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. 2022 Jun 17;58(6):820. doi: 10.3390/medicina58060820

The Epidemiology of Entamoeba histolytica Infection and Its Associated Risk Factors among Domestic and Imported Patients in Taiwan during the 2011–2020 Period

Fu-Huang Lin 1, Bao-Chung Chen 2, Yu-Ching Chou 1, Wu-Chien Chien 1,3,4, Chi-Hsiang Chung 1,3,5, Chi-Jeng Hsieh 6, Chia-Peng Yu 1,3,*
Editor: Nicola Luigi Bragazzi
PMCID: PMC9228342  PMID: 35744083

Abstract

Background and Objectives: Amebiasis remains an important public health problem worldwide, and immigration and increased international travel have affected incident disease cases. This study assesses the prevalence of Entamoeba histolytica in Taiwan between 2011 and 2020 by analyzing data from surveillance programs conducted by the Centers for Disease Control of Taiwan (TCDC) on laboratory-confirmed cases. Materials and Methods: The E. histolytica infection-related data reported to the National Infectious Diseases Statistics System at the TCDC from 1 January 2011 to 31 December 2020 were collected, including age, gender, place of residence, and the geographic season of exposure for each case. Results: In total, 3066 cases with E. histolytica infections were included in our analysis. Among them, 1735 (57%) cases were imported, and 1331 (43%) were locally acquired. The average annual incidence rate of E. histolytica infections in Taiwan between 2011 and 2020 was 10.6 and 16.1 per 1,000,000 patients. There were statistical differences in gender, age group, and place of residence (p < 0.001) by the source distribution of cases. Also, these differences were found every year (p < 0.05). There were statistical differences in gender and age group (p < 0.001) by place of residence (p < 0.001). The only difference between the distribution of cases and age group was in gender (p < 0.001). Eight patients with amebiasis died, and the fatality rate was 0.3% (8/3066), of whom 75% (6/8) were male, and 75% (6/8) were over 45 years old. This study demonstrates that multiple linear regression analysis shows positive associations between NO2 concentration and amebiasis cases (B value = 2.569, p = 0.019), O3 concentration and amebiasis cases (B value = 0.294, p = 0.008), and temperature and amebiasis cases (B value = 1.096, p = 0.046). Conclusions: This study is the first report of confirmed E. histolytica cases from TCDC surveillance data between 2011 and 2020. This study showed the importance of long periods, air pollutants, and geographically comprehensive analysis for estimating the effect of amebiasis transmission in Taiwan’s populations.

Keywords: diarrhea, epidemiology, amebiasis, Entamoeba histolytica, retrospective study

1. Introduction

Amebiasis is an infectious disease caused by Entamoeba histolytica [1]. Each year, amebiasis affects an estimated 50 million people worldwide and causes 100,000 deaths [2]. E. histolytica can cause invasive intestinal and extraintestinal diseases [3]. It is mainly parasitic in the intestinal tract, and most infected people have no apparent symptoms. This protozoan may invade the intestinal wall tissue of the host, causing intestinal symptoms, abdominal discomfort, intermittent dysentery or constipation, accompanied by fever, shivering, bloody stool, or mucousy soft stool. Symptoms last for approximately one to three weeks. However, extraintestinal infections, such as liver abscesses, lung abscesses, or brain abscesses, may develop in a few people, leading to severe and potentially fatal risks [4,5].

E. histolytica is associated with contaminated food or sewage, and it is transmitted by the fecal–oral route [6]. The growth of E. histolytica can be divided into two stages. The cyst of E. histolytica can survive outside the host in a low temperature and harsh environment for several months. The infection can occur when the person puts things into their mouth that have touched the feces of the infected person with E. histolytica. After the cyst are swallowed, they become active in the intestinal tract and reproduce to produce the next generation. Amebiasis has a worldwide distribution, but the infection is more common in tropical and subtropical developing countries. Infections are prone to occur in orphanages, correctional institutions, shelters, and prisons, with people living in groups. Investigations in Taiwan have found that the infection is relatively common in correctional institutions and mentally ill shelters, and it is closely related to living habits, sanitary conditions, environmental pollution, and group living conditions. In addition, high risk groups are men who have sex with men, individuals from epidemic areas, foreign workers and immigrants from epidemic areas, and inmate populations [7,8]. Amebiasis is a zoonotic infectious disease. E. histolytica is a common human pathogen, and it also occurs in non-human primates. Other animals, such as dogs, cats, pigs, cows, and mice are less infected [9].

