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1986 FATAL HUMAN ASCARIASIS FOLLOWING SECONDARY MASSIVE INFECTION J. Kevin Baird ALERTAsia Foundation, [email protected]

M. Mistrey University of Natal

M. Pimsler Divisions of Geographic Pathology and of Microbiology and Immunology, Department of Infectious and Parasitic Disease Pathology, Armed Forces Institute of Pathology, Washington, DC

D. H. Connor Divisions of Geographic Pathology and of Microbiology and Immunology, Department of Infectious and Parasitic Disease Pathology, Armed Forces Institute of Pathology, Washington, DC

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Baird, J. Kevin; Mistrey, M.; Pimsler, M.; and Connor, D. H., "FATAL HUMAN ASCARIASIS FOLLOWING SECONDARY MASSIVE INFECTION" (1986). Public Health Resources. 412. http://digitalcommons.unl.edu/publichealthresources/412

This Article is brought to you for free and open access by the Public Health Resources at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Public Health Resources by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Am. J. Trap. Med. Hyg., 35(2), 1986, pp. 314-318 Copyright © 1986 by The American Society of Tropical Medicine and Hygiene

FATAL HUMAN ASCARIASIS FOLLOWING SECONDARY MASSIVE INFECTION

J. K. BAIRD, M. MISTREY,* M. PIMSLER, AND D. H. CONNOR Divisions ofGeographic Pathology and ofMicrobiology and Immunology, Department ofInfectious and Parasitic Disease Pathology, Armed Forces Institute ofPathology, Washington, DC 20306-6000 and *Department ofPathology, University ofNatal, P.O. Box 17039, Congella 4014 Natal, Republic ofSouth Africa

Abstract. More than '796 Ascaris lumbricoides worms weighing 550 g were recovered at autopsy from a 2-year-old black South African girl. Most ofthe worms were taken from necrotic small intestine, but worms were also in the stomach, esophagus, intrahepatic and extrahepatic bile ducts, and gallbladder. The worms had caused torsion and gangrene of the ileum, which was interpreted as the cause of death. Worms were formalin-fixed and individually weighed. There were 796 intact worms and 112 appreciably large (>0.2 g) fragments of worms. Statistical analysis of the weights revealed 2 distinct populations of worms: 16 large worms (0.5-2.3 g) and 778 small worms (0.03-0.95 g). The difference in weight between these 2 groups of worms was significant (male and female worms treated separately; P < 0.05 to P < 0.001). These observations reveal that the patient acquired a massive and fatal infection with A. lumbricoides while hosting a relatively light worm burden.

Massive infection by Ascaris !umbricoides in­ quired adult A. lumbricoides per human host is 5 variably causes serious complications that may less than 15. • 6 The number of worms reported require surgical intervention or chemotherapy. I as causing intestinal obstruction varies widely­ The most common ofthese complications is in­ from 4 worms in a 45-day-old infant? to as many testinal obstruction ofthe small bowel by a bolus as 1,800 in a young woman." In general, patients of worms.>:' A survey of 3 rural hospitals in with serious complications have 50-500 worms. Louisiana revealed an incidence of 2 intestinal Infants and children tolerate fewer worms than obstructions per 1,000 patients with ascariasis. 2 fully grown people. Young children (1-5 years Thus, ascariasis may create a serious public health old) are most frequently infected because of their problem in some areas." 4. 5 tendency to indiscriminately place things in their Ascariasis in humans is a consequence of mouths.v" ingestion of A. lumbricoides eggs containing in­ In reviewing 7 cases ofmassive infection with fective larvae. The ascarid of the pig, A. suum, A. lumbricoides, Jung reported populations of also causes ascariasis in humans. Eggs ofA. lum­ worms that were uniformly small in size.II This bricoides develop infective larvae after deposi­ finding suggested that the infections were ac­ tion in appropriate soil. Ascariasis is acquired quired through ingestion of a large number of through ingestion of egg-laden soil or food. The infective worms at once, or repeatedly overhours number ofeggs ingested is believed to be directly or within a day or two. Jung referred to these as proportionate to the number of adult worms in "single-brood" infections. He also suggested that the lumen of the small intestine approximately the uniform absence of pre-existing A. lumbri­ 60 days later. The usual number ofnaturally ac- coides infections in the 7 patients indicated that a normal worm burden may confer protection to the host from subsequent infection, even an ex­ Accepted 28 October 1985. traordinarily large number of secondary invad­ ers. In the present report we describe fatal ascaria­ Address reprint requests to: Dr. D. H. Connor, Chairman,DepartmentofInfectiousand ParasiticDis­ sis in a 2-year-old South African girl. Statisiical ease Pathology, Armed ForcesInstitute of Pathology, analysis of the worm weights of the specimens Washington, DC 20306-6000. suggests that a massive infection with A. lum- 314 MASSIVE INFECTION WITH ASCARIS 315

r!Jricoides w~s ac~uired su~sequent to a pre-ex­ ~;'s}t' i ng infectIOnwith an ordinary number ofadult 4 wbrms.

