INTRODUCTION
Intestinal capillariasis caused by Capillaria philippinensis, a fish-borne nematode, is an important, emerging zoonotic helminth that has become more prevalent in recent years.1 Fish contract the parasite from water containing the feces of infected birds or humans. Humans are infected by consuming small freshwater fish, either raw or partially cooked. The parasite can reproduce within an individual host, resulting in a large number of worms in the small intestine. Consequently, if the parasite burden increases to massive levels, it can cause disease. This kind of infection was first recorded in the Philippines.2,3 Subsequently, cases have been reported in the Philippines,4 Indonesia,5 the Lao People’s Democratic Republic,6 Japan,7 Taiwan,8 India,9 Iran,10 and Egypt.11,12 Capillariasis has also been found to be carried from an outside source into Europe.5,13,14 In Thailand, the cases have been reported in at least 25 provinces.15–21 This report describes the clinical and epidemiological characteristics of a new group of intestinal capillariasis patients (85 cases) from a hospital-based study in Thailand, and potential clues for diagnosis are discussed. The information presented here could possibly be useful for clinicians who care for patients residing in endemic areas. Infection could be avoided by expanding focus on health communication by responsible units. The public health control strategy is still important to break possible morbidity and mortality due to this helminthic disease in this area.
MATERIALS AND METHODS
Between 2000 and 2014, 85 cases of intestinal capillariasis have been diagnosed at Khon Kaen University’s Srinagarind hospital (male:female = 66:19; mean age ± SD [range] = 43 ± 15 [10–81] years). All of these patients had experienced chronic diarrhea for more than 1 month and were found negative for human immunodeficiency virus. All patients were hospitalized, treated, and prospectively studied. Epidemiological data, clinical diagnosis, and treatment data were collected and analyzed. Diagnoses were confirmed by eggs and/or larvae and/or adult C. philippinensis in the patients’ feces. The stool specimens were examined in the same hospital visit using both direct smear3 and formalin-ethyl acetate concentration methods.22 Although 16 of the 85 cases encountered since 2006 were initially found to be negative for C. philippinensis using the direct smear and formalin-ethyl acetate concentration methods, they were found positive when subjected to serological examination using an immunoblotting technique against Trichinella spiralis larval antigen.23 All patients received mebendazole at 200 mg twice per day for 30 consecutive days or albendazole at 200 mg twice per day for 10 consecutive days.7,24 This retrospective study was approved by the Khon Kaen University Ethics Committee for Human Research (HE 581335).
RESULTS
Over the study period, 85 patients were found to have intestinal capillariasis. Stool examinations found eggs and/or larvae and/or adults of C. philippinensis (Figure 1). All of whom had a history of eating raw or insufficiently cooked freshwater fish or prawns. The provinces from which these cases emerged are shown in Figure 2. Eighty-three of the cases were found in the northeastern region. Macroscopic fecal characteristics, signs, and symptoms are presented in Tables 1–3 and Figures 3 and 4. Infected individuals had mainly experienced chronic diarrhea, borborygmi, abdominal pain, and abdominal bloating. Intestinal pseudo-obstruction was found in three cases (3.5%) after treatment. Macroscopic fecal characteristics took the form of chronic diarrhea with night time defecation. Clinical signs, such as weight loss, muscle weakness, fatigue, dizziness, anorexia, and edema, were frequently present. Laboratory parameters are presented in Table 4. Anemia, low serum levels of potassium, cholesterol, total protein, and albumin, as well as malabsorption of fat were discovered.
The representative morphology of Capillaria philippinensis in fecal specimens. (A) Adult male and female of C. philippinensis indicating stichocyte (Sc), salient vulva (Vu), uterus (UT), larvae (Lv) and eggs (Eg) in the UT (Bar = 100 μm). (B) Adult male C. philippinensis spicule (Sp), extended spicule (Ss), and Sc and (C) magnification of the posterior end of C. philippinensis adult male from (B, rectangular area) (Bar = 100 μm). (D and E) Adult female of C. philippinensis (Bar = 50 μm), (D) indicating Sc, salient Vu, and Eg in the UT. (E) Adult female of C. philippinensis whole body indicating Sc, salient Vu, and Lv. (F) The larva and Eg of C. philippinensis recovered from fresh feces of a patient, the Eg (the upper right figure) are peanut shaped, flattened bipolar plugs sized about 40 μm long and 20 μm wide (Bar = 20 μm).
