 - 2 2 7 Elsevier Science Publishers B.V., Amsterdam - - Printed in The Netherlands

219

E X P E R I M E N T A L I N F E C T I O N S W I T H H Y O S T R O N G Y L US R UBID US AND THE EFFECTS ON PERFORMANCE OF GROWING PIGS

T.B. STEWART

Department of Veterinary Microbiology and Parasitology, School of Veterinary Medicine, Louisiana State University, Baton Rouge, LA 70803 (U.S.A.) O.M. HALE Department of Animal Science, University of Georgia, Coastal Plain Station, Tifton, GA 31793 (U.S.A.) O.G. MARTI* Animal Parasite Research Laboratory, U.S. Department of Agriculture, Agriculture Research Service, Tifton, GA 31793 (U.S.A.) (Accepted 17 September 1984)

ABSTRACT Stewart, T.B., Hale, O.M. and Marti, O.G., 1985. Experimental infections with Hyostrongylus rubidus and the effects on performance of growing pigs. Vet. Parasitol., 17 : 219--227. Pigs infected with Hyostrongylus rubidus at the rate of 550 larvae k g - ' body weight followed 15 days later with 220 larvae k g - ' body weight gained less weight (P<0.010) than uninfected control pigs. Feed efficiency (feed/gain) was 8% better (P>0.10) in control than in infected pigs. Peak H. rubidus eggs per gram counts (EPG) occurred 22 days after each infection of pigs. H. rubidus EPG at necropsy were correlated with total number of adults recovered and with female/male ratio. High EPG were associated with H. rubidus populations composed of approximately equal numbers of males and females. Digestion trials consisted of pigs infected with 335 larvae k g - ' body weight compared to uninfected controls. Control pigs had higher (P<0.05) crude protein digestion coefficients, excreted less (P<0.05) N in feces and had a higher (P<0.05) N balance than infected pigs.

INTRODUCTION E x p e r i m e n t a l i n f e c t i o n s o f p i g s w i t h H y o s t r o n g y l u s rubidus h a v e b e e n reported to produce no visible clinical disease at dosage levels below 200 000 i n f e c t i v e l a r v a e p e r p i g ( P o r t e r , 1 9 4 0 ; K e n d a l l e t al., 1 9 6 9 ; B u r d e n a n d K e n d a l l , 1 9 7 2 ) . M o s t p a t h o l o g i c a l c h a n g e s s u c h as g a s t r i c e r o s i o n a n d *Present address: Insect Biology and Population Management Research Laboratory, U.S. Department o f Agriculture, Agriculture Research Service, Tifton, GA 31793 (U.S.A.)

0304-4017/85/$03.30

© 1985 Elsevier Science Publishers B.V.

220 excessive mucus were described as insignificant and attributed to mechanical damage produced by worm activity. Lean et al. (1972a) reported that experimental infection with as many as 1 5 0 0 0 0 infective larvae of H. rubidus per pig did not change the rate of growth or feed conversion efficiency of swine, whereas, Davenport (1967) reported reduced weight gains in pigs after exposure to 3000--15 000 infective larvae of H. rubidus per pig. Dey-Hazra et al. (1972) found that 12-kg pigs infected with 12 000 infective larvae of H. rubidus each leaked plasma proteins into the gastrointestinal tract at a 5 times greater rate than uninfected pigs. However, Stockdale (1974) reported that the growth rate and total serum proteins were not changed after infection with 43 000 larvae of H. rubidus per pig, and Lean et al. (1972b) stated that hemoglobin, packed-cell volume, and red and white cell counts were not affected by 150 000 H. rubidus larvae per pig. The following experiments were designed to compare the performance of H. rubidus-infected pigs with uninfected controls and to make detailed parasitological observations on H. rubidus-infected pigs. MATERIALS AND METHODS The strain of Hyostrongylus rubidus used for the experimental infections of pigs was obtained from naturally-infected pigs in the environs of Tifton, Georgia. Eggs taken from gravid female H. rubidus, recovered from the stomach of pigs slaughtered locally, were cultured in sphagnum moss. The infective larvae recovered from these cultures were used to infect parasite-free pigs. The inocula used to produce experimental infections were mixtures of larvae isolated from cultures made from eggs obtained directly from female worms and those passed in feces by pigs harboring worms from first or second laboratory passage.

