Transmission of some species of internal parasites in horses born in 1993, 1994, and 1995 on the same pasture on a farm in central Kentucky

veterinary parasitology ELSEVIER

Veterinary Parasitology70 (1997) 225-240

Transmission of some species of internal parasites in horses born in 1993, 1994, and 1995 on the same pasture on a farm in central Kentucky E.T. Lyons *, S.C. Tolliver, S.S. Collins, J.H. Drudge, D.E. Granstrom Department of Veterinary Science, Gluck Equine Research Center, Universityof Kentucky, Lexington, KY 40546-0099, USA Received 25 September 1996; accepted 5 December 1996

Abstract Data are presented on the last 3 years of a 7-year study (1989-1995) on transmission of natural infections of internal parasites in horse foals (n = 27) born in 1993, 1994, and 1995 on the same pasture on a farm in central Kentucky. The foals were in a closed breeding herd of horses. Research on the first 4 years (1989-1992) of the study was published earlier (Lyons et al., 1991. 1994). Thirty-five species of endoparasites were identified, including 24 species of small strongyles. Monthly, seasonal, and host-age transmission patterns were elucidated for the parasites. Comparison of data between the first 4 years and last 3 years of the study indicates similarities, but also differences, including an increase in prevalence and numbers of Thelazia lacrymalis and Anoplocephala perfoliata. © 1997 Elsevier Science B.V. Keywords: Closed breeding herd; Horses; Internal parasites; Long-termstudy; Transmission

1. Introduction Long-term observations on transmission of natural infections of internal parasites in equids are difficult because suitable conditions and circumstances are usually not readily available. There has been a unique opportunity to follow natural acquisition of endopara-

* Correspondingauthor. 0304-4017/97/$17.00 © 1997 Elsevier Science B.V. All rights reserved. PH S0304-4017(96)01155-7

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E.T. Lyons et al./ Veterinat3' Parasitology 70 (1997) 225-240

sites for 7 years (1989-1995) in foals born in the same field to horses in a closed breeding system. Most of the data for the first 4 years (1989-1992) were published earlier (Lyons et al., 1991, 1994), and the continuing investigations for Years 5 - 7 are presented here. Surveys for multispecies of endoparasites in the same equids are minimal in North America, especially in recent years. Two publications on this type of survey are those by Reinemeyer et al. (1984) and Torbert et al. (1986).

2. Materials and methods 2.1. Animals

Horse foals (n = 27) tbr the present research were born on the same pasture (Field No. 10) on a farm in central Kentucky over a 3-year period: 1993 (n = 11), 1994 (n = 7), and 1995 (n = 9). They were kept in Field No. 10 with their dams until slaughter and necropsy, one (the oldest) each month beginning in August, as opposed to June in the earlier studies, until all had been processed. There were two exceptions to the slaughter schedule in 1993. That year, necropsy of the first foal (No. 1) was earlier (May) than planned because the animal bad joint ill; in October, two foals (data averaged) were killed, the scheduled one (No. 4) and an additional one (No. 5) that became orphaned. In 1995, no foal was killed in October because necropsy facilities were temporarily unavailable. Specific data on month of necropsy, age, sex, and birth date are given in Table 1. The sire of the foals was a Thoroughbred and the dams were Thoroughbreds or mixed lighthorses. 2.2. Histoo,

Parasiticides have not been used in the breeding band since 1979, except for treatment of an occasional replacement animal. None of the test foals was ever given an antiparasitic compound. The majority of the other equids on the farm have been on a routine parasite control program, with ivermectin being the most commonly used product. 2.3. Parasitological procedures

Methods for the necropsy recovery of internal parasites from the foals and for determining fecal egg counts (epg) and larval counts (lpg) per gram of feces were as previously described (Drudge et al., 1963, 1975; Lyons and Drudge, 1975; Lyons et al., 1976, 1981, 1983, 1994). Attempts were not made to recover and enumerate early third-stage larvae of small strongyles from the mucosa of the large intestine. Contents of the large intestines were examined for small strongyles from foals in 1994 (n = 3) and in 1995 (n = 4). The other sites examined for parasites in all foals are shown in Figs. 1-4.

