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Effect of gastrointestinal nematode and liver fluke infections on weight gain and reproductive performance of beef heifers
Veterinary Parasitology 107 (2002) 227–234
Effect of gastrointestinal nematode and liver fluke infections on weight gain and reproductive performance of beef heifers夽 A.F. Loyacano a,∗ , J.C. Williams b , J. Gurie a , A.A. DeRosa b a
b
Dean Lee Research Station, Louisiana State University AgCenter, 8105 Tom Bowman Dr., Alexandria, LA 71302, USA Department of Veterinary Science, Louisiana State University AgCenter, 111 Dalrymple Bldg., Baton Rouge, LA 70803-6002, USA
Received 4 October 2001; received in revised form 15 May 2002; accepted 16 May 2002
Abstract Spring born, crossbred beef heifers (n = 372) were utilized over four years to measure reductions in body weights, reproductive performance and calf weights caused by gastrointestinal nematodes (primarily Ostertagia ostertagi) and the bovine liver fluke (Fasciola hepatica) and to differentiate losses attributable to each type of parasitism. Each year, weaned heifers were allotted to one of the four treatment regimens: Group 1, untreated controls; Group 2, treated for nematodes; Group 3, treated for liver fluke; and Group 4, treated for both nematodes and liver fluke. Nematodes were controlled with subcutaneous injections of either ivermectin (Ivomec® , Merial) or doramectin (Dectomax® , Pfizer), both at the recommended dose of 200 ug/kg bodyweight. Clorsulon (Curatrem® , Merial) drench was given at the recommended rate of 7 mg/kg bodyweight to control flukes. Treatments and fecal collections were initiated at allotment each year and were repeated at 28–84-day intervals until palpation for pregnancy diagnosis. Open heifers were removed from the study at this time. Treatment dates were based on expected length of treatment efficacy, the stage of growth of the heifers and the seasonal risk of infection by the parasites. Pregnant females were pooled and received their assigned treatments prior to their calving and breeding seasons and remained together until their calves were weaned. Heifers treated for nematode infections were heavier and had higher condition scores (P < 0.01) than untreated control heifers at initiation of breeding, and maintained that difference through pregnancy diagnosis. Liver fluke infection did not affect heifer gains or condition scores prior to palpation (P < 0.01). At palpation, heifers treated for both forms of parasitism had the highest condition scores and weight gains (P < 0.01), and 夽 Approved for publication by the Director of the Louisiana Agricultural Experiment Station as manuscript number 00-74-0324. ∗ Corresponding author. Fax: +1-318-473-6535. E-mail address: [email protected] (A.F. Loyacano).
0304-4017/02/$ – see front matter © 2002 Elsevier Science B.V. All rights reserved. PII: S 0 3 0 4 - 4 0 1 7 ( 0 2 ) 0 0 1 3 0 - 9
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also higher pregnancy rates than control heifers and heifers treated for nematodes only (P < 0.01). Pregnancy rates for heifers treated for flukes only were not significantly different from those treated for both nematodes and flukes. Heifers treated for nematodes weaned heavier calves than those not treated for nematodes (P < 0.05). © 2002 Elsevier Science B.V. All rights reserved. Keywords: Beef cattle:Nematoda; Beef cattle:Trematoda; Gastrointestinal nematodes; Fasciola hepatica; Parasitism effects; Cattle performance
1. Introduction Essentially all grazing cattle in the southcentral and southeastern United States are exposed to substantial infections by gastrointestinal nematodes (GINs) through much of the year (Williams, 1986). In poorly drained areas such as flood plains and coastal marshes, which provide suitable habitat for their lymnaeid snail intermediate host (Fossaria bulimoides), 50–100% of yearling and older cattle may be infected with the bovine liver fluke, Fasciola hepatica (Malone and Loyacano, 1991). Although all classes of cattle are infected by these parasites, replacement heifers are among those most susceptible to production losses as a result of depressed appetite, reduced feed digestibility, and/or disruption of normal metabolic or hormonal processes as a result of parasitic infections (Dargie, 1987; Gibbs, 1987; Williams et al., 1992; Herd, 1993). Many studies have been conducted to determine the effect of various anthelmintic treatment regimens on weight gains and reproductive performance. Many have shown that effective treatment for subclinical GIN infections increases weight gain and body condition score but not necessarily pregnancy rate (Loyacano et al., 1991; Ryan et al., 1992; Purvis et al., 1994). Treatment for liver fluke has also been reported to increase stocker calf gains (Armstrong and Miller, 1980; Malone et al., 1982). However, the designs for these studies may have been inappropriate because the treatment for fasciolosis (albendazole) is also a more effective nematocide than the product (thiabendazole) administered to control animals. In a subsequent trial using a valid control group (Loyacano et al., 1996), it was found that treating weanling calves with subclinical liver fluke infections had no significant effect on weight gains. Treatment for fluke infections has also been suggested to improve reproduction in cattle via an increase in growth and improved general body condition (Rickard et al., 1992). Other studies have suggested (Dargie, 1987; Lopez-Diaz et al., 1998) that fertility in heifers may be adversely affected by fasciolosis via an interruption of normal sex hormone metabolism in the liver, resulting in a delay in sexual maturity. The Dean Lee Research Station is located in central Louisiana in the Red River flood plain. The topography, soil types, vegetation and rainfall patterns at this site all are conducive to the maintenance of significant populations of GIN and F. hepatica. Although GIN infection is almost universal and liver fluke infection rates can approach 100% in young cattle, infection rates in beef replacement heifers are primarily subclinical at this location. The purpose of this research was to measure reductions in body weight gain and reproductive performance of beef replacement heifers and in the weaning weights of their first calves which might be attributed to subclinical nematode and liver fluke infections.
