cancer incidence in thailand, 1988 19911 - cancer...

Vol. 4. 475-483, July/August 1995 Cancer Epidemiology, Biomarkers & Prevention 475

Cancer Incidence in Thailand, 1988_19911

V. Vatanasapt, N. Martin, H. Sriplung, K. Chindavijak,S. Sontipong, S. Sriamporn, D. M. Parkin,2 and J. Ferlay

Faculty of Medicine. Khon Kaen University, Srinagarind Hospital, Khon Kaen

401)02. Thailand IV. V., S. Sr.]; Faculty of Medicine, Chiang Mai University,

Maharaj Nakorn Hospital. Chiang Mai 50002, Thailand (N. M.J; Faculty of

Medicine, Prince of Songkla University. Hat-Yai, Songkhla 901 12, Thailand

[H. S.]: National Cancer Institute, Rama VI Road. Bangkok 10400, Thailand

[K. C.. S. So.]: and International Agency for Research on Cancer, 150 coors

Albert-Thomas. 69372 Lyon Cedex 08. France ID. M. P., J. F.]

Abstract

Results from three cancer registries (Chiang Mai, KhonKaen, and Songkhla) in different regions of Thailand andfrom a cancer survey in the population of Bangkokduring the years 1988-1991 are presented, together withan estimate of the incidence of cancer for the country asa whole. Overall, liver cancer is the most frequentmalignancy, but there are large regional differences inincidence and in histological type, with very high rates ofcholangiocarcinoma in the northeast (associated withendemic opisthorchiasis) but a more even distribution ofhepatocellular carcinoma. Lung cancer is second infrequency, with the highest rates in northern Thailand,where the incidence in women (Age Standardized Rate,37.4 per 100,000) is among the highest in the world. Alink with tobacco smoking is suggested by similarly raisedrates, especially in women, for cancers of the larynx andpancreas. Cervical cancer is the most commonmalignancy in women, with relatively little regionalvariation in risk, while the incidence of breast cancer islow. Other cancer sites showing moderately increasedrates include the lip and oral cavity, particularly infemales from the north and northeast, where the chewingof betel nut remains common among older generations,nasopharyngeal cancer, carcinoma of the esophagus inthe southern region, and penile cancer, especially in thenorth and northeast. Previous studies which haveinvestigated the etiological factors underlying thesepatterns are reviewed, and the implications for futureresearch and for national cancer control policies arediscussed.

Introduction

In Thailand, as in several other countries in Asia, rapid socio-

economic development and the control of noncommunicabledisease have resulted in the emergence of cancer as the thirdmost common cause of death after “heart disease” and accidents

and poisoning (1). Although in the past some information on

cancer patterns was available from hospital statistics, it was not

Received I ))/ I 9/94: revised I /5/95; accepted I /6/95.I Financial support for this project was provided by the Cancer Research Foun-

dation for the National Cancer Institute and the Oncological Society of Thailand.2 To whom requests for reprints should be addressed.

until 1986 that the first population-based cancer registry was

founded at Chiang Mai, in the northern region (2). This was

followed in 1988 by the registry in Khon Kaen in the northeast

(3), and in 1990 in Songkhla in the south. In 1991, it was

decided that these three registries would produce a combined

analysis of their results, including estimates for the country as

a whole. Because there was no registry present in the densely

populated central region, a population-based cancer survey was

planned and carried out in Bangkok in 1992, with the objective

of collecting data on residents of the metropolitan areadiagnosed with cancer between 1988 and 1990.

This study is a summary of the full report on the project

(4), which presents an overview of the cancer profile in the

country as a whole, a comparison of regional differences, and

a review of previous epidemiological studies. It thus provides a

guide to future priorities for research into cancer cause and

control.

Materials and Methods

Geography and Peoples

The Thai people almost certainly originated in southern

China and migrated southwards to occupy what is nowmodern Thailand, Laos, and eastern Myanmar up to the 13th

century AD. This population is culturally and religiously(almost entirely Buddhist) quite homogeneous, with regionaldifferences but variations in the basic pattern. Subsequent

migrations brought large numbers of Chinese. These were

estimated to be 2.5 million in 1958, but migration virtuallyceased in 1948; individuals of Chinese origin have taken

Thai names and are now assimilated to varying degrees,

making up about 10-14% of the population. Most Thais of

Chinese origin live in central Thailand (especially Bangkok)

or other urban centers. About 10% of the population iscomprised of other ethnic groups, including some 500,000

hill tribe peoples of northern Thailand, most originating insouthern China and migrating in the last 200 years, and the

peoples of the southernmost seven provinces, who are ofMalay origin and predominantly Muslim in religion.