E.T. Lyons et al. / VeterinaryParasitology70 (1997) 225-240

227

Table 1 Data on month of necropsy, age, sex, and birth date of foals (n = 27) born in the same field on a farm in central Kentucky in 1993, 1994, and 1995. The foals were kept with their dams until slaughter and necropsy Month of

1993 a foal

necropsy

ID

May c 1 August 2 September 3 October 4 October a 5 November 6 December 7

1994 foal

Age at necropsy (days)

Sex

Birth date b (1993)

88 127 160 184 58 205 231

F F M M F M F

26/2 5/4 8/4 11/4 23/8 26/4 27/4

1994 foal January February March April

8 9 10 11

226 257 264 195

ID

Age at necropsy (days)

1 2

144 157

3 4

210 241

1995 foal Sex Birth date (1994)

ID

Age at necropsy (days)

. F M . F F

. 1 2 3 . 4 5

. 151 155 186 . 205 217

. 25/3 18/4 . 19/4 23/4

1995 foal F F M F

30/5 4/6 24/6 30/9

5 6 7

241 270 294

Sex

Birth date (1995)

M F M

17/3 11/4 14/4

F M

23/4 12/5

M M F F

18/5 22/5 22/6 4/6

1996 foal F F F -

23/5 28/5 31/5 -

6 7 8 9

238 274 281 304

ID, identification number; F, female; M, male. Year of necropsy. b Day/month. c Slaughtered because of joint ill. a Slaughtered because dam died.

2.4. Meteorological data Data on air temperature (Fahrenheit; a v e r a g e ) and precipitation (inches; cumulative) were r e c o r d e d near the study area. T h e y included m o n t h l y and annual measurements.

3. Results

3.1. Parasite data by month of necropsy of foals (n = 27) born in 1993 (I), 1994 (II), and 1995 (lid Gasterophilus intestinalis w e r e the p r e d o m i n a n t bot species present (Fig. I ( A - D ) ) in the foals (I, II, and III). F i r s t / s e c o n d instars were f o u n d in the m o u t h f r o m A u g u s t to D e c e m b e r ; peak numbers w e r e in A u g u s t (II) and O c t o b e r (I, liD. In the stomach, second instars w e r e present f r o m O c t o b e r to January; highest numbers w e r e in O c t o b e r (III) and N o v e m b e r (I, II). A l s o in the stomach, third instars w e r e first present in N o v e m b e r , and the greatest n u m b e r s w e r e in January (II), February (I), and M a r c h (III). Gasterophilus nasalis w e r e found (one second instar) in the s t o m a c h o f one foal (liD. Thelazia lacrymalis were found in the eyes o f all but five foals (Fig. I(E)); these parasites w e r e present f r o m A u g u s t to April, and in highest numbers in S e p t e m b e r (I, II),

E.T. Lyons et al. / Veterinary Parasitology 70 (1997) 225 240

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Table 2 Species and number of small strongyles recovered from the lumen of the large intestines of three foals born in the same field on a farm in central Kentucky in 1994 Genus and species

Counts Individual foal (ID) 2

All foals

4

6

Total

Agg. av.

% of total

Cyathostomum catinatum Cyathostomum coronatum Cylicocyclus insigne Cylicocyclus leptostomous Cylicocyclus nassatus Cylicodontophurus mettami Cylicostephanus asymetricus Cylicostephanus calicatus Cylicostephanus goldi Cylicostephanus longibursatus Cylicostephanus minutus Gyalocephalus capitatus Poteriostomum imparidentatum Triodontophorus tenuicollis

7050 150 300 0 950 0 0 200 2200 8350 750 0 0 100

37 000 250 200 1500 8600 200 200 700 6100 19200 2000 500 200 400

83 300 2600 4000 100 24000 0 2000 8700 30000 129000 2000 0 0 0

127 350 3000 4500 1600 33 550 200 2200 9600 38300 156550 4750 500 200 500

42 450 1000 1500 533 11 183 67 733 3200 12767 52185 1583 167 67 167

33 1 1 <1 9 <1 1 3 10 41 1 <1 <1 <1

Total mature small strongyles Total immature small strongyles Total small strongyles

20050 7350 27 400

77050 18000 95 050

285700 69900 355 600

382800 95250 478 050

127600 31750 159 350

80 20 100

ID, identification number; Agg. av., aggregate average.

