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Heath, Harley W. M.D.; Marshall, Susan G. M.D.

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The Pediatric Infectious Disease Journal: December 1997 - Volume 16 - Issue 12 - p 1182-1185
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Paragonimiasis, an often chronic parasitic infection caused by lung flukes of the trematode genus Paragonimus, has been increasingly recognized in the United States during the past 15 years in immigrants from endemic areas such as Southeast Asia. We describe a pediatric case with a unique presentation and briefly review the spectrum of this disease.

Case report. An 11 1/2-year-old Hmong Laotian boy was brought into the emergency room by his parents with a 2- to 3-month history of decreasing stamina and increasing dyspnea on exertion. He described an intermittent nonproductive cough and decreased appetite and was thought to have lost weight. He denied fever, chills, night sweats, headache, palpitations, hemoptysis, chest pain, vomiting, diarrhea or urticaria. There were no pets at home. At the time of immigration to the United States 16 months earlier, all family members had negative purified protein derivative intradermal tests except one brother, who was positive but had a normal chest radiograph and subsequently received isoniazid for 12 months.

Physical examination of the patient revealed a somewhat cachectic but non-toxic-appearing male in minimal respiratory distress. Height was 143 cm and weight was 26.5 kg, corresponding to the 40th and ≪5th percentiles, respectively. He was afebrile with a pulse of 106/min, respiratory rate of 24/min and blood pressure of 110/75 mm Hg. Findings included mild intercostal retractions, absent breath sounds on the left, a cardiac point of maximal impulse just lateral to the sternum in the right 4th intercostal space and 1+ digital clubbing. There was no adenopathy or hepatosplenomegaly.

By pulse oximetry the hemoglobin oxygen saturation in room air was 98%. A chest radiograph revealed complete opacification of the left hemithorax with a rightward mediastinal shift and compression of the left main stem bronchus. A complete blood count showed 14 500 white blood cells/mm3 (56% neutrophils, 1% band forms, 38% lymphocytes, 2% monocytes and 2% eosinophils), hematocrit 46%, and 422 000 platelets/mm3. A Westergren erythrocyte sedimentation rate was 16 mm/h, and serum electrolytes were normal except for a bicarbonate of 29 meq/l. Ultrasound examination of the chest showed a massive left pleural effusion laden with mobile, dependent, echogenic debris. Thoracentesis yielded 100 ml of straw-colored fluid containing 930 red blood cells/mm3 and 11 700 white blood cells/mm3, with a differential of 94% eosinophils, 4% monocytes and 2% neutrophils. Pleural fluid lactic dehydrogenase (LDH) was 14 500 IU/l, total protein 8.4 g/dl and glucose <20 mg/dl. Computed tomography of the head was normal. Three stool specimens were negative for parasites, and a purified protein derivative intradermal test was nonreactive with a positive Candida control.

Because debris in the pleural fluid prevented further therapeutic thoracentesis, a left lateral thoracotomy was performed during which 1800 ml of an odorless, cloudy, pea soup-like fluid containing a pale yellow, cottage cheese-like, proteinaceous material was removed, along with a solitary, 6-mm-long, reddish brown fluke subsequently identified as Paragonimus westermani(Fig. 1). The left lung was atelectatic and encased in a thin, transparent peel which was easily removed, allowing full reexpansion of a normal appearing lung. Microscopic analysis of the fluid showed abundant Charcot-Leyden crystals and occasional small, irregularly shaped nodules of dystrophic calcification; no ova were identified and cultures for bacteria, fungi and acid-fast bacilli were negative.

FIG. 1:
Gross appearance of the single Paragonimus westermani fluke discovered at surgery (scale is in centimeters). Adult flukes are typically reddish brown and ovoid, measuring 7 to 16 mm by 4 to 8 mm, similar in size and appearance to a coffee bean.

The hospital course was complicated only by transient air leak requiring chest tube replacement, and the child received a 3-day course of praziquantel and was discharged on Postoperative Day 9 with a normal chest examination and radiograph. On further questioning the parents acknowledged that partially cooked crayfish had been part of the family's diet while they stayed in a refugee camp in Thailand en route to the United States.

The patient was subsequently lost to our follow-up but was seen a year later at the same hospital for an unrelated orthopedic problem and was described to be in excellent health and actively participating in soccer.

Discussion.P. westermani is endemic to Southeast Asia, China, Japan and India. Other species of Paragonimus are common in parts of Asia, Africa and South and Central America. Although some species inhabit North America, locally acquired disease is extremely rare.1 The parasite's life cycle consists of: (1) egg deposition in water; (2) hatching within 3 weeks into free-swimming miracidia; (3) penetration into snails (first intermediate host); (4) maturation into cercariae in 3 to 5 months; (5) penetration into crustaceans such as crabs and crayfish (second intermediate host); (6) encystment and development into metacercariae within 2 months; (7) infection of humans or other mammals (definitive hosts) via consumption of raw or undercooked crustaceans; (8) excystment of metacercariae in the small intestine followed within 1 week by penetration through the intestinal wall into the peritoneal cavity and development into young flukes; (9) migration, usually through the diaphragm and pleural cavity into the lung; and (10) maturation during the ensuing 5 to 6 weeks into the adult worm, which can discharge as many as 300 000 ova in 1 day.2, 3 The adult fluke usually becomes encapsulated in an abscess cavity from which ova intermittently rupture into small bronchioles. The ova are then expectorated or swallowed and passed via feces into the environment, completing the life cycle.