Experiment I Sixteen cross-bred female pigs (average 23.4 kg b o d y weight) approximately 2 m o n t h s of age were divided into 2 similar groups. Pigs in the first group were given infective larvae of Hyostrongylus rubidus orally at the rate of 550 larvae kg -1 of body weight, followed 15 days later with a second dose of 220 larvae kg -1. A second group of 8 pigs was used as uninfected control. The pigs were from the Georgia Coastal Plain Experiment Station herd in which low levels of infection with Ascaris suum, Strongyloides ransomi, and Oesophagostomum spp. were known to occur, but no infections with H. rubidus have been found. All pigs were individually fed a balanced diet based on corn and soybean meal. Forty-two days after initial infection, dietary protein of all pigs was reduced from 16% to 14%. Feed and water were available ad lib., except that feed was withdrawn 24 h prior to slaughter. Pigs were weigh~;d period-

221 ically and the a m o u n t of feed consumed was determined for each animal. Parasite eggs per gram (EPG) of feces were determined for each animal by flotation in saturated NaCI. Average dally gain (ADG) and feed conversion (F/G) were based on information collected for 70 days following initial infection. All pigs were killed 76--83 days after initial infection. The gastro-intestinal tracts were opened and the nematodes present were recovered, identified, and counted according to standard techniques. Stomachs were digested with pepsin--HC1 at 37°C to recover H. rubidus. Aliquots of H. rubidus recovered from the infected pigs were examined and counted to determine the sex ratio. Ten H. rubidus females from each pig were selected at random and the numbers of ova in utero were counted. EPG were determined in all infected pigs for 56 consecutive days, beginning on the 18th day after initial infection. (All pigs had negative EPG until the 19th day.) EPG were determined in the remaining pigs at regular intervals.

Experiment H In each of 3 digestion trials, 8 cross-bred barrows (average 11.7, 12.2 and 18.2 kg body weight in Trials 1, 2 and 3, respectively) were divided into 2 similar groups. Pigs in the first group were given infective larvae of H. rubidus at the rate of 335 larvae kg -1 of body weight and pigs in the second group were used as uninfected controls. Infected and control pigs were transferred to individual metabohsm cages for collection and separation of feces and urine on Day 8 after infection. Pigs were maintained in the metabolism cages for a 9-day adjustment period and a 5-day total collection period that began on Day 17 postinfection. During digestion Trials 1 and 2, pigs were given 1.5 kg feed daily, and in Trial 3, 1.75 kg feed dally in small self-feeders. Any feed spilled or left in the self-feeders was weighed dally and subtracted from the total a m o u n t supplied. Total fecal o u t p u t was collected daily during each 5-day collection period, frozen and later thawed and composited for analysis. The urine was collected in plastic pans that contained 25 ml of 50% concentrated sulfuric acid plus 200 ml water. The daily collection of acidified urine was diluted to constant volume, sampled and composited in containers maintained under refrigeration and then frozen until analyzed. Composition of diet fed during the digestion--absorption experiment was similar to that fed to pigs in Experiment I except that the crude protein c o n t e n t was 15.1% t h r o u g h o u t the trials. Proximate analyses of the diet and feces were conducted by AOAC (1980) methods except N contents of the diet, feces and urine which were determined with a Technicon Autoanalyzer II (Industrial Method No. 329 W/A, Technicon Industrial Instruments Inc., Tarrytown, NY 10591).

