# Epidemiological and Clinical Parameters Features of Patients with Clonorchiasis in the Geum River Basin, Republic of Korea

Authors: Hee-Eun Shin; Myoung-Ro Lee; Jung-Won Ju; Byong-Suk Jeong; Mi-Yeoun Park; Keoung-Sook Lee; Shin-Hyeong Cho
Journal: Interdisciplinary Perspectives on Infectious Diseases
 (2017)

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## Abstract

This study was conducted to evaluate the infection rates ofClonorchis sinensis and laboratory findings in infected people. The 3,167 fecal samples, from nine villages in Okcheon-gun, were examined.


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## Body

## 1. Introduction

Clonorchis sinensis is endemic in East Asian countries including China, Japan, Taiwan, Vietnam, and Korea [1, 2]. Worldwide, it is currently estimated that 15–20 million people are infected and 1.5–2.0 million people show symptoms or complications [3–5]. Although a rapid decrease in the overall prevalence of intestinal parasites has been observed in Korea, the prevalence ofC. sinensis has remained high in riverside areas [6]. Nationwide surveys reportedC. sinensis infection rates of 4.6% in 1971, 1.8% in 1976, 2.6% in 1981, 2.7% in 1986, 2.2% in 1992, 1.4% in 1997, 2.4% in 2004, and 1.9% in 2012 [7, 8]. Infection with the snail-transmitted trematode has been particularly frequent along several major Korean rivers, including the Geum, Nakdong, and Seomjin [9]. The rates ofC. sinensis infection observed in the Geum River basin were 12.0% in 1981 [9], 4.6% in 2006 [10], and 3.1% in 2007 [11].Freshwater fish is well-known as the major second intermediate host forC. sinensis, which can infect humans who ingest infected fish that is raw or undercooked [10]. The prevalence of infection is higher in males and increases with age in Korea [12]. Clonorchiasis patients suffer from symptoms such as epigastric pain, abdominal tenderness, fever, jaundice, and diarrhea [3]. Moreover, chronic infection withC. sinensis may cause more severe diseases such as cholangiocarcinoma [13]. The presence of the worms in the walls of the smaller bile ducts causes necrosis, inflammation, and biliary stricture through several mechanisms [14].Early diagnosis and treatment are very important in preventing complications from clonorchiasis. The diagnosis depends mostly on detection of eggs in a patient’s feces by either the formalin-ether concentration technique (FECT) or the Kato-Katz thick smear method [15]. Although molecular diagnostic techniques have been developed, early diagnosis of clonorchiasis remains difficult because subclinical infection withC. sinensis often occurs without obvious signs. Laboratory blood tests to look for changes in overall health are often part of a regular medical checkup. Individuals with abnormal blood test results should be further examined with a test suitable for early diagnosis. Previous studies reported thatC. sinensis infected groups had differences in their serum alkaline phosphatase (ALP), aspartate aminotransferase (AST), alanine aminotransferase (ALT), γ-glutamyltranspeptidase (γ-GTP), and alpha-fetoprotein (AFP) test results and presented with peripheral eosinophilia [2, 16]. However, there is no diagnostic set of results from common blood and biochemical tests, except for those tests that can indicate compromised liver function.In this study, we investigated sociodemographic and behavioral risk factors forC. sinensis infection in inhabitants living near the Geum River. We additionally evaluated the results of subjects’ laboratory blood tests in order to look for possible early diagnostic indicators of clonorchiasis.