Taiwan is a developed, island-type country with a moist subtropical climate, except for the tropical southern part. The monthly average of temperature is 16 °C to 29 °C, and the relative humidity is 75% to 90%. The climatic conditions in Taiwan are suitable for the survival and the spread of amebiasis, resulting in approximately 100 local cases in Taiwan every year [10], a decrease in the quality of life of patients, threats to life and health, and the consumption of medical resources. Nevertheless, few studies reported the epidemiological characteristics of amebiasis-related infection in Taiwan. This study assesses the occurrence of amebiasis infections and their effect on environmental factors, and it examines regional and demographic associations.

2. Materials and Methods

2.1. Ethical Policy

The data came from the Taiwan Centers for Disease and Control (TCDC), and it is public health surveillance rather than research that involved human subjects. Thus, institutional review board approval and informed consent were not required for these deidentified secondary data analyses [11,12,13].

2.2. Data Source

The geographical coordinates of Taiwan are 23°4 North and 121°0 East, and it has a population of approximately 23 million on a land area of 36,188 km2 for a population density of 627/km2. The National Infectious Diseases Statistics System (NIDSS) has reported amebiasis cases to the Centers for Disease Control of Taiwan (TCDC) from 1990. As amebiasis infection is a reportable disease in Taiwan, physicians must report all cases by entering the data into local databases and electronically forwarding the data to the TCDC within 24 h of case confirmation, using TCDC-developed software [14]. Over 84% of physicians reported the notifiable disease to the TCDC after the diagnosis [15]. After receiving the report, a TCDC-assigned epidemiological team (parasitologist, field epidemiologist, and public health nurse) follows the patient, verifies the diagnosis, and collects patient information. Investigations included face-to-face interviews, telephone calls and correspondence with healthcare providers, and interviews with E. histolytica-infected patients.

The E. histolytica infection-related data reported to the NIDSS at the TCDC from 1 January 2011 to 31 December 2020 were collected, including age, gender, place of residence, and geographic season of exposure for each case [10].

2.3. Case Definition

This study refers to the TCDC guidelines for patients with amebiasis infection [16], and it defines the clinical, laboratory, and epidemiological conditions of the case. The clinical conditions are mild, chronic-to-severe diarrhea, mucus and blood filaments in feces, acute and severe diarrhea, intermittent diarrhea, abdominal pain, fever, nausea, and vomiting. However, most E. histolytica carriers have no obvious clinical symptoms. The test must meet one of the following conditions: (1) Clinical specimens (feces, tissue or abscess extracts, and other types) are confirmed to be E. histolytica through the molecular biology nucleic acid test of the TCDC laboratory. (2) Intestinal and extraintestinal tissue slices or ulcers were cured, and active E. histolytica was found. (3) The case has clinical symptoms (fever or right upper quadrant pain). It is diagnosed as a liver abscess by ultrasound or computed tomography, and the serological test is positive for the antibody of E. histolytica. Epidemiological requirements must meet one of the following conditions: (1) Had close contact with a confirmed case. (2) Consumed food and drinking water that has been directly or indirectly contaminated by feces of patients or carriers. Furthermore, the “definition of a notified case” refers to one of the following conditions: (1) It meets the clinical conditions. (2) It meets the inspection conditions after testing by a medical laboratory. The “definition of a confirmed case” refers to one of the following conditions: (1) The first item of the test conditions is met. (2) It meets the clinical conditions (fever or right upper quadrant pain) and the second or third test conditions.

2.4. Laboratory Examination

The stool and the blood samples were collected from patients suspected of having E. histolytica infection [17]. For the Entamoeba spp, the microscopic examination was screen in various hospital laboratories. To confirm the diagnosis and to identify the amebic species, positive specimens were sent to the TCDC laboratory [18]. The antibody detection methods were tested with IHA (Dade Behring Diagnostics, Marburg, Germany) and TechLab (Blacksburg, VA, USA) [19,20]. DNA-based diagnostic tests were based on the amplification of the small-subunit rRNA gene of E. histolytica, E. dispar [21,22].