D e c e m b e r (III), January (III), and March (I). Anoplocephala perfoliata were recovered from the intestine in A u g u s t to March; peak n u m b e r s were in D e c e m b e r (II), January (III), and February (I) (Fig. I(F)). Parascaris equorum larvae were present in the lungs in M a y and A u g u s t - A p r i l , with the exception of D e c e m b e r (Fig. 2(A)). Highest n u m b e r s were in September (III), October (HI), N o v e m b e r (I), February (II), and March (II). In the small intestine, i m m a t u r e / a d u l t P. equorum were recovered in all months; the highest n u m b e r s were in M a y (I), A u g u s t (II, III), and January ( l i d (Fig. 2(B)). Strongyloides westeri were present in all m o n t h s except April; only one foal was infected (20 specimens) in 1994 (February). M a y (I) and D e c e m b e r (III) were the m o n t h s with the highest n u m b e r s (Fig. 2(C)). E n c y s t e d m u c o s a l stages of small strongyles were found in the large intestine in all months, and highest n u m b e r s were observed in D e c e m b e r (I, II) and January (III) (Fig. 2(D)); the aggregate average for all 3 years was 14433 larvae. F o r the seven foals (II, III) for which counts and identification of l u m i n a l stages of small strongyles were made,

Fig. 1. Number of parasites recovered at necropsy (by month) from foals born in 1993, 1994, and 1995. Gasterophilus intestinalis: (A) first instars (mouth); (B) second instars (mouth); (C) second instars (stomach); (D) third instars (stomach). (E) Thelazia lacrymalis (eyes). (F) Anoplocephala perfoliata (large intestine). ND, no data,

E.T. Lyons et al. / Veterinary Parasitology 70 (1997) 225 240

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Table 3 Species and number of small strongyles recovered from the lumen of the large intestines of four foals born in the same field on a farm in central Kentucky in 1995 Genus and species

Counts Individual foal (ID)

All foals

1

3

5

7

Total

Agg. av.

% of total

Cyathostomum catinatum Cyathostomum coronatum Cyathostomum labiatum Cyathostomum labratum Cyathostoraumpateratum Cylicocyclus insigne Cylicocyclus leptostomus Cylicocyclus nassatus Cylicodontophorus mettami Cylicostephanus asymetricus Cylicostephanus calicatus Cylicostephanus goldi Cylicosmphanus longibursatus Cylicostephanus minutus Poteriostomum imparidentatum Triodontophorus tenuicollis

4900 450 0 0 0 0 0 1400 200 300 0 2000 7400 400 100 0

7750 300 150 0 150 0 450 5150 100 550 250 1700 7850 900 0 100

16 825 100 0 0 0 0 2102 14423 0 334 450 2968 14369 384 300 100

65 950 1100 0 500 0 250 4400 29900 250 0 1900 6500 25250 6100 1500 750

95 425 1950 150 500 150 250 7952 50873 550 1184 2600 13168 54869 7784 1900 950

23 857 488 38 125 38 63 1988 12718 138 296 650 3292 13718 1946 475 238

40 1 < 1 < 1 < 1 < 1 3 21 < 1 < 1 < 1 5 23 3 1 < 1

Total mature small strongyles Total immature small strongyles Total small strongyles

17150 1550 18700

25400 1350 26750

53355 9938 63293

144350 3650 148000

240255 16488 256733

60066 4122 64188

94 6 100

ID, identification number; Agg. av., aggregate average.