## 2. Materials and Methods

### 2.1. Study Site

The study was undertaken during the period of January to December 2013. A total of 3,167 inhabitants (1,227 males and 1,940 females) from nine villages in the Okcheon-gun County of the Chungcheongbuk-do Province of Korea were examined (Figure1). The ages of the inhabitants ranged from 9 to 99 years, and the average age was 68.4 years (Table 1).Table 1
Distribution of the participants.
Location
Gender
Number of inhabitants examined
Age
0–19
20–29
30–39
40–49
50–59
60–69
70–79
80≤
Okcheon-eup
Male
213
4
3
8
13
28
42
90
25
Female
389
2
1
5
8
36
88
183
67
Total
602
6
4
13
21
64
130
273
92
Annae-myeon
Male
136
0
0
1
9
23
42
48
13
Female
188
2
0
3
8
31
44
82
18
Total
324
2
0
4
17
54
86
130
31
Annam-myeon
Male
76
0
0
0
2
9
12
39
14
Female
145
0
0
1
1
14
27
78
24
Total
221
0
0
1
3
23
39
117
38
Cheongsan-myeon
Male
162
0
0
1
6
25
50
70
10
Female
273
0
0
3
6
41
71
119
33
Total
435
0
0
4
12
66
121
189
43
Cheongseong-myeon
Male
165
0
0
2
6
18
41
83
15
Female
236
0
0
0
4
28
58
103
43
Total
401
0
0
2
10
46
99
186
58
Dongi-Myeon
Male
146
0
1
6
11
22
29
61
16
Female
190
0
1
3
13
25
46
80
22
Total
336
0
2
9
24
47
75
141
38
Gunbuk-Myeon
Male
125
1
2
6
9
18
24
53
12
Female
175
2
3
2
11
15
40
79
23
Total
300
3
5
8
20
33
64
132
35
Gunseo-myeon
Male
79
0
0
1
3
11
22
33
9
Female
137
0
0
2
3
17
26
65
24
Total
216
0
0
3
6
28
48
98
33
Iwon-myeon
Male
125
2
1
4
4
24
28
48
14
Female
207
1
0
4
5
28
58
91
20
Total
332
3
1
8
9
52
86
139
34
Total
Male
1,227
7
7
29
63
178
290
525
128
Female
1,940
7
5
23
59
235
458
880
273
Total
3,167
14
12
52
122
413
748
1,405
401Figure 1
Geographic locations of the surveyed areas. Map shows (a) the Korean Peninsula and (b) the Okcheon-gun County of the Chungcheongbuk-do Province of Korea. The Geum River is shown in blue. Individual villages are shown on the map as follows: ① Okcheon-eup, ② Annae-myeon, ③ Annam-myeon, ④ Cheongsan-myeon, ⑤ Cheongseong-myeon, ⑥ Dongi-myeon, ⑦ Gunbuk-myeon, ⑧ Gunseo-myeon, and ⑨ Iwon-myeon.


### 2.2. Fecal Examination

Stool specimens were collected in plastic stool containers and transferred to the laboratory of the Korea National Research Institute of Health during the period from February through May 2013. All participants were recruited for stool collection by a random household sampling method. Stool specimens were examined using the formalin-ether concentration technique (FECT) to assess the prevalence of parasitic infection, and the eggs per gram (EPG) were calculated using Stoll’s egg counting method. Patients who tested positive for eggs (egg-positive) were considered infected, and those who tested negative for eggs (egg-negative) were considered uninfected.


### 2.3. Laboratory Examination

Blood samples (5 mL per individual) were collected from 97 participants using both 2-[2-[bis(carboxymethyl)amino]ethyl-(carboxymethyl)amino]acetic acid (EDTA) coated tubes and serum-separating tubes (SSTs). Samples were examined using 15 hematological parameters: hemoglobin (Hb), hematocrit (Hct), red blood cell count (RBC), white blood cell count (WBC), platelet distribution width (PDW), platelet counts, mean corpuscular volume (MCV), mean corpuscular hemoglobin (MCH), mean corpuscular hemoglobin concentration (MCHC), percent eosinophils (EOS), percent basophils, percent monocytes, percent neutrophils (NEUT), percent lymphocytes, and mean plasma volume (MPV). In addition, we analyzed 18 biochemical parameters using an automatic blood analyzer (Olympus AU 400): AST, ALT, lactate dehydrogenase (LDH), ALP, creatine phosphokinase (CPK),γ-GTP, total protein, albumin, total cholesterol, high-density lipoprotein (HDL), low-density lipoprotein (LDL), triglycerides (TG), total bilirubin, direct bilirubin, blood urea nitrogen (BUN), creatinine, uric acid (UA), and random blood sugar (RBS).


### 2.4. Questionnaire Survey

We questioned all participants to identify correlations betweenC. sinensis infection and known risk factors. The questionnaire was given to all participants verbally during an interview by a trained worker in a public health center. The following general information was collected: participant gender, age, current residence, and whether they consumed alcohol. We also asked questions about clonorchiasis risk-related behaviors: Did the patient have a history of eating raw freshwater fish, and if so when, where was the fish from, and what species of fish was consumed? Did the patient have a previous history ofC. sinensis infection, or of bile duct or liver diseases, or of cooking freshwater fish? Had the patient ever experienced symptoms such as anorexia, indigestion, jaundice, abdominal discomfort, or anemia?