Thailand is divided into 72 provinces grouped within 4

geographical regions: the northern, northeastern, southern, and

central regions (Fig. 1). The northern region is mountainouswith relatively cool winter temperatures and is the home of

several minority tribes, some indigenous and others are more

recent migrants. The northeast is a semi-arid plateau which,

because it is the poorest part of the country, is attracting

increasing industrial development. The population is culturally

similar to that of neighboring Laos and speaks a distinct lan-

guage (Isan) related to modern Lao. The central region is one

of the most fertile rice-growing areas on earth and contains the

densely populated Bangkok Metropolis (population, 5.8 mil-lion). The south is physically quite heterogeneous, with its long

coastline and hilly interior given over to agriculture (fruit andrubber plantations), fishing, and tin mining.

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I

Songkhla

476 Cancer in Thailand

Fig. 1. Thailand: regions, and the areas covered by the cancer registries.

Sources of Cancer Data

Chiang Mai. A population-based registry was founded in 1986in the University hospital. Data on cancer patients in thishospital and in 6 private and 29 community hospitals in theprovince of Chiang Mai (Fig. 1) are actively collected by theregistry staff. Cases for the period 1988-1991 are included.

Khon Kaen. A population-based registration was started in1987, with data collection from the registry of the University

hospital, as well as from the regional hospital and other (27)public and private hospitals in the Khon Kaen province (Fig. 1).Cases for the period 1988-1991 are included.

Songkhla. This registry began operation in 1990, receivingdata from the two hospital registries in the University city (HatYai), as well as one other major hospital in the provincialcapital (Songkhla). Cases for the period 1989-1991 areincluded.

All three cancer registries use death certificates as anadditional source of information on cancer cases, although thereis some variation in the procedures for the follow-up of deathcertificate notifications. A certified cause of death is not veryaccurate in Thailand, with between 7 and 19% of certificates

issued by nonmedical personnel. Cancer is clearly underenu-merated, with many deaths recorded as “heart failure” or “oldage.” However, it is unlikely that there are many “false-posi-tive” diagnoses; therefore, death certificates provide a usefulcheck on probable cancer cases not identified during life.

Bangkok. Bangkok has no population-based registry. A cancersurvey was carried out during 1991 to identify all cancer casesin the residents of Bangkok diagnosed in the 3-year period 1988to 1990. Data were collected from all government and majorprivate hospitals (with more than 100 beds) in the city andadjacent provinces. The three university hospitals and fewmedical center hospitals already had well-established hospital

cancer registries. In the other government hospitals, data oncancer cases were collected via medical record departments

(including in- and out-patients) and from the pathology depart-ments. For private hospitals, most cases were identified from

in-patient records. All death certificates for Bangkok residentswho died during 1988-1990 and which mentioned cancer as a

cause were compared with the file of registered cases, andunmatched deaths due to “cancer” were included as “deathcertificate only” cases, with no trace-back to the originalsource.

Population Denominators

The person-years at risk were calculated for the relevant periodsin each registration area, based upon annual projections by agegroup and sex (5). The average annual populations of the four

areas were: 1.33 million for Chiang Mai, 1.74 million for KhonKaen, 1.17 million for Songkhla, and 5.78 million for Bangkok.Data from the 1990 census (6) were used in the estimation of

incidence in the national population. The regional populationsare: northern, 10.6 million; northeastern, 19.0 million; southern,7.0 million; and central, 17.9 million.

Methods

Average annual incidence rates, per 100,000, were calculatedwith age standardization performed by the direct method usingthe “world standard population.” ICD-O (7) was used by allcenters to code cancer cases; this was converted to ICD-9 forreporting purposes.

The data quality in the different centers was evaluated bycomparing the percentage of cases with histological verificationof diagnosis and the percentage registered from information onthe death certificate only (8).

To estimate cancer incidence in the national population in1990, the average annual age- (5-year age group) and sex-specific incidence rates in the four registries (Chiang Mai,1988-91; Khon Kaen, 1988-91; Songkhla, 1989-91; andBangkok, 1988-90) were applied to the populations of therespective regions in 1990. The sum of these provides the

estimated numbers of cancers by sex, site, and age group for thecountry as a whole, and the corresponding incidence rates arecalculated using the 1990 census population.

Results

There were an estimated 29,950 new cancer cases in men and29,517 in women in Thailand in 1990. Fig. 2 illustrates thepercentage distribution of the 10 most common cancers in eachsex. Tables 1 and 2 show, for males and females, respectively,the age-standardized incidence rates for the major cancers in

each of the four registry areas and the estimate for Thailand asa whole. For comparison, age-standardized rates from the

United States, Singapore, and Osaka (Japan) are also shown (8).



Liver

Oral cavity � 3.2

Oesophagus � 2.5

Prostate � 2.2

Cancer Epidemiology, Blomarkers & Prevention 477

3 The abbreviations used are: ASR, Age Standardized Rate; OR, odds ratio; OV,

Opisthorchis vicerrini.

Lung

Males

� 15.6

Stomach � 3.6

Colon � 3.5

Bladder � 3.1

Skin’ � 2.5

Larynx � 2.4

26.8

Females

Cen,is _____ _______

Liver 12.0

Breast � 11.1

Lung � 8.8

Ovary � 3.7

Oral Cavity � 3.6

Thyroid � 3.2

Colon � 2.9

Leukaemia � 2.7

Skin’ � 2.5

18.9

#{149}excluding melanoma

Fig. 2. The ten leading cancers in Thailand, 1990, as a percentage of the total, by sex.