there was the same pattern in both years of increased numbers in later months (Tables 2 and 3) (Fig. 2(E)). The average number of luminal stages for the seven foals was 104970. These foals had either seven genera and 14 species (II) or six genera and 16 species (III) of small strongyles. Strongylus edentatus, recovered from the ventral abdominal wall, in general increased gradually in numbers each month of the year of study, with the peak occurring in the winter and spring months (Fig. 2(F)). Strongylus vulgaris (Fig. 3(A,B)) were present in the cranial mesenteric artery in every month; numbers were highest in May (I), March (II), and January (III); they were most numerous in the May (I) foal, afflicted with joint ill. The highest number of S. vulgaris in the large intestine was in February (I, II) and January (III) foals. Data on stomach nematodes are not graphically depicted because of their sparseness in the foals. Trichostrongylus axei (10 specimens) were found in only one foal (I).

Fig. 2. Number of parasites recovered at necropsy (by month) from foals born in 1993, 1994, and 1995. Parascaris equorum: (A) immature (lungs); (B) immature/mature (small intestine). (C) Strongyloides westeri (small intestine). Small strongyles: (D) large intestine, mucosa-encysted; (E) large intestine, lumen. (F) Strongylus edentatus (ventral abdominal wall). ND, no data.

E.T. Lyons et al. / Veterinary Parasitology 70 (1997) 225-240

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233

Habronema muscae immature/mature (2-33 specimens each) were found in one (I), three (II), and eight (III) foals. Oxyuris equi (data not presented graphically) adults were found in the large intestine of seven foals (I, II, and III); one to three foals harbored 3-17 specimens each. Immature O. equi (50-500 specimens/foal) were found in one (II) and two (III) foals. From fecal egg/larval counts, the following data were obtained. Ascarid eggs were found in 7 of 11 (I), 3 of 7 (II), and 3 of 9 (III) foals. Strongyle eggs were present in all but two foals, with ranges from 0 to 2190 epg counts. Eggs of S. westeri were found in only two foals. Larvae of S..vulgaris were cultured from five (I) and (III) foals each, but not from II foals. Small strongyle larvae (2-920 lpg counts) were present in fecal cultures of all foals. Larvae of S. westeri were recovered from cultures of two (I) foals and five (III) foals, but none of the II foals. 3.2. Parasite data (aggregate average) by age at necropsy of foals (n = 65) born in 1989-1995 Gasterophilus intestinalis (Fig. 4(A)) first instars in the mouth and second instars in the stomach were most abundant in 6-month-old foals. The greatest numbers of second instars in the mouth were in 2-month-old animals and of third instars in the stomach were in 9-month-old animals. Numbers of T. lacrymalis were highest in 10-month-old foals (Fig. 4(B)). Eightmonth-old foals harbored the greatest number of A. perfoliata (Fig. 4(B)). Three-monthold foals had more ascarids, immature/mature, in the small intestine than any other age group (Fig. 4(C)). Strongyloides westeri numbers were greatest in 4-month-old animals (Fig. 4(D)). Encysted small strongyles were most numerous in 8-month-old foals (Fig. 4(D)). Luminal stages of immatures and adults (not graphically summarized) were present in highest numbers in 9-month-old animals. Combined data on species of adult small strongyles identified from foals (n = 12) born in 1989, 1994, and 1995 are shown graphically in Fig. 5(A-C)). Eight genera and 24 species were identified. Nine species comprised the majority in total numbers, prevalence, and percentage of the population of adult small strongyles. Strongylus edentatus, located in the ventral abdominal wall, were found in highest numbers in 9-month-old foals (Fig. 4(E)). Strongylus vulgaris were most numerous in the cranial mesenteric artery in 3-month-old animals (Fig. 4(E)) and in the lumen of the large intestine in 9-month-old animals (Fig. 4(C)). The stomach worms T. axei and H. muscae were present in numbers too low for Fig. 3. Combined parasite data from all foals (n = 65) by age (months) at necropsy in the 7-year study (1989-1995). (A) Gasterophilus intestinalis first, second, and third instars (mouth/stomach). (B) Thelazia lacrymalis (eyes); Anoplocephala perfoliata (large intestine). (C) Parascaris equorum, immature/mature (small intestine); S. vulgaris (large intestine). (D) Strongyloides westeri (small intestine); small strongyles (large intestine, mucosa-encysted). (E) Strongylus edentatus (ventral abdominal wall); Strongylus vulgaris (cranial mesenteric artery). (F) Strongyle eggs per gram of feces (epg); small strongyle larvae per gram of feces (lpg). Agg. av., aggregate average.