Citation: The American Journal of Tropical Medicine and Hygiene 98, 1; 10.4269/ajtmh.17-0465
The representative morphology of Capillaria philippinensis in fecal specimens. (A) Adult male and female of C. philippinensis indicating stichocyte (Sc), salient vulva (Vu), uterus (UT), larvae (Lv) and eggs (Eg) in the UT (Bar = 100 μm). (B) Adult male C. philippinensis spicule (Sp), extended spicule (Ss), and Sc and (C) magnification of the posterior end of C. philippinensis adult male from (B, rectangular area) (Bar = 100 μm). (D and E) Adult female of C. philippinensis (Bar = 50 μm), (D) indicating Sc, salient Vu, and Eg in the UT. (E) Adult female of C. philippinensis whole body indicating Sc, salient Vu, and Lv. (F) The larva and Eg of C. philippinensis recovered from fresh feces of a patient, the Eg (the upper right figure) are peanut shaped, flattened bipolar plugs sized about 40 μm long and 20 μm wide (Bar = 20 μm).
Citation: The American Journal of Tropical Medicine and Hygiene 98, 1; 10.4269/ajtmh.17-0465
The representative morphology of Capillaria philippinensis in fecal specimens. (A) Adult male and female of C. philippinensis indicating stichocyte (Sc), salient vulva (Vu), uterus (UT), larvae (Lv) and eggs (Eg) in the UT (Bar = 100 μm). (B) Adult male C. philippinensis spicule (Sp), extended spicule (Ss), and Sc and (C) magnification of the posterior end of C. philippinensis adult male from (B, rectangular area) (Bar = 100 μm). (D and E) Adult female of C. philippinensis (Bar = 50 μm), (D) indicating Sc, salient Vu, and Eg in the UT. (E) Adult female of C. philippinensis whole body indicating Sc, salient Vu, and Lv. (F) The larva and Eg of C. philippinensis recovered from fresh feces of a patient, the Eg (the upper right figure) are peanut shaped, flattened bipolar plugs sized about 40 μm long and 20 μm wide (Bar = 20 μm).
Citation: The American Journal of Tropical Medicine and Hygiene 98, 1; 10.4269/ajtmh.17-0465
Map of Thailand showing provinces in which intestinal capillariasis has been discovered. The figures in parentheses indicate the number of cases.
Citation: The American Journal of Tropical Medicine and Hygiene 98, 1; 10.4269/ajtmh.17-0465
Map of Thailand showing provinces in which intestinal capillariasis has been discovered. The figures in parentheses indicate the number of cases.
Citation: The American Journal of Tropical Medicine and Hygiene 98, 1; 10.4269/ajtmh.17-0465
Map of Thailand showing provinces in which intestinal capillariasis has been discovered. The figures in parentheses indicate the number of cases.
Citation: The American Journal of Tropical Medicine and Hygiene 98, 1; 10.4269/ajtmh.17-0465
Macroscopic fecal characteristic of 85 intestinal capillariasis patients*
| Characters | |
|---|---|
| Chronic diarrhea (> 1 month) | 85 (100%) |
| Abnormal defecation | 85 (100%) |
| Night time diarrhea | 85 (100%) |
| Gross blood | 1 (1.2%) |
| Gross Mucous | 5 (5.9%) |
| Foul smell | 48 (56.5%) |
| Food debris in stool | 61 (71.8%) |
Out of 85 cases, Capillaria phillipinensis eggs were found in 39 cases; C. phillipinensis and Opisthorchis viverrini eggs were found in 22 cases; C. phillipinensis eggs and Strongyloides stercoralis larvae were found in 11 cases; C. phillipinensis eggs, O. viverrini eggs, and S. stercoralis larvae were found in five cases; C. phillipinensis and Echinostome eggs were found in two cases; C. phillipinensis eggs, Echinostome eggs, and S. stercoralis larvae were found in two cases; C. phillipinensis, O. viverrini, and minute intestinal flukes eggs were found in one case; C. phillipinensis eggs, S. stercoralis larvae, and hook worm eggs were found in one case; C. phillipinensis and Taenia eggs were found in one case; C. phillipinensis eggs, O. viverrini eggs, Taenia eggs, and S. stercoralis larvae were found in one case.
