- Email: [email protected]
Prevalence and epidemiology of trichostrongylids in Wyoming cattle with consideration of the inhibited development of Ostertagia ostertagi
veterinary parasitology ELSEVIER
VeterinaryParasitology64 (1996) 285-297
Prevalence and epidemiology of trichostrongylids in Wyoming cattle with consideration of the inhibited development of Ostertagia ostertagi A. Malczewski a,., W.R. Jolley b, L.F. ¢6roodard b a W. StefahskiInstitute of Parasitology, Polish Academy of Sciences, L. Pasteur 3, P.O. Box 153, 00-973 Warsaw, Poland Department of Veterinary Sctences, Universityof Wyoming, Laramie, WY 82071, USA b
•
•
Received 8 June 1995; accepted 1 October 1995
Abstract During 1988, monthly collections of abomasa and the cranial portion of the small intestine of 208 native Wyoming cattle were examined for adult and larval helminth parasites. Egg counts were performed on colonic faecal specimens. The animals ranged from 7 months to 8 years of age and were sampled at slaughter houses or diagnostic laboratories from five different counties in the State. Most of the cattle had ranged for a long time on non-irrigated, high altitude grass plains from about 1250 to 2500 m above sea level. All animals examined were found infected. Nematode genera (and number of species) found included Ostertagia (4), Trichostrongylus (2), Haemonchus (1), Cooperia (4) and Nematodirus (2). One trematode, Fasciola hepatica, and a cestode, Moniezia benedeni, also were found. Trichostrongylus axei, Trichostrongylus longispicularis and Cooperia lyrata were found for the first time in Wyoming, Ostertagia circumcincta was found for the first time in cattle in Wyoming, and Haemonchus placei, tentatively identified in a previous survey, was def'mitively confirmed. Predominant species (and prevalence) were Ostertagia ostertagi (98%), Cooperia oncophora (60.6%), Ostertagia bisonis (41.8%), Cooperia bisonis (33.6%) and T. axei (27.9%). One or more of the four species of Ostertagia were found in all animals. Inhibited O. ostertagi and O. bisonis larvae predominated from November to April and reached a peak in January to comprise 88% of the total nematode burden for that month. The adult population of abomasal nematodes peaked in April and predominated thereafter until October. Haemonchus placei also spent the autumn-winter period in an inhibited state of development. Faecal egg counts were lowest during winter months, when the highest numbers of worms were present as L 4 larvae, as determined by luminal and mucosal counts. Nematode populations in the
* Correspondingauthor. Tel/Fax: + 48-22-222562. 0304-4017/96/$15.00 Copyright © 1996 Elsevier Science B.V. All rights reserved. SSD! 0304-4017(95)00924-8
286
A. Malczewski et al. / Veterinary Parasitology 64 (1996) 285-297
small intestine peaked in June and persisted until November. The results of this study showed the magnitude and species composition of nematode parasitism in cattle raised on high altitude grass plains, underscored the inaccuracy of faecal egg counts as an indicator of worm burden during fall and winter seasons, and provided information on which anthelmintic treatment timing would be most efficacious. Keywords: Cattle-Nematoda; Epidemiology-Nematoda;Ostertagia ostertagi
1. Introduction The trichostrongylids have long been recognized as important parasites of cattle. Within the last two decades, Ostertagia ostertagi has emerged as the most important member of the group due to its ability to enter the mucosa of the abomasum and suspend development in a larval stage. The state of dormancy/hypobiosis/larval inhibition, appears to be a survival mechanism that enables the worm to preserve its reproductive potential through inclement seasons until conditions favour exogenous development and transmission. Larval inhibition in northern, cool regions of the USA has been demonstrated in Washington (Malczewski et al., 1975), Oregon (Kistner et al., 1979), Idaho and Maine (Gibbs, 1979), Michigan (Schillhorn Van Veen and Melancon, 1984) and Ohio (Herd, 1980) from autumn until spring. In contrast, the phenomenon has been shown to occur in the warm, southern states of Georgia (Ciordia et al., 1971), southern California (Baker et al., 1981), Texas (Suderman, 1979), Louisiana (Williams and Knox, 1976; Williams, 1981, Williams, 1986; Williams et al., 1983, Williams et al., 1987), and Missouri (Brauer, 1983) from spring through summer. However Zimmerman et al. (1993) considered, that "inhibition in the northwest does not fall strictly into either the northern or southern pattern. Data from both Montana and Oregon support the concept of a wide and variable transition zone in the northwest". With any parasitic disease, recognition of changes in seasonal incidence, prevalence and relative burden is a key to planning an effective control program. Previous surveys of cattle in Wyoming for internal parasites conducted from 1957 to 1961 (Honess, 1957; Honess and Bergstrom, 1963, Honess and Bergstrom, 1966) and 1973 to 1977 (Werner and Bergstrom, 1983) included only 32 necropsies and were based mainly on faecal egg counts. Information concerning the seasonal dynamics of gastrointestinal nematode populations in Wyoming cattle has been inadequate, especially regarding O. ostertagi. Cattle numbers in Wyoming exceeded 1.3 million animals in 1988, constituting a important component of the state's economy. Determination of the seasonal dynamics of bovine trichostrongylid infections in general, With emphasis on inhibition of O. ostertagi in particular, was undertaken to facilitate more effective control of detrimental nematode infections in native livestock. Ungulates raised on the high, grass plains of Wyoming and other regions with similar environmental conditions require management techniques specific for their climatic and meteorologic conditions. Trichostrongylid epidemiology is underdefined for the region. The objectives of the present study were: (1) to determine by necropsy the monthly prevalence and magnitude of helminth parasite populations in abomasa and cranial part of the small intestine of cattle native to Wyoming, and (2) to
A. Malczewski et a l . / Veterinary Parasitology 64 (1996) 285-297
287
Table 1 Age distribution of Wyoming cattle examined for abomasal and small intestinal nematodes in 1988 Approximate age in months
No. of animals
7 10 12 18 24 30 36 48 60 72 96
1 2 28 100 48 11 5 7 4 I 1
establish whether or not inhibited development of the nematode O. ostertagi in cattle native to Wyoming occurs and its timing.
2. Materials and methods
The entire abomasum, anterior 3 m portion of the small intestine and samples of colonic faeces were collected from 208 native Wyoming cattle, slaughtered for beef (196) or necropsied (12) at the Wyoming State Veterinary Laboratory (WSVL) for routine diagnostic purposes (Table 1); livers were also examined. An average of 17 collections was made monthly from January through December 1988. Collection points in the state (and numbers of animals examined) were Lander (102), Worland (9), Torrington (70) and Laramie (27). The cattle ranged in age from 7 months to 8 years, and most had been on pasturage consisting mainly of native perennial grasses at elevations from about 1250 to 2500 m above sea level during some or most of their lives. Visceral and faecal specimens were transported to the WSVL in Laramie for examination by standard methods (Ritchie et al., 1966). Adult and larval worms were collected, counted and identified from luminal contents or digested portions of abomasai mucosa. The differences in monthly numbers of adult worms with developing stages (including late L 4 larvae and L 5 juveniles), and inhibited early L 4 (EL 4) larvae, were statistically analysed by the t-test. Numbers of eggs per gram of faeces were determined with the salt flotation technique of Willis (Willis, 1921). Differences in the monthly egg counts were statistically analysed at a 95% confidence level.
3. Results
3.1. Helminth species Thirteen nematode, one trematode and one cestode species were found in the abomasum, small intestine or liver of cattle examined in the survey (Table 2). All of the
288
A. Malczewski et al./ Veterinary Parasitology 64 (1996) 285-297
208 native cattle examined were infected with one or more helminth species, with O.
ostertagi (98%), Cooperia oncophora (60.6%), Ostertagia bisonis (41.8%), Cooperia bisonis (33.6%) and Trichostrongylus axei (27.9%) predominating. The remaining species found were few in number and low in prevalence. Trichostrongylus axei, Trichostrongylus longispicularis and Ostertagia lyrata were identified for the first time in Wyoming, and Ostertagia circumcincta was found in native cattle for the first time. Haemonchus placei, tentatively identified from native cattle in a previous study (Honess and Bergstrom, 1963) was definitively identified in the present survey. The flatworms were incidental to the study objectives.
