Am. J. Trop. Med. Hyg., 66(5), 2002, pp.

578–583
Copyright © 2002 by The American Society of Tropical Medicine and Hygiene

EPIDEMIOLOGY OF AMEBIASIS IN A REGION OF HIGH INCIDENCE OF AMEBIC

LIVER ABSCESS IN CENTRAL VIETNAM
JOERG BLESSMANN, LINH PHAM VAN, PHUONG ANH TON NU, HAO DUONG THI, BERTRAM MULLER-MYHSOK,
HEIDRUN BUSS, AND EGBERT TANNICH
Bernhard Nocht Institute for Tropical Medicine, Hamburg, Germany; Medical College, University of Hué, Hué City, Vietnam

Abstract. The recent identification of Entamoeba dispar as a separate species, which is nonpathogenic for humans
but morphologically indistinghuishable from Entamoeba histolytica, has prompted the World Health Organization to
recommend reinforced efforts for reassessment of the epidemiology of amebiasis and, in particular, of E. histolytica. In
this regard, the distribution of amebic liver abscess (ALA) cases were analyzed in the province of Thua Thien Hué (TT
Hué) in central Vietnam, a region known for its high incidence of invasive amebiasis. In addition, in a particular area
of Hué City, a parasitologic and seroepidemiologic survey was performed to identify possible risk factors for transmis-
sion of E. histolytica. Based on the analysis of hospital charts from April 1990 to April 1998, 2,031 cases of ALA were
identified, indicating an ALA incidence of at least 21 per 100 000 inhabitants per year. Incidence varied substantially
between the various districts of TT Hué and directly correlated with population density. The risk for ALA was
significantly higher in summer and was age and sex dependent because 95% of the cases were adults, of which more than
80% were males. There was no clustering of cases within households and recurrent cases of ALA occured more
frequently than predicted in the study population. Despite the higher incidence of ALA in males, the parasitologic and
seroepidemiologic survey revealed a significant higher infection rate for intestinal protozoon parasites, including E.
histolytica in females. Besides level of education and access to a toilet or tapwater, use of river water was identified as
an important risk factor for E. histolytica infection.

INTRODUCTION fected individuals is usually low and does not exceed 1% of

the population.6–8 Thus, studies on the prevalence of the
Amebiasis is defined as a human infection with the fecally-
orally spread protozoan parasite Entamoeba histolytica, re- parasite and on the outcome of infection requires the enroll-
gardless of the clinical outcome.1 Normally present in the ment of a fairly large number of individuals. The second is
that the clinical spectrum of E. histolytica-associated intesti-
large bowel, the ameba usually persist for months or even
nal symptoms is broad, ranging from mild diarrhea to severe
years as asymptomatic luminal gut infections. However, oc-
hemorrhagic colitis.9 However, in most areas endemic for
casionally the parasite penetrates the intestinal mucosa and
induces colitis or disseminates to other organs, most com- amebiasis, diarrhea is a common disease due to the high
monly to the liver, where it causes abscess formation. At the prevalence of other diarrhea-causing infectious agents, and
present time, the factors that trigger ameba invasion are un- therefore, it is difficult to assess whether intestinal complaints
known. are indeed the result of a present E. histolytica infection.
Despite its medical importance and the fact that E. his- In contrast to intestinal amebic disease, the diagnosis of
tolytica is endemic in large parts of the world, little is known amebic liver abscess (ALA) seems to be more reliable, since
about the epidemiology of amebiasis. The last estimate on the only a few but uncommon diseases such as pyogenic liver
global magnitude of the disease was made approximately 15 abscess present the typical combination of ALA-associated
years ago.2 At that time, based on a comprehensive analysis clinical symptoms, sonographic findings, and a good response
to treatment with metronidazole.9 Although no precise data
of the current literature, it was suggested that approximately
500 million people are infected worldwide with E. histolytica. are available, it appears that the incidence of ALA differs
However, this estimate was made before the identification of between various amebiasis-endemic areas. A comprehensive
E. dispar as a separate species, which also colonizes the hu- review of the current literature on amebic diseases from 1929
man gut but which is morphologically indistinguishable from to 1997 listed 5,642 reported cases of ALA, most of them
E. histolytica.3 Unlike E. histolytica, E. dispar has never been from Mexico and southeast Asia.10 Recently, a region around
found to be associated with amebic disease, and this ameba Hué City in central Vietnam was identified as an area with an
species is therefore considered to be a harmless gut commen- extraordinary high number of ALA patients,11 which might
sal. Accordingly, most of the earlier data on the worldwide constitute an excellent site for studies on the epidemiology of
distribution of E. histolytica are of limited value. amebiasis. Here we report on the analysis and distribution of
Recently, the World Health Organization has recom- more than 2,000 ALA cases in the province of Thua Thien
mended reassessment of the epidemiology of E. histolytica Hué (TT Hué), as well as on a parasitologic and seroepide-
using test systems, which are able to differentiate between the miologic survey conducted in a particular area of Hué City.
two ameba species.1 From the few studies that have been
MATERIALS AND METHODS
conducted so far, it is evident that E. dispar is substantially
more prevalent than E. histolytica,4–8 and that only a small The study has been approved by the Scientific Council of
proportion of individuals specifically infected with E. his- Education, Training and Ethics of Hué Medical School on
tolytica will progress into having amebic disease.8 In addition September 11, 1998.
to the need to further differentiate ameba species, there are ALA patients. The files of the Central Hospital of Hué City
two major problems for studying the epidemiology of ame- from April 1990 to April 1998 were analyzed and all 2,031
biasis. The first is that although E. histolytica is endemic in charts of patients treated for ALA were selected. The diag-
most tropical and subtropical countries, the number of in- nosis of ALA was based on clinical signs (e.g., weight loss,

