Intestinal Ascariasis: New

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1 37 Brian A. Ellman1 J. Michael Wynne2 Arthur Freeman3 Received April 1 1, 1 978; accepted after revision March 1 7, Department of Radiology, Llvingstonc Hospital, Port Elizabeth, South Africa. Present address: Parkland Memorial Hospital, Dallas, TX Address reprint requests to B. A. ElIman. 2Department of Paediatric Surgery, Livingstone Hospital, Port Elizabeth, South Africa. Present address: Department of Surgery, University of Queensland, Brisbane, Australia. 3Department of Paediatrics, Uvingstone Hospital, Port Elizabeth, South Africa. AJR 135:37-42, July X/80/ $00.00 American Roentgen Ray Society Intestinal Ascariasis: New Plain Film Features Radiographs from 30 children with intestinal obstruction caused by a bolus of Ascaris worms were analyzed. Worms could be seen outlined against intestinal gas; the interface between worm bolus and adjacent gas shadows was irregular. Gas trapped within the worm bolus had irregular outlines. There were also fine linear radiolucent shadows and small bubbles. Fluid levels were sometimes distorted by a projecting worm bolus, resulting in a hump eftect. Some of the radlolucencies were within the worms. These features were used in an analysis of radiographs from 68 children who did not have bolus obstruction. Of 44 children with proven ascariasis, 28 (64%) had suggestive radiologic features. In four of 24 children without Ascaris ova in the stools, confusion with fecal shadows resulted in a false-positive diagnosis on the radiographs. Recognition of the worm infestation in asymptomatlc patients is important because intestinal malabsorption may contribute to nutritional deficiency. It has been estimated that one-fourth of the world s population is infested with ascariasis [1 1. This infestation usually occurs by swallowing food mixed with soil contaminated by human feces. Probably 4 million persons in the United States harbor the worm [2]. Children in poor socioeconomic conditions are most frequently infested. A reversible malabsorption is induced that contributes to the nutritional depletion in these children [1, 3-5] and so renders them susceptible to other infections. Pathology The pathology of ascariasis, its complications, and treatment were recently reviewed [6]. Each female worm lays some 200,000 eggs daily [6]. These survive for long periods in the soil, and infestation occurs by swallowing soil contaminated with human feces. When swallowed, the eggs hatch in the stomach. Larvae then penetrate the gastric wall. These larvae, measuring sm, enter the portal circulation and migrate to the lungs. In sufficient numbers they induce a pneumonitis. The larvae travel up the trachea to be swallowed again and so pass to the jejunum where they mature and survive for periods up to I year, reaching lengths of cm. One individual can accumulate in excess of 1,000 worms. The two most common abdominal complications are intestinal obstruction by a bolus of worms and biliary disease due to invasion of the biliary system. Subjects and Methods Group 1 There were 72 patients with bolus obstruction due to Ascaris admitted to the pediatric

2 38 ELLMAN ET AL. AJR:135, July Fig. 1 -Worms outlined longitudinally against intestinal gas. Lumen of intestine of central worm filled by gas. Fig. 2.-Worms seen end-on within loop of small bowel. Central lucency produces a target-type appearance. Gas shadows continue as radiolucent lines curving toward irregular collection of worms on patient s right. wards at Livingstone Hospital over a 4 year period, The diagnosis was based on typical gas patterns, a palpable mass, and ova in the stool. Erect and supine abdominal films, available from 30 of the 72 cases, were reviewed. A careful analysis of patterns was made in order to define the features. Our observations led us to suspect that Ascaris might be recognized in patients who did not have an obstructing bolus and in asymptomatic carriers. In order to study this, we observed a further group of children admitted to the pediatric wards. Group 2 A group of 65 patients in whom there was no indication of bolus obstruction was selected. In 32 (group 2A), there was some abdominal complaint but no evidence of obstruction. Supine and erect abdominal films were selected for review. Worms were proven in 24 of these patients because of proven biliary invasion, incidental discovery at laparotomy, or the discovery of ova in the stools. In eight, stool examination was negative. In only two were worms previously identified on the radiographs. Another 36 children (group 2B) with nonsurgical complaints had supine abdominal films performed for this study. In 1 9 of these, there was family or past history of worms or chest problems that gave rise to some clinical suspicion of worm infestation. All 36 cases had stool examination for worms, and ova were found in 20 cases. Each film in group 2 was examined by two of us working together. A careful search was made for individual worms outlined by gas in the small intestine, linear radiolucent shadows, and fine bubbles. The worm status of the patients was not known to those examining the films. Laboratory Studies In order to confirm our observation of gas within the lumen of worms, we studied the almost identical Ascaris suum, whose host is the pig. Freshly resected pig jejunum was examined radiographically. A group of the worms was immersed in barium, warmed, and Fig. 3.-Gas and barium in still-living worm passed after vermifuge. Patient had recent barium meal. mixed with feces at varying temperatures. This was repeated with Ascaris lumbricoides. The Ascaris intestine is a very thin distensible tube and does not contain muscle. Food is pumped through it by a muscular pharynx. Results Group 1 Individual worms occasionally were seen clearly outlined in longitudinal, oblique, or transverse projection against the gas shadows (figs. 1 and 2). These linear or bubble-shaped