Abdominal manifestations of 85 intestinal capillariasis patients
| Abdominal gurgling | 83 (97.6%) |
| Abdominal pain | 51 (60%) |
| Abdominal discomfort | 58 (68.2%) |
| Burning abdomen | 17 (20%) |
| Abdominal bloating | 69 (81.2%) |
Clinical signs of 85 intestinal capillariasis
| Weight loss | 84 (98.9%) |
| Appetite | 23 (27%) |
| Anorexia | 52 (61.2%) |
| Nausea | 29 (34.1%) |
| Vomiting | 19 (22.3%) |
| Fatigue | 69 (81.1%) |
| Muscle weakness | 54 (63.5%) |
| Dizziness | 44 (51.7%) |
| Hypoesthesia | 29 (34.1%) |
| Edema | 60 (70.5%) |
| Fever | 9 (10.5%) |
Clinical image of malnourish patient (no. 1) suffered from chronic intestinal capillariasis showing cachexia with poor skin turgor (A) before treatment, (B) 74 days after treatment, (C) 140 days after treatment. This figure appears in color at www.ajtmh.org.
Citation: The American Journal of Tropical Medicine and Hygiene 98, 1; 10.4269/ajtmh.17-0465
Clinical image of malnourish patient (no. 1) suffered from chronic intestinal capillariasis showing cachexia with poor skin turgor (A) before treatment, (B) 74 days after treatment, (C) 140 days after treatment. This figure appears in color at www.ajtmh.org.
Citation: The American Journal of Tropical Medicine and Hygiene 98, 1; 10.4269/ajtmh.17-0465
Clinical image of malnourish patient (no. 1) suffered from chronic intestinal capillariasis showing cachexia with poor skin turgor (A) before treatment, (B) 74 days after treatment, (C) 140 days after treatment. This figure appears in color at www.ajtmh.org.
Citation: The American Journal of Tropical Medicine and Hygiene 98, 1; 10.4269/ajtmh.17-0465
Clinical image of chronic intestinal capillariasis patient (no. 2) suffered from leg pain due to deep vein thrombosis caused by stagnation. (A) Showing grade 4+ of pitting edema of both legs. (B) Sixteen days after treatment. This figure appears in color at www.ajtmh.org.
Citation: The American Journal of Tropical Medicine and Hygiene 98, 1; 10.4269/ajtmh.17-0465
Clinical image of chronic intestinal capillariasis patient (no. 2) suffered from leg pain due to deep vein thrombosis caused by stagnation. (A) Showing grade 4+ of pitting edema of both legs. (B) Sixteen days after treatment. This figure appears in color at www.ajtmh.org.
Citation: The American Journal of Tropical Medicine and Hygiene 98, 1; 10.4269/ajtmh.17-0465
Clinical image of chronic intestinal capillariasis patient (no. 2) suffered from leg pain due to deep vein thrombosis caused by stagnation. (A) Showing grade 4+ of pitting edema of both legs. (B) Sixteen days after treatment. This figure appears in color at www.ajtmh.org.
Citation: The American Journal of Tropical Medicine and Hygiene 98, 1; 10.4269/ajtmh.17-0465
Laboratory parameters of 85 intestinal capillariasis
| Blood | |
| Hemoglobin (gm/dL) | 12.2 ± 2.6 (4–18) |
| Hematocrit (%) | 37.1 ± 7.7 (12–54) |
| WBC/mm3 | 8,750 ± 3,901 (4,460–32,300) |
| Eosinophilia (%) | 4.2 ± 3.7 (0–15) |
| Absolute eosinophil count | 333.8 ± 307.2 (0–1,650) |
| Potassium (mEq/L) | 3.4 ± 0.7 (1.5–4.9) |
| Cholesterol (mg/dL) | 118.9 ± 42.3 (51–291) |
| Total protein (gm/dL) | 5.2 ± 1.4 (2.9–7.9) |
| Albumin (gm/dL) | 1.7 ± 0.8 (0.6–4.6) |
| Globulin (gm/dL) | 3.4 ± 1.0 (1.4–5.7) |
| Stool | |
| Found red blood cells | 4 (4.7%) |
| Positive occult blood | 37 (43.5%) |
| Positive fat test | 22 (25.9%) |
| Positive Charcot–Leyden crystals | 14 (16.4%) |
WBC = white blood cell.