578
 EPIDEMIOLOGY OF AMEBIASIS IN CENTRAL VIETNAM 579

fever, abdominal pain and tenderness), ultrasound results 1990 and April 1998. Over the eight-year observation period,
(space-occupying, round, hypoechoic liver lesions), and a the number of ALA patients admitted to the hospital was
good response to therapy with metronidazole or dehydro- relatively stable, approximately 260 cases per year, with a
emetine as shown by disappearance of clinical symptoms and slightly but not significantly higher number in 1993 (Figure 1).
reduction in abscess size. Serologic analysis for E. histolytica However, a significant difference in the number of ALA ad-
using a commercially available enzyme-linked immunosor- missions was found between the dry, hot summer season from
bent assay (ELISA) was conducted on 200 of these patients, April to September (56% of cases) and the rainy and cooler
of which 189 (94.5%) were positive. The address, age, gender, winter season from October to March (44%; P < 0.001).
and date of admission of the various ALA patients were ob- Complete addresses were available for 1,813 of ALA pa-
tained based on information listed in their hospital charts. tients, which indicated that the majority of the cases (1,763)
The male and female distribution in the various age groups were residents of the nine districts in the province of TT Hué
was calculated on the basis of the 1989 Vietnam census. The (Figure 2). Only a few cases (50) were from the neighboring
area and the number of inhabitants of the various districts of provinces of Quang Tri and Quang Nam. The highest inci-
the province of TT Hué and the commune of Phu Cat, Hué dence of ALA was found in the district of Hué City and
were obtained from the 1999 statistical yearbook of the TT lowest incidence was found in the districts of A Luoi and Nam
Hué statistical office.12 Dong. The latter two districts are located in the mountain
Parasitologic and serologic survey. According to the infor- area along the border with Laos. With the exception of Quang
mation obtained from the hospital files, Phu Cat, one of the Dien, the incidence of ALA in the various districts showed a
25 communes into which Hué City is divided, was identified as direct correlation with population density (Table 1).
the area of highest ALA incidence. A closer look revealed Data on gender were available for 2,023 ALA patients and
that a considerable number of ALA patients were residents of data on gender and age were available for 1,911 patients. The
an area within Phu Cat that comprised a very dense populated results indicate that ALA was rare in children, since more
triangle between Chi Lang Street, Bach Dang Channel, and than 95% of all ALA patients were adults (> 15 years old)
the Perfume River. All 961 households within the triangle with a peak incidence in the 30–49-year-old age groups. In
were randomized and 50% of the households were visited addition, incidence of ALA was sex dependent and was much
between January and July 1999. After informed consent was higher in males. Overall, the male to female ratio was 4 to 1.
obtained, all adult household members between 20 and 55 However, the ratio varied with age. Whereas in children no
years old were interviewed using a structured questionnaire substantial sex differences were found for the incidence of
to obtain information about household characteristics, living ALA, the male to female ratio of adult ALA patients was
conditions, personal habits, and educational level. In addition, approximately 7:1 for the 30–49-year-old age groups and ap-
stool and serum samples were collected. Stool samples were proximately 2.5:1 for the age groups more than 60 years old
analyzed using the E. histolytica-specific lectin coproantigen (Figure 3). There were no substantial differences in the age
ELISA (TechLab, Inc., Blacksburg VA) according to the and sex distribution of ALA patients between the various
manufacturer’s instructions. In addition, stool samples were districts.
examined microscopically for the presence of protozoan para- Lack of induction by ALA of long-lasting immunity against
sites and helminth eggs using the formol-ether-concentration development of recurrent ALA. In patients living in Hué
technique and subsequent staining with Lugol’s iodine solu- City, nine current ALA, were reported, all of which occurred
tion.13 Serum samples were tested for the presence of anti- in males. The average time between the first and the second
bodies to E. histolytica using an ELISA based on a recombi- abscess was 27 months (range ⳱ 6–40 months). The mean
nant E. histolytica surface antigen as previously described.14 observation period for all 666 males with ALA from Hué City
This assay has been shown to be highly specific, even when was 4.13 years. Thus, the risk for a man to develop a second
used in amebiasis-endemic countries, and it is able to detect ALA within one year was 0.33%, which is more than five
antibodies to E. histolytica for approximately 6–12 months times higher than the risk for males to develop an ALA
after successful anti-amebic therapy.15
Statistical analysis. All data collected were computer-coded
and analyzed by use of Jandel Sigma Stat (Chicago, IL), SPSS
(Chicago, IL), or StatView (Cary, NC) software. Binomial or
chi-square tests were used for comparisons between two
groups. Multiple logistic regression was used to test for the
simultaneous involvement of several factors that might influ-
ence anti-amoeba antibody status. A P value < 0.05 was con-
sidered to be statistically significant. For the determination of
relative risks (RRs), the program RELRISK (Ott J, http:link-
age.rockefeller.edu) was used. Confidence intervals and stan-
dard errors were determined by standard methodology.