2.5. Surveillance of Environmental Factors

This study analyzes the monthly data of air pollutants provided by the air quality monitoring network of the Environmental Protection Agency from 2011 to 2020 [23], including total suspended particulates (TSP), particulate matter 2.5 (PM2.5), nitrogen dioxide (NO2), sulfur dioxide, carbon monoxide (CO), and ozone (O3). The monthly data of weather factors (temperature, rainfall, relative humidity, atmospheric pressure, rainfall days, and sunshine hours) provided by the Meteorological Bureau of the Ministry of Communications from 2011 to 2020 were analyzed [24]. Statistical analysis and correlation tests were used to understand the temporal and the spatial variation trend of air pollutants and meteorological factors and their correlation with amebiasis case numbers.

2.6. Statistical Analysis

We identified amebiasis cases from 2011 to 2020 from the database, and we examined their epidemiological differences and trends. The continuous variables were described as means and standard deviations. Categorical data was analyzed by the chi-square test. This study also computed the odds ratio by logistic regression and the 95% confidence interval in the parameter estimation. All analyses were performed using the Statistical Package for the Social Sciences software software (IBM SPSS Statistics 21; Asia Analytics Taiwan Ltd., Taipei, Taiwan). Statistical significance was defined as a p-value of <0.05.

3. Results

3.1. Surveillance

Figure 1 presents the amebiasis importation rate and the number of domestic and imported cases in Taiwan by year from 1 January 2011 through 31 December 2020. The annual case numbers ranged from 255 to 379. The importation per 1,000,000 inbound travelers was 22.2 in 2011 and 92.9 in 2020. In addition, during the study period, the annual incidence of amebiasis, male and female cases, cases in each age group, cases in different seasons, and cases in different residences are shown in Figure 2.

Figure 1.

Figure 1

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Amebiasis importation rate and the number of domestic and imported cases in Taiwan by year.

Figure 2.

Figure 2

Figure 2

Figure 2

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Incidence of confirmed amebiasis among patients in Taiwan according to (A) population, (B) sex, (C) age group, (D) season, and (E) residency by year from 2011 to 2020.

3.2. Outcome of Epidemiological Features

Confirmed E. histolytica infection cases were 3066 for which data related to the risk of infection (sex, age group, and area of residence) with their statistical significances were obtained (Table 1). A comparison of the risk factors and cases each year revealed the following findings: (1) No significant differences for the season were observed; (2) For cases of style, sex, age group, and residency, all epidemiological features were statistically significant (p < 0.05) (Table 2). A comparison of the risk factors and cases of the season revealed the following findings: No significant differences in sex, age group, and residency were observed (Table 3). A comparison of the risk factors and the cases of residency revealed the following findings: For sex and age group, all epidemiological features were statistically significant (p < 0.05) (Table 4). A comparison of the risk factors and cases of sex revealed the following findings: No significant differences for age group were observed (Table 5).

Table 1.

The characteristics of domestic and imported cases of amebiasis in Taiwan from 2011 and 2020.

Variables All Cases Domestic Cases Imported Cases p
N = 3066, % N = 1331, % N = 1735, %
Sex
Male 1707 55.7 1085 81.5 622 35.9 <0.001
Female 1359 44.3 246 18.5 1113 64.1
Age
<20 26 0.8 10 0.8 16 0.9 <0.001
20–29 1075 35.1 283 21.3 792 45.6
30–39 1185 38.6 450 33.8 735 42.4
40–49 408 13.3 252 18.9 156 9.0
50–59 186 6.1 164 12.3 22 1.3
≥60 186 6.1 172 12.9 14 0.8
Season
Spring 773 25.2 346 26.0 427 24.6 0.251
Summer 785 25.6 321 24.1 464 26.7
Fall 808 26.4 345 25.9 463 26.7
Winter 700 22.8 319 24.0 381 22.0
Residency
Taipei area 1055 34.4 516 38.8 539 31.1 <0.001
Northern 410 13.4 172 12.9 238 13.7
Central 527 17.2 214 16.1 313 18.0
Southern 466 15.2 157 11.8 309 17.8
Gao-Ping 489 15.9 216 16.2 273 15.7
Eastern 119 3.9 56 4.2 63 3.6
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Table 2.

Analysis of the characteristics of domestic and imported cases of amebiasis in Taiwan from 2011 and 2020 by year.

