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Parasites of the Air PassagesParasites of the Air Passages FREE TO VIEW

Danai Khemasuwan, MD, MBA; Carol F. Farver, MD; Atul C. Mehta, MD, FCCP
Author and Funding Information

From Pulmonary, Allergy and Critical Care Medicine (Drs Khemasuwan and Mehta), Respiratory Institute, and the Department of Anatomical Pathology (Dr Farver), Cleveland Clinic Foundation, Cleveland OH.

Correspondence to: Atul C. Mehta, MD, FCCP, Pulmonary, Allergy and Critical Care Medicine, Respiratory Institute, Cleveland Clinic Foundation, 9500 Euclid Ave, A-90, Cleveland, OH 44195; e-mail: Mehtaa1@ccf.org


Reproduction of this article is prohibited without written permission from the American College of Chest Physicians. See online for more details.


Chest. 2014;145(4):883-895. doi:10.1378/chest.13-2072
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Parasitic infestations affect millions of the world’s population. Global immigration and climate change have led to changes in the natural distribution of parasitic diseases far removed from endemic areas. A broad spectrum of helminthic and protozoal parasitic diseases frequently affects the respiratory system. The wide varieties of clinical and radiographic presentations of parasitic diseases make the diagnosis of this entity challenging. Pulmonologists need to become familiar with the epidemiology, clinical presentation, pathophysiologic characteristics, and bronchoscopic findings to provide proper management in a timely fashion. This review provides a comprehensive view of both helminthic and protozoal parasitic diseases that affect the respiratory system, especially the airways.

Figures in this Article

Helminthic and protozoal infestations cause significant morbidity and mortality worldwide. A decline in parasitic infestations has been observed in the past decade as a result of improved socioeconomic conditions and better hygiene practices. However, the rapid urbanization of cities around the world, global warming, international traveling, and increasing numbers of immunocompromised individuals have increased the vulnerability of the world population to parasitic diseases.1 The diagnosis of parasitic diseases of the respiratory system is challenging because the clinical manifestations and radiologic findings are nonspecific. Thus, a high index of suspicion and detailed interrogation regarding travel history are critical. Most parasitic infestations of the respiratory system either involve the airways or require bronchoscopy for diagnosis. Helminthes can affect the airways during both the larval and the mature adult phases of their life cycle. The larvae can cause airway inflammation (paragonimiasis), whereas migration of the mature adult worms may cause mechanical obstruction of the airways (ascariasis). This article provides a comprehensive review of both helminthic and protozoal infestations, including clinical, radiographic, bronchoscopic, and pathologic manifestations, that may be helpful to pulmonologists in managing this important entity (Table 1).

Table Graphic Jump Location
Table 1 —Parasitic Infection of Respiratory System

N/A = not available.

Nematodes, also known as roundworms, have a symmetrical, tube-like body with an anterior mouth and a longitudinal digestive tract.

Ascariasis

Ascaris lumbricoides is one of the most common parasitic infestations, affecting > 1 billion of the world’s population and causing > 1,000 deaths annually.1A lumbricoides is transmitted via the feco-oral route. An Ascaris larva migrates to the lungs through either the lymphatics or the venules of the portal system. Larval ascariasis causes Löffler’s syndrome, a concomitance of wheezing, pulmonary infiltrations, and eosinophilia.2 It can cause alveolar inflammation, necrosis, and hemorrhage. Diagnosis of an ascariasis infestation during its larval phase is difficult. The sputum may show numerous eosinophils; stool examination, however, remains negative for eggs during the larval stage.3 The diagnosis requires a high degree of suspicion. Occasionally, the diagnosis can be confirmed by identifying larvae in the sputum. Solitary pulmonary nodules can also develop if the larva dies causing granulomatous inflammation.4 Adult ascaris has been reported to cause airways obstruction in a child, producing a complete lobar collapse.5 Mebendazole and albendazole are the most effective agents against ascariasis.

Ancylostomiasis (Hookworm Disease)

The most common hookworms are Ancylostoma duodenale and Necator americanus. The latter is found in parts of the southern United States. Hookworm larvae enter human hosts via the skin, producing itching and local infection. The larvae are also infective via the oral route.6 Hookworm infestations involve larval migration through the lungs via the bloodstream, resulting in a hypersensitivity reaction. Patients usually present with transient eosinophilic pneumonia (Löffler’s syndrome).6 If the patient ingests a large number of larvae, he/she may develop a condition known as “Wakana disease,” characterized by nausea, vomiting, dyspnea, and eosinophilia. This clinical picture represents a severe hypersensitivity-like reaction to A duodenale.6 Larval migration may also cause alveolar hemorrhage.7 Similar to ascariasis, the diagnosis of a hookworm infestation during the larvae phase could be difficult to make. CT scanning of the chest may reveal transient, migratory, patchy alveolar infiltrates.8 Sputum examination may reveal occult blood, eosinophils and, rarely, migrating larvae (Fig 1A).9 Bronchoscopic examination may reveal airway erythema and high eosinophil counts in BAL fluid (BALF).10 Patients can become profoundly anemic and malnourished. These manifestations may provide clinical clues to support the diagnosis. The antiparasitic agents for hookworm are mebendazole and albendazole.

Figure Jump LinkFigure 1. A, Hookworm larva in the sputum sample (wet smear, original magnification × 88). Morphologically, hookworm larvae have long buccal cavities, whereas Strongyloides larvae have short buccal cavities. (Reprinted with permission from Beigel et al.9) B, Bloody aliquot from BAL sample and Strongyloides larvae from BAL (hematoxylin and eosin [H&E], original magnification × 200). Note: short buccal cavity distinguishes Strongyloides from the hookworm (inset) (H&E, original magnification × 400). C, Strongyloides larvae (arrow) present in alveolar space in lung with diffuse alveolar damage (H&E, original magnification × 400). D, Bronchoscopic findings in anterior basal segment of right lower lobe. The syngamosis male is smaller and attached to the copulatory bursa of the female body (arrow). The parasite can be seen in bronchoscopy because they reside in the bronchial mucosa. (Reprinted with permission from Kim et al.19) E, Cross-sections of coiled Dirofilaria worms within involved artery causing surrounding infarction of lung tissue. Note the smooth cuticle at the external layer (Movat stain, original magnification × 200). F, Schistosomal ova in the lung biopsy specimen. The arrow points to ova within the granulomatous reaction (H&E, original magnification × 100).Grahic Jump Location
Strongyloidiasis

Strongyloides stercoralis is a common roundworm that is endemic throughout the tropics but is found worldwide in all climates. Infective filariform larvae can penetrate the skin and infect human hosts. The larvae migrate through the soft tissues and enter the lungs via the bloodstream. A majority of roundworms migrate up the bronchial tree to the pharynx and are swallowed, entering the GI tract.11 The larvae can reenter the circulatory system, returning to the lungs and causing autoinfection.11 The life cycle of Strongyloides can be completed entirely within one host. The term “hyperinfection syndrome” describes the presentation of sepsis from enteric flora, mostly in immunocompromised patients.12 The hallmarks of hyperinfection are an exacerbation of GI and pulmonary symptoms and the detection of more larvae in the stool and sputum.13 Common pulmonary symptoms include wheezing, hoarseness, dyspnea, and hemoptysis. A chest radiograph usually demonstrates focal or bilateral interstitial infiltrates. Pleural effusions are present in 40% of patients, and lung abscess is found in 15%.14 Diffuse alveolar hemorrhage is usually found in patients with disseminated strongyloidiasis. ARDS may result as a reaction to the death of the organisms. Migration of a massive number of larvae through the intestinal wall can result in sepsis, because larvae may convey gram-negative bacteria into the bloodstream.13