### 2.5. Statistical Analysis

Statistical analyses were performed using the SPSS 18.0 program (ver. 18.0; Chicago, Illinois, USA). Only participants with complete records were included in the final analysis. A chi-square test and independentt-test were used to check for statistically significant differences between questionnaire answers from the infected versus noninfected groups. In addition, we confirmed that the differences between the groups’ laboratory results for peripheral blood cells were statistically significant, by an independent t-test. Differences were considered statistically significant when p values were less than 0.05 (p<0.05). Finally, a Pearson correlational analysis was performed to compare EPG to each of the laboratory test results for infected patients.


### 2.6. Ethical Aspects

The study protocol was approved by the Ethics Committee of the Korea National Research Institute of Health, Centers for Disease Control & Prevention, Republic of Korea (2013-06EXP-04-R). All participants and local health center workers were informed of the study’s purpose and procedures. Written informed consent for the research was obtained from all participants prior to enrolment. The participants found to have intestinal parasitic infections were treated with praziquantel (2-(cyclohexanecarbonyl)-3,6,7,11b-tetrahydro-1H-pyrazino[2,1-a]isoquinolin-4-one) and other appropriate antiparasitic drugs at the end of the survey.


## 2.1. Study Site

The study was undertaken during the period of January to December 2013. A total of 3,167 inhabitants (1,227 males and 1,940 females) from nine villages in the Okcheon-gun County of the Chungcheongbuk-do Province of Korea were examined (Figure1). The ages of the inhabitants ranged from 9 to 99 years, and the average age was 68.4 years (Table 1).Table 1
Distribution of the participants.
Location
Gender
Number of inhabitants examined
Age
0–19
20–29
30–39
40–49
50–59
60–69
70–79
80≤
Okcheon-eup
Male
213
4
3
8
13
28
42
90
25
Female
389
2
1
5
8
36
88
183
67
Total
602
6
4
13
21
64
130
273
92
Annae-myeon
Male
136
0
0
1
9
23
42
48
13
Female
188
2
0
3
8
31
44
82
18
Total
324
2
0
4
17
54
86
130
31
Annam-myeon
Male
76
0
0
0
2
9
12
39
14
Female
145
0
0
1
1
14
27
78
24
Total
221
0
0
1
3
23
39
117
38
Cheongsan-myeon
Male
162
0
0
1
6
25
50
70
10
Female
273
0
0
3
6
41
71
119
33
Total
435
0
0
4
12
66
121
189
43
Cheongseong-myeon
Male
165
0
0
2
6
18
41
83
15
Female
236
0
0
0
4
28
58
103
43
Total
401
0
0
2
10
46
99
186
58
Dongi-Myeon
Male
146
0
1
6
11
22
29
61
16
Female
190
0
1
3
13
25
46
80
22
Total
336
0
2
9
24
47
75
141
38
Gunbuk-Myeon
Male
125
1
2
6
9
18
24
53
12
Female
175
2
3
2
11
15
40
79
23
Total
300
3
5
8
20
33
64
132
35
Gunseo-myeon
Male
79
0
0
1
3
11
22
33
9
Female
137
0
0
2
3
17
26
65
24
Total
216
0
0
3
6
28
48
98
33
Iwon-myeon
Male
125
2
1
4
4
24
28
48
14
Female
207
1
0
4
5
28
58
91
20
Total
332
3
1
8
9
52
86
139
34
Total
Male
1,227
7
7
29
63
178
290
525
128
Female
1,940
7
5
23
59
235
458
880
273
Total
3,167
14
12
52
122
413
748
1,405
401Figure 1
Geographic locations of the surveyed areas. Map shows (a) the Korean Peninsula and (b) the Okcheon-gun County of the Chungcheongbuk-do Province of Korea. The Geum River is shown in blue. Individual villages are shown on the map as follows: ① Okcheon-eup, ② Annae-myeon, ③ Annam-myeon, ④ Cheongsan-myeon, ⑤ Cheongseong-myeon, ⑥ Dongi-myeon, ⑦ Gunbuk-myeon, ⑧ Gunseo-myeon, and ⑨ Iwon-myeon.


## 2.2. Fecal Examination

Stool specimens were collected in plastic stool containers and transferred to the laboratory of the Korea National Research Institute of Health during the period from February through May 2013. All participants were recruited for stool collection by a random household sampling method. Stool specimens were examined using the formalin-ether concentration technique (FECT) to assess the prevalence of parasitic infection, and the eggs per gram (EPG) were calculated using Stoll’s egg counting method. Patients who tested positive for eggs (egg-positive) were considered infected, and those who tested negative for eggs (egg-negative) were considered uninfected.