3 AJR:135, July 1980 INTESTINAL ASCARIASIS 39 4 translucencies associated with isolated worms indicated that these shadows might be due to gas within the worm lumen. Radiographs of still living worms passed after a vermifuge revealed gas bubbles in some, confirming this view (fig. 3). Often the worms could only be identified as a conglomerate mass (fig. 4). Conversely, gas trapped within the worm bolus assumed definite patterns (fig. 5). With the patient erect, the worm bolus often demonstrated an irregularity or nodularity. This resulted in distortion of the fluid level, producing a hump (fig. 6). This hump frequently contained irregular gas bubbles or linear radiolucent shadows which increased its significance (fig. 7). This appearance has not previously been described to our knowledge. Sand-eating among children of this socioeconomic group is common. The ingestion of silica by parasites can render them visible (fig. 8). Gaseous distention of the small bowel was a frequent occurrence, but fluid levels were not always present. Complete intestinal obstruction with markedly distended bowel and multiple fluid levels suggests damage to the bowel wall and impending gangrene due to release of toxins from the worm bolus [15]. Group 2 Individual worms were seen outlined against small intestinal gas in three of the patients. They had increased intestinal gas due to ileus or some other cause. The most constant finding was the presence of linear radiolucent shadows, singly or in small groups. This finding was remarkably consistent among group 1 patients and in both those with and without abdominal symptoms in group 2. Fine bubbles were difficult to distinguish from normal shadows but were used as supportive evidence, particularly if arrayed in rows. All patients had stool examination at radiography (table 1 ). In 28 (64%) of the 44 patients with proven ascariasis, there was radiologic evidence of worm infestation (sensitivity). In 20 (83%) of the 24 patients with negative stool examination, there was no radiologic evidence of ascariasis (specificity). There were four (1 7%) false-positive diagnoses. The infestation was correctly determined from the radiographs in 48 (70%) of the 68 patients. In 20 (30%) the results were inaccurate (1 6 false negative and four false positive). Three of the false-positive diagnoses were made among the first 32 cases reviewed. Reexamining these films after disclosure of the worm status made it apparent that we

4 40 ELLMAN ET AL. AJR:135, July 1980 Fig. 6.-Distension of loops of small bowel with hump sign produced by worm bolus intruding into lumen (arrow). Fig. 7.-Hump sign (arrow) with bolus of worms clearly seen below (arrowhead). Partial small bowel obstruction. 4 Fig. 8.-Linear opacities due to sand within worm intestine in child with pica (arrow). had paid insufficient attention to the distribution and pattern of fecal shadows in the bowel. The diagnostic accuracy was greatest among the last 17 patients, all of whom were in group 2B and had no abdominal complaints. Seven of eight children with ova in the stools were correctly diagnosed. Radiographs of freshly resected pig jejunum containing worms showed intraluminal gas shadows (figs. 9A and 9B). TABLE 1 : Group 2: Ascariasis Findings Stools vs Radiographs No Patients Positive stools: Positive radiographs 28 Negative radiographs i Negative Subtotal stools: Positive radiographs 4 Negative radiographs Q Subtotal Total no. patients 68 Sometimes the linear lucency appeared between the worm and the jejunal wall (fig. 9C). The pattern of shadows appeared similar to those we found in children (fig. 1 0). When removed from the intestine, the worms rapidly expelled the intraluminal gas and delayed studies failed to demonstrate any gas. Neither Ascaris suum nor Ascaris lumbricoides could be induced to swallow air or barium outside the intestine. Discussion The appearance of worms on barium studies is well recognized [8], and this is generally believed to be the most reliable radiologic method of recognizing them. In plain films worms are sometimes recognized against gas in the intestine [9-1 1]. Several authors have drawn attention to the value of the plain film in the diagnosis of obstruction by a bolus of worms [ ]. However, it appears that the worms themselves were only identified in one out of four patients with this form of obstruction [15].?.