Variables Year p
2011 2012 2013 2014 2015 2016 2017 2018 2019 2020
Cases
 Domestic 120 86 88 103 155 148 188 164 157 122 <0.001
 Imported 135 172 183 197 196 167 191 171 195 128
Sex
 Male 151 112 139 155 187 175 239 197 194 158 <0.001
 Female 104 146 132 145 164 140 140 138 158 92
Age group
 <20 1 3 4 2 2 2 1 0 7 4 0.003
 20–29 101 86 107 100 136 124 112 114 120 75
 30–39 84 105 100 127 130 127 145 134 127 106
 40–49 30 27 44 44 45 33 57 50 46 32
 50–59 17 20 9 17 19 11 37 19 25 12
 ≥60 22 17 7 10 19 18 27 18 27 21
Season
 Spring 69 67 70 66 94 72 92 87 91 65 0.467
 Summer 53 73 84 76 91 93 100 78 78 59
 Fall 72 62 61 93 85 82 90 102 94 67
 Winter 61 56 56 65 81 68 97 68 89 59
Residency
 Taipei area 78 103 95 102 129 104 118 117 136 73 <0.001
Northern area 37 38 31 50 36 40 48 47 51 32
 Central area 41 45 39 40 57 58 73 64 45 65
Southern area 45 39 45 44 55 58 53 49 37 41
Kao-Ping area 40 25 40 48 61 49 78 47 73 28
Eastern area 14 8 21 16 13 6 9 11 10 11
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Table 3.

Association between season and gender, age groups, and region of residence from a survey of domestic and imported cases of amebiasis between 2011 and 2020 in Taiwan.

Variables Season p
Spring Summer Fall Winter
Sex
 Male 441 423 442 401 0.448
 Female 332 362 366 299
Age group
 <20 5 4 9 8 0.737
 20–29 285 274 282 234
 30–39 298 297 315 275
 40–49 89 110 108 101
 50–59 43 55 51 37
 ≥60 53 45 43 45
Residency
 Taipei area 257 271 270 257 0.163
 Northern 98 109 119 84
 Central 129 137 136 125
 Southern 148 99 117 102
 Kao-Ping 112 138 136 103
 Eastern 29 31 30 29
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Table 4.

Association between region of residence and gender and age groups from a survey of domestic and imported cases of amebiasis between 2011 and 2020 in Taiwan.

Variables Region of Residence p
Taipei Area Northern Area Central Area Southern Area Kao-Ping Area Eastern Area
Sex
 Male 569 215 322 225 310 66 <0.001
 Female 486 195 205 241 179 53
Age group
 <20 6 3 8 3 4 2 <0.001
 20–29 316 168 203 195 164 29
 30–39 416 165 220 170 171 43
 40–49 181 47 46 33 82 19
 50–59 75 14 21 29 37 10
 ≥60 61 13 29 36 31 16
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Table 5.

Association between gender and age groups from a survey of domestic and imported cases of amebiasis between 2011 and 2020 in Taiwan.

Variables Sex p
Male Female
Age group
 <20 19 7 <0.001
 20–29 532 543 a
 30–39 595 590 b
 40–49 266 c 142
 50–59 162 d 24
 ≥60 133 e 53
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a: Cases with age 20–29 years old (OR = 1.470, 95% CI = 1.266–1.706 (p < 0.001)) in females compared with males; b: Cases with age 30–39 years old (OR = 1.434, 95% CI = 1.239–1.660 (p < 0.001)) in females compared with males c: Cases with age 40–49 years old (OR = 1.582, 95% CI = 1.273–1.966 (p < 0.001)) in males compared with females d: Cases with age 50–59 years old (OR = 5.833, 95% CI = 3.776–9.010 (p < 0.001)) in males compared with females e: Cases with age ≥60 years old OR = 2.082, 95% CI = 1.502–2.887 (p < 0.001)) in males compared with females.

A total of 1735 confirmed cases of E. histolytica were imported from abroad during 2011–2020. The purpose of entering Taiwan was mainly for tourism and business (including foreign workers). The country with the most cases of infection was Indonesia, with 1385 cases (Table 6) of which the number of cases in 2014 was the highest in the past seven years (197 cases). The annual import rate is shown in Figure 1, and the annual distribution of imported cases is shown in Figure 2.

Table 6.

The number of imported amebiasis cases reported by country, 2011–2020.