3.2. Abomasal nematodes All of the cattle harboured one or more of the four species of Ostertagia, O. ostertagi (98%), O. bisonis (41.8%), O. circumcincta (2.4%) or O. lyrata (0.48%) (Table 2). The Ostertagia species in 100%, T. axei in 27.9% and H. placei in 6.7%, numerically dominated the worm population in the digestive tract every month of the year (Table 2, Fig. lb). Total worm numbers were greatest in January (21019) and lowest in September (800) (Table 3, Fig. lb). Inhibited EL 4 larvae were predominant in November (967), December (2861) and January (18435), comprising 61%, 73% and 88%, respectively, of the populations. The monthly composition of populations by developmental stage is shown in Fig. 2. Adult and developing stages peaked in April, but predominate over inhibited larvae from February through October. The lowest numbers of adult and developing stages persisted from September through November (Table 3). There were clear variations in the proportion of inhibited larvae to adult and developing forms, e.g. in January when the inhibited EL 4 stage predominated (88%), adult and developing forms were least prevalent (12%); the reverse was seen in April, when adults and developing forms were most prevalent (84%) and EL4s were few (16%) (Table 3, Fig. 2). Analysis with the t-test showed the differences between monthly numbers of adults and those of developing stages and inhibited EL 4 larvae to be significant each month from February through October, with the exception of May. This supported the gross observation of predominance of the adult and developing stages for those months. The most prevalent nematode species in the abomasum was O. ostertagi, found in all cattle but four (Table 2). Ostertagia bisonis was more prevalent during the autumnwinter months than in summer. Haemonchus placei, in contrast, was found in one to three animals during consecutive months of April through September with a peak prevalence of 23% in June (Table 2). Trichostrongylus axei was found every month, from a low of 6% of animals in March to a high of 60% in April, but did not demonstrate any observable seasonal trends (Table 2). The relative monthly prevalence of the dominant abomasal species is shown in Fig. 3.
3.3. Small intestinal nematodes Cooperia species were predominant in the small intestine, with C. oncophora in 60.6%, C. bisonis in 33.6%, Cooperia zurnabada in 13.0% and Cooperia punctata in
20 11 13
12 20 20 20
23 24
April May June
July August September October
November December
23 24
12 20 20 20
20 11 13
13 15 17
204 98
22 24
12 19 18 20
20 11 13
87 41.8
8 10
3 7 6 4
2 5 7
8 12 14
O,B
O,O
13 15 17
No. cattle
No. cattle
5 2.4
-
1
1 1
1 1
O,C
Worm
1 0.48
-
. -
-
1 -
O,L
58 27.9
6 4
5 2 7 3
5 2.4
1
2 1 . 1 -
-
-
12 4 5
1
T,L -
T,A 7 2
14 6.7
1
1 2 1 -
2 2 3
-
2
H,P
C,B
70 33.6
4 8
5 9 . 6 10
5 2 4
8
4 5
126 60.6
3 7
10 12 10 14
13 6 9
15
12 15
C,O
.
1 0.48
-
-
1
. -
-
-
C,P
.
C,Z
27 13
2 4
4 1 5 3
1
1
1
3 2
.
N,H
9 4.3
2 -
-
-
-
-
2
2 3
.
N,SP
1 0.48
1
-
-
-
F,H
9 4.3
1 1
1 2
-
-
-
4 -
M,B
70 33.6
4 8
5 9 6 I0
5 2 4
8
4 5
O,O:
Ostertagia ostertagi; O,B: Ostertagia bisonis; O,C: Ostertagia circumincta; O,L: Ostertagia lyrata; T,A: Trichostrongylus axei; T,L: Trichstrongylus longispicularis; H,P: Haemonchus placei; C,B: Cooperia bisonis; C,O: Cooperia oncophora; C,P: Cooperia punctata; C,Z: Cooperia zurnabada; N,H: Nematodirus helvetianus; N,SP: Nematodirus species (undetermined); F,H: Fasciola hepatica; M,B: Monezia benedeni.
Totals 208 208 Mean prevalence (%)
13 15 17
January February March
Month
Table 2 Monthly examinations, helminth parasite species and prevalence in W y o m i n g cattle in 1988
~"
t,J
I ".~ b~ ~0
,,~
~
~ 8"
O.
13 15 17 20 11 13 12 20 20 20 23 24
January February March April May June July August September October November December
13
(~)
1490 2021 1494 5345 974 2837 2050 1530 628 651 545 951
(7) (43) (44) (44) (72) (53) (54) (68) (42) (55) (30) (22)
1094 1851 1012 4524 174 547 331 150 16 80 67 107
(5) (39) (29) (37) (13) (10) (9) (7) ( 1) (7) (3) (3)
18435 389 494 1920 116 117 135 27 156 92 967 2861
(87) (8) (14) (16) (9) (2) (3) (1) (10) (8) (53) (66)
276 452 442 414 87 1908 1278 535 703 351 252 392
Intestinal (%)
C4
D2
A~
(%)
Abomasal
Mean nematode counts
Al , adults; D 2, developing stages; 13, inhibited larvae; C 4, combined stages.
No. examined
Month
( 1) (10) (13) (3) (6) (35) (34) (24) (47) (30) (14) (9)
(%)
21295 4713 3442 12203 1351 5409 3794 2242 1503 1174 1831 4311
Total
Table 3 Monthly examinations, abomasal and intestinal nematode counts, and faecal nematode egg counts from Wyoming cattle in 1988
4,5 3.5 32.0 64.0 4.8 61.0 46.0 53.0 7.5 28.0 7.0 6.9
Mean eggs per gram
"-4
t,o
e,
I,o
A. Malczewski et a l . / Veterinary Parasitology 64 (1996) 285-297 80 ~
291
A
L
O
I
20
[]
B
ABOMASAL SMALL INTESTINAL
•
25
0
z
iiiiiiii!iiii!ii
0
~
iiiiiliiii!i!ililili!iiiiii[
i'i~ii~ii!~!! !iii!il
5
!ii!i!iiiii!i!i!iii!iiiiiiiil iii!ii!ii!ii!ii!i~i!it
!i JAN
r FEB
iiiiiiiiiiiil MAR
AI~R
MAY
JUN
JUI.
MONTH
AUG
SEP
Fig. 1. (A) Mean monthly faecal egg counts. (B) Mean monthly abomasal, small
OCT
NOV
I)]~("
intestinal a n d c o m b i n e d total
worm counts.
0.48% of the cattle. Cooperia oncophora and C. bisonis had similar patterns of prevalence during the annual cycle. Trichostrongylus longispicularis in 2.4%, Nematodirus heloetianus in 4.3% and an unidentified Nematodirus species in 0.48% of the
292
A. Malczewski et a l . / Veterinary Parasitology 64 (1996) 285-297
100
•
90 Z
80
0
70
ADULT WORMS
[]
DEVELOPINGSTAGES
[]
INHIBITEDLARVAE
87
66
50
© 40
© 30 ~" 20 10 0
i
JAN
FEB MAR APR MAY J U N
J U L A U G SEP
OCT NOV DEC
MONTH Fig. 2. Life cycle stage compositionof abomasal lrichostrongylidpopulation in Wyomingcattle.