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2. Materials and methods 2.1. Heifers Three hundred and seventy-two Angus- or Brangus-sired heifers, spring born at this location from 1993 through 1996, were used in this study. Each year on approximately November 1, a sort by computer-generated random numbers was used to randomly allot one-third of the weaned heifers to each of three separate, adjacent 10 ha pastures. The heifers allotted to each pasture were then sorted by random numbers to the four treatment groups. Each year, each pasture contained equal numbers of heifers assigned to each treatment group. Eighty-four heifers were available from the 1993 calving season and 96 heifers were available in each of the succeeding three years. In 1993, there were 28 heifers in each pasture, seven from each treatment group. In the succeeding three years, there were 32 heifers in each pasture, eight per treatment group. Ninety-three heifers were allotted to each treatment group over the 4 years of the trial. Heifers in each of the two pasture groups were exposed to two Angus bulls and one group was exposed to two Brangus bulls from mid-April until the end of June. The same bulls were assigned to the same pastures each year and were examined for breeding soundness prior to each breeding season. Pasture groups remained intact until October when they were palpated for pregnancy diagnosis. Open heifers were then culled and pregnant heifers were pooled and moved to another pasture where they remained until their calves were weaned the following October. Separate yearly calf crops were used in each year of the study. After weaning of their calves, heifers were removed from the study and went into the general breeding herd. 2.2. Pastures The 10 ha pastures provided adequate amounts of growing forage for the heifers during most of the trial period and stocking rates were within normal stocking rates for yearling cattle at this location. Bermudagrass (Cynodon dactylon) and dallisgrass (Paspalum dilatatum) provided perennial warm season grazing. Pastures were overseeded with annual ryegrass (Lolium multiflorum) in October of each year to provide winter forage. Appropriate levels of ammonium nitrate were applied as needed. Bermudagrass hay was provided ad lib when sufficient quantities of growing forage were not available (60–90 days/year). Limited amounts of ground corn (1–2.5 kg per heifer for 30–60 days prior to the breeding season) were provided when necessary to meet the nutritional requirements for developing replacement heifers. 2.3. Treatment The heifers were given no anthelmintic treatments prior to entrance into the study. Treatment regimens were: Group 1, untreated controls; Group 2, treated for GIN only; Group 3, treated for Fasciola only, and Group 4, treated for GIN and Fasciola. For GIN control, Ivomec® (ivermectin, Merial) (years 1, 2 and 4) or Dectomax® (doramectin, Pfizer) (year 3) at the prescribed dosage of 200 ug/kg bodyweight were administered via subcutaneous injection. Curatrem® (clorsulon, Merial) drench was administered orally at the recommended
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dosage of 7 mg/kg bodyweight to control the liver fluke. Treatments (total of 7) were administered at allotment each year on approximately November 1, and were repeated in early December, early February, mid-March, at the beginning of the breeding season in mid-April, at the end of the breeding season in late June and at palpation in late September. Treatment dates were based on the anticipated risk of infection (weather conditions, nutritional status, pasture infection and history) until the heifers were palpated for pregnancy. Individual fecal samples were collected rectally from approximately half of the heifers at each treatment date to monitor infection levels. Nematode eggs per gram of feces counts (EPG) were determined by a centrifugation–flotation procedure with a saturated sucrose solution as a flotation medium (Cox and Todd, 1962). Liver fluke EPG counts were determined via a selective sieve and sedimentation method (Flukefinder, Pullman, WA). Subjective body condition scores (BCS) from 1 (emaciated) to 9 (excessively fat) were assigned at each treatment date by treatment blinded observers. Heifer weights were recorded at all treatment dates and calf weights were recorded at birth, 205 days of age and at weaning at approximately 250 days of age. The treatment regimen used was purely experimental and intended only for maximal suppression of GIN and/or liver fluke infections in order to more accurately measure effect of the treatments on prevention of cattle performance reductions.
3. Statistical analysis Data were analyzed following the general linear model procedure (P < 0.05) (SAS Institute, 1996) with significance levels set at P < 0.05 for all measured variables. The numbers of heifers were different between year 1 and years 2, 3 and 4 and number of calves and fecal samples collected were different between years, pastures, and treatments. Data were analyzed with year, pasture and treatment as main effects and all interactions between main effects were included in the model. Data were analyzed again with all non-significant (P < 0.05) interactions included in the error term. Year and pasture effects were significant as was expected and are not discussed in this report. Rainfall and temperature varied from year to year, affecting parasite burdens and forage production and nutrients available to the heifers and consequent effect on heifer performance. There were known minor differences in soil types, topography and forage production of the pastures utilized in this study which may also have affected parasite burdens and heifer performance. Least square means are presented in the tables. Fecal egg counts were transformed to the natural log(count + 1) for analysis and the least-square means were back transformed to geometric means for presentation. All data presented are calculated means for the 4-year period.
4. Results 4.1. Heifer performance Treatment group significantly affected heifer performance (Table 1). Initial weights at allotment did not differ among treatment groups. At breeding in March, heifers with
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Table 1 Effect of gastrointestinal nematodes and F. hepatica on heifer weights, gains (kg), body condition scores (BCS) and pregnancy rates (%)a Treatment group
1. No treatment 2. Nematodes only 3. Liver flukes only 4. Nematodes and flukes a
Initial Breeding weight Weight BCS 239 a 240 a 240 a 237 a
291 a 316 b 295 a 318 b
4.9 a 5.2 b 5.0 a 5.3 b
Breed end
Palpation
Gain
Weight
BCS
Weight
BCS
53 a 76 b 55 a 78 b
332 a 356 b 338 a 361 b
4.9 a 5.3 c 5.0 b 5.4 c
369 a 400 b 379 a 410 b
5.0 a 5.4 b 5.3 b 5.6 c
Total gain
Pregnancy rate
130 a 160 c 138 b 170 d
54 a 63 a 67 ab 78 b
Means within columns with the same letters are not different (P < 0.01).
