Am. J. Trop. Med. Hyg., 64(3, 4), 2001, pp.

131–136
Copyright 䉷 2001 by The American Society of Tropical Medicine and Hygiene

EFFECT OF CLIMATIC FACTORS AND POPULATION DENSITY ON VARICELLA

ZOSTER VIRUS EPIDEMIOLOGY WITHIN A TROPICAL COUNTRY
SOMSAK LOLEKHA, WATCHAREE TANTHIPHABHA, PENPARK SORNCHAI, PENSRI KOSUWAN, SUMIT SUTRA,
BOONYARAT WARACHIT, SUDA CHUP-UPPRAKARN, YANEE HUTAGALUNG, JOHN WEIL, AND HANS L. BOCK
Department of Pediatrics, Faculty of Medicine,
Ramathibodi Hospital, Mahidol University, Bangkok, Thailand; Department of Pediatrics, Faculty of Medicine, Chiang Mai
University, Chiang Mai, Thailand; Pediatrics Unit, Nakornping Hospital, Chiang Mai, Thailand; Department of Pediatrics,
Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand; Pediatrics Unit, Had Yai Regional Hospital, Had Yai,
Song Kla, Thailand; Smithkline Beecham Biologicals, Rixensart, Belgium

Abstract. Blood samples were collected from healthy subjects, aged 9 months–29 years in urban and rural com-
munities from 4 distinct regions in Thailand, to determine the seroprevalence rate of varicella-zoster virus (VZV)
antibody and its relationship with demographic, climatic, and socioeconomic factors. The overall seroprevalence rate
was 52.8% and increased from 15.5% in the 9-month to 4-year-old group to 75.9% in the 20–29 year-olds. The age-
adjusted seroprevalence was significantly higher in the cooler than in the warmer regions. In the warmer regions
only, the age-specific seroprevalence was significantly higher in the urban population than in the rural population. In
Thailand, climate is the main determinant of VZV seroprevalence. The delayed onset of natural immunity is more
marked in warmer climate areas. Population density is a secondary determinant; in the warmer areas, the pattern of
adolescent and adult susceptibility was greater in rural than in urban areas.