The diagnosis can be confirmed by the presence of larvae in the stool, duodenal aspirate, sputum, pleural fluid, or BALF or lung biopsy specimens (Figs 1B, 1C).15 The sensitivity of a stool examination for ova and larvae is 92% when performed on three consecutive samples.16 An enzyme-linked immunosorbent assay (ELISA) measures IgG responses to the Strongyloides antigen. However, false-negative results can occur during acute infection because it takes 4 to 6 weeks to mount the immune response.17 The ELISA is sensitive but nonspecific because of cross-reactivity with filarial infestations.15 Oral ivermectin remains the treatment of choice for uncomplicated Strongyloides infestation.13,18

Syngamosis

Nematoda of the genus Mammomonogamus affect the respiratory tract of domestic mammals. Occasionally, however, humans can become infested via the respiratory tract. Most cases of human syngamosis are reported from tropical areas, including South America, the Caribbean, and Southeast Asia.19 Two hypotheses have been proposed regarding its life cycle. One is that humans become infested via the ingestion of food or water contaminated with larvae or embryonated eggs. The larvae complete the life cycle in the pulmonary system, and the adult worms migrate to the central airways as the preferred site of infection.20 An alternative hypothesis is that patients are infected by the adult worms present in contaminated food or water. This mode of transmission is supported by its short incubation period (6-11 days).21 The diagnosis requires flexible bronchoscopy unless the worms are expelled through vigorous coughing (Fig 1D). The removal of parasites through bronchoscopy is sufficient to improve symptoms. To date, no studies have supported the effectiveness of antihelminthic therapy.21,22

Dirofilariasis

Dirofilaria immitis is the filarial nematode that primarily infects dogs. Humans are considered accidental hosts because D immitis is unable to mature to an adult form. D immitis is transmitted to humans by mosquitoes harboring infective third-stage larvae. The larva travels to the right ventricle and develops into an immature adult worm. It is then swept into the pulmonary arteries. The worm dies as a result of the inflammatory response and evokes granuloma formation.23 A majority of patients with pulmonary dirofilariasis are asymptomatic. However, some patients (about 5%) may develop cough, hemoptysis, chest pain, fever, dyspnea, and mild eosinophilia.24 A peripheral or a pleural-based solitary pulmonary nodule is a typical presentation. The nodule may show increased fluorodeoxyglucose avidity on a PET scan25,26 and is often confused with malignancy. Calcification occurs within only 10% of these nodules. CT scanning may show a branch of the pulmonary artery entering the nodule.27 Serology has poor specificity because of cross-reactivity with other helminths. The diagnosis is established by identifying the worm in the excised lung tissue (Fig 1E). Needle biopsy and brushings are usually nondiagnostic because of the small sample size. The condition does not require any specific treatment because it is a self-limiting condition.24

Tropical Pulmonary Eosinophilia

Tropical pulmonary eosinophilia (TPE) is a syndrome of immunologic reaction to microfilaria of the lymphatic-dwelling organisms Brugia malayi and Wuchereria bancrofti. It is a mosquito-borne infestation. The larvae reside in the lymphatics and develop into mature adult worms. The microfilariae are released into the circulation and may be trapped in the pulmonary circulation.28 Trapped microfilariae demonstrate a strong immunogenicity and trigger antimicrofilarial antibodies, resulting in asthma-like symptoms. The hallmark of TPE is a high absolute eosinophil count (5,000-80,000/mm3).29 The radiologic features include reticulonodular opacities, predominantly in the middle and the lower lung zones; miliary mottling; and predominant hila with increased vascular markings at the bases.30 Chest CT scanning may demonstrate bronchiectasis, air trapping, calcification, and mediastinal lymphadenopathy.31 Pulmonary functions indicate a restrictive defect with mild airways obstruction.29 BALF may contain numerous eosinophils. Occasionally, microfilaria can be identified on brushings or needle biopsy specimens.32 The chronic phase of TPE may lead to progressive and irreversible pulmonary fibrosis.28

The standard treatment of TPE is diethylcarbamazine (DEC). Patients usually show improvement within 3 weeks. However, a mild form of interstitial lung disease with diffusion impairment may remain.33

Toxocariasis

Toxocara canis and cati are roundworms that affect the dog and cat, respectively. These roundworms are common parasites that cause visceral larva migrans and eosinophilic lung disease in humans. Toxocariasis is transmitted to humans via ingestion of food that is contaminated with parasite eggs. The larvae can migrate throughout the host’s body, including the lungs.34 The pathology of visceral larva migrans is a hypersensitivity response to the migrating larvae. Visceral larva migrans can present with fever, cough, wheezing, seizures, and anemia. Leukocytosis and severe eosinophilia are demonstrated in a peripheral smear. A chest radiograph reveals pulmonary infiltrates with hilar and mediastinal lymphadenopathy. Bilateral pleural effusion can occur.35 Noncavitating pulmonary nodules have also been reported.36 The diagnosis of toxocariasis is established by an ELISA for the larval antigens.37

The treatment of choice is DEC; however, it may exacerbate the inflammatory reaction because of the resulting death of the larvae. It is advisable to combine DEC with corticosteroids.34

Trichinella Infection

Trichinella spiralis is the most common Trichinella species that infects humans. Trichinella is a food-borne disease from undercooked pork containing larval trichinellae. In addition to the pork meat, meat from wild animals such as bear may contain T spiralis.38 The larvae migrate and reside in the GI tract until they develop into an adult form. Fertilized female worms release first-stage larvae into the bloodstream and the lymphatics.39 Pulmonary involvement, although uncommon, produces shortness of breath and pulmonary infiltrates. Dyspnea is caused by parasitic invasion of the diaphragm and the accessory respiratory muscles.39 The diagnosis is confirmed by muscle biopsy, which may demonstrate T spiralis larvae. An ELISA using anti-Trichinella IgG antibodies can confirm the diagnosis in humans.40 A 2-week course of mebendazole, along with analgesics and corticosteroids, is the recommended treatment.39

Trematodes (flatworms) have a flat body with a sucker near the mouth that is used for attachment to the host. Most flatworms are hermaphrodites, except Schistosoma species, which have separate sexes.