Country Year
2011 2012 2013 2014 2015 2016 2017 2018 2019 2020
Asia
(N = 1716)
China 7 5 6 3 4 3 2 4 6
Korea 1 1 1
Japan 1 1 2 1
Philippines 8 19 12 22 20 17 30 18 24 13
Indonesia 106 141 153 164 159 127 148 122 155 110
Vietnam 6 2 5 3 6 6 4 13 4 2
Myanmar 1 1 1 1 1
Cambodia 1 2 1 1
Malaysia 1 1
Thailand 3 3 4 1 2 4 3 4 1
Maldives 1
India 2 2 4 1 1 1
Oceania
(N = 5)
Australia 1 1
Giribas 1
Tuvalu 2
America
(N = 3)
USA 1
Panama 1
Colombia 1
Europe
(N = 2)
U. K. 1
France 1
Miss. Data
(N = 9)		 1 0 1 1 1 1 0 4 0 0
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Travel destinations of 1,695 imported cases of E. histolytica infection in Taiwan (only countries with at least 10 cases of infection with E. histolytica were listed). A total of 1385 (79.8%) had been to Indonesia, 183 (10.5%) to the Philippines, 51 (2.9%) to Vietnam, and 25 (1.4%) to Thailand. The relative risk (RR) of Amebiasis for travelers from Taiwan to Indonesia was 544.0, to the Philippines it was 60.7, to India it was 25.8, to Vietnam it was 16.0, and to Thailand it was 9.3 when compared with traveling to China (Table 7).

Table 7.

Travel destinations of 1695 imported cases of E. histolytica infection in Taiwan between 2011 and 2020.

Country of Destination No. Cases No. of Air Passengers
(100,000)		 RR
China 40 271.8 Reference
Vietnam 51 21.7 16.0
Thailand 25 18.2 9.3
Philippines 183 20.5 60.7
Indonesia 1385 17.3 544.0
India 11 2.9 25.8
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Note: Only countries with at least 10 cases of infection with E. histolytica were listed. RR: relative risk.

During the 10-year investigation period, there were eight death cases due to amebiasis: six males (75%) and two females (25%); two individuals were 20–44 years old, three individuals were 45–64 years old, and three individuals ≥65 years old (Table 8).

Table 8.

Analysis of deaths due to amebiasis in Taiwan from 2011 to 2020.

Variables Year *
Overall 2011 2013 2014 2015 2018
Male 6 1 1 1 2 1
<20 - - - - - -
20–44 2 - - 1- 1 -
45–64 2 1 1 - - -
≥65 2 - - - 1 1
Female 2 1 - - 1 -
<20 - - - - - -
20–44 - - - - - -
45–64 1 1 - - - -
≥65 1 - - - 1 -
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* years 2012, 2016, 2017, 2019, and 2020 had no deaths due to amebiasis.

3.3. Outcome of Environmental Features

Air pollution factors were associated with amebiasis cases by multiple linear regression analysis. The value was R2 = 0.145, F =2.519 (p = 0.027, df = 6, 89). As shown in Table 9: The B value of the non-standardization coefficient is 2.569, standard error is 1.074, and the p value is 0.019 for NO2 pollutants. The B value of the non-standardization coefficient is 0.294, standard error is 0.109, and the p value is 0.008 for O3 pollutants. Furthermore, climate factors were associated with amebiasis cases by multiple linear regression analysis. The value was R2 = 0.073, F = 1.165 (p = 0.332, df = 6, 89). As shown in Table 10: The B value of the non-standardization coefficient is 1.096, standard error is 0.542, and p value is 0.046 for the temperature factor.

Table 9.

Association between air pollutant factors and amebiasis cases by multiple linear regression analysis.

Variables Non-Standardization Coefficient p
B Value Standard Error
TSP (μg/m3) −0.099 0.087 0.259
PM 2.5 (μg/m3) −0.320 0.279 0.254
SO2 (ppb) 0.607 1.761 0.731
CO (ppm) −63.818 36.994 0.088
NO2 (ppb) 2.569 1.074 0.019
O3 (ppb) 0.294 0.109 0.008
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R2 = 0.145; F = 2.519 (p value: 0.027); df = (6, 89). N = 96.

Table 10.

Association between climate factors and amebiasis cases by multiple linear regression analysis.

Variables Non-Standardization Coefficient p
B Value Standard Error
Temperature (°C) 1.096 0.542 0.046
Precipitation (mm) 0.001 0.010 0.890
Relative humidity (%) −0.524 0.392 0.184
Mean Pressure (hPa) 0.349 0.451 0.441
Number of Days with Precipitation ≥0.1 mm (day) 0.137 0.519 0.792
Sunshine Duration (hr) −0.038 0.041 0.353
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R2 = 0.073; F = 1.165 (p value: 0.332); df = (6, 89). N = 96.