E.T. Lyons et al. / Veterina~." Parasitology 70 (1997) 225-240

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600 500

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"6

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Z

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determination of age when highest infections occurred. Oxyuris equi (data not shown in graph form) were more plentiful in 7-month-old animals than any other age group. Counts were highest for strongyle epg in 4-month-old foals and for small strongyle lpg in 7-month-old foals (Fig. 4(F)). 3.3. Meteorological data

General characteristics of data on air temperature and precipitation are presented relative to departure from the norm for the 7-year study period. January had above-normal ( + 3 ° to + 10°) temperature for each year except 1994 ( - 6 ° ) . The early months (January-May) were warmest ( + 5° to + 6 °) in 1991. Summer

Fig. 5. Combined data on adult small strongyles recovered from the lumen of the large intestine at necropsy from 12 foals born in 1989 (n = 5), 1994 (n = 3), and 1995 (n = 4) showing: (A) numbers (average) of the nine predominant species; (B) prevalence (%) of all 24 species; (C) population (%) relative to the nine predominant species and all other species. Cra., Craterostomum; Cva., Cyathostomum; Cyc., Cylicocyclus;

Cyd., Cvlicodontophorus; C~'s., Cylicostephanus; G., Gyalocephalus; P., Poteriostomum; T., TriodontophoT RS .

E.T. Lyons et al. / Veterinary Parasitology 70 (1997) 225-240

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E. 7". Lyons et al. / Veterinary Parasitology 70 (1997) 225-240

months (June-August) were warmest ( + 2° to + 4 °) in 1991, 1993, and 1995. December 1989 was the coldest ( - 13°) month. The years 1990 and 1991 were overall the wannest (aggregate average of + 3°) of the 7-year period. For 1992, May-October were cooler than normal ( - 2 ° to -5°), but November and December were warmer ( + 1°). In 1993, September-December were cooler than normal ( - 1° to - 3°). November and December in 1994 were unusually warm ( + 5°). In 1995, September-December were cooler than usual ( - 1° to -5°). Annual temperatures (aggregate average) were virtually normal for 1989 and 1992-1995. Precipitation was highest above normal for the months of February ( + 7") in 1989, December ( + 7 " ) in 1990, December ( + 4 " ) in 1991, July ( + 4 " ) in 1992, June and November ( + 3 " ) in 1993, March, April, and August ( + 2 " ) in 1994, and May ( + 5 " ) in 1995. The month with the biggest deficit was July ( - 3") in 1994. Annual precipitation, relative to normal, was +9" in 1989, + 1" in 1990, +6" in 1991, + 2 to +4" in 1992, 1993, and 1995, and - 1" in 1994.

4. Discussion Various aspects of the data on endoparasites in the 7-year study relative to month of necropsy and age at necropsy of the foals are discussed. Also, comparisons with other studies are made. Mouth stages (first/second instars) of G. intestinalis were found 1 month (August) earlier than in the first 4 years; thus, these stages were recovered from the mouth from August to January during the 7-year period. Second-instar G. intestinalis were first found in the stomach 1 month (October) later than previously, but were last present in January both in present and past segments of the 7-year study. In a previous, more extensive study in Kentucky over a 22-year period (1951-1973) (Drudge et al., 1975), second-instar G. intestinalis were found in the stomach of horses in every month of the year, and the highest numbers were present in December, which is I month later than in the 7-year study. In the present study, third-instar G. intestinalis were first found in the stomach in November, which was 3 months later than in the earlier 4-year study. Third instars were present in the stomach in all months of the study by Drudge et al. (1975) and numbers were highest in March (1 month later than in the 7-year study) and in June. In the adjacent state of Ohio, prevalence of G. intestinalis was 71% in horses in a study in 1981 and 1982 (Reinemeyer et al., 1984). For the present research, there was a general expected trend of older foals having greater numbers of G. intestinalis specimens present. The infection pattern of G. intestinalis in the 7-year study was typical based on the known life cycle of this species of parasite (Wells and Knipling, 1938). Botflies begin laying eggs on horse hairs in early summer. After a few days, first instars have developed and are capable of hatching from eggs when stimulated by the lips and tongue of the horse. During about a 3-4-week period in the mouth, first instars develop to second instars, which are then swallowed. In the stomach, the second instars develop in about a month to third instars. Thus, third instars are found in the stomach about 2 months after first instars enter the horse's mouth. Build-up of bots in the horse occurs