untreated GIN infections (Groups 1 and 3) had lower mean weights (P < 0.01) than heifers that had been treated for GIN (Groups 2 and 4). Heifers with untreated GIN infections also had lower BCS than treated heifers. These relationships persisted until palpation in October. At the end of the breeding season (July 1), condition scores for heifers that were not treated for either GIN or flukes (Group 1) had significantly lower BCS than heifers that were treated for flukes only (Group 3). Heifers treated for flukes only had significantly lower BCS than heifers treated for GIN only. At palpation, Group 1 heifers had lower average scores than Group 2 and Group 3 heifers and Group 4 heifers had the highest condition scores. Untreated Group 1 heifers had significantly lower pregnancy rates than heifers that were treated for both GIN and flukes (Group 4). Treating for GIN alone (Group 2) did not significantly increase pregnancy rates and heifers treated for flukes only (Group 3) did not have significantly higher pregnancy rates than untreated control heifers or heifers that were treated for GIN only. However, the pregnancy rates for Group 3 heifers were not significantly lower than those of heifers that were treated for both forms of parasitism. 4.2. Calf performance Treatment had a substantial effect on calf weights (Table 2). Calves from the untreated Group 1 dams were lighter at birth than calves from Group 4 heifers that had been treated for GIN and flukes. Calves from heifers not treated for GIN (Groups 1 and 3) were lighter at weaning than those from heifers that were treated for GIN (Groups 2 and 4). When weights were adjusted for calf age and sex, calves from heifers treated for flukes only (Group 3)
Table 2 Least square means for treatment effect on calf weights (kg)a Treatment group
Birth weight (n)
Wean weight (n)
Adjusted wean weight
1. No treatment 2. Nematodes only 3. Liver flukes only 4. Nematodes and flukes
32 a (48) 34 ab (54) 32 a (59) 35 b (69)
196 a (34) 214 b (49) 199 a (49) 220 b (57)
223 a 240 bc 229 ab 248 c
a
Means within columns with the same letters are not different (P < 0.05). n is the number of calves.
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Table 3 Least square means for treatment effect on gastrointestinal nematode fecal egg counts (EPG)a Treatment group
Initial EPG
Prebreed EPG
End breed EPG
Palpation EPG
1. No treatment 2. Nematodes only 3. Liver flukes only 4. Nematodes and flukes
92 a 86 a 98 a 82 a
15 a 5b 14 a 5b
29 a 11 a 19 a 13 a
35 a 23 a 18 a 31 a
a
Means within columns with the same letters are not different (P < 0.05).
were not significantly heavier than calves from untreated Group 1 heifers nor significantly lighter than calves from Group 2 heifers which were treated for nematodes only. 4.3. Fecal egg counts Initial individual heifer GIN counts ranged from 0 to 600 EPG. On a yearly basis, mean initial counts ranged from 58 to 119 EPG. Individual heifer fluke egg counts ranged from 0 to 6.5 EPG and annual mean initial counts ranged from 2.17 to 2.96 EPG. Initial GIN fecal egg counts were not significantly different between treatments (Table 3). At the beginning of the breeding season, an average of 46 days post-treatment, heifers treated for GIN (Groups 2 and 4) had significantly lower (P < 0.05) average egg counts than those that had not been treated for GIN (Groups 1 and 3). At the end of the breeding season and at palpation when fecal samples were collected at 60–84 days following treatment, there were no significant treatment effects on nematode egg counts. Fecal egg counts in this study were not used as a measure of treatment efficacy. They were used to monitor the presence of parasite infection and to verify that the heifers were exposed to continual infection. Initial fluke egg counts were not different between treatments (Table 4). Initial prevalence or infection rate was 30%. At the beginning of the breeding season and throughout the trial periods, heifers treated for flukes had significantly lower egg counts than heifers that were not treated for flukes. Mean egg counts for control heifers increased from 0.23 at trial initiation to 1.5 at palpation. Although mean fluke egg counts never exceeded 1.55 eggs per gram, counts for untreated heifers increased over time and greatly exceeded the counts of treated heifers at the end of the trial. The patent infection rate for heifers with untreated fluke infections was 80% at palpation compared to 35% for heifers treated for flukes. Table 4 Least square means for treatment effect on F. hepatica fecal egg counts (EPG)a Treatment group
Initial EPG
Prebreed EPG
End breed EPG
Palpation EPG
1. No treatment 2. Nematodes only 3. Liver flukes only 4. Nematodes and flukes
0.23 a 0.30 a 0.38 a 0.49 a
0.37 a 0.40 a 0.00 b 0.06 b
0.86 a 0.87 a 0.22 b 0.26 b
1.50 a 1.55 a 0.15 b 0.50 b
a
Means within columns with the same letters are not different (P < 0.05).