## 2.3. Laboratory Examination

Blood samples (5 mL per individual) were collected from 97 participants using both 2-[2-[bis(carboxymethyl)amino]ethyl-(carboxymethyl)amino]acetic acid (EDTA) coated tubes and serum-separating tubes (SSTs). Samples were examined using 15 hematological parameters: hemoglobin (Hb), hematocrit (Hct), red blood cell count (RBC), white blood cell count (WBC), platelet distribution width (PDW), platelet counts, mean corpuscular volume (MCV), mean corpuscular hemoglobin (MCH), mean corpuscular hemoglobin concentration (MCHC), percent eosinophils (EOS), percent basophils, percent monocytes, percent neutrophils (NEUT), percent lymphocytes, and mean plasma volume (MPV). In addition, we analyzed 18 biochemical parameters using an automatic blood analyzer (Olympus AU 400): AST, ALT, lactate dehydrogenase (LDH), ALP, creatine phosphokinase (CPK),γ-GTP, total protein, albumin, total cholesterol, high-density lipoprotein (HDL), low-density lipoprotein (LDL), triglycerides (TG), total bilirubin, direct bilirubin, blood urea nitrogen (BUN), creatinine, uric acid (UA), and random blood sugar (RBS).


## 2.4. Questionnaire Survey

We questioned all participants to identify correlations betweenC. sinensis infection and known risk factors. The questionnaire was given to all participants verbally during an interview by a trained worker in a public health center. The following general information was collected: participant gender, age, current residence, and whether they consumed alcohol. We also asked questions about clonorchiasis risk-related behaviors: Did the patient have a history of eating raw freshwater fish, and if so when, where was the fish from, and what species of fish was consumed? Did the patient have a previous history ofC. sinensis infection, or of bile duct or liver diseases, or of cooking freshwater fish? Had the patient ever experienced symptoms such as anorexia, indigestion, jaundice, abdominal discomfort, or anemia?


## 2.5. Statistical Analysis

Statistical analyses were performed using the SPSS 18.0 program (ver. 18.0; Chicago, Illinois, USA). Only participants with complete records were included in the final analysis. A chi-square test and independentt-test were used to check for statistically significant differences between questionnaire answers from the infected versus noninfected groups. In addition, we confirmed that the differences between the groups’ laboratory results for peripheral blood cells were statistically significant, by an independent t-test. Differences were considered statistically significant when p values were less than 0.05 (p<0.05). Finally, a Pearson correlational analysis was performed to compare EPG to each of the laboratory test results for infected patients.


## 2.6. Ethical Aspects

The study protocol was approved by the Ethics Committee of the Korea National Research Institute of Health, Centers for Disease Control & Prevention, Republic of Korea (2013-06EXP-04-R). All participants and local health center workers were informed of the study’s purpose and procedures. Written informed consent for the research was obtained from all participants prior to enrolment. The participants found to have intestinal parasitic infections were treated with praziquantel (2-(cyclohexanecarbonyl)-3,6,7,11b-tetrahydro-1H-pyrazino[2,1-a]isoquinolin-4-one) and other appropriate antiparasitic drugs at the end of the survey.


## 3. Results

### 3.1. Infection Status

During the study period, 3,167 fecal samples were examined by the formalin-ether concentration technique (FECT). The total intestinal parasite infection rate of was 12.2% (385 cases) including 379 single infections (353 withC. sinensis,24 withMetagonimus yokogawai,four withTrichuris trichiura, two withGymnophalloides seoi, and two withGiardia lamblia) and six coinfections (two or more parasite species in a single sample). Coinfections withC. sinensis andM. yokogawairepresented 0.2% (six cases) of the total infections. TheC. sinensis infection rate was 11.1%, and the mean EPG value was 171.7 ± 513.4 (Table 2). The river-adjacent village of Dongyi-myeon had the highest infection rate (20.8% with a mean EPG 262.4 ± 774.5). The second highest infection rate was 14.0% (mean EPG 58.5 ± 82.6) in the village of Annam-myeon. The lowest infection rate was 6.0% (mean EPG 95.3 ± 186.7) and was observed in the Gunseo-myeon village. The prevalence ofC. sinensis infection was shown to be highest among patients aged 70–79 years (10.7%).Table 2
Infection rates ofC. sinensisaccording to surveyed area.
Villages
Number of inhabitants examined
Infected (%)
Mean EPG ± SD
Okcheon-eup
602
48 (8.0)
94.6 ± 186.7
Annae-myeon
324
42 (13.0)
123.8 ± 267.6
Annam-myeon
221
31 (14.0)
58.5 ± 82.6
Cheongsan-myeon
435
43 (9.9)
221.3 ± 621.4
Cheongseong-myeon
401
43 (10.7)
344.0 ± 736.1
Dongi-myeon
336
70 (20.8)
262.4 ± 774.5
Gunbuk-myeon
300
33 (11.0)
31.4 ± 41.0
Gunseo-myeon
216
13 (6.0)
95.3 ± 186.7
Iwon-myeon
332
30 (9.0)
136.2 ± 200.6
Total
3,167
353 (11.1)
171.7 ± 513.4