Schistosomiasis

Five schistosomes species cause disease in humans: Haematobium, Mansoni, Japonicum, Intercalatum, and Mekongi.7 After malaria, schistosomiasis is the most common cause of mortality among parasitic infections, annually affecting 200 million individuals worldwide.1Schistosoma haematobium resides in the urinary bladder, whereas Schistosoma mansoni and Schistosoma japonicum reside in the mesenteric beds.34 Humans become infested through the skin from contact with fresh water containing Schistosomal cercaria (infective larva). After the cercarias have penetrated the skin, they migrate to the lung and the liver. There are several case reports of a high incidence of acute schistosomiasis (Katayama fever) among travelers with a history of swimming in Lake Malawi and rafting in sub-Saharan Africa.41

In acute schistosomiasis, patients present with dyspnea, wheezing, dry cough, abdominal pain, hepatosplenomegaly, myalgia, and eosinophilia.42 Patients experience shortness of breath because of an immunologic reaction to antigens released by the worms. The level of circulating immune complexes correlates with the symptoms and with the intensity of infection.

In chronic schistosomiasis, embolization of the eggs in the portal system causes periportal fibrosis and portal hypertension. Pulmonary involvement can occur as a result of the systemic migration of parasitic eggs from the portal system. The eggs trigger an inflammatory response that leads to pulmonary arterial hypertension (PAH) and subsequent development of cor pulmonale in 2% to 6% of patients.43 Apoptosis of the endothelial cells in the pulmonary vasculature plays a role in the pathogenesis of schistosomal-associated cor pulmonale.44

Chest radiographs and CT scanning may show a diffuse reticulonodular pattern or ground-glass opacities.45 In the acute phase, BALF may reveal eosinophilia in the absence of parasites. The diagnosis is confirmed by microscopic examination of stool and urine or by rectal biopsy. However, the sensitivity of these tests is low for an early infection. ELISA can be used as a screening test and is confirmed by enzyme-linked immune-electrotransfer blot. These tests become positive within 2 weeks after the infestation. Schistosomal ova can be found in the lung biopsy specimen (Fig 1F).

Acute schistosomiasis is treated with praziquantel. The treatment is repeated within several weeks because it has no antihelminthic effect on the juvenile stages of the parasites.46 Acute pneumonitis, which is believed to be related to lung embolization by adult worms in the pelvic veins, can be observed 2 weeks after the treatment.47 Patients with schistosomal-associated PAH can be treated with PAH-specific therapy along with antiparasitic medications.47

Paragonimiasis

Paragonimus species, including westernmani, cause paragonimiasis that usually involves the lungs. The mode of transmission is ingestion of the metacercaria (infective larvae) from undercooked crustaceans. Undercooked meat of crab-eating mammals (wild boars, rats) can infect humans as an indirect route of transmission.48 The larvae penetrate the intestinal wall and migrate through the diaphragm and the pleura into the bronchioles.49 The eggs are produced by the mature adult worms, which are expelled in the sputum or swallowed and passed with the stool. Typically acute symptoms include fever, chest pain, and chronic cough with hemoptysis.50 Pleural effusion and pneumothorax may be the first manifestation during the migration of the juvenile worms through the pleura. A chest radiograph demonstrates patchy infiltrates, nodular opacities, pleural effusion, and fluid-filled cysts with ring shadows.34 Chest CT scans may reveal a band-like opacity abutting the visceral pleura (worm migration tracks), bronchial wall thickening, and centrilobular nodules. Bronchoscopic examination may reveal airway narrowing from mucosal edema (Fig 2A).51 A lung biopsy specimen may show chronic eosinophilic inflammation (Fig 2B). The diagnosis is confirmed by the presence of eggs or larvae in the sputum sample or BALF (Fig 2C). The pleural fluid, when present, is an acidic exudate with eosinophilia, mostly sterile, without the presence of any organisms.52 Eosinophilia and elevated serum IgE levels are also observed in more than 80% of infected patients.34 Serologic tests with ELISA and a direct fluorescent antibody are highly sensitive and specific for establishing the diagnosis.53 Praziquantel and triclabendazole are the treatments of choice, with a cure rate of 90% and 98.5%, respectively.34

Figure Jump LinkFigure 2. A, Bronchoscopic findings showed mucosal nodularity on the right upper lobe (RUL). (Reprinted with permission from Jeon et al.51) B, Microscopic examination of bronchial tissue obtained from the RUL bronchus showing thickening of the basement membrane and chronic inflammation with eosinophilic infiltration (H&E, original magnification × 200). (Reprinted with permission from Jeon et al.51) Inset: Paragonimus kellicotti egg in a BAL sample. The arrow points to the operculum ridges of the egg (Papanicolaou, original magnification × 400). (Image courtesy by Gary Procop, MD.) C, Granulomas in the pleura in a patient with paragonimiasis. The arrow points to a light brown egg within the granuloma (H&E, original magnification × 100). (Image courtesy by Gary Procop, MD.) D, Protruded hydatid cyst from left lower lobe bronchus. (Image courtesy by Farid Rashidi, MD.) E, Echinococcus cyst fragments in lung biopsy specimen. The arrows highlight the collapsed chitinous layer of a death hydatid cyst (H&E, original magnification × 44). F, Echinococcus cyst fragments in lung biopsy specimen. The fragmented ecchinococus cyst with collapsed chitinous layer resides within the granulomatous reaction (H&E, original magnification × 200). See Figure 1 legend for expansion of other abbreviation.Grahic Jump Location

Cestodes are a subclass of tapeworms; parasites in this group have no digestive system. These parasites live in the digestive tract of mammals. The body is composed of multiple, successive segments (proglottids). Tapeworms are exclusively hermaphrodites with both male and female reproductive systems in their body.

Echinococcosis

Echinococcus granulosus and multilocularis are the parasite species that cause hydatid disease in humans. E granulosus is endemic in sheep-herding areas of the Mediterranean, Eastern Europe, the Middle East, and Australia. An estimated 65 million individuals in these areas are infected.1 Humans become accidental hosts either by direct contact with the primary hosts (usually dogs) or by the ingestion of food contaminated with feces, containing parasite eggs.34 The larvae reach the lymphatics of the intestines and the bloodstream and then migrate to the liver, the main habitat in human hosts.

Two different presentations of echinococcosis are noted: (1) cystic hydatidosis and (2) alveolar echinococcosis. An ecchinococcal infection becomes symptomatic after 5 to 15 years, secondary to local compression or dysfunction of the affected organ. Pulmonary cysts expand at a rate of 1 to 5 cm/y, and calcification is less common.54 Pulmonary symptoms from the intact cyst include cough, fever, dyspnea, and chest pain. The cyst may rupture into a bronchus and cause hemoptysis and/or expectoration of cystic fluid containing parasitic components (hydatoptysis), which is considered a pathognomonic finding of cystic rupture.55 The patients may present with hydropneumothorax or empyema. Occasionally, a ruptured cyst can cause an anaphylactic-like reaction and pneumonia.8 Cystic hydatidosis is diagnosed by chest radiography, which demonstrates a well-defined, homogenous, fluid-filled, round opacity. Ruptured cysts may have characteristic features, including air crescent, pneumocyst, floating membrane (“water lily sign”) (Fig 3), or completely empty cavity images.56 A “meniscus” or “crescent” sign or Cumbo’s sign (onion peel) have also been described. Thoracic ultrasonography may be useful to confirm the cystic structure, demonstrating the characteristic double-contour (pericyst and parasitic membrane endocyst) of intact cysts. However, daughter cysts are also observed occasionally in pulmonary hydatidosis.56 Bronchoscopic examination reveals sac-like cysts in the airway (Fig 2D). A surgical lung biopsy may reveal echinococcus cyst fragments (Figs 2E, 2F).