RESULTS
Association of the incidence of ALA with population den-
sity and its predominance in adult males. Based on the infor- FIGURE 1. Annual number of patients with amebic liver abscess
mation found in the hospital files, 2,031 patients with ALA (ALA) admitted to the Central Hospital of Hué, Vietnam from 1991
were treated at the Central Hospital of Hué between April to 1997.
580 BLESSMANN AND OTHERS

FIGURE 3. Incidence of amebic liver abscess (ALA) in the prov-

FIGURE 2. The province of Thua Thien Hué in Vietnam and its ince of Thua Thien Hué in Vietnam with regard to gender and age.
nine districts. This province is located between the border with Laos Shown is the distribution of ALA patients in the various age groups
and the South China Sea and is flanked by the provinces of Quang Tri and by sex. The number above each bar indicates the number of
and Quang Nam. patients per 100,000 inhabitants per year. These figures are based on
a total of 1,911 ALA patients admitted to the Central Hospital of Hué
between April 1990 and May 1998. Standard errors for percentages
(0.06% per year). In addition, the hospital files suggested that are not given but were less than 0.001% in all cases.
there was no clustering of ALA cases within households. Of
the 1,813 patients for whom complete addresses were avail-
All 961 households in the study site were randomized and
able, 1,811 were from different households. Only in two cases
50% of these households were visited. Stool samples were
did two members from the same family develop ALA within
collected from all adult household members between 20 and
the eight-year observation period.
55 years old. A total of 1,187 stool samples were obtained,
Lack of an association between higher incidence of ALA in
which represented 82% of the expected sample size. In addi-
adult males and an increased rate of infection with E. his-
tion, blood samples were taken from approximately one-third
tolytica. To investigate whether the higher incidence of ALA
of the individuals (416) to test for the presence of anti-
in adult males is due to an increased infection rate with E.
amoebic antibodies in serum. Microscopic analysis of the
histolytica, a parasitologic survey was performed in an area of
stool samples showed a considerably high prevalence of in-
extraordinary high ALA incidence, but with an age and sex
fections with orally transmitted intestinal parasites (Figure 4).
distribution of ALA patients similar to that found for the
A total of 71.4% of the individuals were infected, 41.3% har-
entire province. The selected study area was located within
bored at least one of the various protozoan species, and
the commune Phu Cat of Hue City along the confluence of
57.7% had helminth infections, in particular, Ascaris or Tri-
Bach Dang Channel and the Perfume River. It is character-
churis. With regard to E. histolytica, 0.9% of the stool samples
ized by a relatively high population density and contains a
tested positive for E. histolytica coproantigen and 12.7% of
considerable number of households with poor sanitary con-
ditions and without direct access to reasonable drinking wa-
ter, such as tap water. The incidence of ALA was 106 cases
per 100,000 inhabitants per year, thus being three times
higher than the average ALA incidence for all of Hué City.