The proportion of cases registered with histological con-

firmation of diagnosis, or with no information other than thatfrom the death certificate, is shown for the major cancer sites in

Table 3.

Liver Cancer. The very high incidence of liver cancer in thenortheastern region (which contains about 34.9% of the na-tional population) results in this remaining the major cancer ofmen in the whole country, with an estimated 8000 new cases

every year. Liver cancer is also the second most frequent cancer

of women (12% of all cancers). Less than one-quarter of theliver cancer cases registered had been biopsied, but there werelarge regional differences in the histological type amongst thosewhich had (Table 4). In Khon Kaen, 89% of liver cancers werecholangiocarcinomas, compared with only 2% in Songkhla in

the south, where hepatocellular carcinoma predominates (96%of cases), as it does in Bangkok (71%). Although biopsy ratesmay not be identical for the different types of liver cancer, it is

unlikely that cholangiocarcinomas are overrepresented in bi-opsy series, since diagnosis is relatively straightforward usingultrasound and needle biopsy is relatively hazardous.

Lung Cancer. Lung cancer is second in importance in males(15.6% ofcancers) and fourth in women (8.8%). The incidence,in both sexes, is much higher in the north (Chiang Mai) thanelsewhere in Thailand, and the incidence in females (ASR,337.4/100,000) is very high, considerably above that in the

United States, for example (Table 2). Fifty-one % of the lungcancers registered with a specified histology are adenocarcino-

mas (45% in males and 63% in females), with 33.7% squamous

cell carcinomas (38% in males and 25% in females; Table 5).

There was little geographical variation in this pattern.

Cervical Cancer and Breast Cancer. In women, the major

cancer is cervical cancer (18.9% of cancers in women), almost

twice as frequent overall as cancer of the breast (1 1 . 1 %).

Eighty-seven % of cervical cancer cases were squamous cell in

type, with I 1% adenocancinomas; incidence rates were highest

in Chiang Mai and lowest in Songkhla in the south. Breast

cancer incidence is low, particularly so in the more rural north-

east and south. Fig. 3 shows the age-specific rates for these two

cancers. Cervical cancer incidence rises to a maximum in agegroup 55-59 and then declines, while for breast cancer, mci-

dence rates increase until age 50-54, with almost no changewith age thereafter.

Other cancer sites showing moderately increased rates

include the lip (in Khon Kaen) and oral cavity, particularly in

females, nasopharyngeal cancer, carcinoma of the esophagus in

Songkhla, and cancer of the penis. Incidence rates for other

cancers of the gastrointestinal tract (stomach, colon, rectum,

and pancreas) are low, as are those for the kidney, bladder, and

prostate.

Skin Cancer. Despite the fact that all ofthe registries recordedall diagnosed cases of skin cancer, the incidence rates are low.

Of all skin cancer cases, 10.8% were melanomas, one-half of

which were located on the lower limbs and one-quarter on the

trunk. The distribution of nonmelanoma skin cancers by sex,

histological type, and site is shown in Table 6. In men, squa-

mous cell carcinomas are more common than basal cell; the

reverse is true in women. In men, squamous cell carcinomas

occur mainly on the lower limbs, while in women, the face is

the most common site. Basal cell cancers are located mainly on




Ta ble I Age-standa rdized inciden cc rates (world standard) in Th ailand and corn parison regist ries (male)

Site

Th I d51 an Japan”

(Osaka)

1983-1987

Singapore1983-1987

Chin’se Mala� y

US” (SEER)1983-1987

White BlackNational

estimate 1990

Bangkok

1988-1991)

