Paragonimus westermani | Paragonamiasis | Trematode, lung fluke

 

INTRODUCTION:

Paragonimiasis is a food-borne parasitic infection caused by the lung fluke which can cause a sub-acute to chronic inflammatory disease of the lung. It’s one of the more recognized lung flukes with the widest geographical range.

 

 

CAUSATIVE AGENT :

Kingdom: Animalia
Phylum: Platyhelminthes
Class: Trematoda
Family: Paragonimidae
Genus: Paragonimus
Species: P. westermani

 

More than 30 species of trematodes (flukes) of the genus Paragonimus have been reported to infect animals and humans.  Among the more than 10 species reported to infect humans, the most common is P. westermani, the oriental lung fluke(1), (2).

 

 

HISTORY OF DISCOVERY:

According to History of Human Parasitology by F. E. G. Cox of the Department of Infectious and Tropical Diseases in the London School of Hygiene and Tropical Medicine,  P. westermani was discovered in the lungs of a human by Ringer in 1879 (3) and eggs in the sputum were recognized independently by Manson and Erwin von Baelz in 1880 (4, 5). Manson proposed the snail as an intermediate host and various  Japanese workers detailed the whole life cycle in the snail between 1916 and 1922(6). The species name P. westermani was named after a zookeeper, Mr. P. Westermani, who noted the trematode in a Bengal tiger in an Amsterdam Zoo( 7).

 

CLINICAL PRESENTATION IN HUMANS:

 

Case Study:  “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 [shortness of breath] 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 [coughing up blood], chest pain, vomiting, diarrhea or urticaria [skin rash notable for dark red, raised, itchy bumps]. 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… 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” (8)

 

 

Caption: “ Gross appearance of the single Paragonimus westermani fluke discovered at surgery” (8)

 

Human infection with Paragonimus may cause acute or chronic symptoms, and manifestations may be either pulmonary or extrapulmonary.9

 

Acute Symptoms:

Chronic Symptoms:

 

Confusion with TB

Practitioners should think about TB in chronic patient cases with fevers, cough, weight loss. However if in endemic areas, think about paragonamiasis. Flukes occasionally invade and reside in the pleural space without parenchymal lung involvement(12, 13, 14).

“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.”

In pleural paragonimiasis symptoms may be minimal and diagnosis complicated, since ova are not coughed/spit out or swallowed because there is frequently no cough. Such patients may develop pleural effusions and, because of the coendemicity with Mycobacterium tuberculosis (and co-infection in some patients), such effusions are often misdiagnosed as tuberculous (15, 16).

*** Adapted from Heath, Harley W & Susan G Marshall. "Pleural Paragonimiasis In A Laotian Child.

 

 

 

Extra-pulmonary locations of the adult worms result in more severe manifestations, especially when the brain is involved. Extra-pulmonary paragonimiasis is rarely seen in humans for the worms migrate to the lungs but cysts can develop in the brain and abdominal adhesions resulting from infection have been reported. Cysts may contain living or dead worms; a yellow-brownish thick fluid (occasionally hemmorgahic). When the worm dies or escapes, the cysts gradually shrink, leaving nodules of fibrous tissues and eggs which can calcify (17).

 

Worldwide the most common cause of hemoptysis is paragonamiasis.(18)

 

Other Case Studies:

1.     Pachucki, CT, Levandowski, RA, Brown, VA, Sonnenkalb, BH, Vruno, MJ. American paragonimiasis treated with Praziquantel. New Eng J Med 1984; 311:582-3

2.     Procop, GW, Marty, AM, Scheck, DN, Mease, DR, Maw, GM. North American Paragonimiasis: A case report. Acta Cytol 2000; 44: 75-80.

 

 

 

TRANSMISSION:

Transmission of the parasite P. westermani to humans and mammals primarily occurs through the consumption of raw or undercooked seafood. In Asia, an estimated 80% of freshwater crabs carry P. westermani (19). In preparation, live crabs are crushed and metacercariae may contaminate the fingers/utensils of the person preparing the meal.Accidental transfer of infective cysts can occur via food preparers who handle raw seafood and and subsequently contaminate cooking utensils and other foods (20 ). Consumption of animals which feed on crustaceans can also transmit the parasite, for cases have been cited in Japan where raw boar meat was the source of human infection ( 21, 22)

Food preparation techniques such as pickling and salting do not exterminate the causative agent. For example, in Chinese study eating “drunken crabs”  was shown to be particularly risky because the infection rate was 100% when crabs are immersed in wine for 3-5 minutes and fed to cats/dog (23).