4. Discussion

From 2011 to 2020, there were 3066 confirmed cases of E. histolytica infections in Taiwan: 43% were imported and 57% were indigenous, similar to a previous study [17]. Epidemiology uses demographic methods to characterize the distribution of a particular organism and analyzes the data to ascertain the determinants of that particular distribution [25]. Epidemiology also explores disease distribution and disease occurrence determinants in populations in time and in space and the epidemiological characteristics associated with disease transmission, presentation, and outcome. This discipline has always been driven by policy interventions or disease prevention measures [2,26].

The high incidence rate of men in local cases is the opposite of women in foreign countries. It is inferred that the reason may be different national conditions or different personal hygiene habits. Second, most imported cases are 20–29 years old, whereas most local cases are 30–39 years old. Imported cases are concentrated in summer and fall, whereas local cases are concentrated in spring and fall. The similarity between imported and local cases is that both are concentrated in the northern region. Taiwan’s government can use these similarities and differences in epidemiological characteristics as the basis for implementing its epidemic prevention policy plan or strategy.

Among all epidemiological characteristics, seasonal variation is the least affected factor by the distribution of all confirmed cases. Namely, seasonal variation is insufficient to affect the significant increase or decrease of confirmed cases, indicating that the disease in South Asia, Southeast Asian countries, or even Taiwan is endemic. In other words, there are always traces of E. histolytica in Taiwan that threaten public health and increase the clinical medical burden. At this stage, all of these major issues need to be overcome, prevented, and controlled. The Taiwan government health department should actively propose local prevention strategies, oversea border control, and implement surveillance operations to control the epidemic effectively and to reduce the number of cases so as to eliminate the health threat.

Humans swallow E. histolytica by ingesting water or food or having unclean hands contaminated with E. histolytica viable cysts. Foodborne exposure infection is the most common route of transmission, especially when food handlers do not clean their hands after using the toilet or their feces become agricultural fertilizer. Some clinicians will use irrigation devices to obtain infection during rectal enema in rare cases. In developing countries, such as India and Mexico, large-scale epidemics of waterborne E. histolytica infection often occur [26]. In developed countries, E. histolytica infection is common among travelers, new immigrants, gay men, and prison inmates [27,28], similar to the findings of this study. The transferred cases of E. histolytica from outside the epidemic area showed a high incidence.

According to data from studies in other countries, about half of travelers with enteric E. histolytica infection who return to developed countries are from Asia and Africa [29], similar to the results of this study. The increase in international passenger flows has affected the incidence. This study showed the incidence of E. histolytica infection in Taiwan increased with the increased incidence of E. histolytica among inbound tourists.

This study confirmed the risk of contracting E. histolytica during travel to countries where the disease is endemic. Infections with travel-related enteric pathogens occur during travel and after the journey [30]. Some studies have stated that about 8% of international travelers are seriously ill during or after travel and require medical care [31]. Travelers contribute to the global spread of infectious diseases, including novel and emerging pathogens. Therefore, monitoring travel-related morbidity is an integral part of global public health monitoring. It will become increasingly important with the expansion of global international flights and the growth of the travel population [32]. It is necessary to establish a sensitive, rapid, and accurate surveillance system and to implement an amebiasis screening program for inbound travelers (especially immigrants/foreign workers) from epidemic areas to control amebiasis infection in Taiwan.

According to the newly revised nomenclature, E. histolytica is the pathogenic strain, and the non-pathogenic strain is E. dispar [33]. The two species can be distinguished by various experimental methods, but they cannot be distinguished morphologically [34,35]. Terms such as molecular epidemiology often appear in the infectious disease literature, including the study of molecular typing of pathogenic strains of infectious factors (i.e., pathogens). DNA technology has made an outstanding contribution to the study of amebiasis infection in humans. Biomarkers provide new opportunities to overcome some limitations of traditional scientific methods. However, these biomarkers should be verified in molecular epidemiological studies on bias and confounders [36]. Genetic diversity and kinship conducted by previous studies have confirmed several E. dispar genotypes, which may be related to intestinal or liver tissue damage. They are similar to the symptoms caused by E. histolytica [37]. The intestinal symptoms may also be caused by E. dispar infection [38]. Furthermore, E. dispar infection can often be as a fecal–oral infection indicator. According to previous studies by Taiwanese scholars, the cases cannot rule out the possibility of infection by other pathogens (e.g., E. dispar), mainly because E. histolytica in Taiwan is a legal infectious disease, and its applied experimental diagnostic methods do not cover all possible intestinal infection categories [17].