222

T h e d a t a w e r e a n a l y z e d f o r s t a t i s t i c a l s i g n i f i c a n c e u s i n g a g e n e r a l !eo~tsquares program. RESULTS AND DISCUSSION Experiment

I

P e r f o r m a n c e a n d n e c r o p s y d a t a a n d t h e i r c o r r e s p o n d i n g m e a n s ar e g i v e n in T a b l e I. N o H . r u b i d u s w e r e f o u n d in c o n t r o l p i g s. T h r e e p i g s in t h e i n f e c t e d g r o u p (Pigs 6 - - 8 ) a n d 3 in t h e c o n t r o l g r o u p (Pigs 1 4 - - 1 6 ) h a d A . s u u m a t n e c r o p s y . N o o t h e r p a r a s i t e s w e r e f o u n d a t n e c r o p s y in p i g s o f either group. TABLEI Performance and necropsy data of pigs infected with Hyostrongylus rubidus or uninfected

Pig No. H. rubidus Larvae given

Ascaris suum

ADG (kg) a

F/G a

0.68 0.67 0.51 0.57 0.53 0.72 0.74 0.49

3.30 3.32 3.94 3.22 3.83 3.31 3.00 5.34

2.5

0.61 c

3.66

Adults recovered

Adults recovered

H. ru bidus-infected 1 20450 2 17 100 3 22450 4 17 000 5 21 200 6 18250 7 23 300 8 19 500

2706 454 1310 680 986 2380 1 063 2 043

0 0 0 0 0 2 2 16

.~b

1 368

19 906

Uninfected 9 10 11 12 13 14 15 16

0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0

0 0 0 0 0 2 2 1

0.82 0.76 0.65 0.78 0.75 0.76 0.78 0.62

3.38 3.74 3.15 3.31 2.88 3.70 3.32 3.68

.~b

0

0

0.6

0.74 d

3.40

aADG = average daily gain; F / G = units of feed per unit of gain. bValues for pigs with A. suum n o t included are: ADG, 0.59; F/G, 3.52 for H. rubidusinfected pigs and 0.75 and 3.29, respectively, for uninfected pigs. c'dMeans in the same column with different superscript are different (P<0.01).

223 T h e average daily gain {ADG) o f c o n t r o l pigs ( 0 . 7 4 kg) was greater ( P < 0 . 0 1 ) t h a n t h a t f o r i n f e c t e d pigs (0.61 kg). T h e r e was n o d i f f e r e n c e ( P > 0 . 1 0 ) in u n i t s o f feed p e r unit o f gain ( F / G ) b e t w e e n c o n t r o l ( 3 . 4 0 ) and i n f e c t e d {3.66) pigs; h o w e v e r , c o n t r o l pigs had an 8% b e t t e r F / G ratio t h a n i n f e c t e d pigs. T h e p r e s e n c e o f A. s u u m at n e c r o p s y had n o e f f e c t o n perf o r m a n c e c o m p a r i s o n s b e t w e e n groups. Data c o l l e c t e d f r o m H. rubidus p o p u l a t i o n s r e c o v e r e d f r o m the i n f e c t e d pigs are p r e s e n t e d in Table II. Seventy-six t o 83 days a f t e r initial i n f e c t i o n , a m e a n o f 7.31% o f the total larvae given t o the pigs were r e c o v e r e d as a d u l t w o r m s . T h e same strain o f H . rubidus used in this e x p e r i m e n t has b e e n u s e d p r e v i o u s l y in drug evaluation trials in which pigs were slaughtered 25 days a f t e r i n f e c t i o n . T h e n u m b e r s o f H. rubidus r e c o v e r e d f r o m c o n t r o l animals in those trials r e p r e s e n t e d 31% o f the n u m b e r o f larvae given (Stew a r t e t al., 1 9 7 5 ) . TABLE II Hyostrongylus rubidus population and worm egg count data observed in infected pigs