Chiang Mai

1988-1991

Khon Kaen

1988-1991

Songkhla1989-1991

Lip ( I 4))) )).2 0. 1 0.4 0.3 0.2 0. 1 0. 1 0.3 2.3 0.1

Oral cavity (141-145) 5.1) 4.3 6.9 3.3 8.2 3.4 4.4 2.4 7.2 9.1

Nasopharynx (147) 3.3 3.6 3.6 3.5 2.4 0.6 18.1 4.3 0.5 0.8

Other pharynx (146. 148-149) 3.7 2.7 6.8 1.1 7.5 1.5 2.5 0.8 3.6 7.9

Esophagus (150) 4.1 4.3 3.9 1.7 9.7 8.4 10.9 1.2 4.1) 13.9

Stomach (151) 5.8 4.2 10.7 5.2 3.2 73.6 34.7 6.4 8.0 12.4

Colon (153) 5.5 5.8 5.6 5.4 5.1 14.8 2t).2 6.9 31.1 28.5

Rectum (154) 3.4 3.6 4.2 2.8 3.0 11.6 15.2 8.3 15.4 10.1

Liver (155) 40.5 9.7 27.9 94.8 10.7 41.5 26.8 13.2 2.4 4.2

Gallbladder. etc. (156) 2.2 1.1) 5.1 2.4 0.4 6.0 1.8 1.4 1.6 1.1

Pancreas (157) 1.9 1.5 3.2 1.0 2.7 8.9 5.1 4.1 8.2 11.1

Larynx (161) 4.)) 3.6 8.0 1.5 4.5 4.1) 6.1 1.2 6.8 9.1

Lung (162) 25.)) 21.9 49.8 14.7 16.3 41.5 69.7 34.0 64.3 90.0

Melanoma of skin (172) )).5 0.2 1.2 0.4 0.6 0.2 0.4 0.5 lt).8 0.4

Other skin (173) 4.1 2.8 6.2 4.3 3.7 1.2 8.9 4.3 4.6’ 2.5’

Prostate (185) 3.8 2.8 6.5 2.7 4.5 6.6 7.6 9.0 61.8 82.0

Penis, etc. (187) 2.)) 1(1 3.2 1.8 3.2 t).5 0.7 0.2 0.8 0.7

Bladder (188) 4.9 5.3 8.1 3.4 3.0 8.2 7.4 6.2 23.9 10.5

Thyroid (193) 1.2 0.8 1.6 1.3 1.6 1.1 2.0 2.8 2.2 1.0

Non-Hodgkin lymphoma 2.8 2.3 4.7 2.5 1.5 6.1 6.0 5.5 13.6 7.4(200, 202)

Hodgkin’s disease (201) 0.7 0.3 1.4 0.8 0.5 0.5 0.6 1.2 3.4 2.0

Leukemia (21)4-21)8) 3.7 2.6 5.1 4.7 3.4 5.8 5.5 5.2 10.4 7.6

All sites, excluding other skin 149.6 94.7 202.1 192.7 107.2 265.4 266.2 131.9 325.8 348.8(140-208 excluding 173)

.‘ Source, Ref. 8.

/� US. United States; SEER, Surveillance. Epidemiology, and End Results Program.‘ Excludes squamous and basal cell carcinomas.

the face (63% in men, 82% in women), with 9.4% of cases on

the trunk in men.

Thyroid Cancer. Thyroid cancer is three times more frequentin females than in males. In women, the highest incidence isobserved in Khon Kaen, where the majority of tumors werefollicular cell in type. The ratio of follicular to papillary carci-nomas was 1.4, compared to an average of 0.46 elsewhere.

Discussion

There is quite a large difference in the incidence rates for cancer

as a whole in the different registries. In particular, the overallincidence in Bangkok is low (ASR: 97.4 and 87.5 in men andwomen, respectively) compared with Chiang Mai (ASRs, 208.3

and 189.6) and Khon Kaen (ASRs, 196.9 and 154.4). In part,this reflects the quite different risks of different cancers with,

for example, very high rates of liver cancer in Khon Kaen.However, there is almost certainly a degree of underenumera-

tion in Bangkok, where the data were derived from a one-timeretrospective survey in over 40 hospitals rather than from an

established concurrent cancer registration. Thus, for some can-cers where one might have anticipated rather little regionalvariation in incidence (leukemia, brain and nervous system,melanoma, nonmelanoma skin cancer, and pancreas), the mci-dence rates are almost always lower in Bangkok than in theprovincial registries. Similarly, the percentage of cases regis-tered with histological verification is higher in Bangkok, formost cancer sites, than in Chiang Mai and Khon Kaen (Table

3). Although this may be the result of better diagnostic facilitiesin the capital, it seems equally likely to be the consequence of

failure to identify cases diagnosed without laboratory assis-

tance. This probable underregistration should be taken into

account in interpreting the data in Tables 1 and 2. To a lesserextent, the same questions concerning completeness can be

raised in relation to Songkhla, since some of the data in the

period analyzed were collected retrospectively; incidence rates

for same sites appear rather low, and the percentage of casesdiagnosed histologically is relatively high.

In consequence, it is likely that the data for incidence in

Thailand are an underestimate of the true situation. The mci-dence rates for cancer at all sites (excluding skin; 149.6/

100,000 for men and 125.2/100,000 for women) are about

one-half those observed in Western countries but not verydifferent from those elsewhere in the region. The estimated

all-sites, age-standardized incidence rates (excluding other skin

cancer) for southeastern Asia in 1985 are 122.1/100,000 in men

and 137.7/100,000 in women (9).

The accuracy of the national estimates also depends upon

how representative of their respective regions are the incidence

patterns in the four registration areas. There are few dataavailable with which to check this; however, the regional pat-

terns from the national hospital registration scheme (10), whichwas estimated to cover 38% of hospital admissions in 1982, are

broadly similar, although there are some exceptions. For ex-

ample, lung cancer comprised only 9.2% of female hospital

registrations in the northern region, compared to 18.6% ofregistrations in the Chiang Mai province (10).