• []
OSTERTAGIAOSTERTAGI [] TRICHOSTRONGYLUSAXEI [ ]
OSTERTAGIABISONIS HAEMONCHUSPLACEI
100 90 70 Z
60 50
<
40
30 © 20 ~- 10 JAN
FEB MAR APR MAY JUN
JUL AUG
SEP
o C T NOV DEC
MONTH Fig. 3. Monthly prevalenceof dominant abomasal ~chostrongylids in Wyomingcattle.
A. Malczewski et al. / Veterinary Parasitology 64 (1996) 285-297
293
animals were the least numerous species (Table 2). Individual species did not show important seasonal changes in population composition (Table 2), but when considered as a group, peaked in June and remained high through September (Fig. lb). Throughout the year, however, the small intestinal population failed to equal or exceed the abomasal population (Table 3, Fig. lb). 3.4. Faecal egg counts
Faecal egg counts performed during the season of larval inhibition did not reflect the true intensity of infection. Faecal egg content appeared to vary seasonally, rather than with worm numbers (Table 3, Fig. la and Fig. lb); for example, one steer examined in January harboured more than 200 adult and 69 120 inhibited larvae of Ostertagia species and over 800 adult and developing forms of Cooperia species but only expelled an average of 1 epg of faeces. Furthermore, in November, 12 of 23 faecal samples examined were negative for eggs, despite worm counts indicating that cattle harboured an average number of 1831 worms, about 35% of which were adults (Table 3, Fig. 2). In contrast, faeces of the 20 cattle examined in August contained an average 53 epg, all samples examined were positive, and the worm counts averaged a modest 2242, most of which were adults (Table 3, Fig. 2). 3.5. Foreign species
The finding of O. bisonis in the abomasum of 41.8% and C. bisonis in the small intestine of 33.6% of cattle slaughtered in all packing houses in the survey was of
•
COOPERIAONCOPHORA
[]
COOPERIABISONIS
[]
COOPERIAZURNABADA
lnn
Z
O
U
JAN FEB MAR APR MAY JUN JUL AUG SEP OCT NOV DEC
MONTH Fig. 4. Monthlyprevalenceof dominant intestinaltrichostrongylidsin Wyomingcattle.
294
A. Malczewski et aL / Veterinary Parasitology 64 (1996) 285-297
special interest. The two species are commonly associated with wild ruminants, but appeared in the survey cattle in significant numbers (Table 2, Fig. 3 and Fig. 4).
4. Discussion
4.1. Helminthsfound Thirteen parasitic nematode species were found in the survey. Three, T. axei, T. longispicularis and O. lyrata, were not previously reported from any hosts from Wyoming, and one, O. circumcincta, was previously found in Wyoming sheep but not cattle. Haemonchus placei was tentatively identified from five mature cattle in an early survey by Honess and Bergstrom (1963), but too few specimens were recovered to allow positive identification. In 14 (6.7%) of the 208 cattle examined in the present survey, enough male and female specimens were recovered to allow identification. The one trematode, Fasciola hepatica, and one cestode, Monezia benedeni are common in Wyoming cattle. The finding of Ostertagia and Cooperia species to be the most common nematodes every month agreed generally with earlier surveys, although the presence of the Ostertagia species in all cattle examined is unprecedented. The finding of T. axei in 58 (27.9%) of the survey animals extended the reported range of the species and, by virtue of its prevalence, suggested its potential importance. The identification of four nematode species previously unreported in Wyoming cattle and the clarification of another's identity underscores the value of necropsy-based data collection in studies of this type.
4.2. Abomasal nematodes The consistent monthly numerical dominance of gastrointestinal nematode populations by the six species of abomasal nematodes found in this study reinforces the findings of previous authors (Olsen, 1949; Honess, 1957; Honess and Bergstrom, 1963; Worley and Sharman, 1966; Smith, 1974; Williams, 1986). The Ostertagia species, especially O. ostertagi and O. bisonis, were clearly well adapted to surviving the relative dry, cool environmental conditions common to the high-altitude ranges in Wyoming. Differences in the patterns, mechanisms or locations of larval inhibition may partially explain the differences in prevalence between species. The build-up of inhibited EL 4 larvae, which began slowly in September, peaked in January and decreased abruptly in February, mainly involved the Ostertagia species. A similar pattern for H. placei is probable, as indicated by the finding of inhibited EL 4 larvae in two cattle in February, and developing juveniles in April. The sudden release of inhibition, followed by development to juvenile and adult worms that occurred from mid-January to the peak in the adult population in April may have been due to a combination of factors, including climatic conditions, biological differences between species in development and in cattle management methods. Cattle in Wyoming are often maintained on pasture year-long, where native hay is provided as needed depending largely on weather and forage availability.
A. Malczewski et aL / Veterinary Parasitology 64 (1996) 285-297
295
An illustration of temporal differences in prominence of species can be seen by comparing the prevalence of O. bisonis with that of O. ostertagi, as shown in Fig. 3. Where O. bisonis was most prevalent in late winter (61.5% in January, peaked at 82% in March) and then decreased to a seasonal low in April (10%), O. ostertagi prevalence remained high and steady throughout the year. Trichostrongylus axei contributed to the April peak of adult worms and exhibited steady prominence through the pasture season. After cattle were placed on wintering pastures in late autumn, during the time inhibited EL 4 larvae of Ostertagia species were accumulating. Pasture contamination with eggs and larvae may have been important where animal density was high, despite the relatively low average number of adult worms and egg count. In view of the complimentary, slightly different dynamics of spring development between O. ostertagi and O. bisonis, the latter species may play an important role in Type II ostertagiosis. Acknowledged to be a parasite of wild ruminants (Dikmans, 1942), it has also been reported in cattle of Wyoming (Honess and Bergstrom, 1963) and Colorado (Olsen, 1949), and has caused gastritis in cattle in Montana (Worley and Sharman, 1966). The peak of adults and developing larvae that occurred in April was undoubtedly due to maturation of overwintered, inhibited larvae. Thereafter, for at least the next 5 months, adult populations were probably a result of newly acquired larvae from pasture. Contamination of pastures by the adult worms of the April population peak was undoubtedly significant. The autumn-winter inhibition of Ostertagia species is a phenomenon seen in temperate zones in countries other than the USA, including Canada (Smith, 1974), Scotland (Anderson et al., 1965), England (Michel, 1969, Michel, 1974) and Poland (Malczewski, 1970).
4.3. Small intestinal nematodes The relatively constant monthly numbers of the Cooperia species attests to the level of adaptation of the genus to cattle reared in Wyoming's harsh environment. The finding of insignificant numbers of inhibited small intestinal forms in the cattle in late winter suggests that their survival mechanisms differ from those of Ostertagia. A possible difference may include a greater ability to develop and survive in the exogenous environment, rather than a need for refuge in the host. The mechanisms of such, if they exist, have not been defined. Neither Cooperia species, nor the other, less numerous nematodes of the small intestine are considered to be as clinically important as the abomasal species, particularly those of Ostertagia. The reasons include dominant numbers, higher prevalence, and histopathologic evidence of ostertagial abomasitis. Two aspects of the survey were less informative than was desired. First, in the four study animals less than 1 year of age, no evidence of inhibited larvae or histopathology was found and no conclusions could be reached regarding the value of the calves in interpretation of data. Second, since only the cranial portion of the small intestine was collected for examination, the importance of Nematodirus species was not adequately assessable, because they are more common in lower regions of the gut than was collected. Members of the genus were considered a problem in cattle from a previous study (Honess, 1957).
