OF WASHINGTON, VOLUME 9, NUMBER 1, JANUARY 197 55 Prevalence and Distribution of Helminths of Swine in South Carolina1 C. DANIEL RIDDLES AND DONALD J. FORRESTER"* Department of Entomology and Zoology, Clemson University, Clemson, South Carolina 961 ABSTRACT: The prevalence of helminths of swine in South Carolina during 196869 was: Oesophagostomum spp., % (including O. dentatum, O. quadrispinulatum, and O. hrevicaudum);, %; Strongyloides ransomi, 7%; Metastrongylus spp., 6% (including M. apri, M. pudendotectus, and M. salmi);, 5%;, %; Ascarops strongylina, 1%; Physocephalus sexalatus, <1%; and Macracanthorhynchus hirudinaceus, <1%. Neither Trichinella spiralis nor Hyostrongylus ruhidus were encountered. The highest prevalence of infection by, S. dentatus, P. sexalatus, and M. hirudinaceus occurred in brood, whereas the highest A. suum infections occurred in market. Pigs under 1 weeks of age had the highest prevalence of T. suis and S. ransomi. Little difference in prevalence was noted in purebred vs. crossbred swine except for A. suum and S. ransomi, which were more common in crossbreeds. No significant differences were found in the prevalence and distribution of the helminths geographically. Higher levels of infection were recorded during the summer months for A. suum, T. suis, and S. ransomi, whereas levels of infection by were irregular over a 1month period. Swine which had been treated with anthelmintics did not show reduced helminth populations. Feces of swine from farms which utilized central farrowing houses and concretefloored parlors contained numbers of helminth eggs comparable to those from feces of swine from farms lacking these facilities. However, the prevalence of helminths appeared to be related directly to the overall quality of management, i.e., good management resulted in fewer parasites, although this trend was not statistically significant. The United States Department of Agriculture has estimated the annual loss due to harmful effects caused by internal parasites of swine to be more than 75 million dollars (Stewart and Southwell, 196). A large portion of this loss occurs in the southeastern states. In North Carolina, for example, internal parasites reduce the value of swine by at least one dollar for each pig marketed (Batte and Moncol, 1966). The control of swine parasites, therefore, is a major problem, particularly since intensification and expansion of the swine industry has not been accompanied by the reduction of worm populations (Batte et al., 1965). A knowledge of the parasites present in swine of different ages and breeds over the course of a year is essential to help formulate control programs that may involve management, sanitation, drugs, or combinations thereof. 1 Contribution No. 89 from the South Carolina Agricultural Experiment Station. Supported in part by the Cooperative Extension Service of Clemson University and by a grant from the South Carolina Swine Producers Association. Present address: Department of Biology, Greenville Technical Education Center, Greenville, South Carolina 966. Present address: Department of Veterinary Science, University of Florida, Gainesville 61. With these facts in mind, an ecological study of the helminths of swine in South Carolina was designed in two phases: (1) a determination of the species present, their prevalence, and geographic distribution; () a determination of the seasonal dynamics of several gastrointestinal nematodes. Materials and Methods South Carolina can be divided into three broad geophysical areas, the Piedmont, Sandhill, and Coastal Plain regions (Fig. 1), which vaiy in soil texture, average annual precipitation, annual temperature ranges, and vegetation. The climate is described as temperate for the Piedmont and Sandhill regions and warm temperature to subtropical for the Coastal Plain region (Kish, 1968, 1969). Of the swine population of the state (,), 75% is located in the Coastal Plain region with the other 5% distributed about equally between the Sandhill and Piedmont regions (Lanham and Whitworth, 1967). During May 1968, fresh feces were collected from swine in each of the 6 counties of the state. Table 1 shows the sample sizes Copyright 11, The Helminthological Society of Washington