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over time and continues even after cold weather, when botfly deposition of eggs ceases. This is because the first instars can remain viable in the eggs on horse hair for several weeks. Gasterophilus nasalis were rare in the 7-year study. Only two horses were infected and only one specimen was found in each animal. The Drudge et al. (1975) study reported a prevalence of G. nasalis in the stomach of horses of 28% for second instars and 76% for third instars. Prevalence of G. nasalis in the Reinemeyer et al. (1984) study in horses was 10.9%. Thelazia lacrymalis has greatly increased in prevalence and intensity since the earlier part of the 7-year study. Numbers per foal were somewhat cyclic, being generally higher in late summer/early fall months and in early winter months. Overall, intensity became greater as foals aged. The reason for the increase of T. lacrymalis is unknown. There may have been higher numbers of the intermediate host, the facefly (Musca autumnalis) (Lyons et al., 1976), in the area of the foals. If so, there is no obvious explanation, because near the pasture with the foals there has been no increase of cattle, and thus no fresh manure for facefly breeding (Dougherty and Knapp, 1994). Anoplocephala perfoliata were higher in prevalence and intensity in the last 3 years of the study. Infections were generally greater as foals became older. As with T. lacrymalis, there is no definite explanation for the increase in infection. Maybe the numbers of intermediate hosts, oribatid mites (Romero et al., 1989), became greater periodically on pasture where the foals were born. Also, with more tapeworms in horses, the potential for contamination of pasture with eggs is greater. So there would be an increased chance of more oribatid mites ingesting tapeworm eggs and developing the cysticercoid stage that infects the horse. Parascaris equorum in general were present in higher numbers in the lungs and small intestine in early months. However, they persisted in both organs, although in lower numbers, throughout the study period. Numbers in the small intestine declined greatly with aging of the ,foals and this was probably due to an immune response (Russell, 1948; Clayton, 1978). Strongyloides westeri were more prevalent and in higher intensity in early months of the year and in younger foals. The infection pattern of S. westeri is similar to that of P. equorum in that both species are self-limiting in foals (Russell, 1948; Todd et al., 1949), although P. equorum may occasionally be found in low numbers in older horses (Clayton, 1978). Small strongyle encysted stages in general were more abundant in later months of the 7-year study and in older foals. An obvious exception was the 88-day-old (May 1993), earliest foal examined. This foal, afflicted with joint ill, had a much higher number of encysted small strongyles than foals examined in August-November. Possible reasons are: (1) the foal had a compromised immune system, or (2) there was insufficient time for many encysted stages to undergo development and emergence back to the lumen of the large intestine. Although the variability of infections and relatively low numbers of foals examined must be considered, usually there was not a proportionate increase of encysted stages when luminal stages increased. For example, for two 1995-born foals, numbers of encysted and luminal stages were 19 690 and 63 293, respectively, for the foal examined in December, and 17 850 and 148 000, respectively, for the foal examined