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5. Discussion Therapeutic suppression of nematode infections alone resulted in significantly increased bodyweight, bodyweight gain and BCS in replacement heifers, but not in significantly higher pregnancy rates. Suppression of fluke infections alone significantly increased BCS after the breeding season and increased total weight gain, but did not significantly affect pregnancy rates. Simultaneous suppression of both GIN and flukes resulted in increased pregnancy rates. Since body weights and condition scores of heifers treated for GIN only were not significantly lower than those of the heifers treated for both GIN and liver flukes, the significant increase in pregnancy rates of heifers treated for both GIN and flukes cannot be explained by increases in bodyweight or general condition. These data support observations of Lopez-Diaz et al. (1998) which reported that puberty was delayed 39 days in Friesian heifers which had been infected with 600 F. hepatica metacercariae. Infected heifers in that study had elevated serum E2 levels and lowered P4 levels which were attributed to an alteration in the metabolic clearance rate of estrogens in the liver. The elevated levels of serum E2 were hypothesized to upset the normal prepubertal production of GnRH and LH and delay the development of corpus lutea and the onset of puberty. In a controlled breeding season, this would result in later calving dates and lower calving rates. The data from this study suggested that the effects of GIN and liver flukes on performance were through different mechanisms and that the effect of the two forms of parasitism may be additive. It was apparent that GIN infections can prevent replacement heifers from reaching adequate body weights and condition scores at breeding age and that fluke-induced alterations of metabolic processes in the liver, which stimulate heifers to puberty, may also have been operative. Significant infection with either form of parasitism could reduce heifer fertility. Treatment for one form of parasitism, when both are present in the animals and environment, may not significantly improve heifer reproductive performance. In the case of heifers not treated for nematode infections, results indicated this as a possible cause of reduced calf weights. However, heifers treated for fluke infections only produced calves with age adjusted weaning weights that were not significantly heavier than calves from untreated heifers, but were not significantly lighter than calves from those treated for GIN only. Although economic benefits of GIN control are widely acknowledged, the benefits of controlling concomitant liver fluke infections have often been obscured due to combined nematocidal and flukicidal activity of common anthelmintics (albendazole, ivermectin/clorsulon). Results supportive of the present work have been reported by Holste et al. (1986), Rickard et al. (1992) and Kaplan (1994). The latter authors suggested that the difficulty in quantifying economic benefits of fluke control is because of interactions among physiologic, nutritional-associated diseases, climatic and geographic factors which cause extensive variation in pasture infectivity and variation in infection rate and severity over years and location. Consideration of cost effectiveness with the suppressive treatment regimen used in this study was not feasible, although performance values and gross returns for heifers treated for GIN only and for GIN and flukes would likely have yielded cost effectiveness based on an average cost of the drugs used, US$4.00–6.00 per treatment. Estimated sale value ($1.43 and 1.80 per kg for open heifers and calves, respectively) and pregnancy rates were factored together to calculate average gross returns per heifer of US$507, 545, 516 and 555 for untreated
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heifers, heifers treated for GIN only, heifers treated for flukes only and heifers treated for both forms of parasitism, respectively. Routine strategic treatments where used in this region of high GIN and fluke prevalence, i.e., treatment for GIN and flukes in the fall at weaning, in the spring prior to breeding and again during the following fall prior to calving, should produce results similar to those in the present report. The third treatment for heifers late in their gestation can benefit calves through generally reduced pasture contamination and larval intake and possible improved milk production in dams. It is essential that strategic treatments be based on sound epidemiological data for the parasites in a given geographic region. References Armstrong, D.A., Miller, C.R., 1980. Liver flukes in cattle: life cycle, pathology, economic impact. Norden News, 30–33. Cox, D.D., Todd, A.C., 1962. Survey of gastrointestinal parasitism in Wisconsin dairy cattle. J. Am. Vet. Med. Assoc. 141, 134–139. Dargie, J.D., 1987. The impact on production and the mechanisms of pathogenesis of trematode infections in cattle and sheep. In: Leaning, W.H.D., Guerrero, J. (Eds.), The Economic Impact of Parasitism in Cattle. Proc. MSD AGVET Symp., XXII World Vet. Cong., Montreal, Canada, pp. 35–43. Gibbs, H.C., 1987. The effect of gastrointestinal nematodes on digestion and energy metabolism in calves. In: Leaning, W.H.A., Guerro, J. (Eds.), The Economic Impact of Parasitism in Cattle. Proc. MSD AGVET Symp., XXII World Vet. Cong., Montreal, Canada, pp. 35–43. Herd, R.P., 1993. Control strategies for ruminant and equine parasites to counter resistance, encystment, and ecotoxicity in the USA. Vet. Parasitol. 48, 327–336. Holste, J.E., Wallace, D.H., Hudson, D.B., Benz, G.W., Ericsson, G.F., 1986. Reproductive performance of beef cows treated with ivermectin before calving. Mod. Vet. Pract. 67, 462–464. Kaplan, R.M., 1994. Liver flukes in cattle: control based on seasonal transmission dynamics. Compend. Contin. Ed., Food Animal 5, 687–693. Lopez-Diaz, M.C., Carro, M.C., Cadorniga, C., Diez-Banoa, P., 1998. Puberty and serum concentrations of ovarian steroids during the prepuberal period in Friesian heifers artificially infected with Fasciola hepatica. Theriogen. 50, 587–593. Loyacano, A.F., Williams, J.C., Coombs, D.F., Hawkins, J.A., 1991. Effect of parasites on fertility and gains of beef heifers. Louisiana Agric. 34, 6–7. Loyacano, A.F., Williams, J.C., Gurie, J., 1996. A comparison of albendazole with ivomec and curatrem. Annual Research Report. Dean Lee Research Station, Louisiana State University, pp. 11–16. Malone, J.B., Loyacano, A.F., 1991. Earth observation satellite systems, climate and soil type risk assessment and control of liver flukes. Beef Cattle Sci. Handbook 25, 135–143. Malone, J.B., Smith, P.H., Loyacano, A.F., Hembry, F.G., Brock, L.T., 1982. Efficacy of albendazole for the treatment of naturally acquired Fasciola hepatica in calves. Am. J. Vet. Res. 73, 879. Purvis, H.T., Whittier, J.C., Boyles, S.L., Johnson, L.J., Ritchie, H.D., Rust, S.R., Faulkner, D.B., Lemenager, R.P., Hendrix, K.S., 1994. Weight gain and reproductive performance of spring-born beef heifer calves intraruminally administered oxfendazole. J. Anim. Sci. 72, 817–823. Rickard, L.G., Zimmerman, G.L., Hoberg, E.P., Bishop, J.K., Pettitt, R.J., 1992. Influence of ivermectin and clorsulon on productivity of a cow-calf herd on the southern Oregon coast. Vet. Parasitol. 41, 45–55. Ryan, W., Brown, J., Corah, L., Doornbos, D., Loyacano, A., Spire, M., 1992. Evaluation of the impact of ivermectin treatment on the growth and reproductive performance of replacement heifers. Proc. XVII World Buiatric Cong., and XXV Am. Assoc. Bovine Pract. Conf., St. Paul, MN, Vol. 1, pp. 23–28. SAS Institute, 1996. SAS/STAT Software, Release 6.11. SAS Institute Inc., Cary, NC. Williams, J.C., 1986. Epidemiologic patterns of nematodiasis in cattle. In: Gibbs, H.C., Herd, R.P., Murrell, K.D. (Eds.), Parasites: Epidemiology and Control. Vet. Clin. N. Am., Food Anim. Pract. 2, 235–246. Williams, J.C., Knox, J.W., Loyacano, A.F., 1992. Impact of gastrointestinal parasitism in grazing cattle. Proceedings of the 48th Southern Pasture and Forage Crop Improvement Conference, Auburn University, Auburn, AL, pp. 75–85.