Cancer of the Oral Cavity. Cancer of the oral cavity is

common in Thailand with similar rates in the two sexes (in

other parts of the world, males outnumber females by betweentwo and ten to one). In the north (Chiang Mai) and northeast



Cancer Epidemiology, Biomarkers & Prevention 479

Tab le 2 Age-standardiz ed (world sta ndard) incidence rates in Thail and and comp arison registrie a (female)

Site

Th 1 daian Japan”

(Osaka)

1983-1987

Singapore”1983-1987

Chinese Malay

US” (SEER)1983-1987

White BlackNational estimate

1990

Bangkok

1988-1990

Chiang Mai

1988-1991

Khon Kaen

1988-1991

Songkhla

1989-1991

Lip (141)) 1.4 0.5 0.4 3.5 0.8 0.1 0.2 0.1

Oral cavity (141-145) 3.4 2.6 4.9 3.8 3.7 1.4 1.6 2.9 3.7 3.0

Nasopharynx (147) 1.7 1.8 2.1 1.7 0.9 0.2 7.4 1.5 0.2 0.3

Other pharynx (146, 148-149) 1.0 0.5 2.4 0.6 1.3 0.3 0.3 0.4 1.3 1.7

Esophagus (150) 1.4 1.0 2.0 0.8 3.1 1.8 2.7 0.9 1.3 3.6

Stomach (151) 2.9 2.2 6.1 2.3 1.0 32.7 15.6 5.4 3.5 5.6

Colon (153) 3.7 3.5 4.6 3.9 2.8 10.1 18.1 5.5 23.6 24.2

Rectum (154) 2.2 2.2 3.5 1.6 1.7 6.3 10.5 6.6 9.6 8.1

Liver (155) 16.3 2.7 12.2 39.4 1.9 9.7 7.0 6.3 1.1 1.4

Gallbladder. etc. (156) 1.9 0.7 4.0 2.3 0.7 5.8 1.8 0.9 1.7 1.3

Pancreas (157) 1.3 0.8 3.2 0.6 1.2 5.0 3.4 2.0 6.0 8.6

Larynx (161) 0.7 0.3 2.7 0.1 0.3 0.3 0.7 0.8 1.4 2.0

Lung (162) 12.1 6.1 37.4 4.4 4.3 11.7 21.9 12.1 29.9 28.1

Melanoma of skin (172) 0.4 0.1 0.5 0.7 0.3 0.2 0.3 0.5 8.8 0.6

Other skin (173) 3.3 2.0 4.1 4.4 3.2 0.9 7.4 2.8 0.6’ 0.6”

Breast (174) 13.5 15.9 16.9 9.7 12.1 21.9 31.6 23.2 89.2 65.0

Cervix uteri (1St)) 23.4 20.9 29.7 23.9 18.5 13.2 17.5 8.8 7.3 11.7

Corpus uteri (182) 2.9 2.8 4.2 2.5 2.2 2.7 6.4 4.2 19.2 9.7

Ovary, etc. (183) 4.5 3.4 4.8 6.2 3.2 5.5 8.6 9.6 12.5 7.4

Bladder (188) 1.4 1.2 3.2 0.7 0.5 2.0 2.4 1.3 5.9 3.8

Thyroid (193) 3.6 2.3 3.1 5.4 3.6 3.3 5.9 4.8 5.8 2.7

Non-Hodgkin lymphoma 2.1 1.6 2.5 2.9 0.7 3.4 3.9 4.7 8.9 5.0

(2(X), 202)

Hodgkin’s disease (201) 0.3 0.3 0.5 0.4 0.2 0.2 0.3 0.4 2.5 1.1)

Leukemia (2()4-208) 3.2 2.5 4.7 3.4 3.2 3.8 3.6 3.6 6.4 4.9

All sites, excluding other skin 125.2 85.4 185.5 150.0 78.4 155.2 185.6 1 18.0 276.3 226.5

(140-208 excluding 173)

“ Source. Ref. 8.

I, US, United States; SEER, Surveillance, Epidemiology, and End Results Program.

‘. Excludes squamous and basal cell carcinomas.

Table 3 Quality indicators: percentage of cases histologically verified, and

registered from death certificate only, by registry and major cancer site

Bangkok Chiang Mai Khon Kaen Songkhla

HV” DCO HV DCO HV DCO HV DCO

Oral cavity (140-145) 87 3 90 1 82 3 84 3

Esophagus (150) 68 12 59 - 48 8 69 7

Stomach (151) 66 13 73 6 57 14 72 14

Colon (153) 63 12 67 2 47 21 72 6

Liver(l55) 48 23 39 6 11 19 39 14

Larynx (161) 79 5 84 - 70 7 75 5

Lung (162) 63 15 59 4 46 19 67 10

Skin (172-173) 97 1 97 1 87 1 94 3

Breast (174) 85 3 89 2 76 3 79 10

Cervix (180) 91 1 96 0 70 9 85 3

All sites 76 10 67 9 43 18 74 10

“ HV, histologically verified; DCO, death certificate only; - , zero; 0, <0.5.