Figure Jump LinkFigure 3. Water lily sign. CT scan obtained at level of right middle lobe shows ruptured hydatid cyst. After rupture and discharge of cyst fluid into pleural cavity, endocyst collapses, sediments, and floats in remaining fluid at bottom of original cyst. (Image courtesy by Farid Rashidi, MD.)Grahic Jump Location

Bronchoscopic extraction of the hydatid cyst is possible; however, because of the risk of cyst rupture, it should be considered on a case-by-case basis. Serologic tests are more sensitive in patients with liver involvement (80%-94%) than in those with lung hydatidosis (65%).34 Hydatid cyst rupture can increase the sensitivity of serologic tests to > 90%.55

Cystic hydatidosis is the only infestation that needs surgical treatment. Complete resection of the cyst is the cornerstone of the management of pulmonary hydatidosis: to remove the intact cyst, preserve as much viable lung tissue as possible, and treat the associated parenchymal and bronchial disease. The lung parenchyma around a hydatid cyst is often affected by the lesion and may exhibit chronic congestion, hemorrhage, and interstitial pneumonia, which often resolve after the surgery.57 Spillage of hydatid fluid must be avoided to prevent secondary hydatidosis. Medical therapy may have a role in poor surgical candidates and in intraoperative spillage of fluid from a hydatid cyst. Antihelminthic agents, such as mebendazole or albendazole, have shown only 25% to 34% cure rates.58 The drawback of antihelminthic therapy is that it weakens the cyst wall and increases the risk of rupture. In addition, if the parasite dies because of the drug, the cyst membrane may remain within the cavity and lead to secondary complications, including infections.59 Percutaneous treatment by puncture-aspiration-injection-reaspiration has rarely been used in pulmonary cysts because of the risk of anaphylactic shock, pneumothorax, pleural spillage, and bronchopleural fistulae.60

Pulmonary alveolar echinococcosis is a rare but severe and potentially fatal form of echinococcosis but it is restricted to the Northern Hemisphere. The liver is the first target for the parasite, with a long, silent incubation period. Pulmonary involvement results from either dissemination or the direct extension of the hepatic echinococcosis with intrathoracic rupture through the diaphragm into the bronchial tree, pleural cavity, or mediastinum. Chest radiograph or CT scanning may aid in the diagnosis. ELISAs and indirect hemagglutination assay are available and offer early detection in endemic areas. Radical resection of localized lesions is the only curative treatment yet, is rarely possible in invasive and disseminated disease. Mebendazole and albendazole can be used, but the required treatment duration need is a minimum of 2 years after the radical surgery.61

Mesomycetozoea is a group of organisms at the border of the animal-fungal kingdom.62 They appear in host tissues as sphere-shaped spores.

Rhinosporidiosis

Rhinosporidiosis is a chronic granulomatous infectious disease caused by Rhinosporidium seeberi. This condition has a high prevalence in South Asia, especially Sri Lanka.63 Patients usually present with recurrent polypoidal, friable, hemorrhagic, lesions. The common sites of involvement are the nose and nasopharynx. However, lesions can involve the tracheobronchial tree, leading to partial or complete airway obstruction (Figs 4A, 4B).64 CT imaging is the preferred study because it defines the extent of disease. Therapeutic bronchoscopy plays a major role in bronchial rhinosporidiosis.

Figure Jump LinkFigure 4. A, Bronchoscopy revealed pinkish mulberry-like rhinosporidiosis mass in the right main stem bronchus. (Reprint with permission from Singh et al.64) B, Microscopic examination of the resected specimen shows bronchial subepithelium with sporangia of Rhinosporodium; filled with small round endospores (H&E, original magnification × 100). (Reprint with permission from Singh et al.64) C, Amebic lung abscess from lung biopsy specimen. The arrows point to trophozoites of Entamoeba histolytica (H&E, original magnification × 200). D, Transbronchial needle biopsy specimen of a mediastinal lymph node shows histiocytes containing abundant Leishmania amastigotes (arrows) (H&E, original magnification × 1,000). Inset shows a close-up view of an amastigote. Its ovoid shape, eccentric nucleus, and kinetoplast are discerned (same magnification as image). (Reprint with permission from Kotsifas et al.68) E, Lung infected with Toxoplasmosis gondii (arrow) with diffuse alveolar damage (H&E, original magnification × 100). Inset shows bradyzoites of T gondii present in cytoplasm of alveolar macrophage (H&E, original magnification × 1,000). See Figure 1 legend for expansion of abbreviation.Grahic Jump Location

Dapsone is the only medication to arrest the maturation of the sporangia, but the lesions may recur after months or years.65 Follow-up bronchoscopy is recommended to monitor signs of recurrence.

Protozoa parasites are single-celled organisms that are mostly intracellular in humans (Table 2). Pulmonary amebiasis is caused by Entamoeba histolytica trophozoites invading the intestinal mucosa and entering the bloodstream, effecting systemic infection. Pleuropulmonary amebiasis occurs mainly by local extension from the amoebic liver abscess. Patients usually present with fever, right-upper-quadrant abdominal pain, and cough. Sterile pleural effusion, lung abscess, hepatobronchial fistula, empyema, and pyopneumothorax have also been reported.1 Live trophozoites of E histolytica can be demonstrated in sputum, pleural pus, or lung biopsy specimens (Fig 4C). The presence of amoeba in the stool does not indicate an active E histolytica infection because two other nonpathologic Entamoeba species are found in humans.66 Metronidazole is the treatment of choice for invasive amoebiasis.

Table Graphic Jump Location
Table 2 —Protozoal Infection of Respiratory System

Leishmania causes visceral leishmaniasis, which has been reported in patients who have undergone lung transplants.67 Pulmonary manifestations include pneumonitis, pleural effusion, and mediastinal lymphadenopathy.34Leishmania organisms can also be found in the alveoli (Fig 4D)68 and the BALF.69 The diagnosis of leishmaniasis is confirmed by the presence of the parasites in bone marrow aspirates or by polymerase chain reaction identification in tissue biopsy specimens. Treatments of choice include pentavalent antimonials and liposomal amphotericin B. Miltefosine can be used as an oral agent against visceral leishmaniasis.70

Toxoplasmosis is caused by the protozoan, Toxoplasma gondii. Cats are the primary hosts of T gondii.71 Humans become infected by consuming contaminated undercooked food. Pulmonary toxoplasmosis has been reported with increasing frequency in HIV-infected patients. Pulmonary manifestations include interstitial pneumonia, diffuse alveolar damage, or necrotizing pneumonia.72 Histologic examination of lung biopsy specimens can identify T gondii tachyzoites in necrotic areas in both intracellular and extracellular forms (Fig 4E).73 The diagnosis of toxoplasmosis is based on the detection of the protozoa in bodily tissues. Diagnostic real-time polymerase chain reaction-based assays of BALF have been reported for HIV-positive patients. Toxoplasmosis can be treated with a combination of pyrimethamine and sulfadiazine for 3 to 4 weeks.74

Although helminthic and protozoal parasitic infestations are dominant mainly in tropical and subtropical areas, global warming, immigration, and an increasing use of immunosupressives have changed their distribution. To manage these challenging clinical scenarios, pulmonologists must understand the epidemiology, life cycles, and clinical presentation of these infestations, as well as the bronchoscopic and laboratory findings and treatment options.