INTRODUCTION Northern area (Chiang Mai), Northeastern area (Khon Kaen),

Primary infection with varicella-zoster virus (VZV), com-
monly called chickenpox, is usually considered an inevitable
disease of childhood that has few complications with a low-
case fatality rate in healthy children. However, it can be se-
rious or sometimes fatal in immunocompromised patients,
adolescents, and adults.1,2
Although varicella occurs worldwide, the epidemiology of
the disease is recognized as being different in temperate and
tropical regions. In temperate regions, varicella is a disease
of preschool and school-age children.3–8 In tropical regions,
varicella typically occurs at a later age9–12 with many cases
in adolescents and adults who are at risk of developing more
severe disease. A recent study in Bangkok also showed that
70.4% of the population younger than 20 years of age were
seropositive, and this increased to 98–100% by the age of
40.13
Varicella epidemiology is incompletely understood in
tropical and subtropical regions. Various hypotheses have
been proposed to explain the different age distribution. High
ambient temperature and humidity could affect virus trans-
mission, with the virus inactivated at higher temperatures.12,14
The degree of social interaction among children might result
in less opportunity for exposure.15 There has been no pre-
vious study comparing VZV seroprevalence rates between
climatic zones in the same country and only 1 study com-
paring an urban and rural population in the tropics.15 In the
present study, the objective was to determine whether the
age-specific varicella seroprevalence rates differ between the
various geographic areas in Thailand and under varying cli-
matic conditions and the association with population density
(urban and rural communities) and socioeconomic status.
MATERIALS AND METHODS
From July 1997 to April 1998, 2,000 healthy subjects
ranging from 9 months to 29 years of age were recruited on
a voluntary basis from urban and rural areas of 4 different
regions in Thailand, namely the Central area (Bangkok),
and Southern area (Had Yai in the province of Song Kla).
In the Central area, it is relatively warm year-round, with
usually only one or two cooler weeks in December and Jan-
uary. In the Northern area, it is relatively cold in winter
because the area is about 300 meters above sea level, and is
surrounded by high mountains. The Northeastern area is hot
and dry in the summer and cold in the winter. In the South-
ern area close to the coast, heavy rain is prevalent more than
half of the year, and no winter season is identified in this
region. Within these geographically and climatically distinct
regions, the study populations were recruited from schools,
factories, medical personnel, outpatient clinics, and directly
from the rural communities. Each center planned to enroll
approximately 500 individuals between 9 months and 29
years of age, stratified into 5 age groups as follows: 9
months–4 years, 5–9 years, 10–14 years, 15–19 years, and
20–29 years. Each group was to consist of 100 individuals
of which 50% lived in urban and 50% in rural areas.
An urban area was defined as a municipality or town with
a population over 100,000 and a population density between
300 to 3,600 persons (Bangkok) per square kilometer. A ru-
ral area was defined as the area outside an urban area where
agriculture is the main activity with a population density is
between 40 and 140 per square kilometer.
Adults and children who had no confirmed or suspected
immunosuppressive illness (including human immunodefi-
ciency virus [HIV] infection), and who had had no immu-
nosuppressive therapy or administration of immunoglobulin
or other blood products within the 3-month period preceding
the study were considered to be eligible. The study was ap-
proved by the National Ethical Committee, and all partici-
pants, or in the case of children, their parents or guardians,
gave written informed consent. Pre-study publicity was ar-
ranged in all locations. The investigators went directly to the
study settings; volunteers were recruited without any incen-
tive being offered. A questionnaire was completed for each
subject during an interview with the subject or the parents,
collecting details about socioeconomic background, which

131
132 LOLEKHA AND OTHERS

was measured by classifying subjects into one of 5 income

per month categories, ⬍ 5,000, 5,000–10,000, 10,001–

1,015
243
279
251
242
Urban
20,000, 20,001–50,000, ⬎ 50,000 baht (now is @43 baht ⫽
US$1), as well as any history of chickenpox. As most of the

Address
information regarding socioeconomic background in the
Northeastern area was not completed, this area was excluded
from the analysis for this parameter. A positive varicella his-

1,078
244
297
287
250
Rural
tory was defined as either personal recollection (memory) or
hearsay (being told that he or she had varicella in childhood).
Blood samples were taken from each subject, and sepa-
rated serum was stored at ⫺20⬚C until testing. The testing
was done at the Laboratory of Pediatric Infectious Unit, at
the Ramathibodi Hospital of Mahidol University in Bang-

Male

229
215
229
198
871
kok, Thailand. Specific VZV immunoglobulin (Ig)G anti-
bodies were determined using a commercial enzyme-linked

Gender
immunosorbent assay (ELISA), Enzygnost anti-VZV/IgG
(Dade Behring, Marburg Germany) according to the manu-
facturer’s instructions.

Female

1,222
258
361
309
294
Delta absorbance readings of ⱖ 0.2 were taken as positive
and indicated immunity to VZV infection. Values ⬍ 0.1 were
considered negative and indicated susceptibility to VZV in-
fection. Values between 0.1 and 0.2 obtained twice on the

Study population characteristics overall and by center

same samples were classed as equivocal.

20–29 yr

96
121
99
95
411
All data were entered into an Oracle database, and statis-
tical analysis was performed using Statistical Analysis Sys-
tem (SAS), version 6.12 (SAS Institute Inc., Cary, NC). Uni-
variate logistic regression models were built with each ex-
planatory variable. Significance (P ⫽ 0.25) of explanatory
15–19 yr

98
108
102
97
405
variables was tested using the loglikelihood statistic. A mul-
TABLE 1

tivariate model, including all significant variables found at

step 1, was built using the loglikelihood statistic.
Age distribution (no.)