296
A. Malczewski et al./ Veterinary Parasitology 64 (1996) 285-297
4.4. Control considerations The importance of understanding local or regional epidemiologic factors is clearly defined by previous studies (Williams, 1983; Wescott, 1984; Williams et al., 1986, Williams et al., 1990; Corwin, 1986; Baker and Farver, 1990). The current survey provided a basis for recommendations to control gastrointestinal nematode parasitism in cattle raised on grass ranges at high altitudes. In nearly every case, O. ostertagi should be the focus of control efforts, which would incidentally control other nematode populations that might be present. Drugs with systemic activity must be used to control inhibited EL 4 stages. Cheaper drugs can control lumenal stages of worms responsible for acute disease and contamination of pastures. The selection of drugs to be used and times of treatment may be determined by herd health history, helminth load insofar as can be accurately determined, a n d / o r stocking rate. Faecal egg counts can be used to estimate worm loads after inhibited forms develop into egg-laying adult worms, but should not be relied upon during the off-pasture season when actual worm numbers may be highest and egg counts lowest. Pasture rotation and contamination factors have not been adequately studied in states like Wyoming, where pastures/ranges are relatively large, wild ungulates and cattle harbour many of the same helminth parasites, and cattle are commonly kept on pasture all year. More such epidemiologic information is needed before non-drug methods can be factored into control programs.
Acknowledgements The authors are grateful for the cooperation of Charles Erickson of Wind River Meats, Frank Smith at Kelly Pack and others who aided in the collection and processing of specimens. This study was supported in part by a grant from MSD AGVET.
References Anderson, N., Armour, J., Jenning, F.W., Ritchie, J.D. and Urguhart, G.M., 1965. Parasitic gastritis in cattle. Vet. Rec., 77:1196-1204. Baker, N.F. and Farver, T.B., 1990. Strategic use of anthelmintics to prevent parasitic gastroenteritis in cow-calf herds in California. Am. J. Vet. Res., 51: 1663-1667. Baker, N.F., Fisk, R.A., Bushnell, R.P. and Oliver, M.N., 1981. Seasoaal occurrence of infective nematode larvae on irrigated pasture grazed by cattle in California. Am. J. VeL Res., 42:1188-1191. Braner, M.A., 1983. Epidemiology and bionomics of Ostertagia ostertagi in beef cattle in Missouri. Ph.D. Thesis, University of Missouri, Columbia, p. 161. Ciordia, H., Neville, W.E., Baird, D.M. and McCampbell, H.C., 1971. Internal parasitism of beef cattle on winter pastures: level of parasitism as effected by stocking rates. Am. J. Vet. Res., 32: 1353-1358. Corwin, R.M., 1986. The ContTol of Internal Parasites of Cattle. Edited by Hoechst Russel Agri-Vet. Comp. Dikmans, G., 1942. New host records. Proc. Helminth Soc. Washington, 9: 65. Gibbs, H.C., 1979. Relative importance of winter survival of larval nematodes in pasture and infected carrier calves in a study of parasitic gastroenteritis in calves. Am. J. Vet. Res., 40: 227-231. Herd, R.P., 1980. Animal health and public health aspects of bovine parasitism. J. Am. Vet. Med. Assoc., 32: 1353-1358.
A. Malczewski et al./ Veterinary Parasitology 64 (1996) 285-297
297
Honess, R.F., 1957. Helminths of Wyoming cattle: internal roundworms. Cow Country, 84: 21-25. Houess, R.F. and Bergstrom, R.C., 1963. Intestinal roundworms of cattle in Wyoming. Univ. Wyo. Agric. Exp. Stn. Bull, 410: 1-36. Houess, R.F. and Bergstrom, R.C., 1966. Trichostrongylosis of cattle in Wyoming. Univ. Wyo. Agric. Exp. Stn. Sci. Monogr., 2: 1-29. Kistuer, T.R., Wysc, D. and Averkin, E., 1979. Efficacy of oxfendazole against inhibited Ostertagia ostertagi in natural infected cattle. Aust. Vet. J., 55: 232-235. Malczewski, A., 1970. Gastrointestinal helminths of ruminants in Poland. IIL Seasonal incidence of the stomach worms in calves, with consideration of the effect of the inhibition phenomenon on the spring rise phenomenon. Acta Parasitol. Pol., 18: 417-434. Malczewski, A., Wescott, R.B., Spratling, B.M. and Gorham, I.R., 1975. Internal parasites in Washington cattle. Am. J. Vet. Res., 36: 1671-1675. Michel, J.F., 1969. Observations on epidemiology of parasitic gastroenteritis in calves. J. Helminthol., 43: lll-133. Michel, J.F., 1974. Arrested development of nematodes and some related phenomena. Adv. Parasitol., 12: 279-366. OIsen, O.W., 1949. Emendation of the description of the male of Ostertagia bisonis with a note of its occurrence in cattle. J. Colorado-Wyoming Acad. Sci., 4: 65. Ritchie, J.D.S., Anderson, N., Armour, J., Jarreti, W.F.H., Jennings, F.W. and Urgnhart, G.M., 1966. Infections in calves: parasitology, pathogenesis of a single infection. Am. J. Vet. Res., 27: 659-667. Schillhorn Van Veen, T.W. and Melancun, J.J., 1984. The lrichostrongylid egg output during spring in feedlot cattle. Vet. Parasitol., 14: 159-163. Smith, H.J., 1974. Inhibited development of Ostertagia ostertagi, Cooperia oncophora and Nematodirus helvetianus in parasite free calves. Am. J. Vet. Res., 35: 935-938. Suderman, M.T., 1979. Seasonal hypobiosis of Ostertagia ostertagi/Still 1902/Ransom 1907, in cattle in Brazos County, Texas. M.S. Thesis, Texas A and M University, College Station. Werner, B.A. and Bergstrom, R.C., 1983. Numbers of gastrointestinal helminth eggs of Wyoming cattle in two surveys: 1957 to 1961 and 1973 to 1977. Am. J. Vet. Res., 44: 301-303. Wescott, R.B., 1984. Bovine parasites of particular importance in the Northwest. In: Proceedings of the 17th Annual Meeting of the American Association of Practitioners, Des Moines, 17: 60-63. Williams, J.C., 1981. Bovine ostertagiasis: problems caused by the medium stomach worm. Anita. Nutr. Health, 36: 6-9. Williams, J.C., 1983. Ecology and control of gastrointestinal nematodes of beef cattle. Vet. Clin. N. Am. Large Anim. Pract., 5: 183-205. Williams, J.C., 1986. Epidemiologic patterns of nematodiasis in cattle. Vet. Clin. N. Am. Food Anita. Pract., 2: 235-246. Williams, J.C. and Knox, J.W., 1976. Effect of nematode parasite infection on the performance of stocker cattle at high stocking rates on Costal Bermudagrass pastures. Am. J. Vet. Res., 37: 453-464. Williams, J.C., Knox, J.W., Baumann, B.A., Sniders, T.G., Kimball, M.D. and Hoerner, T,J., 1983. Seasonal changes of gastrointestinal nematode populations in yearling beef cattle in Louisiana with emphasis on prevalence of inhibition Ostertagia ostertagi. Int. J. Parasitol., 13: 133-144. Williams, J.C., Corwin, R.M., Craig, T.M. and Wescott, R.B., 1986. Control strategies for nematodiasis in Cattle. Vet. Clin. N. Am. Food Anita. Pract., 2: 247-260. Williams, J.C., Knox, J.W., Marbury, K.S., Kimball, M.D., Baumann, B.A. and Snider, T.G., 1987. The epidemiology of Ostertagia ostertagi and other gastrointestinal nematodes of cattle in Louisiana. Parasitology, 95: 135-153. Williams, J.C., Knox, J.W., Barras, S.A. and Hawkins, J.A., 1990. Effects of ivermecfin and fenbendazole in strategic treatment of gastroIntestinal nematode infections in cattle. Am. J. Vet. Res., 51: 2034-2039. Willis, H.H., 1921. A simple levitation method for the detection of hookworm ova. Med. J. Aust., 8: 375-376. Worley, D.E. and Sharman, G.A.M., 1966. Gastritis associated with Ostertagia bisonis in Montana range cattle. J. Am. Vet. Med. Assoc., 149: 291-294. Zimmerman, G.L., Worley, D.E. and Riekard, L.G., 1993. Epidemiology of Ostertagia in the northwestern USA. Vet. Parasitol., 46: 303-311.
