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Gastric Ascariasis

By : Prof M S Khuroo         Dated : 02/18/2016

TITLE: GASTRIC ASCARIASIS PRESENTING AS UNIQUE DYSPEPTIC SYMPTOMS IN AN ENDEMIC AREA Short title: Gastric Ascariasis: Case series Authors: 1. Naira Sultan Khuroo, MD, Consultant Radiologist, Digestive Diseases Centre, Dr. Khuroo’s Medical Clinic, Srinagar, Kashmir, India. 2. Mehnaaz Sultan Khuroo, MD, Senior Resident, Department of Pathology, Sher-e-Kashmir Institute of Medical Sciences, Srinagar, Kashmir, India. 3. Mohammad Sultan Khuroo, MD, Director, Digestive Diseases Centre, Dr. Khuroo’s Medical Clinic, Srinagar, Kashmir, India. Address for Correspondence: Prof. Mohammad Sultan Khuroo, Director, Digestive Diseases Centre, Dr. Khuroo’s Medical Clinic, Sector 1 Sher-e-Kashmir Colony, Qamarwari, Srinagar, Kashmir, India, 190010 E-mail: Khuroo@yahoo.com website: www.drkhuroo.org Phone: 00-91-194-2490442 ABSTRACT Background Ascariasis infects more than 1.4 billion people throughout the world. However, gastric ascariasis has been rarely reported in the literature. Objectives Report clinical, gastroscopic and gastric ultrasound findings in a large cohort of patients with gastric ascariasis in an endemic area. Design Case series Setting Tertiary gastroenterology centre. Patients During the period from June 2007 to November 2009, we performed 1522 upper gastrointestinal endoscopies. Twenty-two (1.4 %) patients had diagnosis of gastric ascariasis and formed the study group. Interventions & Main Outcome Measurements Gastroscopies, gastric ultrasound, gastric biopsies, worm extraction from stomach. Results Study group included 8 males and 14 females. All patients were adults with mean ± 1SD age of 43.5± 10.4 years (age range 32 to 60 years). Three patients had associated organic diseases. Of the remaining 19 patients, 5 presented with gastric outlet obstruction caused by worms in antrum blocking the pylorus; 11 patients had intense nocturnal esophageal irritation due to migration of worms from fundus of stomach to esophagus during night in search of food; and 3 other patients had nocturnal chocking due to similar worm migration from stomach to larynx. Gastric ultrasound showed actively motile echogenic strips with central anechoic tubes (Ascarides). Extraction of worms at endoscopy and anthelmintic therapy caused rapid resolution of symptoms pointing to their causation by offending parasites. Limitations Similar studies in other endemic areas are lacking. Conclusions Gastric ascariasis should be considered while evaluating dyspeptic symptoms in patients residing in or belonging to endemic areas. Abbreviations used in this article: EGD=Esophago-gastro-duodenoscopy Key words: Ascariasis, Ascaris lumbricoides, Gastroscopies, Dyspepsia, Pyloric obstruction, Ultrasound. Ascariasis has a global distribution. It has been estimated that more than 1.4 billion throughout the world are infected with Ascaris lumbricoides. The majority of infections occur in Asia, with advanced countries having the lowest rates of infection. Ascariasis is highly endemic in China and Southeast Asia, with prevalence rates of 41% to 92%. In the Indian subcontinent, ascariasis is highly endemic in Kashmir (70%), Bangladesh (82%), and Central and Southwest India (20% to 49%). In Africa, the overall prevalence of the infection varies from 15% to 27%. The prevalence is high in Latin America and has not changed over the years. In Europe, the prevalence is low in large cities but may be high in rural areas and can reach up to 52% in some rural areas. In the United States, ascariasis is the third most common helminth infection (exceeded only by hookworm and Trichuris trichiura infections). Of the 4 million people infected in the United States, large percentages are immigrants from developing countries with infection rates of 20% to 60% (1-4) Ascaris lumbricoides is a soil-transmitted helminth and requires moist, shady soil for embryonation of the eggs. The infection occurs by ingestion of the embryonated eggs. The larvae released in the duodenum undergo a pulmonary migration phase. The normal habitat for the adult worm is the jejunum. The adult worm, Ascaris lumbricoides, is a large, pink, elongated, cylindrical organism, which tapers at both ends. The female worms are 20 to 40 cm long and 3 to 6 mm in diameter; the male worms are 15 to 30 cm long and 2 to 4 mm in diameter. The adult worm maintains itself in the lumen of the gut by virtue of its muscular activity. The alimentary canal of the worm is a tubular longitudinal structure, consisting of mouth, pharyngeal cavity, esophagus, midgut, rectum, and cloacae. Mouth of the worm