Effect of gastrointestinal nematode and liver fluke infections on weight gain and reproductive performance of beef heifers夽 A.F. Loyacano a,∗ , J.C. Williams b , J. Gurie a , A.A. DeRosa b a
b
Dean Lee Research Station, Louisiana State University AgCenter, 8105 Tom Bowman Dr., Alexandria, LA 71302, USA Department of Veterinary Science, Louisiana State University AgCenter, 111 Dalrymple Bldg., Baton Rouge, LA 70803-6002, USA
Received 4 October 2001; received in revised form 15 May 2002; accepted 16 May 2002
Abstract Spring born, crossbred beef heifers (n = 372) were utilized over four years to measure reductions in body weights, reproductive performance and calf weights caused by gastrointestinal nematodes (primarily Ostertagia ostertagi) and the bovine liver fluke (Fasciola hepatica) and to differentiate losses attributable to each type of parasitism. Each year, weaned heifers were allotted to one of the four treatment regimens: Group 1, untreated controls; Group 2, treated for nematodes; Group 3, treated for liver fluke; and Group 4, treated for both nematodes and liver fluke. Nematodes were controlled with subcutaneous injections of either ivermectin (Ivomec® , Merial) or doramectin (Dectomax® , Pfizer), both at the recommended dose of 200 ug/kg bodyweight. Clorsulon (Curatrem® , Merial) drench was given at the recommended rate of 7 mg/kg bodyweight to control flukes. Treatments and fecal collections were initiated at allotment each year and were repeated at 28–84-day intervals until palpation for pregnancy diagnosis. Open heifers were removed from the study at this time. Treatment dates were based on expected length of treatment efficacy, the stage of growth of the heifers and the seasonal risk of infection by the parasites. Pregnant females were pooled and received their assigned treatments prior to their calving and breeding seasons and remained together until their calves were weaned. Heifers treated for nematode infections were heavier and had higher condition scores (P < 0.01) than untreated control heifers at initiation of breeding, and maintained that difference through pregnancy diagnosis. Liver fluke infection did not affect heifer gains or condition scores prior to palpation (P < 0.01). At palpation, heifers treated for both forms of parasitism had the highest condition scores and weight gains (P < 0.01), and 夽 Approved for publication by the Director of the Louisiana Agricultural Experiment Station as manuscript number 00-74-0324. ∗ Corresponding author. Fax: +1-318-473-6535. E-mail address: [email protected] (A.F. Loyacano).
0304-4017/02/$ – see front matter © 2002 Elsevier Science B.V. All rights reserved. PII: S 0 3 0 4 - 4 0 1 7 ( 0 2 ) 0 0 1 3 0 - 9
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also higher pregnancy rates than control heifers and heifers treated for nematodes only (P < 0.01). Pregnancy rates for heifers treated for flukes only were not significantly different from those treated for both nematodes and flukes. Heifers treated for nematodes weaned heavier calves than those not treated for nematodes (P < 0.05). © 2002 Elsevier Science B.V. All rights reserved. Keywords: Beef cattle:Nematoda; Beef cattle:Trematoda; Gastrointestinal nematodes; Fasciola hepatica; Parasitism effects; Cattle performance
1. Introduction Essentially all grazing cattle in the southcentral and southeastern United States are exposed to substantial infections by gastrointestinal nematodes (GINs) through much of the year (Williams, 1986). In poorly drained areas such as flood plains and coastal marshes, which provide suitable habitat for their lymnaeid snail intermediate host (Fossaria bulimoides), 50–100% of yearling and older cattle may be infected with the bovine liver fluke, Fasciola hepatica (Malone and Loyacano, 1991). Although all classes of cattle are infected by these parasites, replacement heifers are among those most susceptible to production losses as a result of depressed appetite, reduced feed digestibility, and/or disruption of normal metabolic or hormonal processes as a result of parasitic infections (Dargie, 1987; Gibbs, 1987; Williams et al., 1992; Herd, 1993). Many studies have been conducted to determine the effect of various anthelmintic treatment regimens on weight gains and reproductive performance. Many have shown that effective treatment for subclinical GIN infections increases weight gain and body condition score but not necessarily pregnancy rate (Loyacano et al., 1991; Ryan et al., 1992; Purvis et al., 1994). Treatment for liver fluke has also been reported to increase stocker calf gains (Armstrong and Miller, 1980; Malone et al., 1982). However, the designs for these studies may have been inappropriate because the treatment for fasciolosis (albendazole) is also a more effective nematocide than the product (thiabendazole) administered to control animals. In a subsequent trial using a valid control group (Loyacano et al., 1996), it was found that treating weanling calves with subclinical liver fluke infections had no significant effect on weight gains. Treatment for fluke infections has also been suggested to improve reproduction in cattle via an increase in growth and improved general body condition (Rickard et al., 1992). Other studies have suggested (Dargie, 1987; Lopez-Diaz et al., 1998) that fertility in heifers may be adversely affected by fasciolosis via an interruption of normal sex hormone metabolism in the liver, resulting in a delay in sexual maturity. The Dean Lee Research Station is located in central Louisiana in the Red River flood plain. The topography, soil types, vegetation and rainfall patterns at this site all are conducive to the maintenance of significant populations of GIN and F. hepatica. Although GIN infection is almost universal and liver fluke infection rates can approach 100% in young cattle, infection rates in beef replacement heifers are primarily subclinical at this location. The purpose of this research was to measure reductions in body weight gain and reproductive performance of beef replacement heifers and in the weaning weights of their first calves which might be attributed to subclinical nematode and liver fluke infections.