Fecal examination revealed C. philippinensis in 69 of the 85 patients (81.2%) before treatment with helminthic drugs. Since 2006, some cases (N = 16) have been diagnosed as suspected intestinal capillariasis and referred from community and provincial hospitals to the Srinagarind Hospital, the university hospital at Khon Kaen University. In these cases, all stool samples were previously found to be negative for C. philippinensis using the direct smear method. Then, the patients had been investigated using several other diagnostic methods (i.e., routine laboratory tests, liver function tests, thyroid function tests, antihuman immunodeficiency virus tests, long gastrointestinal studies, tests for tumor makers for differential gastrointestinal cancer, etc.). All patients presented with the following clinical symptoms: chronic diarrhea, abnormal defecation, nighttime diarrhea, abdominal gurgling for more than 1 month, abdominal pain and bloating, weight loss, and hypoalbuminemia. The patients were prone to eating raw or insufficiently cooked scaled freshwater fish. Repeated stool diagnosis using the formalin ethyl acetate concentration method was negative in all cases. All patient sera were found positive for the IgG antibody using the immunoblotting technique (Figure 5). One day after administration of 400 mg of albendazole, eggs and/or larvae and/or adult of C. philippinensis were found in all fecal samples examined using the direct smear method (Figure 1). All 16 patients were followed treatment with albendazole at 200 mg twice per day until 10 consecutive days. The patients were cured, and no parasites were found in their feces within 2 weeks to 2 months after treatment. The stool consistency changed from watery to form stool within 7 days. Follow-ups revealed no cases of relapse.
The representative patterns of the immunoblot analysis reacted with individual sera from a pooled positive intestinal capillariasis reference (A), a pooled negative healthy control reference (B), and intestinal capillariasis cases (C and D). The numbers on the left and right sides indicate the molecular masses (kDa). The procedure was conducted as previously described by Intapan and others23 and the reacted 54, 40.5, and 36.5 kDa bands were used as diagnostic band pattern for intestinal capillariasis.
Citation: The American Journal of Tropical Medicine and Hygiene 98, 1; 10.4269/ajtmh.17-0465
The representative patterns of the immunoblot analysis reacted with individual sera from a pooled positive intestinal capillariasis reference (A), a pooled negative healthy control reference (B), and intestinal capillariasis cases (C and D). The numbers on the left and right sides indicate the molecular masses (kDa). The procedure was conducted as previously described by Intapan and others23 and the reacted 54, 40.5, and 36.5 kDa bands were used as diagnostic band pattern for intestinal capillariasis.
Citation: The American Journal of Tropical Medicine and Hygiene 98, 1; 10.4269/ajtmh.17-0465
The representative patterns of the immunoblot analysis reacted with individual sera from a pooled positive intestinal capillariasis reference (A), a pooled negative healthy control reference (B), and intestinal capillariasis cases (C and D). The numbers on the left and right sides indicate the molecular masses (kDa). The procedure was conducted as previously described by Intapan and others23 and the reacted 54, 40.5, and 36.5 kDa bands were used as diagnostic band pattern for intestinal capillariasis.