CASE REPORT rC/inical findings A 2-year-old black African girl presented clin- iCallY with malaise, abdominal distention, and ~lion t e n de r palpable worm boluses. She had rapid ~~sp i ra t i on (44/min), bilateral crepitations, and P!1pid pulse (112/min). On the previous day the &child had vomited a worm. On the day of ad- "'m, ission she began gasping, suffered respiratory ):failure, and died.

\1?1, utopsy findings Autopsy 3 days postmortem revealed a mas­ 'sive infection with Ascaris worms. A total of796 :ihtact worms and 112 worm fragments were re­ fi:~ve r e d (Fig. I). Worms and worm fragments ~e i gh ed 550 g. Many worms were in the stomach ~~nd esophagus. No worms or other obstructions ~were in the air passages. Solitary worms were in ~he intrahepatic and extrahepatic bile ducts and FIGURE I. Worms recovered from necrotic small ~gallb l adder . There were boluses ofworms in the intestine, stomach, esophagus, intrahepaticand extra­ ~i l e u m , where they had caused volvulus and in­ hepaticbileducts,and gallbladder ofa 2-year-old black ~fa rct i on . Lungs, meninges, and spleen were con­ South African girl. ifgested. Mesenteric lymph nodes were fleshy, and ;'some were infarcted. There was focal peritonitis In both figures it is evident that a small number t~dj a ce n t to infarcted ileum. of worms weighed appreciably more than the majority ofworms. In both populations the larg­ WORMS est worm was 6 standard deviations from the ~Speci men preparation mean (see Fig. 4). An analysis of variance (AN­ OVA) z-test '< 13 indicated that the largest worm Worms recovered at autopsy were rinsed with that could be considered (with a 95% level of l:tap water and buffered formalin. Worms were confidence) a member ofthe same population of w.;stored in buffered formalin for about 3 months, worm weights was 0.48 g for male worms and Kand then they were individually weighed. The 0.95 g for female worms. Conversely, the prob­ ~worms were grouped by gender and weight into ability (P) that the male worm weighing 0.52 g 'jars. Each jar contained a 0.10 g weight interval or the 2 female worms weighing 1.10 g belong ~of worm s up to 2.4 g. Histologic and taxonomic to their respective worm weight populations was ,~s tud i e s were conducted according to the sex/ less than 5%. This probability decreased with ftweight groups. Selected worms were cut into seg­ increased worm weight to much less than 0.0 I%. ~jne n ts , embedded in paraffin, cut at 5 um, and An ANOVA F-test comparing the aberrantly 'stained with hematoxylin-eosin. heavy worms as a group against the population of smaller worms (male worms < 0.5 g; female Statistical analysis worms < 1.0 g) indicated that P was again less than 5%. These results indicate that the 6 male , t, Histograms in Figures 2 and 3 illustrate the and 10 female worms > 0.5 g and > 1.0 g, re­ weight distributions of male and female 'worms. spectively, were significantly (P < 0.05) larger 316 BAIRD ET AL.

25

20 ...... III E 15 :>-'- ~ ~ GI- g. ~ 10 Lt..oGI GI E ~ ..:. 5

o.,..1tIIt.. 0.08 0.16 0.24 0.32 0.4 0.48 0.56 0.64 0.72 0.8 0.86 Weight in grams

FIGURE 2. Distribution by weight of 145 male Ascaris worms recovered at autopsy of a 2-year-old black South African girl. Each bar represents the frequency of worms in a 0.02 g-interval weight class. than the remaining worms. For comparison, the worms <0.1 g. Almost all female worms <0.2g largest female worm was photographed with the were immature. Female worms < 1.0 g and >0.2 smallest and mean weight female worms (Fig. 4). g were mature and about two-thirds were gravid;