TABLE 1
Population density and incidence of ALA in the various districts of
the province of Thua Thien Hué

Inhabitants Incidence‡
District Inhabitants* (km2)* ALA cases [95% conf. interval]

Hué City 292,169 4,116 858 37 [30–40]

Phu Vang 169,188 604 321 24 [16–32]
Huong Tra 108,850 209 183 21 [13–31]
Huong Thuy 87,957 192 113 16 [8–26] FIGURE 4. Prevalence of intestinal parasites in adult residents of
Quang Dien 89,641 550 94 13 [6–23] Phu Cat, Hué, Vietnam. Shown are the proportions of males and
Phu Loc 142,373 196 101 9 [4–15] females with antibodies to Entamoeba histolytica, E. histolytica co-
Phong Dien 99,293 104 69 9 [3–16] proantigen, and infection with the various protozoan and helminth
Nam Dong 20,796 32 11 7 [0–31] parasites. The number above each bar represents the percentage of
A Luoi 34,867 28 13 5 [0–19] individuals. P values for differences between males and females are
indicated. E.hist. ⳱ Entamoeba histolytica; E.disp. ⳱ Entamoeba dis-
province TT Hué 1,045,134 207 1 763 21 [18–24] par; E.hart. ⳱ Entamoeba hartmanni; E.coli ⳱ Entamoeba coli; Io-
* Data were obtained from the statistical year book 1999, TT Hué statistical office.12 d.but ⳱ Iodamoeba butschlii; E.nana ⳱ Endolimax nana. Standard
† Only those cases from 4/90–4/98 are considered for which complete patient addresses
were available. errors for percentages are not given but were less than 0.1% in all
‡ Number of ALA cases per 100,000 inhabitants per year. cases.
 EPIDEMIOLOGY OF AMEBIASIS IN CENTRAL VIETNAM 581