(Khon Kaen), betel quid chewing remains relatively commonamong female villagers, although the habit has declined inrecent decades (1 1). Local studies have shown this to be asignificant risk factor in both sexes (12, 13). The reason why lipcancer comprises such a high proportion of oral cancers infemales in Khon Kaen (the incidence rate is the highest re-

corded in the world), but is relatively rare elsewhere, is notclear. In men, the highest incidence is observed in Songkhla,which has also the highest rates for cancers of the pharynx and

esophagus (see below); these cancers share common riskfactors (tobacco and alcohol) with oral cancer.

Nasopharyngeal Cancer. The incidence of nasopharyngealcancer is intermediate between the very high rates observed insouthern China and those of European populations. There is a

strong genetic component to the risk of nasopharyngeal cancer(14), so that areas in which a significant proportion of the

population has some Chinese ancestry, such as Thailand, mightbe expected to show an increase in risk (15). Consumption ofsalted fish is a well-known risk factor in Chinese populations

(16). A case-control study by Sriamporn et a!. (17) found that

the consumption of sea-salted fish was a risk factor (OR, 2.5)

in the population of northeast Thailand, as were agricultural

occupations and wood-cutting (OR, 8.0).

Esophageal Cancer. The incidence of esophageal cancer israther low in Thailand, except for Songkhla in the south, where

rates in both sexes are moderately high (similar to SingaporeChinese). Chongsuvivatwong (18) found that tobacco smoking

alone was not associated with a significantly elevated risk, butthe risk for nonsmoking alcohol drinkers was 4.7 (nonsignifi-

cant because of small numbers). Subjects who both smoked and

consumed alcohol were at a significantly higher risk (5.7) thanabstainens. Rubber-processing, an important local industry, didnot confer an increased risk. In another case-control study (19),

past consumption of two species of bean, Archidendron jiringa(“Luk Nieng”) and Parkia timoriana (“Luk Rieng”), was found

to increase risk; in contrast, consumption of raw beans of

Parkia speciosa (“Sataw”) was found to be protective.

Gastrointestinal Cancers. The incidence of other gastrointes-tinal cancers, stomach and colorectal, is low in the Thai pop-ulation. They have not been the subject of any epidemiological



too � --

0 Cervix

80 ‘� Bre��J

! 60 - 7

I �#{176} �20

0 t5�2�25- 3� 35. 4�-6�6� 70.75+

Fig. 3. Age-specific incidence rates per 100,000: cancers of the cervix uteri, and

breast.


Table 4 Distribution by cent ci and histological type : liver cancer. Number of cases and percentage o f known histological type

Bangkok Chiang Mai Khon Kaen Songkhla Total

No. % No. % No. % No. % No. %

Hepatocellular carcinoma

(8170)

259 70.8 135 47.9 23 7.6 47 95.9 464 46.5

Cholangiocarcinoma

(8140, 8141, 8160, 8161, and 8501))

86 23.5 128 45.4 268 89.0 1 2.0 483 48.4

Other 21 5.7 19 6.7 10 3.3 1 2.0 51 5.1

Not specified

(8000, 8()O1, 8002, 801)3, 8004, and 9991))

362 480 2390 84 3316

Total 728 762 2691 133 4314

Table 5 Distribution by histological type and sex: lung cancer

Male Female

No. % %“ No. % %“

Squamous cell carcinoma 453 19.4 38.1 147 11.9 24.7

(8070-8076)

Small cell carcinoma 1 18 5.0 9.9 37 3.0 6.2

(8041-8043)

Adenocarcinoma 535 22.9 45.0 372 30.1 62.6

(8250-8251, 8140-8231, 8260-8550,

and 8571)-857l)

Adenosquamous carcinoma 5 0.2 0.4 6 0.5 1.0

(8560)

Other 7� 3.3 6.6 32 2.6 5.4

Not specified 1 152 49.2 641 51.9

(8(XX)-801 I, 8020-8022, and 9991))

Total 2341 1235

Percentage of those among the known histological cases only.

studies. Rates of colon cancer have increased in Chiang Mai in

the last decade (20), possibly related to increasing consumptionof meat and animal fat and decreasing consumption of vegeta-bles in the Thai population over the last 20 years (21).

