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Human Paragonimiasis After Eating Raw or Undercooked Crayfish --- Missouri, July 2006−September 2010

Paragonimiasis is a parasitic disease caused by Paragonimus trematodes, commonly known as lung flukes. Humans become infected by eating raw or undercooked crayfish (also known as crawfish and crawdads) or freshwater crabs that harbor the parasites. Paragonimiasis most frequently involves the lungs, but can affect other organs, including the brain and skin. In North America, Paragonimus kellicotti causes infections among dogs, cats, and wild carnivores, but rarely infects humans (1). Paragonimiasis is not a nationally notifiable condition. In September 2009, physicians from the Washington University School of Medicine (WUSM) in St. Louis published details of three paragonimiasis cases diagnosed since July 2006 in persons who had eaten raw crayfish from rivers in Missouri (2), prompting the Missouri Department of Health and Senior Services (MDHSS), CDC, and WUSM to collaborate in paragonimiasis surveillance and prevention. During September 2009--September 2010, six additional cases were diagnosed in Missouri. These nine patients, aged 10−32 years, had fever, cough, pleural effusion, and eosinophilia. All had eaten raw or undercooked crayfish from rivers in Missouri while on canoeing or camping trips within 4 months of illness onset. Health-care providers should consider paragonimiasis when examining patients with unexplained fever, cough, eosinophilia, and pleural effusion or other chest radiographic abnormalities and should ask those patients whether they have eaten raw or undercooked crayfish.

The WUSM article (2) and reports of two paragonimiasis cases in October 2009 prompted MDHSS, the Missouri Department of Natural Resources, and the Missouri Division of Tourism to distribute posters warning against eating raw or undercooked crayfish to campers and canoe outfitters in November 2009. After the sixth case was reported in April 2010, MDHSS issued a health advisory on April 30 to enhance health-care provider awareness about paragonimiasis and to request voluntary reporting of cases. MDHSS developed an investigation form and revised the Missouri Health Surveillance Information System for reporting of paragonimiasis. In May, WUSM issued a press release to publicize the series of six cases, resulting in an additional patient (patient 7) seeking evaluation in June, 10 months after illness onset and after having undergone multiple diagnostic tests and failed treatments. In September, a medical center in northwest Missouri reported the other two cases.

Clinical information and exposure histories were collected through medical record review and interviews of patients and the parents of a patient by attending physicians. Sputum, stool, pleural effusion, and lung biopsies, if available, were examined microscopically for Paragonimus parasites or eggs. Serum samples were tested for Paragonimus antibodies by enzyme-linked immunosorbent assay (ELISA) at a commercial laboratory or by immunoblot assay at CDC. Seven patients lived in Missouri and two in Illinois (Table). All nine patients had eaten raw or undercooked crayfish directly taken from rivers in Missouri (i.e., Current, Jacks Fork, Huzzah, Little Niangua, and Meramec) while canoeing or camping within the months of May--August during 2006--2010. Among the eight adults, seven had eaten raw crayfish during group canoe trips, and the other had eaten undercooked crayfish while camping. Seven adults had eaten raw or undercooked crayfish after alcohol consumption; two had eaten raw crayfish on dares. The child had eaten a small raw crayfish while camping to demonstrate outdoor survival skills to other children.

Illness onset ranged from 2−16 weeks after crayfish ingestion. Common signs and symptoms were fever (100%), cough (100%), weight loss (56%), malaise (56%), chest pain (44%), dyspnea (44%), myalgia (44%), and night sweats (44%). Cough was not among the earliest indicators for patients 1, 4, and 7. Patient 1 experienced fever and headache 3 weeks before the onset of mild nonproductive cough. Two patients (patients 4 and 7) experienced upper-abdominal pain 6−8 weeks after crayfish ingestion. Patient 4 underwent emergency cholecystectomy for suspected acute cholecystitis, but his resected gall bladder was normal. Patient 7 experienced acute chest pain 2 weeks after experiencing abdominal pain. In addition, patient 8 experienced bilateral spontaneous pneumothoraces 3 weeks after the onset of fever, dyspnea, and nonproductive cough. These clinical manifestations likely were caused by P. kellicotti migration through the diaphragm into the pleural space and lungs.

During routine clinical care, all patients received a presumptive diagnosis of paragonimiasis 3−45 weeks after illness onset. All had eosinophilia (range: 850−3,900 eosinophils/mm3; eosinophil percentage: 7%−40%) and pleural effusion. Pleural effusions were analyzed for six patients. Five patients had eosinophilic pleural effusion, defined as a pleural effusion with ≥10% eosinophils (eosinophil percentage: 44%−90%; normal: ≤3%). Other chest radiologic abnormalities included pulmonary nodules (four patients), pericardial effusion (three patients), pulmonary infiltrates (three patients), and pneumothorax (one patient). Extrapulmonary complications included migratory skin nodules (four patients), cardiac tamponade (one patient), and cerebral lesions (one patient) associated with blurred vision.