### 3.2. Basic Characteristic

The results of the fecal examinations are summarized in Table3. The infection (egg-positive) rates were significantly higher in males (20.3%, p<0.001) and alcohol drinkers (15.5%, p<0.001) than in females (5.4%) and nonalcohol drinkers (7.9%), respectively. Based on the clonorchiasis risk-related behavioral questions, infection rates were significantly higher (p<0.001) among the inhabitants who had eaten raw freshwater fish (14.7%) or had cooked freshwater fish (15.1%) than those who had not. In addition, significantly higher infection rates (18.3%, p<0.01) were found among inhabitants whose anamneses included bile duct or liver related diseases than among those who reported no history of such diseases (10.7%). However, the infection rates did not differ significantly based on patient age, history ofC. sinensisinfection, or symptom experience.Table 3
C. sinensis infection rates based on sociodemographic and behavioral characteristics.
Variables
Infected (%)
Uninfected (%)
Total (%)
p value
Number
353 (11.1)
2,814 (88.9)
3,167 (100)
Gender
0.000
Male
249 (20.3)
978 (79.7)
1,227 (100)
Female
104 (5.4)
1,836 (94.6)
1,940 (100)
Age (yr)
0.146
≤49
15 (7.5)
185 (92.5)
200 (100)
50–59
55 (13.3)
358 (86.7)
413 (100)
60–69
89 (11.9)
659 (88.1)
748 (100)
≥70
194 (10.7)
1,612 (89.3)
1,806 (100)
Alcohol drinking
0.000
Yes
211 (15.5)
1,152 (84.5)
1,363 (100)
No
142 (7.9)
1,662 (92.1)
1,804 (100)
Raw freshwater fish consumption
0.000
Yes
147 (14.7)
851 (85.3)
998 (100)
No
206 (9.5)
1,963 (90.5)
2,169 (100)
History of cooking freshwater fish
0.000
Yes
149 (15.1)
837 (84.9)
986 (100)
No
204 (9.4)
1,977 (90.6)
2,181 (100)
Symptom experience
0.975
Yes
126 (11.2)
1,002 (88.8)
1,128 (100)
No
227 (11.1)
1,812 (88.9)
2,039 (100)
History ofC. sinensisinfection
0.061
Yes
38 (14.8)
218 (85.2)
256 (100)
No
315 (10.8)
2,596 (89.2)
2,911 (100)
History of bile ducts or liver disease
0.002
Yes
31 (18.3)
138 (81.7)
169 (100)
No
322 (10.7)
2,676 (89.3)
2,998 (100)


### 3.3. Correlation betweenC. sinensis Infection and Risk Factors

To assess the relationship betweenC. sinensis infection and risk factors, we selected factors that showed significant differences between infected and uninfected groups and then analyzed the results by logistic regression. The increased odds of infection (odds ratios (ORs)) for patients with various characteristics are shown in Table 4, along with their respective 95% confidence intervals (CIs). Males, alcohol drinkers, raw freshwater fish consumers, those who had cooked freshwater fish, and those with an anamnesis including bile duct or liver disease were 4.45, 2.14, 1.64, 1.73, and 1.87 times more likely to be infected, respectively.Table 4
Odds ratios (OR) and the 95% confidence intervals (CIs) forC. sinensis infection for patients with different characteristics.
Variables
OR
95% CI
Gender
Female
Reference
Male
4.495
3.530–5.723
Alcohol drinking
No
Reference
Yes
2.144
1.711–2.686
Raw freshwater fish consumption
No
Reference
Yes
1.646
1.313–2.064
History of cooking freshwater fish
No
Reference
Yes
1.725
1.376–2.163
History of bile duct or liver disease
No
Reference
Yes
1.867
1.243–2.803