VeterinaryParasitology64 (1996) 285-297
Prevalence and epidemiology of trichostrongylids in Wyoming cattle with consideration of the inhibited development of Ostertagia ostertagi A. Malczewski a,., W.R. Jolley b, L.F. ¢6roodard b a W. StefahskiInstitute of Parasitology, Polish Academy of Sciences, L. Pasteur 3, P.O. Box 153, 00-973 Warsaw, Poland Department of Veterinary Sctences, Universityof Wyoming, Laramie, WY 82071, USA b
•
•
Received 8 June 1995; accepted 1 October 1995
Abstract During 1988, monthly collections of abomasa and the cranial portion of the small intestine of 208 native Wyoming cattle were examined for adult and larval helminth parasites. Egg counts were performed on colonic faecal specimens. The animals ranged from 7 months to 8 years of age and were sampled at slaughter houses or diagnostic laboratories from five different counties in the State. Most of the cattle had ranged for a long time on non-irrigated, high altitude grass plains from about 1250 to 2500 m above sea level. All animals examined were found infected. Nematode genera (and number of species) found included Ostertagia (4), Trichostrongylus (2), Haemonchus (1), Cooperia (4) and Nematodirus (2). One trematode, Fasciola hepatica, and a cestode, Moniezia benedeni, also were found. Trichostrongylus axei, Trichostrongylus longispicularis and Cooperia lyrata were found for the first time in Wyoming, Ostertagia circumcincta was found for the first time in cattle in Wyoming, and Haemonchus placei, tentatively identified in a previous survey, was def'mitively confirmed. Predominant species (and prevalence) were Ostertagia ostertagi (98%), Cooperia oncophora (60.6%), Ostertagia bisonis (41.8%), Cooperia bisonis (33.6%) and T. axei (27.9%). One or more of the four species of Ostertagia were found in all animals. Inhibited O. ostertagi and O. bisonis larvae predominated from November to April and reached a peak in January to comprise 88% of the total nematode burden for that month. The adult population of abomasal nematodes peaked in April and predominated thereafter until October. Haemonchus placei also spent the autumn-winter period in an inhibited state of development. Faecal egg counts were lowest during winter months, when the highest numbers of worms were present as L 4 larvae, as determined by luminal and mucosal counts. Nematode populations in the
* Correspondingauthor. Tel/Fax: + 48-22-222562. 0304-4017/96/$15.00 Copyright © 1996 Elsevier Science B.V. All rights reserved. SSD! 0304-4017(95)00924-8
286
A. Malczewski et al. / Veterinary Parasitology 64 (1996) 285-297
small intestine peaked in June and persisted until November. The results of this study showed the magnitude and species composition of nematode parasitism in cattle raised on high altitude grass plains, underscored the inaccuracy of faecal egg counts as an indicator of worm burden during fall and winter seasons, and provided information on which anthelmintic treatment timing would be most efficacious. Keywords: Cattle-Nematoda; Epidemiology-Nematoda;Ostertagia ostertagi
1. Introduction The trichostrongylids have long been recognized as important parasites of cattle. Within the last two decades, Ostertagia ostertagi has emerged as the most important member of the group due to its ability to enter the mucosa of the abomasum and suspend development in a larval stage. The state of dormancy/hypobiosis/larval inhibition, appears to be a survival mechanism that enables the worm to preserve its reproductive potential through inclement seasons until conditions favour exogenous development and transmission. Larval inhibition in northern, cool regions of the USA has been demonstrated in Washington (Malczewski et al., 1975), Oregon (Kistner et al., 1979), Idaho and Maine (Gibbs, 1979), Michigan (Schillhorn Van Veen and Melancon, 1984) and Ohio (Herd, 1980) from autumn until spring. In contrast, the phenomenon has been shown to occur in the warm, southern states of Georgia (Ciordia et al., 1971), southern California (Baker et al., 1981), Texas (Suderman, 1979), Louisiana (Williams and Knox, 1976; Williams, 1981, Williams, 1986; Williams et al., 1983, Williams et al., 1987), and Missouri (Brauer, 1983) from spring through summer. However Zimmerman et al. (1993) considered, that "inhibition in the northwest does not fall strictly into either the northern or southern pattern. Data from both Montana and Oregon support the concept of a wide and variable transition zone in the northwest". With any parasitic disease, recognition of changes in seasonal incidence, prevalence and relative burden is a key to planning an effective control program. Previous surveys of cattle in Wyoming for internal parasites conducted from 1957 to 1961 (Honess, 1957; Honess and Bergstrom, 1963, Honess and Bergstrom, 1966) and 1973 to 1977 (Werner and Bergstrom, 1983) included only 32 necropsies and were based mainly on faecal egg counts. Information concerning the seasonal dynamics of gastrointestinal nematode populations in Wyoming cattle has been inadequate, especially regarding O. ostertagi. Cattle numbers in Wyoming exceeded 1.3 million animals in 1988, constituting a important component of the state's economy. Determination of the seasonal dynamics of bovine trichostrongylid infections in general, With emphasis on inhibition of O. ostertagi in particular, was undertaken to facilitate more effective control of detrimental nematode infections in native livestock. Ungulates raised on the high, grass plains of Wyoming and other regions with similar environmental conditions require management techniques specific for their climatic and meteorologic conditions. Trichostrongylid epidemiology is underdefined for the region. The objectives of the present study were: (1) to determine by necropsy the monthly prevalence and magnitude of helminth parasite populations in abomasa and cranial part of the small intestine of cattle native to Wyoming, and (2) to
A. Malczewski et a l . / Veterinary Parasitology 64 (1996) 285-297
287
Table 1 Age distribution of Wyoming cattle examined for abomasal and small intestinal nematodes in 1988 Approximate age in months
No. of animals
7 10 12 18 24 30 36 48 60 72 96
1 2 28 100 48 11 5 7 4 I 1
establish whether or not inhibited development of the nematode O. ostertagi in cattle native to Wyoming occurs and its timing.
2. Materials and methods
The entire abomasum, anterior 3 m portion of the small intestine and samples of colonic faeces were collected from 208 native Wyoming cattle, slaughtered for beef (196) or necropsied (12) at the Wyoming State Veterinary Laboratory (WSVL) for routine diagnostic purposes (Table 1); livers were also examined. An average of 17 collections was made monthly from January through December 1988. Collection points in the state (and numbers of animals examined) were Lander (102), Worland (9), Torrington (70) and Laramie (27). The cattle ranged in age from 7 months to 8 years, and most had been on pasturage consisting mainly of native perennial grasses at elevations from about 1250 to 2500 m above sea level during some or most of their lives. Visceral and faecal specimens were transported to the WSVL in Laramie for examination by standard methods (Ritchie et al., 1966). Adult and larval worms were collected, counted and identified from luminal contents or digested portions of abomasai mucosa. The differences in monthly numbers of adult worms with developing stages (including late L 4 larvae and L 5 juveniles), and inhibited early L 4 (EL 4) larvae, were statistically analysed by the t-test. Numbers of eggs per gram of faeces were determined with the salt flotation technique of Willis (Willis, 1921). Differences in the monthly egg counts were statistically analysed at a 95% confidence level.
3. Results
3.1. Helminth species Thirteen nematode, one trematode and one cestode species were found in the abomasum, small intestine or liver of cattle examined in the survey (Table 2). All of the
288
A. Malczewski et al./ Veterinary Parasitology 64 (1996) 285-297
208 native cattle examined were infected with one or more helminth species, with O.
ostertagi (98%), Cooperia oncophora (60.6%), Ostertagia bisonis (41.8%), Cooperia bisonis (33.6%) and Trichostrongylus axei (27.9%) predominating. The remaining species found were few in number and low in prevalence. Trichostrongylus axei, Trichostrongylus longispicularis and Ostertagia lyrata were identified for the first time in Wyoming, and Ostertagia circumcincta was found in native cattle for the first time. Haemonchus placei, tentatively identified from native cattle in a previous study (Honess and Bergstrom, 1963) was definitively identified in the present survey. The flatworms were incidental to the study objectives.
