Oklahoma State University Library STUDIES ON THE DEVELOPMENT OF TRICHURIS VULPIS II (FROHLICH, 1789) (NEMATODA: TRICHURIDAE) By ROBERT RUBIN Doctor of Vet erinary Medicine Colorado Agricultural and Mechanical College Fort Collins, Colorado 1949 Submitted to the faculty of the Graduate School of the Oklahoma Agricultural and Mechanical College i n partial fulfillment of the requirements for the degree of MASTER OF SCIENCE 1953 i STUDIES ON THE DEVELOPMENT OF TRICHURIS VULPIS n (FROHLICH, 1789) (NEMATODA: TRICHURIDAE) ROBERT RUBIN Master of Science 1953 Thesis and Abstract Approved: Thesis Adviser ii ACKNCMLEDGMENT I wish to express my sincere appreciation to Professors Wendell H. Krull and Philip E. Smith for the guidance and encouragement offered me during this investigation. iii TABLE OF CONTENTS Page INTRODUCTION ..... 1 REVIEW OF LITERATURE 3 METHODS AND MATERIALS 9 DATA ON THE INCIDENCE AND ABUNDANCE OF TRICHURIS VULPIS .... 21 DATA ON EGG DEVELOPMENT 22 STUDIES OF VARIOUS AGED IMMATURE FORMS OF TRICHURIS VULPIS 33 Larva expressed from egg 33 14-day-old-larva 34 21-day-old-larva 36 24-day-old-larva 37 28-day-old-larva 37 32-day-old-larva 37 42-day-old-larva 38 54-day-old-larva . 38 Adult worms .•.• . 39 THE LENGTH OF THE PREPATENT PERIOD FOR TRICHURIS VULPIS IN DOGS . 41 OBSERVATIONS ON THE LONGEVITY OF TRICHURIS VULPIS ..... OBSERVATIONS ON THE HISTOPATHOLOGY OF TRICHURIS VULPIS INFECTIONS . 43 SUMMARY AND CONCLUSIONS 48 REFERENCES CITED. 51 VITA . • • . 65 iv LIST OF TABLES Page Table I Showing the Incidence and Abundance of 1• vulpis in 250 Oklahoma Dogs 21 Table II Showing Developmental Reaction of Eggs of!, v1tl.pis at a Temperature Range of 19.3° C.to 26.4° C.. 24 Table III Showing Developmental Reaction of Eggs of!• vulpis at a Temperature Range of 25.4° C.to 32.2° C.•.. 25 Table IV Showing Developmental Reaction of Eggs of!· vulpis at a Temperature Range of 35.0° c.to 44.4° C, • 26 Table V Showing Developmental Reaction of Eggs of!, vulpis at a Tgmperature Range of 48.3° C.to 55.8 c .... 27 Table VI Showing Developmental Reaction of Eggs of!• vulgi§ at Temperature Ranges of 23.3 C to 29.20 C, 33.3° C to 38.8° C, and 4.4° C,to 5.3° c. 28 Table VII Summarizing the Results of the Developmental Reaction of Eggs of !, vulpis at various Temperature Ranges Presented in Tables II Through VI • • • • • . • • • 30 Table VIII Showing Developmental Reaction of Eggs of!• vulpis in Aerated Water at a Temperature Range of 25.5° c. to 37.7° C. • . • . • • . • • • • . • • • 31 Table IX Showing Measurements of Immature Specimens of Trichuris vulpis at Various Ages ............•.... ,, . 40 Table X Prepatent Periods for!, vulpis in Seven Experimental Dogs .. , •• 41 V LIST OF FIGURES Page PLATE I Figure 1 Cecum with m.unerous 1'_. vulpis from an experimentally infected dog •• 56 Figure 2 An egg containing an unsegmented zygote recovered from feces by salt flotation •.••.••••••• 56 Figure 3 An egg, removed from the uterus of a worm and cultured in water, show­ ing a fully-developed larva within the shell . • • • • • • • 56 Figure 4 A first-stage, infective larva ex­ pressed from an egg. The larva shows the anteriorly-located lancet or mouth spear ••••.•••••• 56 PLATE II Figure 5 Anterior extremity of a larva, ex­ pressed from egg, showing lancet imbedded in the muscular portion of the esophagus • • • • • • 58 Figures 6, Anterior extremities of several larvae, 7, 8 and expressed from eggs, showing various 9 degrees of retraction of the lancet ••• 58 Figure 10 Posterior extremity of a larva, ex­ pressed from egg, showing the eccen­ tric posterior indentation ••• 58 Figure 11 Section of the glandular area in the widest part of the esophagus of a 21-day-old larva. • • • • • • • • • • • • 58 Figure 12 Anterior extremity of a 21-day-old larva, showing the lesser diameter (compare with figure 11) and blunt termination , • • • • • • • • • • 58 vi Page Figure 13 Posterior extremity of a 21-day-old larva, showing loosened cuticle as well as a mass of cells in the body cavity near the junction of the in­ testine and rectum ••• 58 Figure 14 Junction of the muscular and glan~ dular portions of the esophagus of a 21-day-old larva, showing the abrupt transition 58 Figure 15 Junction of the muscular and glan­ dular portions of the esophagus of a 24-day-old larva, showing what are assumed to be nuclei and nucleoli of glandular cells •••••••••• 58 Figure 16 Junction of the glandular portion of the esophagus and intestine of a 21- day-old larva, showing the projection of the tubular part of the esophagus beyond the esophageal glandular cells into the lumen of the intestine 58 Figure 17 The posterior extremity of a 28-day­ old larva, showing the terminal part of the glandular esophagus, the short intestine, and the rectum. Note the loosened posterior cuticle • • • • • 58 Figure 18 Posterior extremity of a 24-day-old larva, showing the appendage (figure 13) located just posterior to the junction of the intestine and rectum 58 PLATE III Figure 19 Posterior extremity of a 54-day-old female, showing the terminal intes­ tine and rectum of the digestive system, as well as part of the re­ productive system, which apparently developed from a primordium similar to that shown in figure 13 •• 60 Figures 20, Anterior, middle and posterior por- 21 and 22 tions of a 42-day-old larva, show­ ing relative diameters ••••.