P. kellicotti eggs were identified in sputum or bronchoalveolar lavage fluid from two patients 40--45 weeks after illness onset. Paragonimus antibodies were positive by ELISA or immunoblot for seven patients (Table). Among seven patients (patients 1 and 4−9) whose serum samples were tested for Paragonimus antibodies by immunoblot, three (patients 1, 4, and 5) tested negative in two consecutive serum samples collected ≥1 month apart. An acute serum from patient 4 was tested by ELISA; the result was positive. Patients 1 and 5 were diagnosed on the basis of their clinical histories and findings and response to therapy.

All patients were treated with 75 mg praziquantel per kilogram of body weight in 3 divided doses for 2--3 days. Their symptoms promptly improved. All symptoms, eosinophilia, and radiographic abnormalities resolved within 1−3 months of treatment.

Reported by

SL Patrick, PhD, G Turabelidze, MD, H Marx, A Grim, MPH, Missouri Dept of Health and Senior Svcs; MA Lane, MD, GJ Weil, MD, TC Bailey, MD, NF Önen, MD, Infectious Disease Div; LM Demertzis, MD, PG Tuteur, MD, Pulmonary Div, Dept of Medicine, EV Hayes MD, SZ Davila, MD, Dept of Pediatrics, Washington Univ School of Medicine, St. Louis; SM Folk, MD, RE Mitchem, DO, E Kammerer, MD, Heartland Regional Medical Center, St. Joseph, Missouri. LP Fannon Jr, Atlanta Research and Education Foundation, Georgia. JL Jones, MD, PP Wilkins, PhD, Div of Parasitic Diseases and Malaria, Center for Global Health; YC Lo, MD, EIS Officer, CDC.

Editorial Note

During 1965--2007, only six other cases of nonimported paragonimiasis were reported in the United States, occurring in Colorado, Iowa, Michigan, Missouri, and Oklahoma. Among those six patients, five had eaten crayfish (38). This report of nine cases recently identified in Missouri highlights the need for increased awareness of this underrecognized disease and public education to prevent it.

The life cycle of P. kellicotti requires two intermediate hosts. The first intermediate host is a snail (e.g., Pomatiopsis lapidaria), and the second is crayfish, principally Cambarus spp. (1). After humans eat raw or undercooked crayfish that harbor P. kellicotti, the parasite penetrates through the intestinal wall into the peritoneal cavity, then through the diaphragm into the pleural space and lungs, and can migrate to other organs, including the brain and skin. Eggs laid in lungs are excreted in sputum, or swallowed and passed with stool. Paragonimus species are endemic in Africa, the Americas, and Asia, but the distribution of P. kellicotti is still being determined (1).

Behavioral factors that led patients in this report to eat raw or undercooked crayfish included alcohol consumption, dares, and demonstration of survival skills. Eight of the nine patients were males. Although crayfish commonly is regarded as food in survival situations, persons who learn or practice survival skills should be cautioned that eating raw or undercooked crayfish carries a risk for paragonimiasis and other diseases (9). Owners and customers of campgrounds and canoe rental businesses should be alerted to thoroughly cook crayfish before eating. The Food and Drug Administration advises cooking shellfish to an internal temperature of 145°F (63°C).*

Early symptoms of paragonimiasis include diarrhea, abdominal pain, and fever, which can occur 2−15 days after eating infected crayfish. Later manifestations include fever, cough, hemoptysis, and chest radiographic abnormalities, which occur when the parasite migrates to lungs. Migration of the parasite to the brain can cause severe complications, including vision loss. Eosinophilia in blood or pleural effusion is a supportive laboratory finding.

Definitive paragonimiasis diagnosis classically is based on viewing Paragonimus eggs or parasites in tissues or bodily fluids by microscope, although the eggs typically are not present until 2−3 months after infection. P. kellicotti eggs were evident in sputum, bronchoalveolar lavage fluid, pleural effusion or biopsies, or lung biopsies in previous reports and in two cases described in this report; the intervals from illness onset to parasitologic diagnosis ranged from 1 month to 5 years (49). Serologic testing is an important tool for diagnosing infections with Paragonimus westermani, a related fluke, but experience with its use in P. kellicotti infection is limited. ELISA is easier to perform, but might not provide positive results until the P. kellicotti infection has progressed 4−24 months (1). CDC's immunoblot assay targets antibodies directed against P. westermani antigens and is highly sensitive (96%) and specific (99%) for P. westermani infection (10). Although existing serologic methods using P. westermani antigens might be less sensitive for early detection of P. kellicotti infection, a positive result is useful in confirming the diagnosis. Immunoblot assay was positive as early as 10 weeks after illness onset in one case described in this report.