56 PROCEEDINGS OF THE HELMINTHOLOGICAL SOCIETY Figure 1. The Piedmont, Sandhill, and Coastal Plain regions of South Carolina with the locations of the eight swine farms sampled monthly from September 1968 to August 1969. from swine populations in each of the three geophysical regions. For each sample information was obtained on type and breed of hog, quality of management ("above average," "average," "below average"), whether market were maintained on ground or concrete, use of a central farrowing house, number of years swine had been raised on the farm, date of last anthelmintic application, and type of drug used. Farms classified as "above average" had balanced feeding programs, proper buildings and equipment, high overall levels of sanitation, and practical programs of prevention and treatment of diseases and parasites. "Average" farms had a moderate number of these practices in use, while "below average" farms utilized none of them. The number of samples collected was divided equally among three pig types: (1) brood, () pigs under 1 weeks of age, and () market, which included some gilts. All of the samples were collected during the week of May 1968. A companion necropsy study was conducted in slaughterhouses, which handled animals from each region of the state. Lungs, diaphragms, kidneys and perirenal fat, and complete gastrointestinal tracts were collected. In some collections the samples were limited to lungs, diaphragms, and kidneys, or to kidneys only. The numbers of animals sampled are summarized in Table 1. In order to study the seasonal dynamics of several nematode parasites, an additional 1 fecal samples were collected each month from September 1968 through August 1969 from swine on two farms in the Piedmont region, two farms in the Sandhill region, and four farms in the Coastal Plain region (Fig. 1). All of the eight farms were considered to be "average" managementlevel farms. Each month 15 fecal samples were taken from each farm, five samples coming from each of the three pig types (brood, pigs under 1 weeks of age, and market ). Each of the 71 fecal samples collected during May 1968 from swine in each county was placed in 5 cc of 6% formalin and later was examined qualitatively for the presence of helminth eggs by a sodium dichromate flotation technique. The 1, fecal samples collected from swine on the eight farms over a 1month period were analyzed quantitatively by a modified McMaster technique using a 5cc liquified mixture of fecal matter and 6% formalin in a saturated salt solution. The formalin Table 1. Numbers of fecal samples and animals examined at necropsy in slaughterhouses in South Carolina during 196869. Region Piedmont Sandhill Coastal Plain Total Swine population 5,1 5,9 8,, samples obtained 196 119 16 71 Complete* * Gastrointestinal tract, lungs, kidneys, and diaphragms. f Lungs, kidneys, and diaphragms. + In half of these samples, only kidneys were examined. 8 6 Numbers of animals sampled by necropsy Partialf :i: x :j: 8? 1 86 All si vine 5 7 96 Copyright 11, The Helminthological Society of Washington
OF WASHINGTON, VOLUME 9, NUMBER 1, JANUARY 197 57 Table. Percentage prevalence of helminths of swine in South Carolina as determined by necropsies and fecal analyses during 196869. Helminths Metastrongylus spp. Ascarops strongylina Physocephalus soxalatus Trichinella spiralis Macracanthorhynchus hirudinaceus Necropsies 57(1)* (1) 15(1) (8) (96) (1) 1(1) (56) 7(1) 6(96) Per cent prevalence Fecal analysis (71) (71) 7(71) 6(71) (71) (71) (71) (71) 7(71) (75) (75) 7(71) 6(75) 5(779) (96) 1(75) <1(75) (56) <1(75) 68(87) * Numbers in parentheses indicate number of swine sampled. feces mixture was obtained by adding 1 g of feces to 5 cc of 6% formalin. Necropsies were performed following standard procedures. Nematodes and acanthocephalans were preserved in 7% glycerinated ethyl alcohol and later mounted in lactophenol and identified. Results and Discussion Prevalence of helminths The prevalence of helminths is shown in Table. The prevalence of the several species of Oesophagostomum, determined from a sample of 19 specimens collected