Human disease generally occurs after consumption of raw or undercooked crabs or crayfish. Salted, pickled and wine-soaked crustaceans retain their infectivity. The metacercariae remain viable in warm water for up to 5 days, in cold water for up to 20 days and in dead, refrigerated crabs for up to 1 month; they are killed by desiccation, deep freezing and heating at 55°C for 20 min.2 Encysted metacercariae can adhere to utensils, surfaces and human hands during meal preparation and can thus cause disease despite adequate cooking of the meal itself.2 Paragonimiasis has also been reported in Japan in association with consumption of raw boar4 and in Korea in association with administration of raw crab juice as a traditional remedy for various illnesses.2

Human infection with Paragonimus may cause acute or chronic symptoms, and manifestations may be either pulmonary or extrapulmonary.5 The acute stage corresponds to the period of invasion and migration of flukes and consists of abdominal pain, diarrhea and urticaria, followed roughly 1 to 2 weeks later by fever, pleuritic chest pain, cough and/or dyspnea. Chronic pulmonary paragonimiasis, the most common clinical pattern, is frequently mild, with chronic cough, brown-tinged sputum (the color being caused by expectorated clusters of reddish brown eggs rather than by blood) and true hemoptysis. In contrast to tuberculosis, pulmonary paragonimiasis is only rarely accompanied by rales or other adventitious breath sounds. Many patients are asymptomatic, and symptomatic patients frequently look well despite a prolonged course. The incubation period ranges from 2 to 20 days, in the case of acute symptoms, to 6 months to several years, in the case of chronic pulmonary or pleural disease.

Extrapulmonary manifestations result from variations in migration and localization of flukes. Common sites include the central nervous system, abdomen and skin, although involvement of virtually every organ has been described.6 Younger children may be more susceptible to extrapulmonary infection; in fact the majority of cerebral paragonimiasis occurs in children <10 years old.7 Fatalities are rare and have been limited to patients with central nervous system involvement.

As in our patient flukes occasionally invade and reside in the pleural space without parenchymal lung involvement.6, 8, 9 In pleural paragonimiasis symptoms may be minimal and diagnosis difficult, because ova are not expectorated or swallowed and there is frequently no cough. Such patients may develop pleural effusions and, because of the coendemicity with Mycobacterium tuberculosis (and coinfection in some patients), such effusions are often misdiagnosed as tuberculous.10, 11

Radiographic features typical of pulmonary paragonimiasis include hazy or nodular opacities, linear streaks, cystic ring shadows, pleural thickening and calcifications.3, 12-14 Pleural thickening or effusion as the sole finding is rarely described. This is perhaps an underestimate, given that most series include only sputum-positive patients. In one study in which a serum complement-fixation test was used for diagnosis, 5 of 25 patients had pleural effusions alone.10 In contrast to tuberculosis, pulmonary paragonimiasis is unlikely to involve the apices or hilar lymph nodes, most commonly involves the lower lung segments and periphery and frequently causes pleural thickening.6

Laboratory results typically show a normal leukocyte count with normal to marked peripheral eosinophilia. In patients with isolated or concomitant pleural space disease, pleural fluid is typically an opaque exudate with virtually all reported effusions showing a glucose <20 g/dl, a protein <6 g/dl, an elevated LDH (typically 1000 to 3000 IU/l) and a leukocyte count <2000/mm3 with mild to moderate eosinophilia.10, 11 As in our case analysis of pleural fluid may facilitate distinction between pleural paragonimiasis and tuberculosis. Unlike those in paragonimiasis tuberculous effusions typically show glucose >50 mg/dl, LDH <1000 IU/l, protein <6 mg/dl and little or no eosinophilia.11 Although definitive diagnosis of paragonimiasis requires observation of ova or flukes in sputum, stool, pleural fluid or pathologic specimens, a serum immunoblot assay with a sensitivity of 96% is available through the Centers for Disease Control and Prevention.

The magnitude of the increases in cellularity, degree of eosinophilia and LDH in pleural fluid in our patient are much higher than those reported previously and are unusual in that they were precipitated, in all likelihood, by a single adult fluke. A 7-year-old boy with parenchymal pulmonary paragonimiasis was recently reported with extraordinarily high peripheral eosinophilia (absolute eosinophil count 84 000/mm3), the kinetics of which paralleled those of serum interleukin 5 values posttreatment.15 Of the various eosinophilogenic cytokines, interleukin 5 has proven the most likely candidate for mediation of parasite-induced eosinophilia15 and, although not measured in our patient, may have played a role in promoting the high degree of pleural fluid eosinophilia.

Praziquantel (75 mg/kg/day orally divided into three doses/day for 2 days) emerged as the treatment of choice more than a decade ago and, with a cure rate of >90%, remains the most effective therapy.16, 17 When chronic empyema is present (as in our case), surgical decortication (with thoracoplasty if decortication alone does not permit lung reexpansion) is indicated, yielding generally good results.18

Acknowledgment. We are indebted to Robert T. Schaller Jr., M.D. for his surgical skill and expertise and for sharing the photo included in this article.

Harley W. Heath, M.D.

Susan G. Marshall, M.D.

Department of Pediatrics (HWH) and Division of Pediatric Pulmonary Medicine (SGM); University of Washington; Children's Hospital and Medical Center

Group Health Cooperative of Puget Sound (HWH)

Seattle, WA

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Paragonimus; paragonimiasis; pleural effusion; tuberculosis; parasitic disease; eosinophilia

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