Pig H. rubidus at No. necropsy

Adults as percentage of

F/M ratio

Eggs/F

Mean last 4 EPG

larvae (%) 1 2 3 4 5 6 7 8

2380 2706 1063 454 1310 680 986 2043

13.04 13.23 4.56 2.66 5.84 4.00 4.65 10.48

1.23 1.03 2.09 2.61 1.30 1.87 1.96 1.49

20.4 26.6 27.5 22.8 20.2 29.1 29.4 33.8

26.0 52.5 14.0 0.3 54.3 18.5 39.3 72.0

~"

1453

7.31

1.70

26.2

34.6

T h e negative c o r r e l a t i o n ( r = - 0 . 8 7 , P < 0 . 0 1 ) f o u n d b e t w e e n the f e m a l e / male r a t i o , and the n u m b e r s o f w o r m s r e c o v e r e d at n e c r o p s y i n d i c a t e d t h a t small H. r u b i d u s b u r d e n s were associated with a high f e m a l e / m a l e ratio. Conversely, large w o r m b u r d e n s were associated w i t h a p p r o x i m a t e l y equal n u m ber o f males and females. B u r d e n and Kendall {1973) p r e s e n t e d d a t a indicating t h a t H. rubidus p o p u l a t i o n s , e x p e r i m e n t a l l y p r o d u c e d in l l - m o n t h old gilts, decrease with t i m e and t h a t t h e decrease was associated with an increase in the f e m a l e / m a l e ratio. T h e high negative c o r r e l a t i o n in the p r e s e n t investigation shows t h a t the decrease in w o r m p o p u l a t i o n and the corr e s p o n d i n g change in sex ratio were n o t solely t i m e - d e p e n d e n t , b u t were also h o s t - d e p e n d e n t . T h e last 4 H. rubidus EPG were positively c o r r e l a t e d with the n u m b e r o f

224

worms at necropsy (r=0.64, P<0.10). Negative correlations of EPG with female/male ratio (r=-0.72, P<0.05) indicate that high EPG are associated with H. rubidus populations of approximately equal numbers of each sex. If random populations of larvae are composed of equal numbers of each sex, then newly established adult populations should be similarly composed. Selective elimination of males would produce an increase in the female/male ratio associated with decreasing populations and is probably a function of their shorter mean life span. Masaba and Herbert (1978) have reported an increase in the female/male ratio with duration of H. rubidus infection. The lack of correlation of eggs per female and numbers of worms (r=-0.01, /'>0.10), and other variables measured indicate that unlike EPG counts, female fecundity is independent of the size or sexual ratio of the worm population. Daily EPG were determined from 18--75 days after initial infection of pigs. The second infection followed the first by 15 days. The mean EPG beginning at the third day after the second infection are presented in Fig. 1. Eggs first appeared in the feces on the 19th day after initial infection and reached a peak of 145 EPG on the 22nd day. A smaller peak of 97 EPG occurred 22 days after the second infection. After a 5-day downward trend, there was a large increase from 40 to 170 EPG between Days 44 and 47 after initial infection, coinciding with reduction of dietary protein from 16 to 14% on Day 42 after initial infection.

2oo 1 1801 160

I

o. 1 4 0 . LU

~ 120,

6oj

Z 100 • 0 o: t.- 8 0 (n 0>3: 40. 20'

O 17

21

2"5

2"9

45 4'9 5'3 5'7 3'3 3"7 4'1 DAYS AFTER PRIMARY INFECTION

6'1

6'5

6'9

7"3

Fig. 1. Hyostrongylus rubidus eggs per gram of feces (EPG) of pigs following primary infection with 550 larvae kg-' of body weight and secondary infection 15 days later with 220 larvae kg-'. The abrupt rise and gradual decline of the EPG is characteristic of H. rubidus (Burden and Kendall, 1972, 1973; Kendall and Small, 1974). Several