has three lips and arranged like the three leaves of a clover. The average life span of the adult worm is 6 to 18 months. The female releases million of eggs into the fecal stream; the daily output is estimated to be 240,000 per worm (4). Although ascariasis is a ubiquitous infection, most ascaris infections are without clinical disease. Clinical disease is mostly restricted to subjects with heavy worm load. The larvae, while passing through the pulmonary migration phase for maturation, cause ascaris pneumonia (5-8). Intestinal ascaris is usually detected as an incidental finding. Ascaris-induced intestinal obstruction is a frequent complication in children with heavy worm loads. It can be complicated by intussusception, perforation, and gangrene of the bowel. Acute appendicitis and appendicular perforation can occur as a result of worms entering the appendix (1,9-11). Hepatobiliary and pancreatic ascariasis is a frequent cause of biliary and pancreatic disease in endemic areas (12). It occurs in adult women and can cause biliary colic, acute cholecystitis, acute cholangitis, acute pancreatitis, and hepatic abscess (13,14). Adult worms show intense motor activity in the intestinal lumen and can often move in to duodenum and stomach (10, 12). However, there are only isolated case reports of gastric ascariasis in the literature (15-25). We believe that magnitude of gastric ascariasis in an endemic area may be under-estimated in the reported cases. With this in mind we report on a large case series to focus on the magnitude the magnitude of gastric ascariasis in an endemic area and define the clinical profile, imaging and natural course of this entity. MATERIALS AND METHODS During the period from June 2007 to November 2009, we performed 1522 upper gastrointestinal endoscopies. Endoscopies were performed by an experienced endoscopist (MSK) with video-esophago-gastro-duodenoscope (Olympus Evis Smartage Gastro GIF V70 Serial, Olympus Japan). Procedures were video-recorded and representative findings documented on high resolution images using software program. All patients had been referred to the endoscopy laboratory from the Digestive Diseases Centre, Dr. Khuroo’s Medical Clinic for evaluation of upper gastrointestinal symptoms. During the endoscopic procedure adult Ascaris worm/s were visualized in the stomach in 22 (1.4 percent) patients. Patients with worms in the stomach were studied prospectively and constitute the study group. Patient’s clinical symptoms with disease duration were recorded on a proforma. Routine hemogram, liver function tests, serum amylase determinations were carried by standard methods. Stool examination was done for parasites and for occult blood. Abdominal ultrasound examinations were done with Logic Book XP ultrasound machine (Wipro/GE Medical Systems). We carefully looked for Ascarides in the hepato-biliary ducts and pancreatic ducts. Ultrasound appearances of worms in the biliary tract and pancreas have been well studied by us and were used to visualize worms in the ducts (26, 27). Gastric ultrasound was done with water filled stomach and appearances of worms in the stomach carefully observed and recorded. Findings at endoscopic procedure were recorded which included number and placement of adult Ascarides and mucosal appearances. Worms were watched at endoscopic examination for 5 to 10 minutes to understand their mobility. Gastric forceps punch biopsies were taken from mucosal lesions and evaluated for histological findings by standard methods. Worms seen at endoscopy were extracted from stomach and all patients received anthelmintic therapy. Patients were followed up and symptoms evaluated in the follow up. This study was approved by the ethical committee Dr. Khuroo’s Medical Clinic and all patients gave a written informed consent to the study. RESULTS Esophago-Gastro-Duodenoscopy (EGD) showed worms in the stomach in 22 patients (Study group). Twelve patients had a single worm in the stomach (fundus and body-3 patients and antrum- 9 patients ); 3 patients had 2 worms (esophagus and stomach-1 patient, antrum-1 patient and stomach and duodenum-1 patient); 3 patients had 3 to 5 worms in antrum and duodenum and 4 patients had numerous (massive infection) worms in the antro-duodenal region. Worms were alive in all patients and were actively motile. Worms in the antrum and in the duodenal bulb made rapid transition from one to another region across the pylorus. Worms had completely blocked the pylorus in 2 patients and tightly closed pylorus had constricted the body of the Ascarides (Fig 1; video 1). Pylorus in these 2 patients showed erythema, erosion and ulceration. In another 3 