3.2. Abomasal nematodes All of the cattle harboured one or more of the four species of Ostertagia, O. ostertagi (98%), O. bisonis (41.8%), O. circumcincta (2.4%) or O. lyrata (0.48%) (Table 2). The Ostertagia species in 100%, T. axei in 27.9% and H. placei in 6.7%, numerically dominated the worm population in the digestive tract every month of the year (Table 2, Fig. lb). Total worm numbers were greatest in January (21019) and lowest in September (800) (Table 3, Fig. lb). Inhibited EL 4 larvae were predominant in November (967), December (2861) and January (18435), comprising 61%, 73% and 88%, respectively, of the populations. The monthly composition of populations by developmental stage is shown in Fig. 2. Adult and developing stages peaked in April, but predominate over inhibited larvae from February through October. The lowest numbers of adult and developing stages persisted from September through November (Table 3). There were clear variations in the proportion of inhibited larvae to adult and developing forms, e.g. in January when the inhibited EL 4 stage predominated (88%), adult and developing forms were least prevalent (12%); the reverse was seen in April, when adults and developing forms were most prevalent (84%) and EL4s were few (16%) (Table 3, Fig. 2). Analysis with the t-test showed the differences between monthly numbers of adults and those of developing stages and inhibited EL 4 larvae to be significant each month from February through October, with the exception of May. This supported the gross observation of predominance of the adult and developing stages for those months. The most prevalent nematode species in the abomasum was O. ostertagi, found in all cattle but four (Table 2). Ostertagia bisonis was more prevalent during the autumnwinter months than in summer. Haemonchus placei, in contrast, was found in one to three animals during consecutive months of April through September with a peak prevalence of 23% in June (Table 2). Trichostrongylus axei was found every month, from a low of 6% of animals in March to a high of 60% in April, but did not demonstrate any observable seasonal trends (Table 2). The relative monthly prevalence of the dominant abomasal species is shown in Fig. 3.
3.3. Small intestinal nematodes Cooperia species were predominant in the small intestine, with C. oncophora in 60.6%, C. bisonis in 33.6%, Cooperia zurnabada in 13.0% and Cooperia punctata in
20 11 13
12 20 20 20
23 24
April May June
July August September October
November December
23 24
12 20 20 20
20 11 13
13 15 17
204 98
22 24
12 19 18 20
20 11 13
87 41.8
8 10
3 7 6 4
2 5 7
8 12 14
O,B
O,O
13 15 17
No. cattle
No. cattle
5 2.4
-
1
1 1
1 1
O,C
Worm
1 0.48
-
. -
-
1 -
O,L
58 27.9
6 4
5 2 7 3
5 2.4
1
2 1 . 1 -
-
-
12 4 5
1
T,L -
T,A 7 2
14 6.7
1
1 2 1 -
2 2 3
-
2
H,P
C,B
70 33.6
4 8
5 9 . 6 10
5 2 4
8
4 5
126 60.6
3 7
10 12 10 14
13 6 9
15
12 15
C,O
.
1 0.48
-
-
1
. -
-
-
C,P
.
C,Z
27 13
2 4
4 1 5 3
1
1
1
3 2
.
N,H
9 4.3
2 -
-
-
-
-
2
2 3
.
N,SP
1 0.48
1
-
-
-
F,H
9 4.3
1 1
1 2
-
-
-
4 -
M,B
70 33.6
4 8
5 9 6 I0
5 2 4
8
4 5
O,O:
Ostertagia ostertagi; O,B: Ostertagia bisonis; O,C: Ostertagia circumincta; O,L: Ostertagia lyrata; T,A: Trichostrongylus axei; T,L: Trichstrongylus longispicularis; H,P: Haemonchus placei; C,B: Cooperia bisonis; C,O: Cooperia oncophora; C,P: Cooperia punctata; C,Z: Cooperia zurnabada; N,H: Nematodirus helvetianus; N,SP: Nematodirus species (undetermined); F,H: Fasciola hepatica; M,B: Monezia benedeni.
Totals 208 208 Mean prevalence (%)
13 15 17
January February March
Month
Table 2 Monthly examinations, helminth parasite species and prevalence in W y o m i n g cattle in 1988
~"
t,J
I ".~ b~ ~0
,,~
~
~ 8"
O.
13 15 17 20 11 13 12 20 20 20 23 24
January February March April May June July August September October November December
13
(~)
1490 2021 1494 5345 974 2837 2050 1530 628 651 545 951
(7) (43) (44) (44) (72) (53) (54) (68) (42) (55) (30) (22)
1094 1851 1012 4524 174 547 331 150 16 80 67 107
(5) (39) (29) (37) (13) (10) (9) (7) ( 1) (7) (3) (3)
18435 389 494 1920 116 117 135 27 156 92 967 2861
(87) (8) (14) (16) (9) (2) (3) (1) (10) (8) (53) (66)
276 452 442 414 87 1908 1278 535 703 351 252 392
Intestinal (%)
C4
D2
A~
(%)
Abomasal
Mean nematode counts
Al , adults; D 2, developing stages; 13, inhibited larvae; C 4, combined stages.
No. examined
Month
( 1) (10) (13) (3) (6) (35) (34) (24) (47) (30) (14) (9)
(%)
21295 4713 3442 12203 1351 5409 3794 2242 1503 1174 1831 4311
Total
Table 3 Monthly examinations, abomasal and intestinal nematode counts, and faecal nematode egg counts from Wyoming cattle in 1988
4,5 3.5 32.0 64.0 4.8 61.0 46.0 53.0 7.5 28.0 7.0 6.9
Mean eggs per gram
"-4
t,o
e,
I,o
A. Malczewski et a l . / Veterinary Parasitology 64 (1996) 285-297 80 ~
291
A
L
O
I
20
[]
B
ABOMASAL SMALL INTESTINAL
•
25
0
z
iiiiiiii!iiii!ii
0
~
iiiiiliiii!i!ililili!iiiiii[
i'i~ii~ii!~!! !iii!il
5
!ii!i!iiiii!i!i!iii!iiiiiiiil iii!ii!ii!ii!ii!i~i!it
!i JAN
r FEB
iiiiiiiiiiiil MAR
AI~R
MAY
JUN
JUI.
MONTH
AUG
SEP
Fig. 1. (A) Mean monthly faecal egg counts. (B) Mean monthly abomasal, small
OCT
NOV
I)]~("
intestinal a n d c o m b i n e d total
worm counts.
0.48% of the cattle. Cooperia oncophora and C. bisonis had similar patterns of prevalence during the annual cycle. Trichostrongylus longispicularis in 2.4%, Nematodirus heloetianus in 4.3% and an unidentified Nematodirus species in 0.48% of the
292
A. Malczewski et a l . / Veterinary Parasitology 64 (1996) 285-297
100
•
90 Z
80
0
70
ADULT WORMS
[]
DEVELOPINGSTAGES
[]
INHIBITEDLARVAE
87
66
50
© 40
© 30 ~" 20 10 0
i
JAN
FEB MAR APR MAY J U N
J U L A U G SEP
OCT NOV DEC
MONTH Fig. 2. Life cycle stage compositionof abomasal lrichostrongylidpopulation in Wyomingcattle.
• []
OSTERTAGIAOSTERTAGI [] TRICHOSTRONGYLUSAXEI [ ]
OSTERTAGIABISONIS HAEMONCHUSPLACEI
100 90 70 Z
60 50
<
40
30 © 20 ~- 10 JAN
FEB MAR APR MAY JUN
JUL AUG
SEP
o C T NOV DEC
MONTH Fig. 3. Monthly prevalenceof dominant abomasal ~chostrongylids in Wyomingcattle.