 

RESERVOIR:

 Animals such as pigs, dogs, and a variety of feline species can also harbor P. westermani (CDC).

 

VECTOR:

No vector but various snail, crab species are intermediate hosts.  In Japan and Korea, the crab specie Eriocheir is an important item of food as well as a notable second intermediate host of the parasite (24).

 

INCUBATION PERIOD:

Time from infection to oviposition ( laying eggs) is 65 to 90 days.  Infections may persist for 20 years in humans (CDC).

 

 

 

 

 

 

 

 

 

MORPHOLOGY:

·         Eggs: Paragonimus westermani eggs range from 80 to 120 µm long by 45 to 70 µm wide.  They are yellow-brown, ovoid or elongate, with a thick shell, and often asymmetrical with one end slightly flattened.  At the large end, the operculum is clearly visible.  The opposite (abopercular) end is thickened.  The eggs are unembryonated when passed in sputum or feces (CDC).

 

 

 

 

 

Key

AC=acetabulum (ventral sucker)                                                                          OV=ovary

 CE=cecum                                                                                                             TE=testes

OS=oral sucker                                                                                                      UT=uterus 

EB=excretory bladder

 

In tissue:

Hemorrhagic holes in the visceral pleura (white arrows) and adult worms acquired from the holes (black arrows). Bump of the visceral pleura is the subpleural worm cyst (red arrow)

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

LIFE CYCLE

Paragonimus has a quite complex life-cycle that involves two intermediate hosts as well as humans. Eggs first develop in water after being expelled by coughing (unembryonated) or being passed in human feces. In the external environment, the eggs become embryonated. In the next stage, the parasite miracidia hatch and invades the first intermediate host such as a species of freshwater snail. Miracida penetrate its soft tissues and go through several developmental stages inside the snail but mature into cercariae in 3 to 5 months. Cercariae next invade the second intermediate host such as crabs or crayfish and encyst to develop into metacercariae within 2 months.  Infection of humans or other mammals (definitive hosts) occurs via consumption of raw or undercooked crustaceans. Human infection with P. westermani occurs by eating inadequately cooked or pickled crab or crayfish that harbor metacercariae of the parasite.  The metacercariae excyst in the duodenum, penetrate through the intestinal wall into the peritoneal cavity, then through the abdominal wall and diaphragm into the lungs, where they become encapsulated and develop into adults.  The worms can also reach other organs and tissues, such as the brain and striated muscles, respectively.  However, when this takes place completion of the life cycles is not achieved, because the eggs laid cannot exit these sites (CDC).

 

 

 

 

 

 

 

 

 

EPIDEMIOLOGY:

 Paragonimus westermani is distributed in southeast Asia and Japan. Other species of Paragonimus are common in parts of Asia, Africa and South and Central America. P.Westermani has been increasingly recognized in the United States during the past 15 years because of the increase of immigrants from endemic areas such as Southeast Asia. Estimated to infects 22 million people worldwide (CDC).

 

 

 

DIAGNOSTIC TESTS

Diagnosis is based on microscopic demonstration of eggs in stool or sputum, but these are not present until 2 to 3 months after infection. However, eggs are also occasionally encountered in effusion fluid or biopsy material. Furthermore, you can use  morphologic comparisons with other intestinal parasites to diagnose potential causative agents. Finally, antibody detection is useful in light infections and in the diagnosis of extrapulmonary paragonimiasis. In the United States, detection of antibodies to Paragonimus westermani has helped physicians differentiate paragonimiasis from tuberculosis in Indochinese immigrants (CDC).

 

MANAGEMENT AND THERAPY

According to the CDC, Praziquantel* is the drug of choice to treat paragonimiasis. The recommended dosage of 75 mg/kg per day, divided into 3 doses over 2 days has proven to eliminate P. westermani (25).  Bithionol is an alternative drug for treatment of this disease but is associated with skin rashes and urticaria.  For additional information, see the recommendations in The Medical Letter (Drugs for Parasitic Infections).