workers have reported that secondary peaks in EPG are suppressed (Burden

225 a n d Kendall, 1 9 7 2 ) , d e l a y e d (Castelino a n d H e r b e r t , 1 9 7 0 ) , or are u n d e t e c t a b l e (Castelino e t al., 1 9 7 1 ) f o l l o w i n g r e i n f e c t i o n . T h e small p e a k s e e n o n t h e 2 2 n d d a y a f t e r t h e s e c o n d i n f e c t i o n suggests t h a t egg p r o d u c t i o n o f a t least a p a r t o f t h e y o u n g e r w o r m p o p u l a t i o n was n o t d e l a y e d , since t h e first p e a k also f o l l o w e d t h e initial i n f e c t i o n b y 22 d a y s . T h e p e a k in E P G w h i c h o c c u r r e d b e t w e e n D a y s 44 and 47 a f t e r initial i n f e c t i o n is p o s s i b l y a r e s p o n s e t o t h e c h a n g e in t h e d i e t o f t h e h o s t (Marti et al., 1 9 7 5 ) . In t h e a b s e n c e o f f u r t h e r r e i n f e c t i o n , n o a d d i t i o n a l m a j o r p e a k s in egg production occurred. Based o n w o r m b u r d e n s a t n e c r o p s y a n d t h e r e d u c t i o n in A D G , H. ru bidus at n e c r o p s y were a s s o c i a t e d w i t h a r e d u c t i o n o f 0.13 k g / d a y . These results i n d i c a t e t h a t H. rubidus i n f e c t i o n s m a y b e m o r e d e t r i m e n t a l t o swine p e r f o r m a n c e t h a n p r e v i o u s l y believed. P o r t e r ( 1 9 4 0 ) a t t r i b u t e d light i n f e c t i o n s t o be t h e r e a s o n f o r t h e failure o f H. rubidus t o p r o d u c e o b v i o u s e f f e c t s in e x p e r i m e n t a l pigs. In a d d i t i o n , Kendall a n d Small ( 1 9 7 4 ) s t a t e d t h a t it was difficult t o s h o w t h a t n a t u r a l i n f e c t i o n s o f H. rubidus are injurious t o pigs. Parasite or h o s t - s t r a i n differences m a y a c c o u n t f o r s o m e o f t h e variations r e c o r d e d in t h e l i t e r a t u r e regarding t h e e f f e c t o f e x p e r i m e n t a l H. rubidus i n f e c t i o n s on swine h e a l t h a n d p e r f o r m a n c e . T h e results o f this investigation s h o w t h a t pigs w i t h m o d e r a t e n u m b e r s o f H. rubidus gain less w e i g h t t h a n similar u n i n f e c t e d pigs. T h e e f f e c t o f a single H. rubidus is so small t h a t s u b s t a n t i a l n u m b e r s are r e q u i r e d b e f o r e t h e i r c o m b i n e d e f f e c t on A D G or F / G can be d e t e c t e d . Experiment H D i g e s t i o n c o e f f i c i e n t s f o r d r y m a t t e r , gross e n e r g y , c r u d e p r o t e i n a n d N i n t a k e , e x c r e t i o n a n d b a l a n c e f o r pigs e x p e r i m e n t a l l y i n f e c t e d a n d f o r t h o s e n o t i n f e c t e d w i t h H. rubidus larvae are s h o w n in T a b l e I I I . Digestion TABLE III Digestion coefficients for dry matter, crude protein and energy and nitrogen intake, excretion and balance in pigs infected with Hyostrongylus rubidus or uninfected a Item

Digestion coefficients (%)

N (g)

N excreted (g)

intake

Infected Uninfected SE

Dry matter

Gross energy

Crude protein

77.7 79.1 0.82

80.1 81.9 0.76

71.6 b 75.7 c 1.39

N (g) balance

Urine Feces

183.1 185.8 1.34

69.3 64.9 b 69.8 58.1 c 2.90 2.35

48.9 b 57.9 c 2.54

aMeans for 12 pigs per treatment. H. rubidus infection at the rate of 335 larvae kg -t body weight. b~Means in each column with different superscripts are different (P< 0.05).