•• 60 Vii . Page Figure 23 Anterior extremity of an adult, showing the lancet attached to the anterior end of the muscular esoph­ agus. Note the shallow mouth cav­ ity which is devoid of lips or papillae • • • . • • • • . • • 60 Figure· 24 Portion of a 42-day-old larva, showing a hooked, tubular repro­ ductive structure, adjacent to the digestive tract, presumed to be the further development of the structure shown in figure 1.3 . • • • . • • • • • • • 60 Figure 25 Section of an adult male, showing two gland-like structures at the junction of the esophagus and in- testine . • • . • • • • . • . 60 Fi gure 26 Section of a 54-day-old female larva, showing the uterus and vagina, but no vulvar opening, at the level of the junction of the esophagus and intestine • • • • . • • • • • • • • • 60 Figure 27 Posterior extremity of a 54-day­ old male larva, showing a well­ formed spicule within the body. 60 Figure 28 Section of an adult female, showing two gland-like structures at the junction of the esophagus and in­ testine, similar to those shown for the male in figure 25 •.•••.• 60 PLATE J.V Figure 29 Photomicrograph of cecal tissue showing cross sections of 32-day­ old larvae in the epithelium and superficial tunica propria, greatly enlarged. • • . • •• 62 Figure 30 Photomicrograph of cecal tissue showing various sections of 54-day­ old larvae embedded in a lymph fol­ licle lying below the muscularis mucosae. The area around the para­ sites is necrotic ••••••••• 62 viii Page PLATE V Figure 31 Photomicrograph of cecal tissue showing cross sections of mature worms and a marked increase in lymphocytes in the tunica pro- pria . o • I> o • • Figure 32 Photomicrograph of cecal tissue containing a cross section of a mature worm to show the relation­ ship of the parasite to the host tissue, greatly enlarged •••• 64 ix INTRODUCTION The whipworm or trichurid worm is a parasitic nematode which in­ habit s the cecum and proximal portion of the large intestine of mammals. It has been observed also in the terminal portion of the small intestine of cer tain hosts. It has been reported from man, from all of the domes­ t ic mammals except the horse 1 and also from numerous wild mammals, par­ ticularly rodents. The life cycle is direct and infection occurs by the ingestion of eggs in which larvae have developed. This worm has a di stinctive shape in that the anterior, longer part of the body is slen­ der and hair-like and the posterior, shorter part, considerably thicker. This whip-like appearance is responsible for the common name of the parasite. The worm lives in the host with part or all of the slender anterior end embedded within the mucosa, while the posterior, thick end is free in the lumen of the cecum or large intestine. Although trichurid worms were described from man and certain of the domestic animals late in the 18th century, no extensive studies of the life cycle were made until about the middle of the 20th century. Even thi s work, which was with the species in the dog, was incomplete since it dealt almost exclusively with the early development of the worm in the host. Very little about later development was included. Only sketchy life cycle data have been reported for the species in the sheep, the ox, and the pig, and the accuracy of some information in the literature regarding these forms is indeed questionable. No 1 2 information is available on the species in the rabbit. The presence of trichurids in the cat and mouse has been taken for granted. Recent work (Enzie, 1951) seems to indicate that there is no trichurid in the cat, in spite of the numerous reports in the literature. The species peculiar to the mouse has never been reported officially in the United States. The human trichurid has been studied sparingly but has been written about many times, and the majority of the articles relate either to egg development or pathology based on clinical cases. The papers on egg de­ velopment studies are for the most part scientific, but those on pathology contain much conflicting information, and results are often inconclusive. Because this parasite is present in man and most of his domestic animals, and because the biology of this worm is incompletely known, further research is necessary.