 

 

PUBLIC HEALTH AND PREVENTION STRATEGIES/VACCINES

Prevention programs should promote more hygienic food preparation by encouraging safer cooking techniques and more sanitary handling of potentially contaminated seafood. The elimination of the first intermediate host, the snail, is not tenable due to the nature of the organisms habits (26).

A key component to prevention is research, more specifically the research of everyday behaviors. This recent study was conducted as a part of a broader effort to determine the status of Paragonimus species infection in Laos (27). An epidemiological survey was conducted on villagers and schoolchildren in Namback District between 2003 and 2005. Among 308 villagers and 633 primary and secondary schoolchildren, 156 villagers and 92 children had a positive reaction on a Paragonimus skin test. Consequently, several types of crabs were collected from markets and streams in a paragonimiasis endemic area for the inspection of metacercariae and were identified as the second intermediate host of the Paragonimus species.

In this case study, we see how high prevalence of paragonamiasis is explained by dietary habits of the population. Amongst schoolchildren, many students reported numerous experiences of eating roast crabs in the field. Adult villagers reported frequent consumption of seasoned crabs (Tan Cheoy Koung) and papaya salad (Tammack Koung) with crushed raw crab. In addition to this characteristic feature of the villagers' food culture, the denizens of this area drink fresh crab juice as a traditional cure for measles, and this was also thought to constitute a route for infection.

 

USEFUL WEB LINKS

http://www.dpd.cdc.gov/DPDx/html/Paragonimiasis.htm

 

REFERENCES

 

1.        Markell and Voge’s Medical Parasitology 9th Edition, pg 198

2.        CDC- http://www.dpd.cdc.gov/DPDx/html/Paragonimiasis.htm

3.        Muller, R. 1996. Liver and lung flukes, p. 274-285. In F. E. G. Cox (ed.), The Wellcome Trust illustrated history of tropical diseases. The Wellcome Trust, London, United Kingdom. http://cmr.asm.org/cgi/content/full/15/4/595#R193

4.        Manson, P. 1881. Distoma ringeri. Med. Times Gaz. 2:8-9.http://cmr.asm.org/cgi/content/full/15/4/595#R175

5.        Muller, R. 1996. Liver and lung flukes, p. 274-285. In F. E. G. Cox (ed.), The Wellcome Trust illustrated history of tropical diseases. The Wellcome Trust, London, United Kingdom . http://cmr.asm.org/cgi/content/full/15/4/595#R193

6.        Grove, D. I. 1990. A history of human helminthology. CAB International, Wallingford, United Kingdom. http://cmr.asm.org/cgi/content/full/15/4/595#R105

7.        Desowitz, R. New Guinea Tapeworms and Jewish Grandmothers: Tales of Parasites and People. New York: WW Norton, 1987.

8.        Heath, Harley W & Susan G Marshall. "Pleural Paragonimiasis In A Laotian Child. ." Pediatric Infectious Disease Journal 16(12)(1997): :1182-1185. http://www.pidj.com/pt/re/pidj/abstract.00006454-199712000-00018.htm;jsessionid=JnzNJ8ynh33JPL3GQ1NvLlxh6MJTQMkC7SscXNvPj6p6Yd5QfyZ4!-858031623!181195628!8091!-1

9.        Chung HL, Ho LY, Hsu CP, Ts'ao WJ. Recent progress in studies of Paragonimus and paragonimiasis control in China. Chin Med J 1981;94:483-94.

10.     http://www.dpd.cdc.gov/DPDx/html/Frames/MR/Paragonimiasis/body_Paragonimiasis_page2.htm

11.     Heath, Harley W & Susan G Marshall. "Pleural Paragonimiasis In A Laotian Child. ." Pediatric Infectious Disease Journal 16(12)(1997): :1182-1185. http://www.pidj.com/pt/re/pidj/abstract.00006454-199712000-00018.htm;jsessionid=JnzNJ8ynh33JPL3GQ1NvLlxh6MJTQMkC7SscXNvPj6p6Yd5QfyZ4!-858031623!181195628!8091!-1

12.     Roberts PP. Parasitic infections of the pleural space. Semin Respir Infect 1988;3:362-82. [Medline Link] [Context Link]

13.     Minh VD, Engle P, Greenwood JR, Prendergast TJ, Salness K, St. Clair R. Pleural paragonimiasis in a Southeast Asian refugee. Am Rev Respir Dis 1981;124:186-8.