226 c o e f f i c i e n t s f o r d r y m a t t e r a n d gross e n e r g y f o r i n f e c t e d a n d c o n t r o l pigs were n o t d i f f e r e n t ( P > 0 , 0 5 ) ; h o w e v e r , t h e r e a p p e a r e d t o be a t r e n d t o w a r d slightly d e p r e s s e d digestion c o e f f i c i e n t s f o r b o t h d r y m a t t e r a n d gross e n e r g y in t h e i n f e c t e d pigs. S o m e i n f e c t e d pigs in e a c h trial s c o u r e d slightly while n o s c o u r i n g o c c u r r e d in c o n t r o l pigs. Mean d r y m a t t e r c o n t e n t o f feces o f i n f e c t e d pigs w a s 38.3% a n d 40.5% f o r c o n t r o l pigs. T h e d i g e s t i o n c o e f f i c i e n t f o r c r u d e p r o t e i n was g r e a t e r ( P < 0 . 0 5 ) f o r c o n t r o l pigs. Also, c o n t r o l pigs e x c r e t e d less ( P < 0 . 0 5 ) N in feces a n d h a d a higher ( P < 0 . 0 5 ) N b a l a n c e t h a n i n f e c t e d pigs. O u r results d o n o t agree w i t h t h o s e o f L e a n et al., ( 1 9 7 2 ) w h o r e p o r t e d n o significant d i f f e r e n c e s in N r e t e n t i o n and a p p a r e n t digestibilities b e t w e e n pigs i n f e c t e d w i t h various levels o f H. rubidus a n d c o n t r o l animals. H o w e v e r , D e y - H a z r a e t al. ( 1 9 7 2 ) f o u n d t h a t pigs i n f e c t e d w i t h H. ru bidus h a d increased gastro-intestinal losses o f p l a s m a p r o t e i n s as d e t e r m i n e d b y i n t r a v e n o u s l y a d m i n i s t e r e d C r - 5 1 - a l b u m i n . These researchers r e p o r t e d a b o u t 5 t i m e s as m u c h p l a s m a leakage on D a y 25 p o s t - i n f e c t i o n in an animal i n f e c t e d w i t h 1 0 0 0 larvae kg -1 b o d y w e i g h t t h a n in c o n t r o l pigs. T h u s , it is possible t h a t o u r pigs e x p e r i e n c e d s o m e p l a s m a leakage w h i c h c o u l d a c c o u n t f o r d i f f e r e n c e s in c r u d e p r o t e i n digestibility, N e x c r e t i o n in t h e feces and N balance b e t w e e n i n f e c t e d pigs a n d c o n t r o l s . T h e r e was n o significant d i f f e r e n c e in a m o u n t o f N e x c r e t e d in urine o f pigs b e t w e e n t r e a t m e n t s .

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227 Lean, I.J., Herbert, I.V. and Castelino, J.B., 1972b. Studies on the pathogenesis of infection with Hyostrongylus rubidus (Nematoda). The effects of levels of infection of up to 150,000 infective stage larvae on the growing pig. II. Blood studies. Br. Vet. J., 128: 147--152. Marti, O.G., Stewart, T.B. and Hale, O.M., 1975. Effect of diet, sex and Hyostrongylus on pigs. J. Anita. Sci., 41: 320. Masaba, S. and Herbert, I.V., 1978. The population dynamics of Hyostrongylus rubidus infections of pigs after infection with 2500 to 40 000 larvae. J. Comp. Pathol., 88: 575--583. Porter, D.A., 1940. Experimental infections of swine with the red stomach worm, Hyostrongylus rubidus. Proc. Helminthol. Soc. Wash., 7: 20--27. Stewart, T.B., Hale, O.M. and Marti, O.G., 1975. Efficacy of two dichlorvos formulations against larval and adult Hyostrongylus rubidus in swine. Am. J. Vet. Res., 36: 771-772. Stockdale, P.H.G., 1974. The pathogenesis of Hyostrongylus rubidus in growing pigs. Br. Vet. J., 366--373.