10–14 yr

96
120
117
106
439
RESULTS

A total of 2,176 volunteers were enrolled in this study.

Eighty-three subjects were excluded from the analysis be-
cause of missing data or age ineligibility. Table 1 shows the
5–9 yr

100
114
118
94
426

study population characteristics overall and by center. There

was no difference in age, gender, and urban versus rural
between the study sites.
Immunity by age and gender as defined by serology.
9 mo–4 yr

Of the total 2,093 serum samples assayed, 1,104 were pos-

97
113
102
100
412

itive for IgG antibody to VZV, giving an overall prevalence

rate of 52.8%. There was no statistically significant differ-
ence in the prevalence rate between males and females
(49.4% and 55.2%, respectively). The overall seroprevalence
Mean age

of varicella increased with age from 15.5% in the 9-month–

12.3
12.8
12.3
12.5
12.5

4-year-old group to 75.9% in 20–29-year-old group (Table

2).
Association between geographic regions and urban/ru-
ral living with seropositivity. The overall prevalence of the
varicella-zoster virus varies significantly by region: Central
Number

subjects

2,093
487
576
538
492
of

and Southern areas 42.7% and 41.7% respectively, Northern

and Northeastern areas 69.0% and 57.9%, respectively (Ta-
ble 2). In the total study population the prevalence was sim-
ilar in rural and urban areas (Table 3); however, in Central
and Southern areas where a warmer climate pattern lasts all
Northeast

year, the seroprevalence is lower in rural areas (Figure 1).

Total
centers

Center

The geographic and climatologic data of the 4 study cen-

Study

South
North

ters and 4 study regions in the year 1997 are shown in Table
4 and Table 5.
 TABLE 2
Varicella-zoster virus (VZV) prevalence by age group and centers

Central South North Northeast Total

VZV sero- 95% CI VZV sero- 95% CI VZV sero- 95% CI VZV sero- 95% CI VZV sero- 95% CI
Age prevalence prevalence prevalence prevalence prevalence
(yr) (%) LL UL (%) LL UL (%) LL UL (%) LL UL (%) LL UL

9 months–4 11.3 5.8 19.4 6.2 2.5 12.3 33.3 24.3 43.3 12 6.4 20.0 15.5 12.2 19.4
5–9 36.0 26.6 46.2 26.3 18.5 35.4 72.9 63.9 80.7 54.3 43.7 64.6 47.7 42.8 52.5
10–14 51.0 40.6 61.4 45.8 36.7 55.2 75.2 66.4 82.7 71.7 62.1 80.0 61.1 56.3 65.6
15–19 50.0 39.7 60.3 58.3 48.5 67.8 80.4 71.4 87.6 65.0 54.6 74.4 63.5 58.6 68.2

CLIMATIC FACTORS AND POPULATION DENSITY ON VZV

20–29 65.5 55.2 75.0 70.3 61.3 78.2 81.8 72.8 88.9 87.4 79.0 93.3 75.9 71.5 80.0
Total 42.7 38.3 47.2 41.7 37.6 45.8 69.0 64.6 72.9 57.9 53.4 62.3 52.7 50.6 54.9
Number of
subjects 497 576 538 592 2,093
VZV ⫽ varicella-zoster virus; CI ⫽ confidence interval; UL ⫽ 95% confidence interval upper limit; LL ⫽ 95% confidence interval lower limit.