Liver Cancer. The incidence of liver cancer in Thailand isvery high, and most of the marked regional variation is due tothe very different risk of cholangiocarcinoma. This is normally

a rather rare tumor comprising, for example, only 15% of liver

cancers in the United States (22). High rates in Thailand havebeen convincingly linked to infestation with the liver fluke OV(23). The local habit of eating uncooked cypninoid fishes that

are infected with OV is the source of the high prevalence innortheastern Thailand (24, 25); this dietary custom is some-

times practiced in the north but not at all in the south. Theregional incidence of cholangiocarcinoma correlates well withthe prevalence of OV infection (26), and there is a similarassociation at the local (district) level in the northeast (27). Ina recent case-control study in subjects from northeastern Thai-land, OV infection, as measured by an elevated titer of anti-OV

antibodies, was strongly associated (OR, 5.0) with cholangio-carcinoma (28), and the percentage of cases attributable toopisthorchiasis was 72% in males and 62% in females. Various

mechanisms have been proposed for the carcinogenic action ofliver fluke infestation, including increased cellular proliferationin response to tissue damage, induction of nitric oxide syn-

thetase by inflammatory cells, and increased activity of certain

carcinogen-metabolizing cytochromes of the P450 group (23).Regular users of betel-nut (predominantly females) also had ahigh risk of cholangiocarcinoma (OR, 6.4; Ref. 28).

The incidence of hepatocellular carcinoma in Thailand isprobably rather uniform between regions (29). A case-controlstudy in residents in northeastern Thailand (30) has confirmedthat chronic carriers of the hepatitis B surface antigen have ahigh relative risk (OR, 15.2). Hepatitis C infection appears to be

rare (31).

In an early study, Shank ci’ a!. (32) found that estimatedmortality rates from liver cancer in two areas were apparentlyrelated to exposure to aflatoxin-contaminated foodstuffs. How-ever, although aflatoxin has been detected in a variety of marketfoods in Thailand (33-35), direct measurement of aflatoxin-albumin adducts in sera from human subjects suggests that

intake is relatively low (36). This is consistent with the lowprevalence of G to T mutations at codon 249 of the p53 gene insera and liver tissues from Thai patients with hepatocellularcarcinoma (37).

Pancreatic Cancer. The incidence of pancreatic cancer inThailand is low, but there is a 3- to 5-fold variation in incidenceby geographical region, with the highest rates noted in Chiang

Mai. This may relate to the greater prevalence of smoking in the

north; certainly, the incidence of both larynx cancer and lungcancer is also high in Chiang Mai, and the sex ratios (M:F) forall three cancers are strikingly low [1.0 (pancreas), 3.0 (larynx),and 1.3 (lung)] in comparison to the other centers and the

comparison populations in Tables 2 and 3.The high incidence of lung cancer in women in northern

Thailand recalls the high rates found in Chinese females, inwhom a high proportion of tumors are adenocarcinomas which,




Table 6 Distribution by histological type and ho dy site: non-melanoma skin cancer

Sq uamous cell carcinoma (8050-8082) Basal cell carcinoma (8090-81 10) Other and

No.

unspecified

%No. % No. %

Male

173.0-173.3 Face 45 23.9 80 63.0 10 26.3

173.4 Scalp and neck 15 8.0 12 9.4 5 13.2

173.5 Trunk 23 12.2 12 9.4 5 13.2

173.6 Upper limb 11 5.9 5 3.9 5 13.2

173.7 Lower limb 65 34.6 2 1.6 7 18.4

173.8. 173.9 Other and unspecified 29 15.4 16 12.6 6 15.7

Total 188 127 38

Female

173.0-173.3 Face 43 38.4 142 82.1 15 37.5

173.4 Scalp and neck 7 6.3 7 4.0 7 17.5

173.5 Trunk 9 8.0 5 2.9 2 5.0

173.6 Upper limb 8 7.1 3 1.7 0 0

173.7 Lower limb 32 28.6 0 0.0 5 12.5

173.8. 173.9 Other and unspecified 13 11.6 16 9.2 11 27.5

Total 112 173 40

although associated with tobacco smoking, generally havelower relative risks than squamous and small cell cancers (38,39). In a case-control study in Chiang Mai (12), smoking ofcigarettes and “Khiyo” (long, indigenous cigars) was associatedwith nonsignificant elevated risks in both sexes, while chewingof miang (fermented wild tea leaves) was associated with anincreased risk of lung cancer in women (OR, 2.2). There hasbeen a rapid increase in tobacco consumption in Thailand since

the 1960s (40), so that incidence rates of tobacco-related

cancers are likely to increase in future.

Melanoma. In common with other low-risk populations, mel-anoma in Thailand affects primarily the lower limb and partic-

ularly the sole of the foot, a distribution noted in an earlierseries of cases from Chiang Mai (41). This is very differentfrom the pattern in populations of European origin in whommelanoma affects primarily the trunk (of men) and lower limb(of women), and risk is enhanced by preexisting nevi and

exposure to sunlight (42).

Nonmelanoma Skin Cancers. Nonmelanoma skin cancers areprobably incompletely registered, since they may be treated in

small hospitals or as out-patients and thus escape case-findingprocedures. However, underregistration is probably less

marked than in Europe, North America, and Australia, whereincidence rates are very much higher. The low incidence inThailand is typical of other Asian populations living in equally

sun-exposed latitudes. The site distribution shows a predomi-nance of head and neck and basal cell cancers in women, whilein men, squamous cell tumors are more common, particularlyon the lower limbs. This pattern was observed in an early studyin Chiang Mai (41). It is very different from that in populations

of European origin in whom basal cell carcinomas are muchmore frequent than squamous cell carcinomas, which are lo-cated mainly on the head and neck (60-80%), with the upperlimb as the next most common site (10-20%) (43). Squamous

cell carcinomas of the lower limbs are rare in European pop-ulations; their frequency in Thailand may be related to trau-matic lesions of the leg and foot, but there are no relevant

studies.

