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| ABSTRACT |
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| INTRODUCTION |
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Since the first case in Taiwan was reported in 1983,4,5 subsequent cases have continued to appear. However, there was no detailed and complete investigation has yet been conducted to study the disease in Taiwan.6 Geographically, Taiwan is the closest area to the Philippines. It is also a key rest stop on the north-south migratory routes for many fish-feeding migratory birds, which are thought to be the major carriers of Capillaria philippinensis.7 In addition, there are also more than 200,000 foreign laborers living in Taiwan who originally came from the major epidemic areas in any given year, and it could potentially facilitate the spread of this disease.8,9 Therefore, there is an urgent need to understand how this disease progresses in Taiwan.
| MATERIALS AND METHODS |
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Since the 30 cases were diagnosed at the 10 medical institutes, crossing various locations in Taiwan and over a span of 21 years, the collection of patient information presented great challenges. This study reviewed all the cases, including analyzing factors such as gender, age, ethnic group, geography, diet, routes of infection, travel history, clinical symptoms, and laboratory results. We also have applied several diagnostic procedures, treatments, and prognoses. The complete data were compared with other countries on disease progression.
| RESULTS |
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As to their travel histories, three patients had visited Thailand, one patient had traveled to the Philippines, and the other patient was a crewmember of a ship and he had visited many countries including the Philippines and Thailand (Table 1
). All cases had developed clinical symptoms of Capillaria philippinensis, including intermittent abdominal pain, borborygmi, diarrhea, and weight loss as well as various degrees of painless lower legs edema.
With regard to the laboratory results, the results of complete blood cell examinations revealed that eight cases were anemic (hemoglobin level
10 mg/dL). Eleven cases had an eosinophil ratio
5%. The biochemical texts reveals that the albumin levels ranged from 0.5 to 3.0 mg/dL with 19 cases showing values
2.0 mg/dL and 5 cases showing values
1.0 mg/dL.
Twenty-one diagnoses were confirmed, based on the presence of Capillaria philippinensis eggs in the feces; whereas nine patients were diagnosed by histopathological findings of eggs, larvae, and adult Capillaria philippinensis. Of the latter nine cases, biopsy specimens were obtained by segmental resection of distal ileum in two cases. In other four cases, specimens were obtained by panendoscopic examination, with two taken from the duodenum and the other two taken from the proximal jejunum. In the remaining three cases, specimens were obtained from the distal ileum by colonofibroscopic examination. Of the remaining patient, the stool examination and histologic examination all confirmed a positive result of Capillaria philippinensis infection.
The progression of the disease from symptom commencement to a confirmed diagnosis ranges from 2 weeks to 6 years, with an average of 8.1 months (see Table 1
). Of the 30 cases, 8 patients were not diagnosed until more than a year after the onset of symptoms. Hospitals with greater diagnostic experience were Mackay Memorial Hospital-Taitung Branch, Hualian Buddhist Tzu-Chi Hospital, and Kaohsiung Medical University Hospital, with each having made six to seven correct diagnoses. The first diagnosed case in Taiwan was case no. 1,46 whereas case no. 5 was the first case published in an English paper.10
With regard to the treatments, cases no.1 and no. 6 were prescribed 400 mg/day albendazole for 3 weeks, whereas the other 28 cases were all given 400 mg/day mebendazole for 34 weeks. All cases recovered with no deaths or recurrences.
| DISCUSSION |
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What is unusual about the 30 Taiwanese cases is that there were 21 aboriginals. Taiwanese aboriginal population accounts for a mere 2% of total population in Taiwan. The population of Taiwan was 22.5 million in 2003. The 21 infected aboriginals all belonged to either Ami or Paiwan. The two tribes mainly inhabit in Taitung and Hualian County. Location-wise, Taitung County is the least-populated county on the main island of Taiwan but had as many as 12 cases, including two cases from the same family (cases no. 6 and no. 9).