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2. Materials and methods 2.1. Heifers Three hundred and seventy-two Angus- or Brangus-sired heifers, spring born at this location from 1993 through 1996, were used in this study. Each year on approximately November 1, a sort by computer-generated random numbers was used to randomly allot one-third of the weaned heifers to each of three separate, adjacent 10 ha pastures. The heifers allotted to each pasture were then sorted by random numbers to the four treatment groups. Each year, each pasture contained equal numbers of heifers assigned to each treatment group. Eighty-four heifers were available from the 1993 calving season and 96 heifers were available in each of the succeeding three years. In 1993, there were 28 heifers in each pasture, seven from each treatment group. In the succeeding three years, there were 32 heifers in each pasture, eight per treatment group. Ninety-three heifers were allotted to each treatment group over the 4 years of the trial. Heifers in each of the two pasture groups were exposed to two Angus bulls and one group was exposed to two Brangus bulls from mid-April until the end of June. The same bulls were assigned to the same pastures each year and were examined for breeding soundness prior to each breeding season. Pasture groups remained intact until October when they were palpated for pregnancy diagnosis. Open heifers were then culled and pregnant heifers were pooled and moved to another pasture where they remained until their calves were weaned the following October. Separate yearly calf crops were used in each year of the study. After weaning of their calves, heifers were removed from the study and went into the general breeding herd. 2.2. Pastures The 10 ha pastures provided adequate amounts of growing forage for the heifers during most of the trial period and stocking rates were within normal stocking rates for yearling cattle at this location. Bermudagrass (Cynodon dactylon) and dallisgrass (Paspalum dilatatum) provided perennial warm season grazing. Pastures were overseeded with annual ryegrass (Lolium multiflorum) in October of each year to provide winter forage. Appropriate levels of ammonium nitrate were applied as needed. Bermudagrass hay was provided ad lib when sufficient quantities of growing forage were not available (60–90 days/year). Limited amounts of ground corn (1–2.5 kg per heifer for 30–60 days prior to the breeding season) were provided when necessary to meet the nutritional requirements for developing replacement heifers. 2.3. Treatment The heifers were given no anthelmintic treatments prior to entrance into the study. Treatment regimens were: Group 1, untreated controls; Group 2, treated for GIN only; Group 3, treated for Fasciola only, and Group 4, treated for GIN and Fasciola. For GIN control, Ivomec® (ivermectin, Merial) (years 1, 2 and 4) or Dectomax® (doramectin, Pfizer) (year 3) at the prescribed dosage of 200 ug/kg bodyweight were administered via subcutaneous injection. Curatrem® (clorsulon, Merial) drench was administered orally at the recommended
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dosage of 7 mg/kg bodyweight to control the liver fluke. Treatments (total of 7) were administered at allotment each year on approximately November 1, and were repeated in early December, early February, mid-March, at the beginning of the breeding season in mid-April, at the end of the breeding season in late June and at palpation in late September. Treatment dates were based on the anticipated risk of infection (weather conditions, nutritional status, pasture infection and history) until the heifers were palpated for pregnancy. Individual fecal samples were collected rectally from approximately half of the heifers at each treatment date to monitor infection levels. Nematode eggs per gram of feces counts (EPG) were determined by a centrifugation–flotation procedure with a saturated sucrose solution as a flotation medium (Cox and Todd, 1962). Liver fluke EPG counts were determined via a selective sieve and sedimentation method (Flukefinder, Pullman, WA). Subjective body condition scores (BCS) from 1 (emaciated) to 9 (excessively fat) were assigned at each treatment date by treatment blinded observers. Heifer weights were recorded at all treatment dates and calf weights were recorded at birth, 205 days of age and at weaning at approximately 250 days of age. The treatment regimen used was purely experimental and intended only for maximal suppression of GIN and/or liver fluke infections in order to more accurately measure effect of the treatments on prevention of cattle performance reductions.
3. Statistical analysis Data were analyzed following the general linear model procedure (P < 0.05) (SAS Institute, 1996) with significance levels set at P < 0.05 for all measured variables. The numbers of heifers were different between year 1 and years 2, 3 and 4 and number of calves and fecal samples collected were different between years, pastures, and treatments. Data were analyzed with year, pasture and treatment as main effects and all interactions between main effects were included in the model. Data were analyzed again with all non-significant (P < 0.05) interactions included in the error term. Year and pasture effects were significant as was expected and are not discussed in this report. Rainfall and temperature varied from year to year, affecting parasite burdens and forage production and nutrients available to the heifers and consequent effect on heifer performance. There were known minor differences in soil types, topography and forage production of the pastures utilized in this study which may also have affected parasite burdens and heifer performance. Least square means are presented in the tables. Fecal egg counts were transformed to the natural log(count + 1) for analysis and the least-square means were back transformed to geometric means for presentation. All data presented are calculated means for the 4-year period.
4. Results 4.1. Heifer performance Treatment group significantly affected heifer performance (Table 1). Initial weights at allotment did not differ among treatment groups. At breeding in March, heifers with
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Table 1 Effect of gastrointestinal nematodes and F. hepatica on heifer weights, gains (kg), body condition scores (BCS) and pregnancy rates (%)a Treatment group
1. No treatment 2. Nematodes only 3. Liver flukes only 4. Nematodes and flukes a
Initial Breeding weight Weight BCS 239 a 240 a 240 a 237 a
291 a 316 b 295 a 318 b
4.9 a 5.2 b 5.0 a 5.3 b
Breed end
Palpation
Gain
Weight
BCS
Weight
BCS
53 a 76 b 55 a 78 b
332 a 356 b 338 a 361 b
4.9 a 5.3 c 5.0 b 5.4 c
369 a 400 b 379 a 410 b
5.0 a 5.4 b 5.3 b 5.6 c
Total gain
Pregnancy rate
130 a 160 c 138 b 170 d
54 a 63 a 67 ab 78 b
Means within columns with the same letters are not different (P < 0.01).