Financial/nonfinancial disclosures: The authors have reported to CHEST that no potential conflicts of interest exist with any companies/organizations whose products or services may be discussed in this article.

Other contributions: We thank Gary Procop, MD, and Farid Rashidi, MD, for contribution of figures.

BALF

BAL fluid

DEC

diethylcarbamazine

ELISA

enzyme-linked immunosorbent assay

PAH

pulmonary artery hypertension

TPE

tropical pulmonary eosinophilia

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Krolewiecki AJ, Ramanathan R, Fink V, et al. Improved diagnosis ofStrongyloides stercoralisusing recombinant antigen-based serologies in a community-wide study in northern Argentina. Clin Vaccine Immunol. 2010;17(10):1624-1630. [CrossRef]
 
Suputtamongkol Y, Premasathian N, Bhumimuang K, et al. Efficacy and safety of single and double doses of ivermectin versus 7-day high dose albendazole for chronic strongyloidiasis. PLoS Negl Trop Dis. 2011;5(5):e1044. [CrossRef]
 
Kim HY, Lee SM, Joo JE, Na MJ, Ahn MH, Min DY. Human syngamosis: the first case in Korea. Thorax. 1998;53(8):717-718. [CrossRef]
 
Severo LC, Conci LMA, Camargo JJP, et al. Syngamosis: two new Brazilian cases and evidence of a possible pulmonary cycle. Trans R Soc Trop Med Hyg. 1988;82(3):467-468. [CrossRef]
 
Weinstein L, Molavi A. Syngamus laryngeus infection (syngamosis) with chronic cough. Ann Intern Med. 1971;74(4):577-580. [CrossRef]
 
de Lara TdeA, Barbosa MA, de Oliveira MR, de Godoy I, Queluz TT. Human syngamosis. Two cases of chronic cough caused byMammomonogamus laryngeusChest. 1993;103(1):264-265. [CrossRef]
 
Theis JH. Public health aspects of dirofilariasis in the United States. Vet Parasitol. 2005;133(2-3):157-180. [CrossRef]
 
Milanez de Campos JR, Barbas CS, Filomeno LT, et al. Human pulmonary dirofilariasis: analysis of 24 cases from São Paulo, Brazil. Chest. 1997;112(3):729-733. [CrossRef]
 
Oshiro Y, Murayama S, Sunagawa U, et al. Pulmonary dirofilariasis: computed tomography findings and correlation with pathologic features. J Comput Assist Tomogr. 2004;28(6):796-800. [CrossRef]
 
Moore W, Franceschi D. PET findings in pulmonary dirofilariasis. J Thorac Imaging. 2005;20(4):305-306. [CrossRef]
 
Chitkara RK, Sarinas PS. Dirofilaria, visceral larva migrans, and tropical pulmonary eosinophilia. Semin Respir Infect. 1997;12(2):138-148.
 
Boggild AK, Keystone JS, Kain KC. Tropical pulmonary eosinophilia: a case series in a setting of nonendemicity. Clin Infect Dis. 2004;39(8):1123-1128. [CrossRef]
 
Vijayan VK. Immunopathogenesis and treatment of eosinophilic lung diseases in the tropics.. In:Sharma OP., ed. Lung Biology in Health and Disease: Tropical Lung Disease.2nd ed. New York, NY: Taylor & Francis; 2006:195-239.
 
Savani DM, Sharma OP. Eosinophilic lung disease in the tropics. Clin Chest Med. 2002;23(2):377-396. [CrossRef]
 
Sandhu M, Mukhopadhyay S, Sharma SK. Tropical pulmonary eosinophilia: a comparative evaluation of plain chest radiography and computed tomography. Australas Radiol. 1996;40(1):32-37. [CrossRef]
 
Ottesen EA, Nutman TB. Tropical pulmonary eosinophilia. Annu Rev Med. 1992;43:417-424. [CrossRef]
 
Vijayan VK, Rao KV, Sankaran K, Venkatesan P, Prabhakar R. Tropical eosinophilia: clinical and physiological response to diethylcarbamazine. Respir Med. 1991;85(1):17-20. [CrossRef]
 
Vijayan VK. Parasitic lung infections. Curr Opin Pulm Med. 2009;15(3):274-282. [CrossRef]
 
Figueiredo SD, Taddei JA, Menezes JJ, et al. Clinical-epidemiological study of toxocariasis in a pediatric population [in Portugese]. J Pediatr (Rio J). 2005;81(2):126-132.
 
Sane AC, Barber BA. Pulmonary nodules due toToxocara canisinfection in an immunocompetent adult. South Med J. 1997;90(1):78-79. [CrossRef]
 
Despommier D. Toxocariasis: clinical aspects, epidemiology, medical ecology, and molecular aspects. Clin Microbiol Rev. 2003;16(2):265-272. [CrossRef]
 
Harbottle JE, English DK, Schultz MG. Trichinosis in bears in northeastern United States. HSMHA Health Rep. 1971;86(5):473-476. [CrossRef]
 
Bruschi F, Murrell K. Trichinellosis.. In:Guerrant R, Walker DH, Weller PF., eds. Tropical Infectious Disease: Principles, Pathogens and Practice. Philadelphia, PA: Churchill Livingstone; 1999:917-925.
 
Gómez-Morales MA, Ludovisis A, Amati M, et al. Validation of an enzyme-linked immunosorbent assay for the diagnosis of human trichinellosis. Clin Vaccine Immunol. 2008;15(11):1723-1729. [CrossRef]
 
Cooke GS, Lalvani A, Gleeson FV, Conlon CP. Acute pulmonary schistosomiasis in travelers returning from Lake Malawi, sub-Saharan Africa. Clin Infect Dis. 1999;29(4):836-839. [CrossRef]
 
Bottieau E, Clerinx J, de Vega MR, et al. Imported Katayama fever: clinical and biological features at presentation and during treatment. J Infect. 2006;52(5):339-345. [CrossRef]
 
Schwartz E. Pulmonary schistosomiasis. Clin Chest Med. 2002;23(2):433-443. [CrossRef]
 
Simonneau G, Robbins IM, Beghetti M, et al. Updated clinical classification of pulmonary hypertension., J Am Coll Cardiol 2009;541(suppl 1):S43-S54. [CrossRef]
 
Salama M, El-Kholy G, Abd El-Haleem S, et al. Serum soluble Fas in patients with Schistosomal cor pulmonale. Respiration. 2003;70(6):574-578. [CrossRef]
 
Xiao SH. Development of antischistosomal drugs in China, with particular consideration to praziquantel and the artemisinins. Acta Trop. 2005;96(2-3):153-167. [CrossRef]
 
Sersar SI, Elnahas HA, Saleh AB, Moussa SA, Ghafar WA. Pulmonary parasitosis: applied clinical and therapeutic issues. Heart Lung Circ. 2006;15(1):24-29. [CrossRef]
 