Of the six cases from Kaohsiung County, four patients were Hakkanese. Minnanese and Hakkanese are two of the major ethnic groups in Taiwan. In comparison with aboriginal tribes who had been residing in Taiwan for more than 400 years, Minnanese and Hakkanese are identified as Taiwanese and they were originally immigrated from Southeastern provinces of China including Fujian, Jiangxi, and Guangdong province in the past 300 years. Generally speaking, Hakkanese resident in the mountainside areas, and their living and dietary habits are different with aboriginal tribes in Taiwan. In this study, the very first case in Taiwan was from Meinong in Kaohsiung County, and the second case in the same location was found 16 years later. Both cases were Hakkanese. They were also the only two cases from a mountainside population.
Geographically, Taiwan is closer to Luzon of the Philippines than any other countries. They are separated only by the Bashi Strait. The distance between Taitung County in Taiwan and Ilocos Norte and Ilocos Sur in the northwestern Luzon of the Philippines is less than 500 km. We found that the first Philippine case of intestinal capillariasis and the very first outbreak in Taiwan were respectively reported.17,18 The geographical proximity may potentially allow fish-feeding migratory birds bringing Capillaria philippinensis to Taiwan. In Taiwan, capillaria-prevalent areas were found to be located in Taitung, Hualian, and Kaohsiung counties, despite single episodes taking place in each of Keelung, Taipei, and Taipei City from northern Taiwan. All three northern patients belonged to the Ami tribe, who had originally lived in Taitung County but had immigrated to the northern cities for the reasons of marriage (the Keelung County case) or work (the Taipei City and Taipei County cases). They often returned to visit their hometowns in Taitung County on a regular basis, so they would have been infected in Taitung County. Thus, northern Taiwan may not be a prevalence area yet. The high-risk groups may include the Ami tribe in Taitung and Hualian counties, the Paiwan tribe in Taitung County, and the Hakkanese in Kaohsiung County.
Case no. 10 began to show clinical symptoms of borborygmi, abdominal pains, and watery diarrhea 2 months after a trip to Thailand, so he would have been infected in Thailand. Case no. 11 was the member of a ship crew who had traveled to many countries including the Philippines and Thailand, so the place where he had contracted with the disease is still unknown. Both cases might have been infected outside of Taiwan.
Accordingly, all cases had shown clinical symptoms of transient abdominal crampy pain, borborygmi, diarrhea, and weight loss. Some patients were found having various degrees of painless lower leg edema. Among the seven cases with chronic infection lasting more than 1 year, four cases had shown symptoms of diarrhea and constipation, which were difficult to diagnose differentially. When a diagnosis was finally made, five cases already showed clinical symptoms of septic shock. The finding of hypoalbuminemia was of significance.
In the literature, the majority of the patients had a history of consuming raw or uncooked fishes, and this is a crucial factor of intestinal Capillaria infection. However, nearly half of the Taiwanese patients (14 of 30 cases) denied having consumed any raw or undercooked fishes. We propose that the infection may occur when the ingested food is contaminated by uncooked visceral contents of infested fish. Therefore, whether patients have consumed raw or uncooked fish ought to be taken into consideration but should not be the basis for ruling out the possibility of intestinal capillariasis.
It is found that the aboriginal elderly in Taiwan often prefer traditional food named Chou-Bao, which is made by soaking small raw fish in homemade fermented millet. The raw fish could facilitate the transmission of Capillaria philippinensis. Unfortunately, we could not verify the number of cases that resulted from consuming Chou-Bao, due to a lack of information from patient records. It is noted that the transmission of Capillaria philippinensis in the Philippines is considered to be related to a traditional dish named Kinilaw (or Kilawin), which is primarily made of raw pilchard fish. Due to the fact that the Taiwanese cases have been sporadic, it has been difficult to study the route of transmission. Hwang examined fish from fish markets in Kaohsiuing and Taitung but found no presence of Capillaria philippinensis.5
Dronda and others19 found that a diagnosis of intestinal capillariasis in the nonepidemic areas is more likely to be delayed, so they emphasized that clinicians in those areas should remain highly alert for any sign of disease outbreak. Reports of delayed diagnoses for more than a year have been found in Japan,20 Korea,21 Egypt,16 and India.22 Among the 30 Taiwanese cases, 8 patients were not confirmed with infection until 1 year later. It is noticeable that five of 8 delayed cases were among the first 8 cases. The physicians and medical technologists in clinical practice should be more trained in diagnosing this disease.