patients massive Ascaride aggregated mass had blocked pyloro-duodenal region (video 2). Worms in the fundus and body made rapid movements and curved up themselves on itself to make loops. Three patients had associated diseases as detected on EGD (Cirrhosis with esophageal varices and hypertensive gastropathy-1; Gastric carcinoma-1 and nodular lymphoid hyperplasia-1). In remaining 19 patients symptoms were primarily related to gastric ascariasis (Primary gastric ascariasis). Mucosa of stomach in 5 patients and duodenal bulb in 4 patients showed multiple hemorrhagic erosions placed at the site the worm mouth of Ascarides were placed. These were localized lesions presumably caused by injury at the site the mouth of Ascaride was biting/holding the mucosa. Study group included 8 males and 14 females. All patients were adults with mean ± 1SD age of 43.5± 10.4 years (age range 32 to 60 years). Symptom duration of 19 patients with primary gastric ascariasis varied from 2 weeks to 6 years and symptoms were broadly divided in to 3 groups. Five patients presented with features of gastric outlet obstruction. These patients had delayed digestion, halitosis, food staying in stomach for hours, vomiting, weight loss and distended stomach with gastric splash. . Clinical examination of malignancy stomach was entertained. EGD showed food residue in stomach in all 5 patients. Cause of gastric stasis was due to a single worm in the antrum blocking the tightly closed pylorus in 2 patients (Fig 1; video 1) and aggregated bunch of motile worms blocking the pyloro-duodenal area in 3 patients (video 2). Eleven patients had retro-sternal irritation and heartburn superficially resembling features of gastro-esophageal reflux disease. However, on close enquiry these patients described intense irritation and a strong feeling of something moving in the lower chest especially during sleep. All these patients had actively motile worms placed in the fundus of the stomach and symptoms were possibly caused by movement of the worms in to esophagus in search of food especially at night. Remaining 3 patients had repeated episodes of chocking during night. These patients woke up during sleep with intense cough and chocking. EGD showed worms in esophagus and fundus in one patient (Fig 2) and fundus of stomach in 2 patients. None of the patients presented with manifest gastrointestinal bleeding. All patients remembered to have vomited worms during the illness. Stool analysis showed ova of Ascaris lumbricoides in all patients. None had any other gut parasite on stool analysis. Hemogram showed moderate iron deficiency anemia in 3 patients with primary gastric ascariasis, however, stool occult blood was negative in all these cases. Liver function tests and serum amylase were within normal limits and hepatobiliary ultrasound did not show worms in the bile/hepatic ducts or pancreatic duct in any of the cases. Gastric ultrasound showed actively motile Ascarides in the stomach (video 3). Ascarides were recognized by characteristic long echogenic strips with central anechoic tubes (representing alimentary canal of the worm) and snake like mobility. Gastric biopsies in all patients with primary gastric ascariasis were unremarkable. Even biopsies from Ascaris induced erosion did not reveal any significant abnormality. None of the biopsies revealed eosinophliic gastritis or eosinophliic granulomas. All worms visualized during EGD were extracted out through mouth. The worm body was tightly gripped by forceps and endoscope withdrawn with forceps holding the worm (see video 1). This meant repeated endoscopic insertion in those with multiple worms. All patients received mebendazole therapy 100 mg twice per day for 3 days. Patients were advised to take regular anthelmintic therapy in the follow up. All patients were followed up. Mean follow up extended from 1 to 30 months (mean±1SD 16.6± 6.4 months). Following worm extraction and anthelmintic medication patients had rapid relief of symptoms and stayed free of symptoms in the follow up. Most striking was disappearance of chocking in 3 patients. All patients with Ascaris-induced gastric outlet obstruction had rapid resolution of gastric stasis. Patients with GERD-like symptoms showed significant resolution of symptoms. DISCUSSION The present case series analyzed the magnitude of gastric ascariasis and its clinical spectrum in an endemic area. We found that over 1.4 percent of patients referred for upper gastrointestinal endoscopies had worms in the stomach. These data point to the fact that gastric ascariasis should be a common entity in regions of the World where this infection is endemic. This is not unexpected