Sexual maturity Taxonomy

Male worms >0.5 g were sexually mature. Fe­ Worms were identified as Ascaris. 14 We at~ male worms> 1.0 g were gravid. All male worms tempted to rule out A. suum. ExaminationB~ <0.5 g were sexually mature, except for 2 of 3 scanning electron microscopy of the ridgesiQf

80 70 60 -I/) E 50 e-, ...0 ~ ~ 40 $ .... ::) 0 CT ... 30 $ $ ... .0 u. E 20 ::) -..-e 10

Weight in grams

FIGURE 3. Distribution by weight of 651 female Ascaris worms recovered at autopsy of a 2-year-old South African girl. Each bar represents the frequency of worms in a 0.05 g-interval weight class. MASSIVE INFECTION WITH ASCARIS 317 nticles on the interior aspect ofthe lips ofthese cill1ens failed to reveal consistent differences on which A. lumbricoides could be differen­ ted from A. suum.P<" The criterion of den ­ le shape (straight vs. convex-sided) showed consistencies not only within the same weight ss, but also on the same dentigerous ridge; th straight and convex-sided denticles were served. The differences in denticle shape ap­ ared to depend upon worm size; the largest rrns had low, rounded nubs as denticles, ereas the smallest worms had sharp, well-de­ ed triangular denticles. A pattern of denticle ar such as this may explain the repeated find­ FIGURE 4. Photograph illustrating the largest, smallest, and mean weight female worms. gs of consistent differences in denticle shape tween A. lumbricoides and A. suum.'>" The carid of the pig is smaller and shorter-lived in worm burden when she acquired her fatal infec­ mans than is A. lumbricoides' ?and would thus tion. ssess more triangular denticles. A similar pat­ The predominance of single-brood infections of wear was observed by scanning electron with human ascariasis reported by Jung!' sug­ icroscopy ofA. suum ofknown age.?" For lack gested that pre-existent infection with A. lum­ .morphological evidence it is difficult to at­ bricoides may prevent development of worms bute this infection to A. lumbricoides. How­ that subsequently infect the host. Similarly, stud­ 23 25 er, the fact that the ascarid ofthe pig reproduces ies conducted by Cort and Ott0 - demonstrat­ orly in humans" persuaded us that the worms ed that chemotherapeutic clearance of estab­ this little girl were A. lumbricoides. lished A. lumbricoides was rapidly followed by reinfection. Their findings indicated that al­ DISCUSSION though humans in endemic areas were contin­ ually ingesting infective eggs, successful devel­ Massive infection with A. lumbricoides with a opment of the worms to egg-producing adult e-existent infection has not been reported. The worms depended upon the absence of an estab­ quency of secondary massive infection is un­ lished infection in the small intestine. The pop­ own because measurements of ascarid worm ulations ofworms studied by lung" suggest that pulations recovered after chemotherapy, sur­ the hypothesized protective effect may be suffi­ ry, or autopsy are rarely reported. Published cient to ward off even massive infection by A . scriptions of worm populations indicate that lumbricoides. ost massive infections with A. lumbricoides Why this protective effect failed in this little nsist of a single brood of worms. girl is not clear. If the protective effect of an Reports of worm sizes in experimental and extant worm population against subsequent in­ turally acquired ascariasis demonstrate that vaders is mediated through the host immune sys­ dividual worm populations are uniform in tem, perhaps the host in this particular instance ight andlor length. We calculated size distri­ was immunocompromised and thus open to tions of worm populations described massive infection while hosting a supposedly sewhere ' l • 2 1. 