Breast Cancer. Thailand has a low incidence of breast cancer,with an age-specific pattern typical of developing countries

(Fig. 3): an increase in risk up to about age 50 and then aflattening off or an actual decrease in risk. There have been

no studies of breast cancer epidemiology in Thailand. The

low risk may be a consequence of previously high levels offertility (early age at first pregnancy and multiple births) andlow caloric intake (late menarche and low body mass).However, patterns of fertility and nutrition are changing fastin Thailand and have affected the regions of Thailand to

different degrees, as shown by the child (0-4) per 1000women (15-49) ratio. This ratio is lowest in Bangkok

(187.6), followed by Chiang Mai (386.0), Khon Kaen

(476.8), and Songkhla (599.9), a ranking paralleling the in-cidence of breast cancer (except for Bangkok, where the low

ratio is a result of many young female immigrants, and the

incidence of breast cancer is an underestimate).

Cervical Cancer. The high incidence of cervical cancer inThailand (estimated national age-standardized incidence is

23.4/100,000) is quite typical of other developing countriesin southern and southeastern Asia. In a case-control study in

Bangkok, Wangsuphachart et al. (44) found trends of increas-ing risk with young age at first intercourse and number ofsexual partners, although these were not statistically significant.However, very few women reported having more than one

sexual partner (only 8% of controls). High parity has also beenfound to be an independent risk factor for cervical cancer in

some high-fertility populations (45); this would be important inThailand, where past fertility of older women is high, particu-

larly in the more economically deprived areas such as the

northeast. In the Bangkok study (44), women with high paritywere at higher risk than nulliparous women, but there was no

significant trend with increasing number of children.In other parts of the world where cervical cancer is fre-

quent and where men have many sexual partners but women do

not, as in Latin America (46), the effect of the sexual behaviorof partners in disease risk has been demonstrated. This may beparticularly relevant in Thailand.

Penile Cancer. A high frequency of penile cancer was noted in

an earlier series based on histopathology data in Bangkok(1951-1956; Ref. 47), 6.3% of cancers in men, and in Chiang

Mai (1966-1975; Ref. 48), 6.5% of cancers in men. Frequen-cies in the population-based data reported here are lower (2.9%in Songkhla and 1.6% in Chiang Mai), and this may correspondto a true decline in incidence. A similar dramatic decline infrequency has been reported for another population with pre-




viously reported high frequencies, in Hanoi, Vietnam (49).

Circumcision, especially in infancy, is protective against penilecancer (50), and Menakanit and Vanittarrakorn (48) noted that23.4% of the cases in their series in Chiang Mai had phimosis.

Bladder Cancer. The incidence of bladder cancer in Thailandis low (as it is in other Asian populations), although there isconsiderable regional variation in incidence. The highest ratesare in Chiang Mai, possibly related to the prevalence of smok-ing as well as to the presence of certain occupations using dyesin several local handicrafts industries.

Thyroid Cancer. The incidence of thyroid cancer is highest inthe northeast, although usually it tends to be more common inisland areas or those near to the sea, where iodine intake is

expected to be high. Elsewhere in Asia (e.g., Singapore and thePhilippines), papillary carcinoma is two to four times morefrequent than the follicular type (51); this pattern is observed in

Bangkok, Songkhla, and Chiang Mai, but the opposite ratio is

found in Khon Kaen. This finding may relate to the low iodineintake in the northeast where, in a recent survey, 10 to 50% ofchildren were found to have thyroid goiters. In contrast, ChiangMai, which was previously an area of low iodine intake, has had

a program of iodized salt prophylaxis since the mid 1960s.In conclusion, cancer is already a major health problem in

Thailand. Liver cancer is the most important neoplasm atpresent, and vaccination against hepatitis B virus and control of

the liver fluke infestation by therapy and education to discour-age the habit of eating raw fish are clearly priority areas.Tobacco-related cancers, which are already of importance (par-ticularly in the north), are also an obvious target for prevention,and the reason for the high rates among females in this region

is a priority area for research. Many of the cancers associatedwith Western life-styles (breast, colon, and rectum) are rare at

present, but with the rapid changes occurring in the Thai pop-ulation, they are likely to emerge as significant problems in thefuture.

Acknowledgments

We acknowledge the contributions of the academic and secretarial staff in each

registry and of the personnel of the hospital cancer registries and records depart-ments in the four registration areas. Margot Geesink was responsible for the

preparation of the manuscript.

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1995;4:475-483. Cancer Epidemiol Biomarkers Prev V Vatanasapt, N Martin, H Sriplung, et al. Cancer incidence in Thailand, 1988-1991.

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