[Context Link]

14.     Johnson JR, Falk A, Iber C, Davies S. Paragonimiasis in the United States: a report of nine cases in Hmong immigrants. Chest 1982;82:168-71. [CrossRef] [Context Link]

15.     1Johnson RJ, Johnson JR. Paragonimiasis in Indochinese refugees: roentgenographic findings and clinical correlations. Am Rev Respir Dis 1983;128:534-8.

[Context Link]

16.     Romeo DP, Pollock JJ. Pulmonary paragonimiasis: diagnostic value of pleural fluid analysis. South Med J 1986;79:241-3. [Fulltext Link] [Context Link]

17.     Markell and Voge’s Medical Parasitology 9th Edition, pg 201

18.     Davis, Gerald S., Elizabeth A. Seward, and Theodore W. Marcy. Medical Management of Pulmonary Diseases. CRC Press, 1999. Pg 345

19.     Pachucki, CT, Levandowski, RA, Brown, VA, Sonnenkalb, BH, Vruno, MJ. American Paragonimiasis treated with praziquantel. New Eng J Med 1984; 311: 582-583.

20.     Yokogawa, M. Paragonimus and Paragonimiasis. Adv Parasitol 1965; 3: 99-158

21.     Markell and Voge’s Medical Parasitology 9th Edition,pg 200

22.     Miyazaki I, Habe S. A newly recognized mode of human infection with the lung fluke, Paragonimus westermani. J Parasitol 1976;62:646-8.

23.     Yokogawa, M. Paragonimus and Paragonimiasis. Adv Parasitol 1965; 3: 99-158

24.     Yokogawa, M. Paragonimus and Paragonimiasis. Adv Parasitol 1965; 3: 99-158

25.     Pachucki, CT, Levandowski, RA, Brown, VA, Sonnenkalb, BH, Vruno, MJ. American Paragonimiasis treated with praziquantel. New Eng J Med 1984; 311: 582-583.

26.     Yokogawa, M. Paragonimus and Paragonimiasis. Adv Parasitol 1965; 3: 99-158

27.     Song HO, Min DY, Rim HJ, Youthanavanh V, Dalunyi B, Sengdara V, Virasack B, Bounlay P.

“Skin Test for Paragonimiasis among Schoolchildren and Villagers in Namback District, Luangprabang Province, Lao PDR.” Korean J Parasitol 2008 Sep; 46(3):179-82.

 

 

 

Photo Credits

1.     Case Study : Heath, Harley W & Susan G Marshall. "Pleural Paragonimiasis In A Laotian Child. ." Pediatric Infectious Disease Journal 16(12)(1997): :1182-1185. http://www.pidj.com/pt/re/pidj/abstract.00006454-199712000-00018.htm;jsessionid=JnzNJ8ynh33JPL3GQ1NvLlxh6MJTQMkC7SscXNvPj6p6Yd5QfyZ4!-858031623!181195628!8091!-1

2.     Eggs: http://www.dpd.cdc.gov/DPDx/images/ParasiteImages/M-R/Paragonimiasis/Paragonimus_egg_wtmt.jpg

3.     Metacercaria: http://www.stanford.edu/class/humbio103/ParaSites2001/paragonimiasis/Paragonimiasis/metacercariae.gif

4.     Adults: http://www.dpd.cdc.gov/DPDx/images/ParasiteImages/M-R/Paragonimiasis/Paragonimus_adult_hematoxylin2.jpg & http://www.dpd.cdc.gov/DPDx/images/MorphologyTables/Trematodes/Paragonimus_adult.gif

5.     In tissue: http://radiology.or.kr/pds/2005/108/Visceral%20pleura.jpg

6.     Life cycle : http://www.dpd.cdc.gov/DPDx/images/ParasiteImages/M-R/Paragonimiasis/Paragonimus_LifeCycle.gif

7.     Epidemiology Map : http://www.cdfound.to.it/img/pw2.jpg