Meehan AM, Virk A, Swanson K, Poeschla EM. Severe pleuropulmonary paragonimiasis 8 years after emigration from a region of endemicity. Clin Infect Dis. 2002;35(1):87-90. [CrossRef]
 
Nakamura-Uchiyama F, Mukae H, Nawa Y. Paragonimiasis: a Japanese perspective. Clin Chest Med. 2002;23(2):409-420. [CrossRef]
 
Vélez ID, Ortega JE, Velásquez LE. Paragonimiasis: a view from Columbia. Clin Chest Med. 2002;23(2):421-431. [CrossRef]
 
Jeon K, Song JU, Um SW, et al. Bronchoscopic findings of pulmonary paragonimiasis. Tuberc Respir Dis. 2009;67(6):512-516. [CrossRef]
 
Mukae H, Taniguchi H, Matsumoto N, et al. Clinicoradiologic features of pleuropulmonaryParagonimus westermanion Kyusyu Island, Japan. Chest. 2001;120(2):514-520. [CrossRef]
 
Lee JS, Lee J, Kim SH, Yong TS. Molecular cloning and characterization of a major egg antigen inParagonimus westermaniand its use in ELISA for the immunodiagnosis of paragonimiasis. Parasitol Res. 2007;100(4):677-681. [CrossRef]
 
Morar R, Feldman C. Pulmonary echinococcosis. Eur Respir J. 2003;21(6):1069-1077. [CrossRef]
 
Saygi A, Oztek I, Güder M, Süngün F, Arman B. Value of fibreoptic bronchoscopy in the diagnosis of complicated pulmonary unilocular cystic hydatidosis. Eur Respir J. 1997;10(4):811-814.
 
Pedrosa I, Saíz A, Arrazola J, Ferreirós J, Pedrosa CS. Hydatid disease: radiologic and pathologic features and complications. Radiographics. 2000;20(3):795-817. [CrossRef]
 
Sakamoto T, Gutierrez C. Pulmonary complications of cystic echinococcosis in children in Uruguay. Pathol Int. 2005;55(8):497-503. [CrossRef]
 
Wen H, Yang WG. Public health importance of cystic echinococcosis in China. Acta Trop. 1997;67(1-2):133-145. [CrossRef]
 
Keshmiri M, Baharvahdat H, Fattahi SH, et al. Albendazole versus placebo in treatment of echinococcosis. Trans R Soc Trop Med Hyg. 2001;95(2):190-194. [CrossRef]
 
Junghanss T, da Silva AM, Horton J, Chiodini PL, Brunetti E. Clinical management of cystic echinococcosis: state of the art, problems, and perspectives. Am J Trop Med Hyg. 2008;79(3):301-311.
 
Eckert J, Deplazes P. Biological, epidemiological, and clinical aspects of echinococcosis, a zoonosis of increasing concern. Clin Microbiol Rev. 2004;17(1):107-135. [CrossRef]
 
Silva V, Pereira CN, Ajello L, et al. Molecular evidence for multiple host-specific strains in the genusRhinosporidiumJ Clin Microbiol. 2005;43(4):1865-1868. [CrossRef]
 
Fredricks DN, Jolley JA, Lepp PW, Kosek JC, Relman DA. Rhinosporidium seeberi: a human pathogen from a novel group of aquatic protistan parasites. Emerg Infect Dis. 2000;6(3):273-282. [CrossRef]
 
Singh RK, Christopher DJ, Isaac TJ, Jeveraj V, Balamugesh T. Endobronchial rhinosporidiosis. J Bronchology Interv Pulmonol. 2013;20(2):164-166. [CrossRef]
 
Job A, Venkateswaran S, Mathan M, Krishnaswami H, Raman R. Medical therapy of rhinosporidiosis with dapsone. J Laryngol Otol. 1993;107(9):809-812. [CrossRef]
 
Tanyuksel M, Petri WA Jr. Laboratory diagnosis of amebiasis. Clin Microbiol Rev. 2003;16(4):713-729. [CrossRef]
 
Morales P, Torres JJ, Salavert M, Pemán J, Lacruz J, Solé A. Visceral leishmaniasis in lung transplantation. Transplant Proc. 2003;35(5):2001-2003. [CrossRef]
 
Kotsifas K, Metaxas E, Koutsouvelis I, Skoutelis A, Kara P, Tatsis G. Visceral leishmaniasis with endobronchial involvement in an immunocompetent adult. Case Rep Med. 2011;2011:561985.
 
Jokipii L, Salmela K, Saha H, et al. Leishmaniasis diagnosed from bronchoalveolar lavage. Scand J Infect Dis. 1992;24(5):677-681. [CrossRef]
 
Croft SL, Engel J. Miltefosine–discovery of the antileishmanial activity of phospholipid derivatives. Trans R Soc Trop Med Hyg. 2006;100(suppl 1):S4-S8. [CrossRef]
 
Dodds EM. Toxoplasmosis. Curr Opin Ophthalmol. 2006;17(6):557-561. [CrossRef]
 
Petersen E, Edvinsson B, Lundgren B, Benfield T, Evengård B. Diagnosis of pulmonary infection with Toxoplasma gondii in immunocompromised HIV-positive patients by real-time PCR. Eur J Clin Microbiol Infect Dis. 2006;25(6):401-404. [CrossRef]
 
Nash G, Kerschmann RL, Herndier B, Dubey JP. The pathological manifestations of pulmonary toxoplasmosis in the acquired immunodeficiency syndrome. Hum Pathol. 1994;25(7):652-658. [CrossRef]
 
Martínez-Girón R, Esteban JG, Ribas A, Doganci L. Protozoa in respiratory pathology: a review. Eur Respir J. 2008;32(5):1354-1370. [CrossRef]
 