In the absence of a policy for the impact of climate change on public health, many countries are developing and implementing response measures for climate change adaptation [38]. Climate disasters in 2020, such as wildfires, hurricanes, and heatwaves, show that climate change has an increasing effect on health, and it will undoubtedly seriously threaten human health. In addition, COVID-19 is a great pandemic. We know that only by preventing a foreseeable public security crisis can we avoid unnecessary illness and death. Studies have shown that global warming may lead to more deaths from heatwaves and the increased incidence and mortality from waterborne diseases, such as foodborne diseases [39]. A previous study indicated that well-known socioeconomic factors contributing to the incidence of E. histolytica found that temperature and precipitation were associated with a higher risk of infection [40]. This study also confirmed that when the temperature increased, the number of E. histolytica cases also increased, and there was a positive correlation between them. These results are similar to those of other studies. To our knowledge, this is the first study to find that when the concentration of the air pollutants O3 and NO2 increased, the number of amebiasis cases also increased, and there was a positive correlation. Our study inferred that the possible reasons might be the high concentration of O3 in the fall and the high concentration of NO2 in the late fall and the early winter, which are prone season(s) for E. histolytica. It was estimated that there was a correlation between these air pollutants and the disease. Therefore, this study suggests that Taiwan’s official policy should closely monitor local climate factors and air pollution concentration changes. Once the environmental data changes slightly or fluctuates violently, the media and the public should be informed. People can quickly respond and follow up to reduce environmental pressures and the threat to public health.

5. Limitations

This study has two strengths. First, it analyzed the laboratory-confirmed cases of amebiasis and then combined confirmed cases with the number of inbound passengers from epidemic countries and data on overseas cases. These data enabled us to analyze the risk of tourists to areas where amebiasis is endemic. This is the first study based on the database compiled by the infrastructure of the Taiwan Tourism Bureau. This study determined the most representative countries of origin and the number of inbound passengers and tried to perform a limited analysis and comparison. This study has two methodological limitations. First, both local and overseas cases are based on surveillance data. Therefore, reporting bias may affect the number of cases. This bias can occur anywhere in the reporting chain—from the patient seeking medical care to the medical care registry recording and confirming cases. Some studies have stated that many notifiable infectious diseases may be underestimated [41]. Some studies indicated that at least 10% of asymptomatic patients infected with pathogenic strains developed amebic colitis [2]. Asymptomatic ameba infection cases may have been in Taiwan during the study period, but they were not collected in the analysis. Our study may underestimate the cases. Second, this study cannot test the impact of individual susceptibility. Therefore, investigating the specific role of other risk factors in the transmission of E. histolytica infection is very important.

6. Conclusions

In conclusion, there is a high risk of contracting E. histolytica for travelers to South and Southeast Asia. It is necessary to establish a sensitive, rapid, and accurate epidemic monitoring system and to implement a screening plan for E. histolytica among inbound passengers/foreign workers from epidemic countries to effectively control E. histolytica infection in Taiwan. In addition, strategies to improve the environment and to maintain the overall ecology should be proposed for the active prevention and control of E. histolytica and to monitor and treat air pollutant concentration, temperature, rainfall, and other climate change factors in Taiwan.

Acknowledgments

The authors are grateful to all our colleagues in the School of Public Health, National Defense Medical Center, Taiwan for their help in the collection of government data.

Author Contributions

Conceptualization, F.-H.L., B.-C.C., W.-C.C. and C.-P.Y.; methodology, F.-H.L., Y.-C.C. and C.-H.C.; software, C.-H.C. and C.-J.H.; validation, F.-H.L. and C.-J.H.; formal analysis, Y.-C.C., C.-H.C. and C.-P.Y.; data curation, Y.-C.C., B.-C.C. and W.-C.C.; writing—original draft preparation, F.-H.L., B.-C.C. and C.-P.Y.; writing—review and editing, F.-H.L., W.-C.C. and C.-P.Y. All authors have read and agreed to the published version of the manuscript.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

Funding Statement

This research received no external funding.

Footnotes

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