the individuals had anti-E. histolytica antibodies in serum. poechoic liver lesions, and showed a good response to anti-
Interestingly, in contrast to the sex distribution of ALA pa- amebic treatment. In addition, these patients had a 94.5%
tients, protozoan parasites as well as anti-amoebic antibodies prevalence of anti-amoebic antibodies. Moreover, in a recent
were significantly more prevalent in females (Figure 4). study, liver abscess aspirates of 50 consecutive ALA-
River water as a source of E. histolytica infections. To iden- suspected patients were cultured for the presence of aerobic
tify possible risk factors for E. histolytica transmission, anti- or anaerobic bacteria, of which 49 (98%) were shown to be
amoebic antibody status of individuals was compared with sterile, excluding the differential diagnosis of pyogenic ab-
household characteristics and living conditions (Table 2). The scesses (Blessmann J and others, unpublished data). The pe-
results indicated no association between the outcome of se- riod between April 1990 and April 1998 was chosen as be-
rology and the number or density of people per household. In cause it represented the time span when the Central Hospital
contrast, a strong association was found between the absence of Hué was the only medical care unit in the entire province
of anti-amoebic antibodies and a higher educational level, where ultrasound was available. Since treatment of ALA in
access to toilets, or access to tap water. In addition, anti- central Vietnam is generally performed by a combination of
amoebic antibodies were significantly more prevalent in indi- abscess puncture and metronidazole therapy,11 all suspected
viduals who regularly use river water. Interestingly, the latter ALA cases from various parts of the province were usually
finding was independent from whether or not these individu- sent to the Central Hospital of Hué. However, according to
als had access to toilets or tap water, suggesting that river information provided by local physicians and health authori-
water constitutes an important source for E. histolytica infec- ties, some less severe cases of ALA may have been treated
tions. This result was further confirmed by multiple logistic with metronidazole alone and were not sent to the hospital.
regression analysis. When age, gender, educational level, Thus, the data from the hospital charts were suitable to de-
number of household members, living area, access to a toilet termine the distribution of ALA cases with respect to gender,
or tap water, and use of river water were used as explanatory age and living site, but probably underestimated the true in-
variables significant influences on antibody positivity were cidence of ALA within the TT Hué population. Nevertheless,
found only with the use of river water (P < 0.03, RR ⳱ 2.540) based on the hospital charts, the incidence of ALA was rather
and gender (P < 0.02, RR ⳱ 0.471). All other variables were high since more than 2,000 cases in a population of approxi-
not significant in this analysis. mately one million inhabitants were recorded, which to our
knowledge represents the highest incidence of ALA on a
DISCUSSION regional level ever reported.
Over the eight-year study period, the annual number of
In an attempt to obtain more precise data on the epidemi- ALA cases was rather constant, suggesting a stable epidemio-
ology of amebiasis, we have analyzed the distribution of ALA logic situation for the transmission of E. histolytica and the
cases in the province of TT Hué in central Vietnam, a region development of ALA in the studied population. Conversely,
of high incidence of invasive amebiasis. In addition, in a spe- incidence of ALA varied substantially between the various
cific area of Hué City, a parasitologic and seroepidemiologic districts of the province TT Hué, but was found to correlate
survey was performed to identify possible risk factors for E. directly with population density. Although information is cur-
histolytica transmission. The ALA cases were analyzed by rently lacking about the relationship between population den-
making use of the hospital charts of patients admitted to the sity and incidence of invasive amebiasis, our results are in
Central Hospital of Hué between April 1990 and April 1998. agreement with observations from the Gambia.16 Here, in a
The diagnosis of ALA was most likely correct for the vast nationwide survey, the prevalence of intestinal E. histolytica/
majority of cases included into the study because all patients E. dispar infections also directly correlated with population
had corresponding clinical signs, space-occupying, round, hy- density. Interestingly, in the same study, a higher prevalence

TABLE 2
Correlation between anti-amoebic antibody status and household characteristics

No. of No. with P values RR*

Household characteristics individuals positive serology % (95% confidence interval)

> 5 individuals per household 297 41 13.8 0.387

ⱕ 5 individuals per household 119 12 10.1 1.43 (0.70–2.82)
Living space per person ⱕ 10 m2 209 28 13.4 0.906
Living space per person > 10 m2 192 24 12.5 1.08 (0.60–1.94)
Education ⱕ 4 school years 141 28 19.9 0.003
Education > 4 school years 273 25 9.2 2.46 (1.37–4.04)
No access to a toilet 152 31 20.4 < 0.001
Access to a toilet 264 22 8.3 2.82 (1.56–5.08)
No access to tap water 80 19 23.8 0.002
Access to tap water 336 34 10.1 2.77 (1.48–5.17)
Use of river water 198 39 19.7 < 0.001
No use of river water 218 14 6.4 3.57 (1.88–6.81)
Access to a toilet and tap water but
use of river water 65 10 15.4 0.019
Access to a toilet and tap water but 3.27 (1.30–8.27)
no use of river water 190 10 5.3
* RR ⳱ relative risk.
582 BLESSMANN AND OTHERS