TABLE 3
Age-specific varicella-zoster virus (VZV): prevalence rate by center, in an urban or rural setting

Central South North Northeast Total

VZV sero- VZV sero- VZV sero- VZV sero- VZV sero-
prev- 95% CI prev- 95% CI prev- 95% CI prev- 95% CI prev- 95% CI
Age alence alence alence alence alence
Address (yr) (%) LL UL (%) LL UL (%) LL UL (%) LL UL (%) LL UL

Rural 9 mo.–4 8.51 2.36 20.38 7.35 2.43 16.33 26.42 35.26 40.33 12.73 5.27 24.48 13.45 9.26 18.64
5–9 24.49 13.34 38.87 13.79 6.15 25.38 81.84 69.97 90.08 61.36 45.50 75.64 46.30 39.51 53.19
10–14 41.67 27.61 56.79 35.09 22.91 48.87 79.03 66.82 88.34 76.92 63.16 87.47 58.90 52.08 65.49
15–19 26.53 14.95 41.08 45.83 31.37 60.83 80.77 67.47 90.37 66 51.23 78.79 55.28 48.08 62.31
20–29 60.78 46.11 74.16 71.21 58.75 81.70 83.64 71.20 92.23 87.76 75.23 95.37 75.57 69.35 81.08
Urban 9 mo.–4 14 5.82 26.74 4.44 0.54 15.15 40.82 27 55.79 11.11 3.71 24.05 17.99 12.79 24.22
5–9 47.06 32.93 61.54 39.29 26.50 53.25 62.26 47.89 75.21 48 33.66 62.58 49.05 42.10 56.02
10–14 60.42 45.27 74.23 55.56 42.49 68.08 70.91 57.10 82.37 66.67 52.53 78.91 63.18 56.44 69.57
15–19 73.47 58.92 85.05 68.33 55.04 79.74 80 66.28 89.97 63.83 48.52 77.33 71.36 64.67 77.43
20–29 71.11 55.69 83.63 69.09 55.19 80.86 79.55 64.70 90.20 86.96 73.74 95.06 76.32 69.62 82.17
CI ⫽ confidence interval; LL ⫽ 95% confidence interval lower limit; UL ⫽ 95% confidence interval upper limit.