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in February. The latter finding may be similar to that reported by Love and Duncan (1992) in ponies in a grazing study. They reported that helminth-naive foals had higher numbers of small strongyles in the large intestinal lumen and lower numbers in the mucosa than did foals and older ponies previously allowed to graze and which had apparently developed some immunity to these parasites. Another observation on foals examined in the 7-year study is that the number (aggregate average) of mucosal stages in the last 3 years was about three times that of the first 4 years. Also, numbers (average) of luminal stages were more than twice as large in the seven foals examined in 1994 and 1995 than in the ten foals examined in 1989. Whether there has been an actual increase in small strongyle numbers in the last 3 years of the study or this is just a natural variation is unknown. In the foals, the number (24) of species of adult small strongyles found was similar to that reported in two other surveys, where 21 species were found in horses (Reinemeyer et al., 1984) and 24 species in ponies (Torbert et al., 1986). The nine predominant species of small strongyles in the foals in the present study were typical for this group of nematodes in equids (Ogbourne, 1978; Reinemeyer et al., 1984). Compared with the 1989-born foals, the 1994/1995-born foals were lacking seven species (Cylicocyclus

elongatus, Cylicocyclus radiatus, Cylicodontophorus bicoronatus, Cylicostephanus poculatus, Craterostomum acuticaudatum, Triodontophorus brevicauda, and Triodontophorus serratus), but they had two additional species (Cyathostomum pateratum and Gyalocephalus capitatus). These nine species, when present, appeared in low numbers ( < 1%) compared with the total number found. Therefore, their presence or absence was probably related more to poor odds of recovering them by the aliquot sample technique, rather than due to a cyclic phenomenon. Increase of S. edentatus specimens in the ventral abdominal wall in later months and as foals became older was expected. This was because of cumulative infection and long parenteral migration and prepatency (about l l months). Strongylus vulgaris numbers were probably highest in the cranial mesenteric artery in the earliest (May 1993) examined foal that was afflicted with joint ill because of a greater susceptibility, possibly resulting from impaired immunity. The general pattern of high numbers of S. vulgaris as immature stages in the cranial mesenteric artery in earlier months and then as adults in the latter months (winter and spring) in the lumen of the large intestine was as expected. This is based on the long parenteral migration during the approximate 6-month prepatent period. Although the stomach nematodes 7". axei and H. muscae were present in low numbers, prevalence of the latter species increased in the last 3 years. Definite reasons for the increase of H. muscae are unknown. Whether some factor may have allowed for a greater abundance of the intermediate host, the house fly (Musca domestica) (Bowman, 1991), is uncertain. Prevalence and number of adult O. equi in the last 3 years were much less than in 1989, but more than in 1990, 1991, and 1992 foals. Data on fecal egg/larval counts followed the general pattern relating to age of the foal and species of nematodes present. The types of eggs found in fecal samples were ascarids and S. westeri in younger foals and strongyles in all ages of foals. From cultures of feces, S. westeri larvae were evident in young foals, small strongyle larvae in all ages of foals, and S. vulgaris only in older foals.

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It is difficult to attribute directly any changes in endoparasite burdens over the 7-year investigation to departure from normal temperature and precipitation. Annual temperatures (aggregate average) were essentially normal for all years except 1990 and 1991, which were somewhat warmer than usual. However, summer months in 1991, 1994, and 1995 were warmer than normal. Regarding annual precipitation, the 2 years with greatest values above normal were 1989 and 1991, although one or two of the spring/summer months had above-normal precipitation in 1992-1994. The possible increase in numbers of small strongyles in the foals in later years could be related to more ideal weather conditions for larval development and transmission on the pasture. Likewise, it is of interest that the other three species of helminths (T. lacrymalis, A. perfoliata, and H. muscae), which became greater in prevalence/numbers the last 3 years of the study, all have intermediate hosts. Perhaps the temperature and precipitation were more favorable during these years, permitting an increase in the populations of arthropod intermediate hosts.

Acknowledgements This investigation (Paper No. 96-14-181) was made in connection with a project of the University of Kentucky Agricultural Experiment Station and is published with the approval of the director. Appreciation is expressed to Tom Priddy, Department of Biosystems and Agricultural Engineering, University of Kentucky, for supplying the meteorological data.