Citation: The American Journal of Tropical Medicine and Hygiene 98, 1; 10.4269/ajtmh.17-0465
DISCUSSION
Food-borne parasites are an emerging public health problem, particularly in Southeast Asian countries25 including Thailand. Importantly, it is possible that C. philippinensis may be the cause of symptoms in many cases, especially in patients who present with chronic diarrhea resulting in protein-calorie malnutrition or electrolyte disturbances. This helminthic infection is extraordinary because of its potential severe, or even fatal, consequences in cases of misdiagnosis or improper treatment.7 Infection with intestinal capillariasis should be considered in cases of differential diagnosis with malabsorbtion syndrome.26 More than 2,000 cases resulting in almost 200 deaths have been recorded worldwide, and the cases were mostly from Asia.24 In Thailand, the first case of intestinal capillariasis was reported in a Thai girl from Samut Pragran province in the central region of the country.15 There have subsequently been sporadic cases reported from different parts of the country. The first outbreak in Thailand was found in Sisaket Province in the northeast, in which there were 20 cases and nine deaths reported.27 A study published in 1983 reported that a total of 100 cases of C. philippinensis infection were found in hospitals in the same area between 1979 and 1981 of which 15 cases were fatal.28 Seventy-three percent (73/100) of the patients were aged between 20 and 49 years, and the disease was approximately 2.3 times more common in males.28 In the same year, three infected patients who lived in the northeast (Nakhon Ratchasima, Sisaket, and Khon Kaen provinces) were reported at Bamrasnaradura hospital in central Thailand.29 From 1983 to 1991, 17 cases were reported at Khon Kaen University’s Srinagarind Hospital in Khon Kaen province with an age range of 21–69 years.19 Sporadic cases were also reported in the northern (i.e., Prayoa, Phetchabun and Chiang Mai provinces)18,30 and central (i.e., Saraburi and Prachinburi provinces)16,31,32 regions. In one case, C. philippinensis eggs and adult in jejunal content were found using enteroscopy after repeated stool examination.20 In another study in Thailand, Saichua et al.21 reviewed a total of 82 cases from 1994 to 2006.
Here, we report 85 new cases of intestinal capillariasis in Thailand from a hospital-based study. It is evident that the disease is not rare in Thailand. The clinical manifestations of intestinal capillariasis commonly present are chronic watery diarrhea, abdominal pain, borborygmus, weight loss, muscle wasting, edema, severe-losing enteropathy, and malabsorption of fat, as well as low serum potassium, cholesterol, total protein, and albumin levels.7,15 Interestingly, in the present report, we found that 3.5% of patients showed intestinal pseudo-obstruction after treatment, as has also been reported in one previous case.31 Clinicians who work in endemic areas should be aware that this symptom can be present. The pathological patterns possibly result from a proteolytic secretion of C. philippinensis or direct penetration of the worm, which cause cellular injury and dysfunction.7 Another possible mechanism may be atrophy or hypotrophy of the small intestinal muscle with poor contraction from malnutrition (a consequence of chronic diarrhea with malnutrition).31
Several kinds of fresh water fish, such as Cyprinus carpio (Pla nui), Puntius gonionotus (Pla Tapien Khao), and Rasbora borapelensis (Pla Sew), which are commonly consumed raw in Thailand, have been reported to be an experimental intermediate host of C. philippinensis.33 People in rural areas of Thailand still consume traditional dishes containing raw fish or prawns, such as koi pla or lap pla (minced fish with lemon juice and spices) and koi kung (raw prawns with lemon juice and spices). The consumption of raw or insufficiently cooked fresh water fish or prawns provides an extremely effective means of C. philippinensis transmission.
Presently, intestinal capillariasis remains problematic in clinical practice.34 First, diagnosis is difficult due to atypical clinical symptoms and misdiagnosis as diarrhea caused by gastrointestinal cancer, human immunodeficiency virus infection, or hyperthyroidism. The disease may also be unrecognized by clinicians if it emerges in a nonendemic area. Second, stool examination exhibits low sensitivity, as the parasitic eggs and/or larvae are purged irregularly. Invasive and high-cost diagnostic tools can assist clinicians (i.e., endoscopy and imaging).34,35 Here, we revealed another highly effective tool for diagnosis. Albendazole treatment could increase the sensitivity of stool examination methods for diagnosis of intestinal capillariasis. Interestingly, this study revealed that approximately 16 (18.8%) samples which were found to be negative using stool examinations before helminthic drug intake were found to be positive after albendazole intake.
In conclusion, the potential clues for diagnosis of intestinal capillariasis are clinical manifestation of chronic diarrhea and borborygmi, history of eating raw fish or prawns, and positive serological test and stool examinations. In cases with negative stool-examination results but positive serological results, repeated stool examination is required within 1 day after anthelminthic drug treatment on confirmation of diagnosis.
Acknowledgments:
We thank the English Consultation Clinic at the Khon Kaen University Faculty of Medicine Research Affairs Division for their assistance.
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