A. Malczewski et al. / Veterinary Parasitology 64 (1996) 285-297
293
animals were the least numerous species (Table 2). Individual species did not show important seasonal changes in population composition (Table 2), but when considered as a group, peaked in June and remained high through September (Fig. lb). Throughout the year, however, the small intestinal population failed to equal or exceed the abomasal population (Table 3, Fig. lb). 3.4. Faecal egg counts
Faecal egg counts performed during the season of larval inhibition did not reflect the true intensity of infection. Faecal egg content appeared to vary seasonally, rather than with worm numbers (Table 3, Fig. la and Fig. lb); for example, one steer examined in January harboured more than 200 adult and 69 120 inhibited larvae of Ostertagia species and over 800 adult and developing forms of Cooperia species but only expelled an average of 1 epg of faeces. Furthermore, in November, 12 of 23 faecal samples examined were negative for eggs, despite worm counts indicating that cattle harboured an average number of 1831 worms, about 35% of which were adults (Table 3, Fig. 2). In contrast, faeces of the 20 cattle examined in August contained an average 53 epg, all samples examined were positive, and the worm counts averaged a modest 2242, most of which were adults (Table 3, Fig. 2). 3.5. Foreign species
The finding of O. bisonis in the abomasum of 41.8% and C. bisonis in the small intestine of 33.6% of cattle slaughtered in all packing houses in the survey was of
•
COOPERIAONCOPHORA
[]
COOPERIABISONIS
[]
COOPERIAZURNABADA
lnn
Z
O
U
JAN FEB MAR APR MAY JUN JUL AUG SEP OCT NOV DEC
MONTH Fig. 4. Monthlyprevalenceof dominant intestinaltrichostrongylidsin Wyomingcattle.
294
A. Malczewski et aL / Veterinary Parasitology 64 (1996) 285-297
special interest. The two species are commonly associated with wild ruminants, but appeared in the survey cattle in significant numbers (Table 2, Fig. 3 and Fig. 4).
4. Discussion
4.1. Helminthsfound Thirteen parasitic nematode species were found in the survey. Three, T. axei, T. longispicularis and O. lyrata, were not previously reported from any hosts from Wyoming, and one, O. circumcincta, was previously found in Wyoming sheep but not cattle. Haemonchus placei was tentatively identified from five mature cattle in an early survey by Honess and Bergstrom (1963), but too few specimens were recovered to allow positive identification. In 14 (6.7%) of the 208 cattle examined in the present survey, enough male and female specimens were recovered to allow identification. The one trematode, Fasciola hepatica, and one cestode, Monezia benedeni are common in Wyoming cattle. The finding of Ostertagia and Cooperia species to be the most common nematodes every month agreed generally with earlier surveys, although the presence of the Ostertagia species in all cattle examined is unprecedented. The finding of T. axei in 58 (27.9%) of the survey animals extended the reported range of the species and, by virtue of its prevalence, suggested its potential importance. The identification of four nematode species previously unreported in Wyoming cattle and the clarification of another's identity underscores the value of necropsy-based data collection in studies of this type.
4.2. Abomasal nematodes The consistent monthly numerical dominance of gastrointestinal nematode populations by the six species of abomasal nematodes found in this study reinforces the findings of previous authors (Olsen, 1949; Honess, 1957; Honess and Bergstrom, 1963; Worley and Sharman, 1966; Smith, 1974; Williams, 1986). The Ostertagia species, especially O. ostertagi and O. bisonis, were clearly well adapted to surviving the relative dry, cool environmental conditions common to the high-altitude ranges in Wyoming. Differences in the patterns, mechanisms or locations of larval inhibition may partially explain the differences in prevalence between species. The build-up of inhibited EL 4 larvae, which began slowly in September, peaked in January and decreased abruptly in February, mainly involved the Ostertagia species. A similar pattern for H. placei is probable, as indicated by the finding of inhibited EL 4 larvae in two cattle in February, and developing juveniles in April. The sudden release of inhibition, followed by development to juvenile and adult worms that occurred from mid-January to the peak in the adult population in April may have been due to a combination of factors, including climatic conditions, biological differences between species in development and in cattle management methods. Cattle in Wyoming are often maintained on pasture year-long, where native hay is provided as needed depending largely on weather and forage availability.
A. Malczewski et aL / Veterinary Parasitology 64 (1996) 285-297
295
An illustration of temporal differences in prominence of species can be seen by comparing the prevalence of O. bisonis with that of O. ostertagi, as shown in Fig. 3. Where O. bisonis was most prevalent in late winter (61.5% in January, peaked at 82% in March) and then decreased to a seasonal low in April (10%), O. ostertagi prevalence remained high and steady throughout the year. Trichostrongylus axei contributed to the April peak of adult worms and exhibited steady prominence through the pasture season. After cattle were placed on wintering pastures in late autumn, during the time inhibited EL 4 larvae of Ostertagia species were accumulating. Pasture contamination with eggs and larvae may have been important where animal density was high, despite the relatively low average number of adult worms and egg count. In view of the complimentary, slightly different dynamics of spring development between O. ostertagi and O. bisonis, the latter species may play an important role in Type II ostertagiosis. Acknowledged to be a parasite of wild ruminants (Dikmans, 1942), it has also been reported in cattle of Wyoming (Honess and Bergstrom, 1963) and Colorado (Olsen, 1949), and has caused gastritis in cattle in Montana (Worley and Sharman, 1966). The peak of adults and developing larvae that occurred in April was undoubtedly due to maturation of overwintered, inhibited larvae. Thereafter, for at least the next 5 months, adult populations were probably a result of newly acquired larvae from pasture. Contamination of pastures by the adult worms of the April population peak was undoubtedly significant. The autumn-winter inhibition of Ostertagia species is a phenomenon seen in temperate zones in countries other than the USA, including Canada (Smith, 1974), Scotland (Anderson et al., 1965), England (Michel, 1969, Michel, 1974) and Poland (Malczewski, 1970).
4.3. Small intestinal nematodes The relatively constant monthly numbers of the Cooperia species attests to the level of adaptation of the genus to cattle reared in Wyoming's harsh environment. The finding of insignificant numbers of inhibited small intestinal forms in the cattle in late winter suggests that their survival mechanisms differ from those of Ostertagia. A possible difference may include a greater ability to develop and survive in the exogenous environment, rather than a need for refuge in the host. The mechanisms of such, if they exist, have not been defined. Neither Cooperia species, nor the other, less numerous nematodes of the small intestine are considered to be as clinically important as the abomasal species, particularly those of Ostertagia. The reasons include dominant numbers, higher prevalence, and histopathologic evidence of ostertagial abomasitis. Two aspects of the survey were less informative than was desired. First, in the four study animals less than 1 year of age, no evidence of inhibited larvae or histopathology was found and no conclusions could be reached regarding the value of the calves in interpretation of data. Second, since only the cranial portion of the small intestine was collected for examination, the importance of Nematodirus species was not adequately assessable, because they are more common in lower regions of the gut than was collected. Members of the genus were considered a problem in cattle from a previous study (Honess, 1957).