133
134 LOLEKHA AND OTHERS
FIGURE 1. Varicella-zoster virus prevalence by age and region in four study areas.
Association between history and seropositivity. Avail-
able data on 705 subjects showed an association between the
past history of VZV and seropositivity. There was a positive
correlation between a history of varicella and seropositivity;
85.2% (601 of 705) of the participants who could recall a
clinical history of chickenpox tested positive for VZV anti-
bodies. However, for 33.9% (425 of 1,255) of subjects who
were seropositive, there was no history of clinical varicella.
Analysis of data in a logistic regression model for the
Central and Southern areas showed age (P ⬍ 0.005), urban
or rural address (P ⬍ 0.005), and previous occurrence of
varicella (P ⬍ 0.005) as significant variables but not income/
socioeconomic background (P ⬎0.05).
DISCUSSION
The overall age-specific VZV seroprevalence rate in our
study is similar to previous reports from other tropical coun-
tries in which seroprevalence reaches ⬎ 90% only in those
over 30 years of age.9–12 Among the 15–19-year-old group,
less than 65% of the study population were seropositive,
TABLE 4
The geographic data of the four study centers in the year 1997
Total
Study site/region population*
Bangkok/Central 5,604,772
Song Kla/Had Yai‡/Southern 1,191,233/134,764
Chiang Mai/Northern 1,573,757
Khon Kaen/Northeastern 1,726,594
* Data from the National Statistical Institute.
† Data from data processing subdivision, Climatology Division, Meteorological Department.
‡ Had Yai is a large district in the Song Kla province.
increasing to 75.9% in the 20–29-year-old group. These val-
ues are similar to those obtained in the Philippines9 and in
a previous study in Bangkok, Thailand, where the seroprev-
alence was 69.2% at 20–29 years of age and increased to
96.1% at 30–39 years of age.13 Consequently, our study was
restricted to subjects up to 29 years of age. Varicella vaccine
has been available in Thailand only since 1997 and is limited
to the private market with no current plans for inclusion in
the national expanded program of immunization (EPI) pro-
gram.
It has been suggested that the transmission potential of
the VZV virus might be adversely affected by a combina-
tion of high ambient temperatures and humidity in tropical
regions.12 This is supported by the seasonal and regional
variations in acute disease found within some Southeast
Asian countries. A review of data from Southeast Asia
showed that the peak incidence of varicella infection oc-
curred during cooler months and in cooler, more temperate
regions.11 In Kerala, India, the highest levels of varicella-
associated mortality occur in January, the coolest part of
the year.12 In Thailand the 1995, 1996, and 1997 Annual
Longitude† Latitude† Above sea
(east) (north) level† (meter)
100.34 13.44 2
100.36 7.12 4
98.59 18.47 312
102.5 16.26 165
 CLIMATIC FACTORS AND POPULATION DENSITY ON VZV
The climatological data of the four study centers and four regions in the year 1997
*Mean
maximum
temperature
Study site/region (⬚C)
Bangkok/Central 33.9/34.2
Song Kla/Had Yai/Southern 33.9/32.0
Chiang Mai/Northern 32.1/33.2
Khon Kaen/Northeastern 33.3/32.9
* Mean maximum and minimum temperature ⫽ mean of the monthly average maximum and minimum temperature over the entire year 1997. Data from National Statistical Institute.
† Mean extreme maximum and minimum temperature ⫽ mean of the monthly highest and lowest temperature over the entire year 1997.
‡ Data: data processing subdivision, Climatology Division, Meteorological Department.
Epidemiological Surveillance Reports showed a seasonal
pattern, with a higher incidence in the cooler months of the
year.16–18 These surveillance reports also included reported
cases by age group in each of the study areas (Table 6).
Between 1995–1997, some 35%–40% of reported cases
were of adolescents aged 15 years or more in the Central
and Southern areas compared to 15%–20% in the Northern
and Northeastern areas.16–18 The results of our study are
comparable with these reports. We found that the Northern
area had the highest seroprevalence rate of varicella infec-
tion in all age groups. The susceptibility in adolescents and
adults was still higher in the Northern area than in temper-
ate countries. Our data confirm the significantly higher se-
roprevalence rates in the Northern as compared to the
Southern and Central area of Thailand. With its higher al-
titude, the cooler Northern areas are more comparable to
temperate regions. Assessing the climatological character-
istics of the 4 regions, the mean of the extreme minimum
temperature (mainly due to relative altitude) is the most
important factor contributing to an increase of VZV sero-
prevalence. In fact the Southern area with the highest mean
extreme minimum temperature of 22⬚C had the lowest se-
roprevalence rate of 41.7% decreasing to 42.7% in the Cen-
tral area (19.2⬚C), 57.9% in the Northeastern area (12.3⬚C)