Figures

Figure Jump LinkFigure 1. A, Hookworm larva in the sputum sample (wet smear, original magnification × 88). Morphologically, hookworm larvae have long buccal cavities, whereas Strongyloides larvae have short buccal cavities. (Reprinted with permission from Beigel et al.9) B, Bloody aliquot from BAL sample and Strongyloides larvae from BAL (hematoxylin and eosin [H&E], original magnification × 200). Note: short buccal cavity distinguishes Strongyloides from the hookworm (inset) (H&E, original magnification × 400). C, Strongyloides larvae (arrow) present in alveolar space in lung with diffuse alveolar damage (H&E, original magnification × 400). D, Bronchoscopic findings in anterior basal segment of right lower lobe. The syngamosis male is smaller and attached to the copulatory bursa of the female body (arrow). The parasite can be seen in bronchoscopy because they reside in the bronchial mucosa. (Reprinted with permission from Kim et al.19) E, Cross-sections of coiled Dirofilaria worms within involved artery causing surrounding infarction of lung tissue. Note the smooth cuticle at the external layer (Movat stain, original magnification × 200). F, Schistosomal ova in the lung biopsy specimen. The arrow points to ova within the granulomatous reaction (H&E, original magnification × 100).Grahic Jump Location
Figure Jump LinkFigure 2. A, Bronchoscopic findings showed mucosal nodularity on the right upper lobe (RUL). (Reprinted with permission from Jeon et al.51) B, Microscopic examination of bronchial tissue obtained from the RUL bronchus showing thickening of the basement membrane and chronic inflammation with eosinophilic infiltration (H&E, original magnification × 200). (Reprinted with permission from Jeon et al.51) Inset: Paragonimus kellicotti egg in a BAL sample. The arrow points to the operculum ridges of the egg (Papanicolaou, original magnification × 400). (Image courtesy by Gary Procop, MD.) C, Granulomas in the pleura in a patient with paragonimiasis. The arrow points to a light brown egg within the granuloma (H&E, original magnification × 100). (Image courtesy by Gary Procop, MD.) D, Protruded hydatid cyst from left lower lobe bronchus. (Image courtesy by Farid Rashidi, MD.) E, Echinococcus cyst fragments in lung biopsy specimen. The arrows highlight the collapsed chitinous layer of a death hydatid cyst (H&E, original magnification × 44). F, Echinococcus cyst fragments in lung biopsy specimen. The fragmented ecchinococus cyst with collapsed chitinous layer resides within the granulomatous reaction (H&E, original magnification × 200). See Figure 1 legend for expansion of other abbreviation.Grahic Jump Location
Figure Jump LinkFigure 3. Water lily sign. CT scan obtained at level of right middle lobe shows ruptured hydatid cyst. After rupture and discharge of cyst fluid into pleural cavity, endocyst collapses, sediments, and floats in remaining fluid at bottom of original cyst. (Image courtesy by Farid Rashidi, MD.)Grahic Jump Location
Figure Jump LinkFigure 4. A, Bronchoscopy revealed pinkish mulberry-like rhinosporidiosis mass in the right main stem bronchus. (Reprint with permission from Singh et al.64) B, Microscopic examination of the resected specimen shows bronchial subepithelium with sporangia of Rhinosporodium; filled with small round endospores (H&E, original magnification × 100). (Reprint with permission from Singh et al.64) C, Amebic lung abscess from lung biopsy specimen. The arrows point to trophozoites of Entamoeba histolytica (H&E, original magnification × 200). D, Transbronchial needle biopsy specimen of a mediastinal lymph node shows histiocytes containing abundant Leishmania amastigotes (arrows) (H&E, original magnification × 1,000). Inset shows a close-up view of an amastigote. Its ovoid shape, eccentric nucleus, and kinetoplast are discerned (same magnification as image). (Reprint with permission from Kotsifas et al.68) E, Lung infected with Toxoplasmosis gondii (arrow) with diffuse alveolar damage (H&E, original magnification × 100). Inset shows bradyzoites of T gondii present in cytoplasm of alveolar macrophage (H&E, original magnification × 1,000). See Figure 1 legend for expansion of abbreviation.Grahic Jump Location

Tables

Table Graphic Jump Location
Table 1 —Parasitic Infection of Respiratory System

N/A = not available.

Table Graphic Jump Location
Table 2 —Protozoal Infection of Respiratory System

References

Martínez S, Restrepo CS, Carrillo JA, et al. Thoracic manifestations of tropical parasitic infections: a pictorial review. Radiographics. 2005;25(1):135-155. [CrossRef]
 
Gelpi AP, Mustafa A. Ascaris pneumonia. Am J Med. 1968;44(3):377-389. [CrossRef]
 
Butts C, Hnderson SO. Ascariasis. Top Emerg Med. 2003;25(1):38-43.
 
Osborne DP, Brown RB, Dimmette RM. Solitary pulmonary nodule due toAscaris lumbrocoidesChest. 1961;40:308-310. [CrossRef]
 
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Hotez PJ, Brooker S, Bethony JM, Bottazzi ME, Loukas A, Xiao S. Hookworm infection. N Engl J Med. 2004;351(8):799-807. [CrossRef]
 
Sarinas PS, Chitkara RK. Ascariasis and hookworm. Semin Respir Infect. 1997;12(2):130-137.
 
Kuzucu A. Parasitic diseases of the respiratory tract. Curr Opin Pulm Med. 2006;12(3):212-221. [CrossRef]
 
Beigel Y, Greenberg Z, Ostfeld I. Clinical problem-solving. Letting the patient off the hook. N Engl J Med. 2000;342(22):1658-1661. [CrossRef]
 
Maxwell C, Hussain R, Nutman TB, et al. The clinical and immunologic responses of normal human volunteers to low dose hookworm (Necator americanus) infection. Am J Trop Med Hyg. 1987;37(1):126-134.
 
Keiser PB, Nutman TB. Strongyloides stercoralisin the immunocompromised population. Clin Microbiol Rev. 2004;17(1):208-217. [CrossRef]
 
Namisato S, Motomura K, Haranaga S, et al. Pulmonary strongyloides in a patient receiving prednisolone therapy. Intern Med. 2004;43:731-736. [CrossRef]
 
Mejia R, Nutman TB. Screening, prevention, and treatment for hyperinfection syndrome and disseminated infections caused byStrongyloides stercoralisCurr Opin Infect Dis. 2012;25(4):458-463. [CrossRef]
 
Woodring JH, Halfhill H II, Berger R, Reed JC, Moser N. Clinical and imaging features of pulmonary strongyloidiasis. South Med J. 1996;89(1):10-19. [CrossRef]
 
Siddiqui AA, Berk SL. Diagnosis ofStrongyloides stercoralisinfection. Clin Infect Dis. 2001;33(7):1040-1047. [CrossRef]
 
Cartwright CP. Utility of multiple-stool-specimen ova and parasite examinations in a high-prevalence setting. J Clin Microbiol. 1999;37(8):2408-2411.
 
Krolewiecki AJ, Ramanathan R, Fink V, et al. Improved diagnosis ofStrongyloides stercoralisusing recombinant antigen-based serologies in a community-wide study in northern Argentina. Clin Vaccine Immunol. 2010;17(10):1624-1630. [CrossRef]
 
Suputtamongkol Y, Premasathian N, Bhumimuang K, et al. Efficacy and safety of single and double doses of ivermectin versus 7-day high dose albendazole for chronic strongyloidiasis. PLoS Negl Trop Dis. 2011;5(5):e1044. [CrossRef]
 
Kim HY, Lee SM, Joo JE, Na MJ, Ahn MH, Min DY. Human syngamosis: the first case in Korea. Thorax. 1998;53(8):717-718. [CrossRef]
 
Severo LC, Conci LMA, Camargo JJP, et al. Syngamosis: two new Brazilian cases and evidence of a possible pulmonary cycle. Trans R Soc Trop Med Hyg. 1988;82(3):467-468. [CrossRef]
 
Weinstein L, Molavi A. Syngamus laryngeus infection (syngamosis) with chronic cough. Ann Intern Med. 1971;74(4):577-580. [CrossRef]
 
de Lara TdeA, Barbosa MA, de Oliveira MR, de Godoy I, Queluz TT. Human syngamosis. Two cases of chronic cough caused byMammomonogamus laryngeusChest. 1993;103(1):264-265. [CrossRef]
 
Theis JH. Public health aspects of dirofilariasis in the United States. Vet Parasitol. 2005;133(2-3):157-180. [CrossRef]
 
Milanez de Campos JR, Barbas CS, Filomeno LT, et al. Human pulmonary dirofilariasis: analysis of 24 cases from São Paulo, Brazil. Chest. 1997;112(3):729-733. [CrossRef]
 
Oshiro Y, Murayama S, Sunagawa U, et al. Pulmonary dirofilariasis: computed tomography findings and correlation with pathologic features. J Comput Assist Tomogr. 2004;28(6):796-800. [CrossRef]
 
Moore W, Franceschi D. PET findings in pulmonary dirofilariasis. J Thorac Imaging. 2005;20(4):305-306. [CrossRef]
 
Chitkara RK, Sarinas PS. Dirofilaria, visceral larva migrans, and tropical pulmonary eosinophilia. Semin Respir Infect. 1997;12(2):138-148.
 