296
A. Malczewski et al./ Veterinary Parasitology 64 (1996) 285-297
4.4. Control considerations The importance of understanding local or regional epidemiologic factors is clearly defined by previous studies (Williams, 1983; Wescott, 1984; Williams et al., 1986, Williams et al., 1990; Corwin, 1986; Baker and Farver, 1990). The current survey provided a basis for recommendations to control gastrointestinal nematode parasitism in cattle raised on grass ranges at high altitudes. In nearly every case, O. ostertagi should be the focus of control efforts, which would incidentally control other nematode populations that might be present. Drugs with systemic activity must be used to control inhibited EL 4 stages. Cheaper drugs can control lumenal stages of worms responsible for acute disease and contamination of pastures. The selection of drugs to be used and times of treatment may be determined by herd health history, helminth load insofar as can be accurately determined, a n d / o r stocking rate. Faecal egg counts can be used to estimate worm loads after inhibited forms develop into egg-laying adult worms, but should not be relied upon during the off-pasture season when actual worm numbers may be highest and egg counts lowest. Pasture rotation and contamination factors have not been adequately studied in states like Wyoming, where pastures/ranges are relatively large, wild ungulates and cattle harbour many of the same helminth parasites, and cattle are commonly kept on pasture all year. More such epidemiologic information is needed before non-drug methods can be factored into control programs.
Acknowledgements The authors are grateful for the cooperation of Charles Erickson of Wind River Meats, Frank Smith at Kelly Pack and others who aided in the collection and processing of specimens. This study was supported in part by a grant from MSD AGVET.
References Anderson, N., Armour, J., Jenning, F.W., Ritchie, J.D. and Urguhart, G.M., 1965. Parasitic gastritis in cattle. Vet. Rec., 77:1196-1204. Baker, N.F. and Farver, T.B., 1990. Strategic use of anthelmintics to prevent parasitic gastroenteritis in cow-calf herds in California. Am. J. Vet. Res., 51: 1663-1667. Baker, N.F., Fisk, R.A., Bushnell, R.P. and Oliver, M.N., 1981. Seasoaal occurrence of infective nematode larvae on irrigated pasture grazed by cattle in California. Am. J. VeL Res., 42:1188-1191. Braner, M.A., 1983. Epidemiology and bionomics of Ostertagia ostertagi in beef cattle in Missouri. Ph.D. Thesis, University of Missouri, Columbia, p. 161. Ciordia, H., Neville, W.E., Baird, D.M. and McCampbell, H.C., 1971. Internal parasitism of beef cattle on winter pastures: level of parasitism as effected by stocking rates. Am. J. Vet. Res., 32: 1353-1358. Corwin, R.M., 1986. The ContTol of Internal Parasites of Cattle. Edited by Hoechst Russel Agri-Vet. Comp. Dikmans, G., 1942. New host records. Proc. Helminth Soc. Washington, 9: 65. Gibbs, H.C., 1979. Relative importance of winter survival of larval nematodes in pasture and infected carrier calves in a study of parasitic gastroenteritis in calves. Am. J. Vet. Res., 40: 227-231. Herd, R.P., 1980. Animal health and public health aspects of bovine parasitism. J. Am. Vet. Med. Assoc., 32: 1353-1358.
A. Malczewski et al./ Veterinary Parasitology 64 (1996) 285-297
297
Honess, R.F., 1957. Helminths of Wyoming cattle: internal roundworms. Cow Country, 84: 21-25. Houess, R.F. and Bergstrom, R.C., 1963. Intestinal roundworms of cattle in Wyoming. Univ. Wyo. Agric. Exp. Stn. Bull, 410: 1-36. Houess, R.F. and Bergstrom, R.C., 1966. Trichostrongylosis of cattle in Wyoming. Univ. Wyo. Agric. Exp. Stn. Sci. Monogr., 2: 1-29. Kistuer, T.R., Wysc, D. and Averkin, E., 1979. Efficacy of oxfendazole against inhibited Ostertagia ostertagi in natural infected cattle. Aust. Vet. J., 55: 232-235. Malczewski, A., 1970. Gastrointestinal helminths of ruminants in Poland. IIL Seasonal incidence of the stomach worms in calves, with consideration of the effect of the inhibition phenomenon on the spring rise phenomenon. Acta Parasitol. Pol., 18: 417-434. Malczewski, A., Wescott, R.B., Spratling, B.M. and Gorham, I.R., 1975. Internal parasites in Washington cattle. Am. J. Vet. Res., 36: 1671-1675. Michel, J.F., 1969. Observations on epidemiology of parasitic gastroenteritis in calves. J. Helminthol., 43: lll-133. Michel, J.F., 1974. Arrested development of nematodes and some related phenomena. Adv. Parasitol., 12: 279-366. OIsen, O.W., 1949. Emendation of the description of the male of Ostertagia bisonis with a note of its occurrence in cattle. J. Colorado-Wyoming Acad. Sci., 4: 65. Ritchie, J.D.S., Anderson, N., Armour, J., Jarreti, W.F.H., Jennings, F.W. and Urgnhart, G.M., 1966. Infections in calves: parasitology, pathogenesis of a single infection. Am. J. Vet. Res., 27: 659-667. Schillhorn Van Veen, T.W. and Melancun, J.J., 1984. The lrichostrongylid egg output during spring in feedlot cattle. Vet. Parasitol., 14: 159-163. Smith, H.J., 1974. Inhibited development of Ostertagia ostertagi, Cooperia oncophora and Nematodirus helvetianus in parasite free calves. Am. J. Vet. Res., 35: 935-938. Suderman, M.T., 1979. Seasonal hypobiosis of Ostertagia ostertagi/Still 1902/Ransom 1907, in cattle in Brazos County, Texas. M.S. Thesis, Texas A and M University, College Station. Werner, B.A. and Bergstrom, R.C., 1983. Numbers of gastrointestinal helminth eggs of Wyoming cattle in two surveys: 1957 to 1961 and 1973 to 1977. Am. J. Vet. Res., 44: 301-303. Wescott, R.B., 1984. Bovine parasites of particular importance in the Northwest. In: Proceedings of the 17th Annual Meeting of the American Association of Practitioners, Des Moines, 17: 60-63. Williams, J.C., 1981. Bovine ostertagiasis: problems caused by the medium stomach worm. Anita. Nutr. Health, 36: 6-9. Williams, J.C., 1983. Ecology and control of gastrointestinal nematodes of beef cattle. Vet. Clin. N. Am. Large Anim. Pract., 5: 183-205. Williams, J.C., 1986. Epidemiologic patterns of nematodiasis in cattle. Vet. Clin. N. Am. Food Anita. Pract., 2: 235-246. Williams, J.C. and Knox, J.W., 1976. Effect of nematode parasite infection on the performance of stocker cattle at high stocking rates on Costal Bermudagrass pastures. Am. J. Vet. Res., 37: 453-464. Williams, J.C., Knox, J.W., Baumann, B.A., Sniders, T.G., Kimball, M.D. and Hoerner, T,J., 1983. Seasonal changes of gastrointestinal nematode populations in yearling beef cattle in Louisiana with emphasis on prevalence of inhibition Ostertagia ostertagi. Int. J. Parasitol., 13: 133-144. Williams, J.C., Corwin, R.M., Craig, T.M. and Wescott, R.B., 1986. Control strategies for nematodiasis in Cattle. Vet. Clin. N. Am. Food Anita. Pract., 2: 247-260. Williams, J.C., Knox, J.W., Marbury, K.S., Kimball, M.D., Baumann, B.A. and Snider, T.G., 1987. The epidemiology of Ostertagia ostertagi and other gastrointestinal nematodes of cattle in Louisiana. Parasitology, 95: 135-153. Williams, J.C., Knox, J.W., Barras, S.A. and Hawkins, J.A., 1990. Effects of ivermecfin and fenbendazole in strategic treatment of gastroIntestinal nematode infections in cattle. Am. J. Vet. Res., 51: 2034-2039. Willis, H.H., 1921. A simple levitation method for the detection of hookworm ova. Med. J. Aust., 8: 375-376. Worley, D.E. and Sharman, G.A.M., 1966. Gastritis associated with Ostertagia bisonis in Montana range cattle. J. Am. Vet. Med. Assoc., 149: 291-294. Zimmerman, G.L., Worley, D.E. and Riekard, L.G., 1993. Epidemiology of Ostertagia in the northwestern USA. Vet. Parasitol., 46: 303-311.