Health-care providers should consider paragonimiasis and inquire about ingestion of raw or undercooked crayfish among patients with unexplained fever, cough, eosinophilia, and pleural effusion or other chest radiographic abnormalities. Empiric treatment with praziquantel is warranted for patients with signs and symptoms consistent with paragonimiasis and a history of eating raw or undercooked crayfish, regardless of serology results, particularly with an illness of <3 months duration.

Acknowledgments

This report is based, in part, on contributions by R Tolen, St. Joseph--Buchanan County Health Dept; and A Turner, C Butler, C Hinkle, J Bauer, and L Buchanan, Missouri Dept of Health and Senior Svcs.

References

  1. Procop GW. North American paragonimiasis (caused by Paragonimus kellicotti) in the context of global paragonimiasis. Clin Microbiol Rev 2009;22:415--46.
  2. Lane MA, Barsanti MC, Santos CA, Yeung M, Lubner SJ, Weil GJ. Human paragonimiasis in North America following ingestion of raw crayfish. Clin Infect Dis 2009;49:e55--61.
  3. Pachucki CT, Levandowski RA, Brown VA, Sonnenkalb BH, Vruno MJ. American paragonimiasis treated with praziquantel. N Engl J Med 1984;311:582--3.
  4. Procop GW, Marty AM, Scheck DN, Mease DR, Maw GM. North American paragonimiasis: a case report. Acta Cytol 2000;44:75--80.
  5. DeFrain M, Hooker R. North American paragonimiasis: case report of a severe clinical infection. Chest 2002;121:1368--72.
  6. Castilla EA, Jessen R, Sheck DN, Procop GW. Cavitary mass lesion and recurrent pneumothoraces due to Paragonimus kellicotti infection: North American paragonimiasis. Am J Surg Pathol 2003;27:1157--60.
  7. Madariaga MG, Ruma T, Theis JH. Autochthonous human paragonimiasis in North America. Wilderness Environ Med 2007;18:203--5.
  8. Boe DM, Schwarz MI. A 31-year-old man with chronic cough and hemoptysis. Chest 2007;132:721--6.
  9. Bean NH, Maloney EK, Potter ME, et al. Crayfish: a newly recognized vehicle for vibrio infections. Epidemiol Infect 1998;121:269--73.
  10. Slemenda SB, Maddison SE, Jong EC, Moore DD. Diagnosis of paragonimiasis by immunoblot. Am J Trop Med Hyg 1988;39:469--71.

* Additional guidelines for selecting and serving fresh and frozen seafood safely are available at http://www.fda.gov/food/resourcesforyou/consumers/ucm077331.htm.

Additional information about paragonimiasis is available from CDC at http://www.dpd.cdc.gov/dpdx/html/paragonimiasis.htm.


What is already known on this topic?

Paragonimiasis, a rare parasitic disease in the United States, is caused by Paragonimus trematodes (lung flukes) that infect humans who eat raw or undercooked crayfish or freshwater crabs that harbor the parasites.

What is added by this report?

During July 2006--September 2010, nine cases of paragonimiasis were identified by physicians within 4 months of illness onset in patients who had eaten raw or undercooked crayfish from rivers in Missouri while canoeing or camping.

What are the implications for public health practice?

Efforts are needed to educate the public, especially persons involved in recreation along streams and rivers, to avoid eating uncooked crayfish. Health-care providers should consider paragonimiasis in patients who have eaten raw or undercooked crayfish and have unexplained fever, cough, eosinophilia, and pleural effusion or other chest radiographic abnormalities.


TABLE. Characteristics of nine patients with paragonimiasis --- Missouri, July 2006−September 2010

Patient

Age (yrs)

Sex

Crayfish ingestion

Incubation period (wks)

Onset to diagnosis (wks)

Basis of diagnosis

Date

Source river

1

31

Male

Jun 2006

Jacks Fork and Current

2

3

Clinical history and findings, and response to therapy; IB negative

2

26

Female

Jul 2007

Meramec

2

12

ELISA positive

3

32

Male

Aug 2007

Current

3

12

ELISA positive

4

28

Male

Jun 2009

Huzzah

8

12

ELISA positive; IB negative

5

10

Male

May 2009

Current

16

3

Clinical history and findings, and response to therapy; IB negative

6

20

Male

Jun 2009

Jacks Fork

12

36

IB positive

7

22

Male

Aug 2009

Jacks Fork

6

40

Sputum cytology, IB positive

8

18

Male

Jun 2010

Jacks Fork

3

10

IB positive

9

27

Male

Aug 2009

Little Niangua

12

45

Bronchoalveolar lavage fluid cytology, IB positive

Abbreviations: ELISA = enzyme-linked immunosorbent assay; IB = immunoblot assay.



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