from eight pigs, was as follows: O. dentatum (6%), O. quadrispinulatum (7%), and O. brevicaudum (1%). Table. Percentage prevalence of helminths in pigs,* brood, and market in South Carolina as determined by fecal analysis during 196869. Helminths Metastrongyhis spp. Ascarops strongylina. Macracanthorhynchiis hirudinaceus All helminths Pigs* 1 18 16 8 1 * Pigs under 1 weeks of age. 61 6 18 7 5 1 In a sample of 1 lung nematodes from 11 pigs 6,, and % were M. apri, M. pudendotectus, and M. salmi, respectively. No cestodes or trematodes were encountered nor were Trichinella spiralis or Hyostrongylus rubidus recovered. The absence of Hyostrongylus could be attributed possibly to the small number of stomachs examined. Esophageal samples were not inspected for the presence of Gongylonema pulchrum. In Table the prevalence data obtained during the present study are compared with similar information from swine in northern Florida (Spindler, 19), Georgia (Andrews and Connelly, 195; Spindler, 19), and North Carolina (Batte and Moncol, 1966). The results from these studies do not agree closely, but it does appear that, A. suum, and S. ransomi rank high in relative prevalence in swine in these southern states. Table. Comparison of percentage prevalence of helminths of swine in northern Florida, Georgia, and North Carolina with the present study. Area ( year of analysis ) Helminth South Carolina (196869) Georgia and northern Florida* (1991) Georgia^ (191) North Carolina* (196566) Metastrongyhis spp. Ascarops strongylina Physocephalus sexalatus Macracanthorhynchus hirudinaceus Hyostrongylus rubidus * From Spindler, 19. t From Andrews and Connelly, 195. From Batte and Moncol, 1966. 78 5 1 <1 <1 7 7 6 51 5 7 5 15 6 68 55 1 1 71 16 16 7 1 I Copyright 11, The Helminthological Society of Washington
58 PROCEEDINGS OF THE HELMINTHOLOGICAL SOCIETY 1 5' x < i ^ 1 UJ d 1 z to C5 < UJ Trichuris Sfrongyloides /'. y_«^ ^.».^rf' S O N D J F M A M J J A 1968 1969 HUU <n S 1 to >S n "D " m Figure. Average number of TriV/mris and SfrongyZozrfe* eggs in feces collected from all types of swine from September 1968 to August 1969 in South Carolina. Influences on the prevalence of helminths The results of the statewide fecal collection and the necropsy study (Table ) showed that the brood sow was the major host of Oesophagostomum spp., S. dentatus, P. sexalatus, and M. hirudinaceus, that market (both sexes) harbored the highest infections of A. suum, and that pigs under 1 weeks of age contained the highest prevalence of infection by T. suis and S. ransomi. Metastrongylus spp. and A. strongylina were distributed evenly among the three swine types. No significant differences in the prevalence of all nematode eggs in swine feces were found when the results were studied with reference to breed of swine (pure vs. crossbred swine), geographic region in the state (Piedmont vs. Sandhill vs. Coastal Plain), recent anthelmintic O U LL O 1 la*....tttmm*** S 1968 N Pigs under 1 wks of age Market D J F M A M J J A 1969 Figure. Average number of Ascaris eggs in feces collected from pigs under 1 weeks of age, brood, and market from September 1968 to August 1969 in South Carolina. to LJ U_ o d z o < LLJ 1 fhrtfmf.kwfs* 5 5 < a: LU Q. 1 Pigs under 1 wks S " 9 l Market / I / / i / ' i / x / N 15 N D J F M A M J J A 1968 1969 Figure. Average number of Oesophagostomum eggs in feces collected from pigs under 1 weeks of age, brood, and market from September 1968 to August 1969 in South Carolina. experience (medicated vs. nonmedicated), usage of a central farrowing house (used vs. not used), and method of housing for market (concrete vs. ground). However, certain differences in the prevalence of individual nematodes in various age classes of swine were apparent. For example, the prevalence of Ascaris and of Strongyloides eggs was significantly higher* in crossbred (1 and 17%) than in purebred ( and 8%) pigs under 1 weeks of age. Eggs of were significantly* more common in feces from market raised on dirtfloored lots (%) than in feces from market raised on concretefloored lots (%). In reference to the overall quality of husbandry, the degree of good management that existed on the