22 and found the size distribution protective worm burden. Studies of pigs con­ the worms we studied to be extraordinarily ducted by Beaver-? demonstrate that there is pre­ 'de. However, when the male and female worm cedence for multiple-brood Ascaris infections. pulations were separated where the statistical Whether the worm infection described here is alysis indicated, size distributions were in rare or common is of secondary importance to reement with those of reported worm popu­ the hypothesis proposed by lung, II which is that tions from humans. This indicates that most the presence ofa normal worm burden may serve turally acquired infections do not possess a to protect the host from subsequent life-threat­ all number oflarger worms and supports our ening massive infection. Paradoxically, chemo­ ntention that the patient hosted an ordinary therapeutic clearance of A. lumbricoides may 318 BAIRD ET AL. predispose to massive infection with the worm. 9. Pawlowski, Z. S., 1982. Ascariasis: Host "'~'.UUI!~n If this is true, then large scale deworming pro­ biology. Rev. Infect. Dis., 4: 806-8 10. Ochola-Abila, P., and Barrack, S. M. grams to alleviate malnutrition may lead to an Roundworm intestinal obstruction in ' increase in the incidence of massive infection. at Kenyatta National Hospital, Nairobi. Afr. Med. J., 59: 113-117. II. Jung, R. C., 1954. The predominance of ACKNOWLEDGMENTS brood infections in human ascariasis. J. asitol., 40: 405-407. The authors thank Dr. Dean Gibson, HM2 12. Sokal, R. R., and Rohlf, F. J., 1981. David Smith (USN), and HM2 David Rainey 2nd edition. W. H. Freeman and Co., San (USN) for their assistance in the arduous task of cisco. 13. Rohlf, F. J., and Sokal, R. R., 1981. weighing and measuring each worm. Tables, 2nd edition. W. H. Freeman and The views of the authors do not purport to San Francisco. reflect the positions of the U.S. Navy, U.S. Air 14. Chitwood, M., and Lichtenfels, 1. R., 1972. Force, U.S. Army or the U.S. Department of tification of parasitic metazoa in tissue Exp. Parasitol., 32: 407-519. Defense. 15. Sprent, J. F. A., 1952. Anatomical (11stinctieJn This work was supported in part by the World tween human and pig strains ofAscaris. Health Organization Collaborating Centre for the 170: 627-628. Histopathology of Filarial Diseases of Man. 16. Crewe, W., and Smith, D. H., 1971. Human fection with pig ascaris. Ann. Trop. Med. asitol., 65: 84-85. REFERENCES 17. Goldsmid, J. M., 1976. Ascariasis in KJlUae:Sla. Centro Afr. J. Med., 22: 220-223. 1. Beaver, P. c., 1975. Biology of soil-transmitted 18. Lord, W. D., and Bullock, W. L., 1982. helminths: The massive infection. Health Lab. ascaris in humans. N. Engl. J. Med., 306: II Sci., 12: 116-125. 19. Schwartz, B., 1959. Experimental infection 2. Blumenthal, D. S., and Schultz, M. G., 1975. In­ with Ascaris suum. Am. J. Vet. Res., 20: cidence of intestinal obstruction in children in­ 20. Madden, P. A., and Tromba, F. G., 1976. fected with Ascaris lumbricoides. Am. J. Trop. ning electron microscopy of the lip Med. Hyg., 25: 801-805. Ascaris suum adults of known ages. 1. 3. Louw, J. H., 1966. Abdominal complications of tol., 62: 265-271. A. lumbricoides infestation in children. Br. J. 21. Takata, 1.,1951. Experimental infection Surg., 53: 510-521. caris of pig and man. Kitasato Arch. Exper. 4. Jenkins, M. Q., and Beach, M. W., 1954. Intes­ (Tokyo), 23: 49-59. tinal obstruction due to ascariasis: A review of 22. Koino, S., 1922. Experimental infections 31 cases. Pediatrics, 13: 419-425. man body with ascarides. Jpn. Med. 5. Arean, V. M., and Crandall, C. E., 1971. Asca­ 317-320. riasis. Pages 769-807 in R. A. Marcial-Rojas, 23. Cort, W. W., Schapiro, L., and Stoll, N. R., ed., Pathology ofProtozoal andHelminthic Dis­ A study of reinfection after treatment of eases. Williams & Wilkins Co., Baltimore. worm and ascaris in two villages in 6. World Health Organization, 1964. Soil-transmit­ Am. J. Hyg., 10: 614-625. ted helminths. WHO Tech. Rep. Ser. No. 277. 24. Otto, G. F., 1930. Ascaris lumbricoides: p.13. ment and loss of worms and reinfestation. 7. Rathi, A. K., Batra, S., Chandra, J., and Mehrotra, Am. Med. Assoc., 95: 194-195. S. N., 1981. Ascariasis causing intestinal ob­ 25. Cort, W. W., Otto, G. F., and opmuier struction in a 45 day old infant. Indian Pediatr., Ascariasis in Southwest preliminary 18: 751-752. report. South. Med. J., 22: 8. Choe, Y., and Lee, J., 1974. Intestinal obstruction 26. Beaver, P. c., 1952. Observations on the due to a mass of 1,842 ascarides in Western miology of ascariasis in a region of Africa. J. Korean Med. Assoc., 17: 58-62. worm endemicity. J. Parasitol., 38: 44:)-"f)')':