of the parasite was found in the western part of the Gambia, incidence of ALA in males is obviously not due to a higher
which has lower temperatures and a higher humidity com- rate of infection with E. histolytica.10 According to the results
pared with the eastern part of the country. This appears to of our survey in the adult population of Phu Cat, women were
contradict our results, which indicated substantially more found to be more frequently infected with intestinal proto-
cases of ALA during the dry summer season. However, if one zoan parasites and had a significant higher prevalence of anti-
considers that the average time between infection with E. amoebic antibodies. The higher prevalence might be ex-
histolytica and onset of ALA is approximately five plained by an increased exposure to the parasite, since
months,17,18 the higher incidence of ALA in the Vietnamese women primarily serve the household, which includes wash-
population during summer might be the results of increased ing of clothes, dishes, and food at the river bank, as well as
infection rates with E. histolytica during the winter. taking water from the river.
It has not been established whether protective immunity to An unexpected finding of our study was the low prevalence
invasive amebiasis truly develops. Recurrent ALAs have of 0.9% for E. histolytica as shown by the commercially avail-
been repeatedly described, and in a study from Cambodia as able E. histolytica lectin-specific coproantigen ELISA. Al-
many as 8% of the patients developed a second liver ab- though this value is in agreement with results from other
scess.19 However, clinicians in endemic areas have made an- endemic areas,6–8 it does not explain the high incidence of
ecdotal observations that liver abscess infrequently recurs.20 ALA in the Hué population. The results might suggest that
In addition, the analysis of the hospital charts of 1,021 pa- local factors or habits such as the gut flora or diet possibly
tients cured of ALA in Mexico City between 1963 and 1968 contribute to the outcome of E. histolytica infection. Con-
revealed that substantially less of these patients were read- versely, it remains to be established whether the lectin co-
mitted during this time with a diagnosis of ALA than pre- proantigen ELISA is suitable for the detection of E. his-
dicted in the study population. However, there was no knowl- tolytica in stool samples of the Vietnamese population, since
edge of the patients’ current whereabouts or of admissions to the results of this test showed only a weak association with
other hospitals.21 In contrast, the data from Hué City indicate ameba serology. Similar findings were reported from For-
that recurrent ALA occurs more frequently than predicted in taleza, Brazil with the same version of the antigen test,5
the study population. In addition, the number of recurrent whereas a stronger association was found with stool samples
ALAs in our study population is certainly underestimated from Bangladesh, using a newer version of the test.24,25 How-
since knowledge of the clinical course may result in self- ever, based on previous results using stool culture and subse-
treatment of the disease. This became evident during our quent isoenzyme analysis or a polymerase chain reaction
survey in Phu Cat, where we identified at least three patients (PCR) to differentiate amebae,26–28 or using a direct E. his-
with recurrent ALA (confirmed by ultrasound and positive tolytica-specific PCR with stool samples,29 it is evident that
serology) who underwent self-treatment with metronidazole. more than 80% of individuals infected with E. histolytica,
Thus, the number of recurrent ALA cases in the total Hué even when asymptomatic, have anti-amoebic antibodies in
population is believed to be much higher than that predicted serum. Thus, further studies are required using other test sys-
from the hospital charts. Taken together, our findings do not tems such as a direct stool PCR to prove or disprove our
support the concept that ALA induces protection against in- results with the E. histolytica coproantigen ELISA.
vasive amebiasis or at least does not induce long-lasting im-
munity against recurrent ALAs. Furthermore, our results do Acknowledgments: We thank Britta Weseloh for skillful technical
not support the idea of a genetic trait that may predispose for assistance.
the development of ALA,22,23 since no clustering of cases Financial support: This work was funded by the Volkswagen Foun-
within families was found. However, the lack of clustering dation.
may also indicate that fecal-oral spread of the parasite be- Authors’ addresses: Joerg Blessmann, Bertram Muller-Myhsok,
tween family members does not play an important role in Heidrun Buss, and Egbert Tannich, Bernhard Nocht Institute for
transmission of E. histolytica in the study population, and that Tropical Medicine, Bernhard Nocht Str. 74, 20359 Hamburg, Ger-
many, Telephone: 49-40-4281-8477, Fax: 49-40-4281-8512, Email:
the primary source for E. histolytica infection is located out-
tannich@bni.uni-hamburg.de. Linh Pham Van, Phuong Anh Ton Nu,
side the household. This latter idea would be consistent with and Hao Duong Thi, Medical College, University of Hué, 01 Ngo
our findings, which indicate that the use of river water in Hué Quyen, Hué City, Vietnam.
constitutes an important risk factor for E. histolytica infection.
One of the unresolved enigmas in amebiasis is that the
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