and 69.0 % in Northern areas (10.1⬚C).
The second most important factor of delayed onset of var-
icella was rural versus urban living. The most likely expla-
nation for this is population density. In urban settings, higher
population densities may partially overcome the transmis-
sion-interrupting effect of a tropical climate. In India, prior
to large scale immunization, a similar phenomenon was de-
scribed for measles,19 which is even more infectious than
varicella. The empirical observation of varicella affecting
adults in rural settings of tropical countries dates back to
1976;20 however, epidemiologic comparisons with urban
populations were published only 20 years later.15 In a study
from West Bengal, India, nearly all urban adults were im-
mune, and only adults in rural areas were susceptible to var-
icella infection.15 The authors concluded that the delayed on-
set of varicella in tropical areas is a purely rural phenome-
non. The current study of a larger sample size confirmed the
increased risk for delayed-onset varicella in rural populations
of tropical areas. The high seroprevalence rate in urban West
Bengal of 96% at the age of 25 years can obviously not be
explained by impact of climate alone as both maximum and
minimum temperatures of West Bengal (average maximum
temperature is 37–38⬚C, average minimum temperature is
135
TABLE 5
†Mean †Mean
*Mean extreme extreme
minimum maximum minimum ‡Annual ‡Mean
temperature temperature temperature rainfall humidity
(⬚C) (⬚C) (⬚C) (mm) (%)
25.6/24.3 37.4/41.5 19.2/12.0 1,063.7/1,005.6 69/70
26.1/23.9 35.9/38.3 22.0/15.7 2,192.0/1,693.7 78/79
20.3/21.1 39.0/42.2 10.1/5.4 908.6/1,094.1 71/73
22.1/22.1 39.5/40.0 12.3/10.6 898.0/1,308.9 71/73
22–23⬚C) are comparable with the tropical climate of Central
and Southern areas. However, in contrast, the population
density in Calcutta, West Bengal, (5,400/square kilometer)21
is higher than in Thailand and may thus have contributed to
the high seroprevalence rate observed by Mandel and oth-
ers.15 It is widely accepted that there is a high correlation
between a history of varicella infection and seropositivi-
ty,9,10,13,22 and this was also the case in our study. In line with
another study from Thailand,13 we found family income was
not significantly associated with the varicella seroprevalence
rate.
In conclusion, similar to other reports from tropical
countries, the prevalence pattern showed seroconversion in
late childhood or young adulthood, which is often associ-
ated with greater morbidity and mortality. Furthermore, this
study clearly showed a regional variation most likely due
to climatic differences in 4 regions of Thailand. In the
warmer areas a marked delay in natural infection was found
with high extreme minimum temperature being the most
critical climatic factor. In addition, especially in these re-
gions, the pattern of adolescent and adult susceptibility to
VZV is more distinct in rural areas. Thus, our study results
suggest that increased adolescent and adult susceptibility to
VZV in the tropics is related to both climate and population
density.
Consequently, a vaccination program in Thailand and in
other tropical countries should include administration to
susceptible adolescents and adults who are at high risk of
developing severe varicella with complications. Routine
varicella vaccination programs should also be directed at
children, in whom seroprevalnce is low, accessibility is
generally high, and one dose of the vaccine is sufficient.
Acknowledgments: We are grateful to Miss Dusadee Chareonpipop
for performing the anti-VZV serology assay.
Financial support: This study was supported by a grant from
SmithKline Beecham Biologicals, Rixensart, Belgium.
Authors’ addresses: Somsak Lolekha, Chief of Infectious Disease,
Department of Pediatrics, Faculty of Medicine, Ramathibodi Hos-
pital, Rama VI Road, Mahidol University, Bangkok 10400, Thai-
land. Watcharee Tanthiphabha, Department of Pediatrics, Faculty of
Medicine, Chiang Mai University, Chiang Mai 50002, Thailand.
Penpark Sornchai, Pediatrics Unit, Nakornping Hospital, Maerim
District, Chiang Mai 50002, Thailand. Pensri Kosuwan and Sumit
Sutra, Department of Pediatrics, Faculty of Medicine, Khon Kaen
University, Khon Kaen 40002, Thailand. Boonyarat Warachit and
Suda Chup-Upprakarn, Pediatrics Unit, Had Yai Regional Hospital,
Had Yai, Song Kla 90110, Thailand. Yanee Hutagalung, John Weil
136 LOLEKHA AND OTHERS

and Hans L. Bock, SmithKline Beecham Biologicals, Rue de

I’Institut 89, B-1330, Rixensart, Belgium.

14,332
3.30
21.40
39.10
19.20
11.20
5.70
1997
(%)

–
Reprint requests: Somsak Lolekha, Chief of Infectious Disease, De-
partment of Pediatrics, Faculty of Medicine, Ramathibodi Hospital,
Mahidol University, Rama VI Road, Bangkok 10400, Thailand Tel/
fax 662-201-1674, E:mail address: rasll@mahidol.ac.th.
Northeast

14,105
3.40
21.30
41.90
19.30
9.20
4.80
1996
(%)

–
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