untreated GIN infections (Groups 1 and 3) had lower mean weights (P < 0.01) than heifers that had been treated for GIN (Groups 2 and 4). Heifers with untreated GIN infections also had lower BCS than treated heifers. These relationships persisted until palpation in October. At the end of the breeding season (July 1), condition scores for heifers that were not treated for either GIN or flukes (Group 1) had significantly lower BCS than heifers that were treated for flukes only (Group 3). Heifers treated for flukes only had significantly lower BCS than heifers treated for GIN only. At palpation, Group 1 heifers had lower average scores than Group 2 and Group 3 heifers and Group 4 heifers had the highest condition scores. Untreated Group 1 heifers had significantly lower pregnancy rates than heifers that were treated for both GIN and flukes (Group 4). Treating for GIN alone (Group 2) did not significantly increase pregnancy rates and heifers treated for flukes only (Group 3) did not have significantly higher pregnancy rates than untreated control heifers or heifers that were treated for GIN only. However, the pregnancy rates for Group 3 heifers were not significantly lower than those of heifers that were treated for both forms of parasitism. 4.2. Calf performance Treatment had a substantial effect on calf weights (Table 2). Calves from the untreated Group 1 dams were lighter at birth than calves from Group 4 heifers that had been treated for GIN and flukes. Calves from heifers not treated for GIN (Groups 1 and 3) were lighter at weaning than those from heifers that were treated for GIN (Groups 2 and 4). When weights were adjusted for calf age and sex, calves from heifers treated for flukes only (Group 3)
Table 2 Least square means for treatment effect on calf weights (kg)a Treatment group
Birth weight (n)
Wean weight (n)
Adjusted wean weight
1. No treatment 2. Nematodes only 3. Liver flukes only 4. Nematodes and flukes
32 a (48) 34 ab (54) 32 a (59) 35 b (69)
196 a (34) 214 b (49) 199 a (49) 220 b (57)
223 a 240 bc 229 ab 248 c
a
Means within columns with the same letters are not different (P < 0.05). n is the number of calves.
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Table 3 Least square means for treatment effect on gastrointestinal nematode fecal egg counts (EPG)a Treatment group
Initial EPG
Prebreed EPG
End breed EPG
Palpation EPG
1. No treatment 2. Nematodes only 3. Liver flukes only 4. Nematodes and flukes
92 a 86 a 98 a 82 a
15 a 5b 14 a 5b
29 a 11 a 19 a 13 a
35 a 23 a 18 a 31 a
a
Means within columns with the same letters are not different (P < 0.05).
were not significantly heavier than calves from untreated Group 1 heifers nor significantly lighter than calves from Group 2 heifers which were treated for nematodes only. 4.3. Fecal egg counts Initial individual heifer GIN counts ranged from 0 to 600 EPG. On a yearly basis, mean initial counts ranged from 58 to 119 EPG. Individual heifer fluke egg counts ranged from 0 to 6.5 EPG and annual mean initial counts ranged from 2.17 to 2.96 EPG. Initial GIN fecal egg counts were not significantly different between treatments (Table 3). At the beginning of the breeding season, an average of 46 days post-treatment, heifers treated for GIN (Groups 2 and 4) had significantly lower (P < 0.05) average egg counts than those that had not been treated for GIN (Groups 1 and 3). At the end of the breeding season and at palpation when fecal samples were collected at 60–84 days following treatment, there were no significant treatment effects on nematode egg counts. Fecal egg counts in this study were not used as a measure of treatment efficacy. They were used to monitor the presence of parasite infection and to verify that the heifers were exposed to continual infection. Initial fluke egg counts were not different between treatments (Table 4). Initial prevalence or infection rate was 30%. At the beginning of the breeding season and throughout the trial periods, heifers treated for flukes had significantly lower egg counts than heifers that were not treated for flukes. Mean egg counts for control heifers increased from 0.23 at trial initiation to 1.5 at palpation. Although mean fluke egg counts never exceeded 1.55 eggs per gram, counts for untreated heifers increased over time and greatly exceeded the counts of treated heifers at the end of the trial. The patent infection rate for heifers with untreated fluke infections was 80% at palpation compared to 35% for heifers treated for flukes. Table 4 Least square means for treatment effect on F. hepatica fecal egg counts (EPG)a Treatment group
Initial EPG
Prebreed EPG
End breed EPG
Palpation EPG
1. No treatment 2. Nematodes only 3. Liver flukes only 4. Nematodes and flukes
0.23 a 0.30 a 0.38 a 0.49 a
0.37 a 0.40 a 0.00 b 0.06 b
0.86 a 0.87 a 0.22 b 0.26 b
1.50 a 1.55 a 0.15 b 0.50 b
a
Means within columns with the same letters are not different (P < 0.05).
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5. Discussion Therapeutic suppression of nematode infections alone resulted in significantly increased bodyweight, bodyweight gain and BCS in replacement heifers, but not in significantly higher pregnancy rates. Suppression of fluke infections alone significantly increased BCS after the breeding season and increased total weight gain, but did not significantly affect pregnancy rates. Simultaneous suppression of both GIN and flukes resulted in increased pregnancy rates. Since body weights and condition scores of heifers treated for GIN only were not significantly lower than those of the heifers treated for both GIN and liver flukes, the significant increase in pregnancy rates of heifers treated for both GIN and flukes cannot be explained by increases in bodyweight or general condition. These data support observations of Lopez-Diaz et al. (1998) which reported that puberty was delayed 39 days in Friesian heifers which had been infected with 600 F. hepatica metacercariae. Infected heifers in that study had elevated serum E2 levels and lowered P4 levels which were attributed to an alteration in the metabolic clearance rate of estrogens in the liver. The elevated levels of serum E2 were hypothesized to upset the normal prepubertal production of GnRH and LH and delay the development of corpus lutea and the onset of puberty. In a controlled breeding season, this would result in later calving dates and lower calving rates. The data from this study suggested that the effects of GIN and liver flukes on performance were through different mechanisms and that the effect of the two forms