The simplest way to diagnose intestinal capillariasis is by stool examination. Capillaria are closely related to Trichuris and Trichinella species. The eggs of Trichuris trichiura (average size, 50 x 22 µm) and C. philippinensis (average size, 36 x 19 to 45 x 21 µm) are similar although differentiable, and some individuals can be infected with both parasites. If eggs, larvae, or adult Capillaria philippinensis are not found in the stool samples, a panendoscopic examination or surgical operation is then required to obtain biopsy specimens for a histopathological examination. Four Taiwanese cases were diagnosed based on histopathological findings of biopsy specimens from the duodenum (two cases) and proximal jejunum (two cases) of patients by panendoscopic examination. Kang22 and Wongsawasdi and colleagues23 had cases definitively diagnosed based on histopathological findings on panendoscopic jejunal biopsy specimens. By the same procedure, two Taiwanese cases were diagnosed based on duodenal biopsy specimens and another two Taiwanese cases were diagnosed based on jejunal biopsy specimens. In Mukai and others24 and Hong and others,25 definitive diagnoses were made based on colonofiberoscopic ileal biopsy. Three Taiwanese cases were also diagnosed by the same procedure. Lee and others21 reported definitive diagnoses based on histopathological findings from diagnostic surgical exploration. El-Dib16 addressed that one Egyptian case was found by abdominal laparoscopy for diagnostic purposes. For cases no. 2 and no. 7 in Taiwan, a definitive diagnosis was made by histopathological findings after showing clinical symptoms of peritonitis, and it was complicated with septic shock (case no. 2) and intestinal obstruction (case no. 7). Consequently, they had to undergo surgery for distal ileum removal.
Our study reveals some crucial results. The diagnosis of intestinal capillariasis is commonly delayed, and it may sometimes require biopsy examinations. The areas where Capillaria philippinensis has spread, the number of afflicted countries, and the infected cases may far exceed what we know so far. Taiwan has become a capillaria-prevalent area after the Philippines, Thailand, and Egypt, with infections mainly occurring in the aboriginal population in eastern Taiwan. The fact that the Taiwanese aboriginal tribes are closely related to the Philippines aboriginals in origin might play a role in the high infection rate. Future research focusing on the routes of transmission of Capillaria philippinensis in Taiwan will be necessary.
Received March 5, 2004. Accepted for publication February 25, 2005.
* Address correspondence to Wen-Cheng Chung, Department of Parasitology, Taipei Medical University, Taipei, Taiwan. E-mail: hsuehu{at}nfa.gov.tw ![]()
Authors addresses: Li-Hua Lu, No. 699, Section 1, Chung-Chi Road, Wuchi, Taichung, Taiwan, ROC 43503. Mau-Roung Lin, Jean-Dean Liu, and Wen-Cheng Chung, No. 250, Wu-Shing Street, Taipei, Taiwan, ROC 11031, E-mail: hsuehu{at}nfa.gov.tw. Wai-Mau Choi, No. 690, Section 2, Guang-Fu Road, Hsinchu City, Taiwan, ROC 30071. Kao-Pin Hwang, No. 123, Ta-Pei Road, Niao-Sung, Kaohsiung, Taiwan, ROC 83301. Yung-Hsiang Hsu, No. 707, Section 3, Chung-Yang Road, Hualien, Taiwan, ROC 97002. Ming-Jong Bair, No. 1, Lane 303, Chang-Sha Street, Taitung, Taiwan, ROC 95054. Tsang-En Wang and Tsang-Pai Liu, No. 92, Section 2, Chung-Shan North Road, Taipei, ROC 10449.
Reprint requests: Wen-Cheng Chung, Department of Parasitology, Taipei Medical University, No. 250 Wu-Shing St., Taipei 110, Taiwan, ROC, Telephone: 886-2-2377-2843, Fax: 886-2-2377-2843, E-mail: wcchung{at}tmu.edu.tw.
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