References Bowman, D.D., 1991. Georgis' Parasitology for Veterinarians. 6th edn. W.B. Saunders, Philadelphia, PA, 430 PP. Clayton, H.M., 1978. Ascariasis in foals. Vet. Rec., 102: 553-556. Dougherty, C.T. and Knapp, F.W., 1994. Oviposition and development of face flies in dung from cattle on herbage and supplemented herbage diets. Vet. Parasitol., 55:115-127. Drudge, J.H., Szanto, J., Wyant, Z.N. and Elam, G.W., 1963. Critical tests of thiabendazole as an anthelmintic in the horse. Am. J. Vet. Res., 24: 1217-1222. Drudge, J.H., Lyons, E.T., Wyant, Z.N. and Tolliver, S.C., 1975. Occurrence of second and third instars of Gasterophilus intestinalis and Gasterophilus nasalis in stomachs of horses in Kentucky. Am. J. Vet. Res., 36: 1585-1588. Love, S. and Duncan, J.L., 1992. The development of naturally acquired cyathostome infection in ponies. Vet. Parasitol., 44: 127-142. Lyons, E.T. and Drudge, J.H., 1975. Occurrence of the eyeworm Thelazia lacrymalis in horses in Kentucky. J. Parasitol., 61: 1122-1124. Lyons, E.T., Drudge, J.H. and Tolliver, S.C., 1976. Thelazia lacrymalis in horses in Kentucky and observations on the face fly (Musca autumnalis) as a probable intermediate host. J. Parasitol., 62: 877-880. Lyons, E.T., Drudge, J.H., Swerczek, T.W., Crowe, M.W. and Tolliver, S.C., 1981. Prevalence of Strongylus vulgaris and Parascaris equorum in Kentucky Thoroughbreds at necropsy. J. Am. Vet. Med. Assoc., 179: 818-819.

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Lyons, E.T., Tolliver, S.C., Drudge, J.H., Swerczek, T.W. and Crowe, M.W., 1983. Parasites in Kentucky Thoroughbreds at necropsy: Emphasis on stomach worms and tapeworms. Am. J. Vet. Res., 44: 839-844. Lyons, E.T., Tolliver, S.C., Drudge, J.H., Granstrom, D.E., Stamper, S. and Collins, S.S., 1991. Transmission of some internal parasites in horses born in 1989 on a farm in central Kentucky. J. Helminthol. Soc. Wash., 58: 213-219. Lyons, E.T., Tolliver, S.C., Stamper, S., Drudge, J.H., Granstrom, D.E. and Collins, S.S., 1994. Transmission of some species of internal parasites in horses born in 1990, 1991, and 1992 in the same pasture on a farm in central Kentucky. Vet. Parasitol., 52: 257-269. Ogbourne, C.P., 1978. Pathogenesis of cyathostome (Trichonema) infections in the horse. A review. Commonwealth Institute of Helmintbology, Commonwealth Agricultural Bureau of the United Kingdom, Miscellaneous Publication No. 5, 25 pp. Reinemeyer, C.R., Smith, S.A., Gabel, A.A. and Herd, R.P., 1984. The prevalence and intensity of internal parasites of horses in the USA. Vet. Parasitol., 15: 75-83. Romero, J., Denegri, G., Nuin, C., Valera, A. and Espinosa, G., 1989. Experimental reproduction of cysticercoids from Anoplocephala perfoliata Blanchard, 1848 in Scheloribates sp. Berlese, 1908 (Acarina-Oribatulidae). J. Vet. Med., B36: 442-446. Russell, A.F., 1948. The development of helminthiasis in Thoroughbred foals. J. Comp. Pathol., 58: 107-127. Todd, A.C., Kelley, G.W., Wyant, Z.N., Hansen, M.F. and Hull, F.E., 1949. Worm parasites in Thoroughbred sucklings and weanlings. A survey of incidence, development, and control. Ky. Agric. Exp. Stn. Bull., 541: 24 pp. Torbert, B.J., Klei, T.R., Lichtenfels, J.R. and Chapman, M.R., 1986. A survey in Louisiana of intestinal helminths of ponies with little exposure to anthelmintics. J. Parasitol., 72: 926-930. Wells, R.W. and Knipling, E.F., 1938. A report of some recent studies on species of Gasterophilus occurring in horses in the United States. Iowa State Coll. J. Sci., 12: 181-203.