farms appeared to be directly related to the incidence of nematodes although these differences were not statistically significant. From September 1968 through August 1969 monthly egg counts of four nematodes, A. suum, T. suis,, and S. ransomi, were made on feces collected from swine on eight farms. Combined egg counts for all four species of nematodes varied irregularly between and 16 eggs/sample throughout the 1month period. A slight rise, although not significant, was seen in the counts for the month of July. Feces from brood coii * 5% level of significance; chisquare test. Copyright 11, The Helminthological Society of Washington
OF WASHINGTON, VOLUME 9, NUMBER 1, JANUARY 197 59 tained the highest combined egg counts for 8 of the 1 months. Market and young pigs passed a higher number of eggs in their feces in July and August than at other times of the year. The number of Trichuris eggs in feces was highest during the summer and fall months (Fig. ), although the incidence of this nematode was low throughout the study. Numbers of Strongyloides eggs were highest also during July and August in feces of pigs under 1 weeks of age (Fig. ). The numbers of Ascaris eggs increased significantly in feces from brood during November, and in feces of market during June and July (Fig. ). Irregular peaks of egg production were characteristic of throughout the 1 month period (Fig. ). Ackno wledgmen ts The authors thank Dr. T. B. Stewart, Mr. C. W. Ackerman, Dr. W. E. Johnston, Dr. J. B. Kissam, and Mrs. Janice Riddle for advice and assistance in various aspects of this study. Literature Cited Andrews, J. S., and J. W. Connelly. 195. Worm parasites in swine raised under a moderate degree of sanitation. Proc. Helm. Soc. Wash. 1: 61. Batte, E. G., D. J. Moncol, A. C. Todd, and R. S. Isenstein. 1965. Critical evaluation of an antheknintic for swine. Vet. Med./Small Anim. Clin. 6: 5955., and. 1966. Internal parasites of swine. North Carolina State Univ. Anim. Science Rep. 171, Vet. Series No. 7: 15. Kish, A. J. 1968. Clemson University and South Carolina Agricultural Experiment Station climatological data. Agric. Weather Res. Ser. No. 19: 1.. 1969. Clemson University Agricultural Experiment Station weather records. Lanham, W. J., and C. H. Whitworth. 1967. South Carolina livestock and poultry statistics. U.S.D.A. Crop and Livestock Series No. 5: 1. Spindler, L. A. 19. The incidence of worm parasites in swine in the southern United States. Proc. Helm. Soc. Wash. 1:. Stewart, T. B., and B. L. Southwell. 196. The economic importance of internal parasites of swine and their control by management and treatment. Ga. Coastal Plain Exp. Sta. Mimeo Ser. N.S. 1: 11. Transplantation of Heterakis gallinarum Larvae: Effects on Development of H. gallinarum and the Transmission of Parahistomonas wenrichi EVERETT E. LUND United States Department of Agriculture, Agricultural Research Service, National Animal Parasite Laboratory, Beltsville, Maryland 75 ABSTRACT: Following the rectal transfer of 1dayold larvae of Heterakis gallinarum from young chickens to young turkeys, 5% of the worms were lost in the first hr, and only % of those transferred survived days or more. Most of these remained to maturity, but their development was retarded about 5 days. Parahistomonas wenrichi was detected in the cecal discharges of seven of the 1 turkeys only 7 days after they had received the 1day larvae rectally, days sooner than has ever been observed for infections acquired by natural means. These early infections must have been initiated by histomonads liberated during the first % days following the transfer of the larvae, this being also die time of greatest loss of larvae in the recipient birds. Infections with P. wenrichi are probably initiated principally, if not exclusively, by organisms liberated by the death and dissolution of the larvae harboring them. During a recent study of the acquisition of histomonads by the cecal worm, Heterakis gallinarum (Schrank, 1788) Madsen, 199, worms were grown 1 days in one host and then transferred to the rectum of another to complete their development (Lund, 1971). Such Copyright 11, The Helminthological Society of Washington