Boggild AK, Keystone JS, Kain KC. Tropical pulmonary eosinophilia: a case series in a setting of nonendemicity. Clin Infect Dis. 2004;39(8):1123-1128. [CrossRef]
 
Vijayan VK. Immunopathogenesis and treatment of eosinophilic lung diseases in the tropics.. In:Sharma OP., ed. Lung Biology in Health and Disease: Tropical Lung Disease.2nd ed. New York, NY: Taylor & Francis; 2006:195-239.
 
Savani DM, Sharma OP. Eosinophilic lung disease in the tropics. Clin Chest Med. 2002;23(2):377-396. [CrossRef]
 
Sandhu M, Mukhopadhyay S, Sharma SK. Tropical pulmonary eosinophilia: a comparative evaluation of plain chest radiography and computed tomography. Australas Radiol. 1996;40(1):32-37. [CrossRef]
 
Ottesen EA, Nutman TB. Tropical pulmonary eosinophilia. Annu Rev Med. 1992;43:417-424. [CrossRef]
 
Vijayan VK, Rao KV, Sankaran K, Venkatesan P, Prabhakar R. Tropical eosinophilia: clinical and physiological response to diethylcarbamazine. Respir Med. 1991;85(1):17-20. [CrossRef]
 
Vijayan VK. Parasitic lung infections. Curr Opin Pulm Med. 2009;15(3):274-282. [CrossRef]
 
Figueiredo SD, Taddei JA, Menezes JJ, et al. Clinical-epidemiological study of toxocariasis in a pediatric population [in Portugese]. J Pediatr (Rio J). 2005;81(2):126-132.
 
Sane AC, Barber BA. Pulmonary nodules due toToxocara canisinfection in an immunocompetent adult. South Med J. 1997;90(1):78-79. [CrossRef]
 
Despommier D. Toxocariasis: clinical aspects, epidemiology, medical ecology, and molecular aspects. Clin Microbiol Rev. 2003;16(2):265-272. [CrossRef]
 
Harbottle JE, English DK, Schultz MG. Trichinosis in bears in northeastern United States. HSMHA Health Rep. 1971;86(5):473-476. [CrossRef]
 
Bruschi F, Murrell K. Trichinellosis.. In:Guerrant R, Walker DH, Weller PF., eds. Tropical Infectious Disease: Principles, Pathogens and Practice. Philadelphia, PA: Churchill Livingstone; 1999:917-925.
 
Gómez-Morales MA, Ludovisis A, Amati M, et al. Validation of an enzyme-linked immunosorbent assay for the diagnosis of human trichinellosis. Clin Vaccine Immunol. 2008;15(11):1723-1729. [CrossRef]
 
Cooke GS, Lalvani A, Gleeson FV, Conlon CP. Acute pulmonary schistosomiasis in travelers returning from Lake Malawi, sub-Saharan Africa. Clin Infect Dis. 1999;29(4):836-839. [CrossRef]
 
Bottieau E, Clerinx J, de Vega MR, et al. Imported Katayama fever: clinical and biological features at presentation and during treatment. J Infect. 2006;52(5):339-345. [CrossRef]
 
Schwartz E. Pulmonary schistosomiasis. Clin Chest Med. 2002;23(2):433-443. [CrossRef]
 
Simonneau G, Robbins IM, Beghetti M, et al. Updated clinical classification of pulmonary hypertension., J Am Coll Cardiol 2009;541(suppl 1):S43-S54. [CrossRef]
 
Salama M, El-Kholy G, Abd El-Haleem S, et al. Serum soluble Fas in patients with Schistosomal cor pulmonale. Respiration. 2003;70(6):574-578. [CrossRef]
 
Xiao SH. Development of antischistosomal drugs in China, with particular consideration to praziquantel and the artemisinins. Acta Trop. 2005;96(2-3):153-167. [CrossRef]
 
Sersar SI, Elnahas HA, Saleh AB, Moussa SA, Ghafar WA. Pulmonary parasitosis: applied clinical and therapeutic issues. Heart Lung Circ. 2006;15(1):24-29. [CrossRef]
 
Meehan AM, Virk A, Swanson K, Poeschla EM. Severe pleuropulmonary paragonimiasis 8 years after emigration from a region of endemicity. Clin Infect Dis. 2002;35(1):87-90. [CrossRef]
 
Nakamura-Uchiyama F, Mukae H, Nawa Y. Paragonimiasis: a Japanese perspective. Clin Chest Med. 2002;23(2):409-420. [CrossRef]
 
Vélez ID, Ortega JE, Velásquez LE. Paragonimiasis: a view from Columbia. Clin Chest Med. 2002;23(2):421-431. [CrossRef]
 
Jeon K, Song JU, Um SW, et al. Bronchoscopic findings of pulmonary paragonimiasis. Tuberc Respir Dis. 2009;67(6):512-516. [CrossRef]
 
Mukae H, Taniguchi H, Matsumoto N, et al. Clinicoradiologic features of pleuropulmonaryParagonimus westermanion Kyusyu Island, Japan. Chest. 2001;120(2):514-520. [CrossRef]
 
Lee JS, Lee J, Kim SH, Yong TS. Molecular cloning and characterization of a major egg antigen inParagonimus westermaniand its use in ELISA for the immunodiagnosis of paragonimiasis. Parasitol Res. 2007;100(4):677-681. [CrossRef]
 
Morar R, Feldman C. Pulmonary echinococcosis. Eur Respir J. 2003;21(6):1069-1077. [CrossRef]
 
Saygi A, Oztek I, Güder M, Süngün F, Arman B. Value of fibreoptic bronchoscopy in the diagnosis of complicated pulmonary unilocular cystic hydatidosis. Eur Respir J. 1997;10(4):811-814.
 
Pedrosa I, Saíz A, Arrazola J, Ferreirós J, Pedrosa CS. Hydatid disease: radiologic and pathologic features and complications. Radiographics. 2000;20(3):795-817. [CrossRef]
 
Sakamoto T, Gutierrez C. Pulmonary complications of cystic echinococcosis in children in Uruguay. Pathol Int. 2005;55(8):497-503. [CrossRef]
 
Wen H, Yang WG. Public health importance of cystic echinococcosis in China. Acta Trop. 1997;67(1-2):133-145. [CrossRef]
 
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