as worms inhabit jejunum and show active motility and should be reaching duodenum and stomach very often. However, there are only isolated cases of this entity reported in the literature. This points to the fact that impact of disease caused by ascariasis has been grossly underestimated. Similar prospective studies from centers from endemic regions shall clarify the impact of ascaris infection in causing dyspeptic symptoms. Ascariasis is rare in many parts of Europe and the United States and this entity shall be rarely encountered in natives of these countries. However, increased movement and migration of Afro-Asians to such countries make it necessary for clinicians in these countries to be aware of this entity (1-4). Gastric ascariasis presented with unique symptoms in our patients. Pyloric obstruction was caused by tightly blockade of pyloric opening by a single worm in 2 cases. Pylorus in these patients was tightly closed and constricted body of the Ascaride. In remaining 3 patients massive Ascaride aggregated masses blocked pyloro-duodenal junction. Gastric ascariasis has been reported to cause chronic intermittent gastric outlet obstruction in several case reports (28-30). Choudhuri et al reported 3 such cases and Ascarides were demonstrated in the stomach by radiology in two patients and at endoscopy in one patient. Majority of our patients presented with esophageal symptoms superficially resembling gastro-esophageal reflux. However intense retro-sternal irritation at night pointed to wandering behavior of the worms to esophagus in search of food during night. Choking at night was extension of the worm behavior to invade laryngeal opening and was unique. There are no published reports of such symptoms caused by gastric ascariasis in the literature, although ascariasis has been considered in differential diagnosis of peptic ulcer disease (31). Majority of the case reports in the literature on gastric ascariasis are surprise and shocking incidental visualization of worms in the stomach and are reported as such (15,16,18,19,21,24,33,34). However, there are several reports in which worms in stomach have been reported to cause esophageal or gastric bleeding (17, 20, 23, 25, 32). None of our patients had manifested gastro-intestinal bleeding. We visualized hemorrhagic lesions caused by mouth of the worm holding/biting gastric mucosa and these lesions may be the cause of gastrointestinal bleeding in such cases. Ultrasound was very useful in diagnosis of gastric ascariasis (35). We have reported on diagnosis of worms by ultrasound in biliary tree and pancreas (26). However, diagnosis of worms in ducts needs considerable experience as the worms show only slow mobility or are motion less and difficult to pick up by those not experienced in ultrasound. In contrast, Ascarides in gall bladder though a rare entity are easy to diagnose in view of the snake like motility (27). Gastric ascariasis can be easily picked up by ultrasound examination of water filled stomach as worms show active snake like motility. We believe gastric ultrasound is ideal to do population based studies to define its actual magnitude in endemic areas. Management of gastric ascariasis is based on 2 simple principles, one to extract the offending worms and second to institute effective anthelmintic therapy so that worms downstream in jejunum do not travel upstream. All our patients had effective relief of symptoms and pointed to cause of symptoms by the parasite. As re-infections are common in endemic areas we recommend regular anthelmintic treatment to avoid symptom recurrences. Dyspepsia is a common symptom in the community. As a significant percentage of dyspeptic patients were caused by gastric ascariasis, this entity should be considered as a differential diagnosis of dyspepsia. There are few indicators when this entity should be kept high in the list. First pointer is if the patient had history of vomiting worms any time during the symptoms duration. Second pointer to be considered is if the symptoms have unusual and unique character as reported in this study. Gastric ultrasound done on water filled stomach should be the investigation of choice and EGD employed for therapeutic purposes to extract the worms. REFERENCES 1. Crompton DWT: The prevalence of ascariasis. Parasitol Today 1988; 4:162. 2. Botero D: Epidemiology and public health importance of intestinal nematode infections in Latin America. Prog Drug Res 1975; 19:28. 3. Bundy DAP: Immunoepidemiology of intestinal helminthic infections: The global burden of intestinal nematode disease. Trans R Soc Trop Med Hyg 1994; 88:259. 4. 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