5 AJR:135, July 1980 INTESTINAL ASCARIASIS 41 Fig. 9.-Laboratory studies of Ascaris suum in pigs. A, Pig intestine containing A. suum. Linear radiolucencies within worms. B, Gas in lumen of A suum after removal from intestine. C, Linear radiolucencies due to gas trapped between worms. - : Fig Colon lies over linear, somewhat irregular vertical radiolucencies (A). which cannot be confidently identified as worms. Long regular lucent shadow (B) lying just outside colon shadow is unmistakable. Worm containing gas appears transversely against small intestinal gas (C). Descriptive terms used to describe the bolus have included whirlpool (cited in [1 7]), medusa [1 6], like breadcrumbs or beehives [1 4], and tangled thick cord [1 2]. Several of these authors have drawn attention to the visualization of worms against intestinal gas either longitudinally or transversely. Atken and Dickman [1 3] described closely packed short irregular wisp-like or wiggly radiolucent lines. Bean [1 7] drew attention to the incidental visualization of isolated worms on routine sample films. We emphasize the distinction between the appearance of worms in the intestine of the unobstructed patient and the tangled worm mass in the patient with bolus obstruction. The former merely indicates the infestation and suggests one possible cause of the patient s symptoms. A bolus of worms, however, indicates the cause of the patient s symptoms and frequently the radiograph establishes a definitive diagnosis. In both situations the appearances may sometimes be mimicked by feces in the colon, and it is necessary to study no only the gas pattern but also the distribution of the shadows and their relation to other colonic gas shadows. The mottled pattern produced by the admixture of gas and feces in the colon can sometimes mimic the pattern produced by aggregates of worms and gas in the small bowel. When the colon can be identified with certainty, the differentiation can be made, since worms do not infest the colon except in transit in the feces. When the radiologic features of a bolus are in doubt, correlation with the clinical findings, in particular the presence of a mass, will usually be confirmatory. During the period in which these patients were seen, we did not perform barium enema studies to distinguish feces from worms but reserved this examination for cases where the other features are insufficient to exclude intussusception. In the unobstructed child, radiologic detection due to the presence of gas in the worm lumen may be related to the feeding pattern of the worms. The time interval since the last meal, in addition to the size and number of the worms may determine the likelihood of radiologic demonstration. When stressed by removal from the host, worms immediately expelled the gas.

6 42 ELLMAN ET AL. AJR:135, July 1980 Worms may cause malabsorption amounting to a loss of 7%-9% of the daily caloric intake [3]. This may be critical in the undernourished child and be at least partly responsible for some of the diseases from which these children suffer. Identification and treatment of the parasite is therefore of considerable value. Because of the large number of ova laid by each female worm, stool examination, especially if repeated, is normally diagnostic and is used for screening. Only when the infestation is small, when the worms are all male, or when the worms have not yet matured will the stools be free of ova [6]. Since plain radiographs have an accuracy of only 70%, they should not be used as a screening method for worms. However, abdominal films are frequently part of the diagnostic workup of patients with abdominal symptoms. The identification of worms can be of value in suggesting an underlying cause of the symptoms and in detecting asymptomatic cases. ACKNOWLEDGMENTS We thank J. E. Williams, Department of Radiology, University of Queensland, for assistance with laboratory work and photography; Hiram Baddely for advice and criticism; Dianna Hallford for manuscript preparation; and Nancy Schreiber for photography. REFERENCES 1. World Health Organization Expert Committee Report. Control of ascariasis. WHO Technical Report series 378. Geneva: World Health Organization, Warren KS. Helminthic disease endemic in the United States. Am J Trop Med Hyg 1974;23: , Blumenthal OS, Schultz MG. Effects of ascaris infection on nutritional status in children. Am J Trop Med Hyg 1976;25: Sivakamar B, Reddy V. Absorption of vitamin A in children with ascariasis. J Trop Med Hyg 1975;78: Mahalanabis 0, Jalan KN, Maitra TK, Agarwal 5K. Vitamin A absorption in ascariasis. Am J Clin Nutr 1976;29 : Pawlowski ZS. Ascariasis. C!in Gastroenterol 1978;7: Piggott J, Hansbarger EA Jr, Neafie RC. Human ascariasis. Am J C/in Patho! 1970;53: Makidono J. Observations on ascaris during fluoroscopy. Am J Trop Med Hyg 1956;5: Moseley JE, Rabinowitz JG. The small bowel in infants and children. In: Marshak RH, Lindner AE, eds. Radiology of the small intestine. Philadelphia: Saunders, 1970: Middlemiss JH. Gastrointestinal parasites. In: Margulis AR, Burhenne HJ, eds. Alimentary tract roentgeno!ogy. St. Louis: Mosby, 1973: Astley R. Radiology of the gastro-intestinal tract. In: Anderson CM, Burke V, eds. Paediatric gastro-entero/ogy. London: Blackwell Scientific, 1975: lsaacs I. Roentgenographic demonstration of intestinal ascariasis in children without using barium. AJR 1956;96: Atken DW, Dickman FN. Surgery in obstruction of small intestine due to ascariasis. JAMA 1957;1 64: Okumura M, Nakashima Y, Curti P, De Paula W. Acute intestinal obstruction by ascaris: analysis of 455 cases. Rev Inst Med Trop Sao Paulo 1974;16: Louw JH. Abdominal complications of ascaris lumbricoides infestation in children. Br J Surg 1966;53 : Samuel E, Laws JW. The small bowel. In: Sutton 0, ed. Textbook ofradiology, 2d ed. London: Livingstone, 1975: Bean WJ: Recognition of ascariasis by routine chest or abdomen roentgenograms. AJR 1965;94 :