of parasitism may be additive. It was apparent that GIN infections can prevent replacement heifers from reaching adequate body weights and condition scores at breeding age and that fluke-induced alterations of metabolic processes in the liver, which stimulate heifers to puberty, may also have been operative. Significant infection with either form of parasitism could reduce heifer fertility. Treatment for one form of parasitism, when both are present in the animals and environment, may not significantly improve heifer reproductive performance. In the case of heifers not treated for nematode infections, results indicated this as a possible cause of reduced calf weights. However, heifers treated for fluke infections only produced calves with age adjusted weaning weights that were not significantly heavier than calves from untreated heifers, but were not significantly lighter than calves from those treated for GIN only. Although economic benefits of GIN control are widely acknowledged, the benefits of controlling concomitant liver fluke infections have often been obscured due to combined nematocidal and flukicidal activity of common anthelmintics (albendazole, ivermectin/clorsulon). Results supportive of the present work have been reported by Holste et al. (1986), Rickard et al. (1992) and Kaplan (1994). The latter authors suggested that the difficulty in quantifying economic benefits of fluke control is because of interactions among physiologic, nutritional-associated diseases, climatic and geographic factors which cause extensive variation in pasture infectivity and variation in infection rate and severity over years and location. Consideration of cost effectiveness with the suppressive treatment regimen used in this study was not feasible, although performance values and gross returns for heifers treated for GIN only and for GIN and flukes would likely have yielded cost effectiveness based on an average cost of the drugs used, US$4.00–6.00 per treatment. Estimated sale value ($1.43 and 1.80 per kg for open heifers and calves, respectively) and pregnancy rates were factored together to calculate average gross returns per heifer of US$507, 545, 516 and 555 for untreated
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heifers, heifers treated for GIN only, heifers treated for flukes only and heifers treated for both forms of parasitism, respectively. Routine strategic treatments where used in this region of high GIN and fluke prevalence, i.e., treatment for GIN and flukes in the fall at weaning, in the spring prior to breeding and again during the following fall prior to calving, should produce results similar to those in the present report. The third treatment for heifers late in their gestation can benefit calves through generally reduced pasture contamination and larval intake and possible improved milk production in dams. It is essential that strategic treatments be based on sound epidemiological data for the parasites in a given geographic region. References Armstrong, D.A., Miller, C.R., 1980. Liver flukes in cattle: life cycle, pathology, economic impact. Norden News, 30–33. Cox, D.D., Todd, A.C., 1962. Survey of gastrointestinal parasitism in Wisconsin dairy cattle. J. Am. Vet. Med. Assoc. 141, 134–139. Dargie, J.D., 1987. The impact on production and the mechanisms of pathogenesis of trematode infections in cattle and sheep. In: Leaning, W.H.D., Guerrero, J. (Eds.), The Economic Impact of Parasitism in Cattle. Proc. MSD AGVET Symp., XXII World Vet. Cong., Montreal, Canada, pp. 35–43. Gibbs, H.C., 1987. The effect of gastrointestinal nematodes on digestion and energy metabolism in calves. In: Leaning, W.H.A., Guerro, J. (Eds.), The Economic Impact of Parasitism in Cattle. Proc. MSD AGVET Symp., XXII World Vet. Cong., Montreal, Canada, pp. 35–43. Herd, R.P., 1993. Control strategies for ruminant and equine parasites to counter resistance, encystment, and ecotoxicity in the USA. Vet. Parasitol. 48, 327–336. Holste, J.E., Wallace, D.H., Hudson, D.B., Benz, G.W., Ericsson, G.F., 1986. Reproductive performance of beef cows treated with ivermectin before calving. Mod. Vet. Pract. 67, 462–464. Kaplan, R.M., 1994. Liver flukes in cattle: control based on seasonal transmission dynamics. Compend. Contin. Ed., Food Animal 5, 687–693. Lopez-Diaz, M.C., Carro, M.C., Cadorniga, C., Diez-Banoa, P., 1998. Puberty and serum concentrations of ovarian steroids during the prepuberal period in Friesian heifers artificially infected with Fasciola hepatica. Theriogen. 50, 587–593. Loyacano, A.F., Williams, J.C., Coombs, D.F., Hawkins, J.A., 1991. Effect of parasites on fertility and gains of beef heifers. Louisiana Agric. 34, 6–7. Loyacano, A.F., Williams, J.C., Gurie, J., 1996. A comparison of albendazole with ivomec and curatrem. Annual Research Report. Dean Lee Research Station, Louisiana State University, pp. 11–16. Malone, J.B., Loyacano, A.F., 1991. Earth observation satellite systems, climate and soil type risk assessment and control of liver flukes. Beef Cattle Sci. Handbook 25, 135–143. Malone, J.B., Smith, P.H., Loyacano, A.F., Hembry, F.G., Brock, L.T., 1982. Efficacy of albendazole for the treatment of naturally acquired Fasciola hepatica in calves. Am. J. Vet. Res. 73, 879. Purvis, H.T., Whittier, J.C., Boyles, S.L., Johnson, L.J., Ritchie, H.D., Rust, S.R., Faulkner, D.B., Lemenager, R.P., Hendrix, K.S., 1994. Weight gain and reproductive performance of spring-born beef heifer calves intraruminally administered oxfendazole. J. Anim. Sci. 72, 817–823. Rickard, L.G., Zimmerman, G.L., Hoberg, E.P., Bishop, J.K., Pettitt, R.J., 1992. Influence of ivermectin and clorsulon on productivity of a cow-calf herd on the southern Oregon coast. Vet. Parasitol. 41, 45–55. Ryan, W., Brown, J., Corah, L., Doornbos, D., Loyacano, A., Spire, M., 1992. Evaluation of the impact of ivermectin treatment on the growth and reproductive performance of replacement heifers. Proc. XVII World Buiatric Cong., and XXV Am. Assoc. Bovine Pract. Conf., St. Paul, MN, Vol. 1, pp. 23–28. SAS Institute, 1996. SAS/STAT Software, Release 6.11. SAS Institute Inc., Cary, NC. Williams, J.C., 1986. Epidemiologic patterns of nematodiasis in cattle. In: Gibbs, H.C., Herd, R.P., Murrell, K.D. (Eds.), Parasites: Epidemiology and Control. Vet. Clin. N. Am., Food Anim. Pract. 2, 235–246. Williams, J.C., Knox, J.W., Loyacano, A.F., 1992. Impact of gastrointestinal parasitism in grazing cattle. Proceedings of the 48th Southern Pasture and Forage Crop Improvement Conference, Auburn University, Auburn, AL, pp. 75–85.