### 3.4. Laboratory Findings

Among the hematological results, the MCV, MCHC, and the percentages of eosinophils (EOS) and neutrophils (NEUT) were significantly different (p<0.05) between the infected and uninfected groups. However, the RBC, WBC, platelet, basophil, monocyte, and lymphocyte counts were not significantly different nor were the PDW, MCH, MPV, Hb, or Hct results. The biochemical tests revealed that LDH and ALP were mildly elevated, whereas the total protein, albumin, TG, and RBS were significantly decreased in the infected group. However, levels of AST, ALT, CPK, γ-GTP, total cholesterol, HDL, LDL, total bilirubin, direct bilirubin, BUN, creatinine, and uric acid were not significantly different between the groups (Table 5). The Pearson correlation analysis only revealed a statistically significant correlation (p=0.014) between EPG and eosinophil count (Figure 2).Table 5
Comparison of laboratory findings betweenC. sinensis infected and uninfected group.
Laboratory findings
Infected group(n=57)
Uninfected group(n=40)
p value
Mean ± SD
Mean ± SD
Hematological parameters
MCV (fL)
94.7 ± 7.1
92.0 ± 4.1
0.032
MCHC (g/dl)
33.7 ± 1.3
34.5 ± 0.8
0.001
EOS (%)
3.3 ± 2.1
2.3 ± 1.9
0.022
NEUT (%)
46.4 ± 10.9
51.2 ± 10.5
0.035
Biochemical parameters
LDH (IU/L)
199.3 ± 51.4
176.7 ± 40.4
0.023
ALP (IU/L)
37.9 ± 12.5
30.7 ± 9.6
0.003
Total protein (g/dl)
7.2 ± 0.8
8.5 ± 2.0
0.000
Albumin (g/dl)
3.8 ± 0.2
4.0 ± 0.2
0.008
TG (mg/dl)
141.3 ± 90.3
202.6 ± 102.7
0.003
RBS (mg/dl)
111.4 ± 26.6
125.0 ± 34.3
0.040Figure 2
Relationship between parasite quantity (EPG) and eosinophil count inC. sinensis infected patients. Pearson correlation analysis shows a significant positive correlation inC. sinensis infected patients between the eggs per gram (EPG) in their stool and their eosinophil counts (Pearson’s r=0.36, p=0.014, and n=57). The results of linear regression analysis are shown (line slope is y=0.002x+2.855 and r2=0.13).


## 3.1. Infection Status

During the study period, 3,167 fecal samples were examined by the formalin-ether concentration technique (FECT). The total intestinal parasite infection rate of was 12.2% (385 cases) including 379 single infections (353 withC. sinensis,24 withMetagonimus yokogawai,four withTrichuris trichiura, two withGymnophalloides seoi, and two withGiardia lamblia) and six coinfections (two or more parasite species in a single sample). Coinfections withC. sinensis andM. yokogawairepresented 0.2% (six cases) of the total infections. TheC. sinensis infection rate was 11.1%, and the mean EPG value was 171.7 ± 513.4 (Table 2). The river-adjacent village of Dongyi-myeon had the highest infection rate (20.8% with a mean EPG 262.4 ± 774.5). The second highest infection rate was 14.0% (mean EPG 58.5 ± 82.6) in the village of Annam-myeon. The lowest infection rate was 6.0% (mean EPG 95.3 ± 186.7) and was observed in the Gunseo-myeon village. The prevalence ofC. sinensis infection was shown to be highest among patients aged 70–79 years (10.7%).Table 2
Infection rates ofC. sinensisaccording to surveyed area.
Villages
Number of inhabitants examined
Infected (%)
Mean EPG ± SD
Okcheon-eup
602
48 (8.0)
94.6 ± 186.7
Annae-myeon
324
42 (13.0)
123.8 ± 267.6
Annam-myeon
221
31 (14.0)
58.5 ± 82.6
Cheongsan-myeon
435
43 (9.9)
221.3 ± 621.4
Cheongseong-myeon
401
43 (10.7)
344.0 ± 736.1
Dongi-myeon
336
70 (20.8)
262.4 ± 774.5
Gunbuk-myeon
300
33 (11.0)
31.4 ± 41.0
Gunseo-myeon
216
13 (6.0)
95.3 ± 186.7
Iwon-myeon
332
30 (9.0)
136.2 ± 200.6
Total
3,167
353 (11.1)
171.7 ± 513.4


## 3.2. Basic Characteristic

The results of the fecal examinations are summarized in Table3. The infection (egg-positive) rates were significantly higher in males (20.3%, p<0.001) and alcohol drinkers (15.5%, p<0.001) than in females (5.4%) and nonalcohol drinkers (7.9%), respectively. Based on the clonorchiasis risk-related behavioral questions, infection rates were significantly higher (p<0.001) among the inhabitants who had eaten raw freshwater fish (14.7%) or had cooked freshwater fish (15.1%) than those who had not. In addition, significantly higher infection rates (18.3%, p<0.01) were found among inhabitants whose anamneses included bile duct or liver related diseases than among those who reported no history of such diseases (10.7%). However, the infection rates did not differ significantly based on patient age, history ofC. sinensisinfection, or symptom experience.Table 3
C. sinensis infection rates based on sociodemographic and behavioral characteristics.
Variables
Infected (%)
Uninfected (%)
Total (%)
p value
Number
353 (11.1)
2,814 (88.9)
3,167 (100)
Gender
0.000
Male
249 (20.3)
978 (79.7)
1,227 (100)
Female
104 (5.4)
1,836 (94.6)
1,940 (100)
Age (yr)
0.146
≤49
15 (7.5)
185 (92.5)
200 (100)
50–59
55 (13.3)
358 (86.7)
413 (100)
60–69
89 (11.9)
659 (88.1)
748 (100)
≥70
194 (10.7)
1,612 (89.3)
1,806 (100)
Alcohol drinking
0.000
Yes
211 (15.5)
1,152 (84.5)
1,363 (100)
No
142 (7.9)
1,662 (92.1)
1,804 (100)
Raw freshwater fish consumption
0.000
Yes
147 (14.7)
851 (85.3)
998 (100)
No
206 (9.5)
1,963 (90.5)
2,169 (100)
History of cooking freshwater fish
0.000
Yes
149 (15.1)
837 (84.9)
986 (100)
No
204 (9.4)
1,977 (90.6)
2,181 (100)
Symptom experience
0.975
Yes
126 (11.2)
1,002 (88.8)
1,128 (100)
No
227 (11.1)
1,812 (88.9)
2,039 (100)
History ofC. sinensisinfection
0.061
Yes
38 (14.8)
218 (85.2)
256 (100)
No
315 (10.8)
2,596 (89.2)
2,911 (100)
History of bile ducts or liver disease
0.002
Yes
31 (18.3)
138 (81.7)
169 (100)
No
322 (10.7)
2,676 (89.3)
2,998 (100)


## 3.3. Correlation betweenC. sinensis Infection and Risk Factors

To assess the relationship betweenC. sinensis infection and risk factors, we selected factors that showed significant differences between infected and uninfected groups and then analyzed the results by logistic regression. The increased odds of infection (odds ratios (ORs)) for patients with various characteristics are shown in Table 4, along with their respective 95% confidence intervals (CIs). Males, alcohol drinkers, raw freshwater fish consumers, those who had cooked freshwater fish, and those with an anamnesis including bile duct or liver disease were 4.45, 2.14, 1.64, 1.73, and 1.87 times more likely to be infected, respectively.Table 4
Odds ratios (OR) and the 95% confidence intervals (CIs) forC. sinensis infection for patients with different characteristics.
Variables
OR
95% CI
Gender
Female
Reference
Male
4.495
3.530–5.723
Alcohol drinking
No
Reference
Yes
2.144
1.711–2.686
Raw freshwater fish consumption
No
Reference
Yes
1.646
1.313–2.064
History of cooking freshwater fish
No
Reference
Yes
1.725
1.376–2.163
History of bile duct or liver disease
No
Reference
Yes
1.867
1.243–2.803


## 3.4. Laboratory Findings

Among the hematological results, the MCV, MCHC, and the percentages of eosinophils (EOS) and neutrophils (NEUT) were significantly different (p<0.05) between the infected and uninfected groups. However, the RBC, WBC, platelet, basophil, monocyte, and lymphocyte counts were not significantly different nor were the PDW, MCH, MPV, Hb, or Hct results. The biochemical tests revealed that LDH and ALP were mildly elevated, whereas the total protein, albumin, TG, and RBS were significantly decreased in the infected group. However, levels of AST, ALT, CPK, γ-GTP, total cholesterol, HDL, LDL, total bilirubin, direct bilirubin, BUN, creatinine, and uric acid were not significantly different between the groups (Table 5). The Pearson correlation analysis only revealed a statistically significant correlation (p=0.014) between EPG and eosinophil count (Figure 2).Table 5
Comparison of laboratory findings betweenC. sinensis infected and uninfected group.
Laboratory findings
Infected group(n=57)
Uninfected group(n=40)
p value
Mean ± SD
Mean ± SD
Hematological parameters
MCV (fL)
94.7 ± 7.1
92.0 ± 4.1
0.032
MCHC (g/dl)
33.7 ± 1.3
34.5 ± 0.8
0.001
EOS (%)
3.3 ± 2.1
2.3 ± 1.9
0.022
NEUT (%)
46.4 ± 10.9
51.2 ± 10.5
0.035
Biochemical parameters
LDH (IU/L)
199.3 ± 51.4
176.7 ± 40.4
0.023
ALP (IU/L)
37.9 ± 12.5
30.7 ± 9.6
0.003
Total protein (g/dl)
7.2 ± 0.8
8.5 ± 2.0
0.000
Albumin (g/dl)
3.8 ± 0.2
4.0 ± 0.2
0.008
TG (mg/dl)
141.3 ± 90.3
202.6 ± 102.7
0.003
RBS (mg/dl)
111.4 ± 26.6
125.0 ± 34.3
0.040Figure 2
Relationship between parasite quantity (EPG) and eosinophil count inC. sinensis infected patients. Pearson correlation analysis shows a significant positive correlation inC. sinensis infected patients between the eggs per gram (EPG) in their stool and their eosinophil counts (Pearson’s r=0.36, p=0.014, and n=57). The results of linear regression analysis are shown (line slope is y=0.002x+2.855 and r2=0.13).


## 4. Discussion

We surveyed the characteristics and laboratory test results of patients withC. sinensis, living near the downstream portion of the Geum River basin. The overall prevalence ofC. sinensis was 11.1% (353 cases). The infection rate was higher than previously reported. The prevalence of clonorchiasis in Geum River basin, for example, was reported to be 9.3% in 2002 [17] and 7.6% in 2007 [11], respectively. Among the examined villages, the infection rate was high in inhabitants within 5 km of the riverside in areas such as Dongyi-myeon (20.8%).The clinical manifestations of the infection depend on the number of flukes, and the egg counts (EPG) give an indirect measure of the intensity of the parasitic infection. The EPG results in our study were lower than those previously reported from inhabitants of the Geum River basin in 1981 [9] and 2002 [17]. Our results indicate that over the last 30 years the infection intensity (EPG) has decreased, but infection rate has increased. These results suggest thatC. sinensisinfections are still prevalent along the Geum River basin.The general pattern ofC. sinensis infection frequency shows a peak in the 50–59-year-old age group [10]. However, our results showed that the infection rate was highest in those aged 70–79 years. This peak in infection frequency among people in their seventies is likely to result from an accumulation of reinfection events or chronic infection withC. sinensis. The likelihood ofC. sinensisinfection was much higher for males than for females. In addition, the odds of infection were higher for alcohol drinkers, natural raw freshwater fish consumers, those who cooked freshwater fish, and those with a history of bile duct or liver diseases. Some of the results of our study are similar to those of previous researchers. In previous studies, the prevalence ofC. sinensishas been higher in males, those who live in rural areas, those who have lived for long periods of time in riverside areas, and those who have eaten raw freshwater fish [4, 17–20].The laboratory blood tests performed here are often included as part of a regular medical checkup to look for changes in patient health. In a previous report, laboratory tests showed eosinophilia with elevated ALP in aC. sinensis infected group, but other parameters such as AST, ALT, γ-GTP, and total bilirubin were not significantly affected [16]. Liao et al. (2006) demonstrated that ALP is increased in patients with liver or bile duct disease [21]. These results were similar to our findings that the mean ALP, LDH, and eosinophil counts were significantly increased. We also confirmed a correlation between infection intensity (EPG) and eosinophil counts. Among our 33 laboratory tests, the eosinophil count was the only test whose results significantly correlated with the EPG.


## 5. Conclusions

In conclusion, our report confirms that there are risk factors ofC. sinensis infection and that several standard laboratory test results significantly differ between infected and uninfected groups. The inhabitants residing in Geum River basin should pay attention to clonorchiasis, and further work should be focused on the early diagnosis and treatment of patients with clonorchiasis because most patients infected withC. sinensis do not have symptoms.



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*Source: 7415301-2017-04-26.xml*