UseofLocal Variations Trachoma Endemicity in Taiwan ...

Bull. Org. mond. Sante 1968, 39, 567-586Bull. Wid Hlth Org.

Use of Local Variations in Trachoma Endemicityin Taiwan to Elucidate Some of the Clinicaland Epidemiological Aspects of the Disease

F. A. ASSAAD,1 F. MAXWELL-LYONS2 & T. SUNDARESAN3

A trachoma prevalence survey was conducted in 1960-61 in Taiwan prior to the intro-duction of large-scale treatment operations and marked local differences in trachomaendemicity were encountered among adjoining neighbourhoods. Use is made of these localvariations in depicting differences in the salient clinical and epidemiological features oftrachoma under various degrees of endemicity.

The study suggests that a reduction in the risk of infection is first reflected in a loweringof the intensity of clinical signs and in an increase in the spontaneous cure rate and isfollowed later by a reduction in the incidence and hence, in the long run, in the prevalenceof the disease.

A scoring system applied to all cases (active and healed) reflects spontaneous cureand gives a more accurate index of endemicity than either of its 2 components relating tointensity or gravity.

Taiwan Province comprises a total of 78 islands,14 in the Taiwan group and 64 in the Peng-hu group.Most of the islands are very small and some areuninhabited. The main island, Taiwan, is about240 miles (390 km) long, is 88 miles (140 km) wideat its widest part and has an area of 13 837 mi2(35 838 kM2). Two ranges of mountains, one centraland one to the east, cover approximately two-thirdsof the total area of the island (Fig. 1). The cultivableland lies mostly to the west ofthe central mountainrange. The climate is semi-tropical with abundantrain and sunshine. The December 1959 inter-census figures gave a total population estimate(excluding armed forces and aliens) of 10431 341.

In 1960-61 a trachoma prevalence survey of theentire province was carried out before large-scaletreatment operations were commenced. A stratifiedmulti-stage (by administrative division) samplingprocedure was adopted and this is described inAnnex 1. The December 1958 inter-census esti-mates, excluding armed forces and aliens, provided

1 Virus Diseases, Division of Communicable Diseases,World Health Organization, Geneva, Switzerland.

2 Formerly, Virus Diseases, Division of CommunicableDiseases, World Health Organization, Geneva, Switzerland.

* Health Statistical Methodology, Division of HealthStatistics, World Health Organization, Geneva, Switzerland.

the basis for sampling and a uniform samplingfraction, 1/250 of the total population, was appliedto all strata. The lin, a "neighbourhood" of125 persons on the average, was taken as thesampling unit 4 (Fig. 2).Of the 36 731 persons (in 6101 households) in the

sample, 36 507 persons (in 6092 households 5) wereexamined. The examination procedure entailed theuse of focal illumination and a x 10 monocularloupe for examining the cornea and upper limbusand a x 2 magnifier for viewing the conjunctiva.The 38 sampled communities (strata) gave activ~e

trachoma prevalence rates ranging from 8.1 % to47.2% (Table 1, Fig. 3), the majority falling in therange of 15%-25 % 6. The difference in endemicitydid not follow a geographical pattern and was notrelated to elevation or climate (Fig. 1 and 3). Rank-ing the communities in order of active trachoma

' The aggregation of the lins in the northern tip and alongthe strip of land on the western coast of the island reflects thepattern of population density which in turn is a function ofelevation (Fig. 1 and 2).

6 The 9 households on which no information is availableall contained only 1 person.

* In calculating trachoma prevalence rates, all casespresenting one cardinal sign are included; an earlier studyindicated that most, if not all of these cases, were trachoma-tous (Assaad & Maxwell-Lyons, 1966).

2246 567-

568 F. A. ASSAAD, F. MAXWELL-LYONS & T. SUNDARESAN

FIG. 1TAIWAN PROVINCE

ELEVATION* O5100m TAIWAN ISLAND

250 m-<lOOOm50Sm-< 250m

El Om-< 50m

S Salt fields --

.-E Fishing grounds

islands

w"08IJ333

prevalence (from I for the community with thelowest rate to 38 for the one with the highest) andtesting the urban-rural sequence using the ''runstest (Siegel, 1956) shows that the distribution ofurban and rural communities within the 38 rankscould have arisen by mere chance. The percentagestandard error 1 (coefficient of variation) variedfrom 7.6o% to 38.6o% of the estimate of the activetrachoma rate in the observed sample (Table 1).The magnitude of the percentage standard errorwas not directly related to the sample size per stratum.In any one community the variation in trachomaendemicity was not limited to the primary samplingunits, the chlis, the chens or the hsiangs (see Annex 1)but extended to the lins within these primary sam-pling units (Tables 2 and 3). In nearly all the strata

I To obtain sampling errors ratio, 2-stage estimates werecomputed (Deming, 1950).

FIG. 2DISTRIBUTION OF SAMPLE LINS IN TAIWAN PROVINCE

SAMPLE LINS

* Urbano Rural I: :.*

S

00 0 26 ilins

g*~~~~~~~~~ 0

0 o~~0

I0~~~~~~~~~

17 lin, 00

We H 8.>A1 Q 4

the lins gave active trachoma rates which variedover a very wide range.The marked local variation in trachoma endemicity

is made use of later in this paper in elucidating someof the clinical and epidemiological features oftrachoma in Taiwan.

METHODS

The 351 sample lins 2 were divided into 9 domainsof study, of progressively higher endemicity ex-pressed in terms of the active trachoma prevalencerate. Except for domain 9, the group with thehighest endemicity, each domain comprised thelins having an active trachoma rate within a 5 %range (Table 4).

2 One lin in which only 2 individuals were examined isexcluded from the study.

CLINICAL AND EPIDEMIOLOGICAL ASPECTS OF TRACHOMA IN TAIWAN 569

FIG. 3PREVALENCE OF ACTIVE TRACHOMA

IN ADMINISTRATIVE DIVISIONS OF TAIWAN PROVINCEa

PREVALENCE RATE (%)

<10LI0I-<1515-<2020-<25 -30-<4045 <50- -

311081335

a No community has a rate falling in the ranges 25-<30or 40-<45.

No difference in prevalence rates, even withinindividual age-groups, was noted between sexes.Therefore, no attempt is made to present the resultsseparately by sex.'Of the 3 population groups on the island, the

Taiwanese Chinese, the mainland Chinese,2 and theaborigines, only the Taiwanese Chinese were in-cluded in the present study. Of the total of 36 507persons examined, 33 016 (90.4 %) were reported asTaiwanese Chinese, 2569 (7.0%) as 'MainlandChinese and 922 (2.5%) as aborigines. The main-

, The tabulations relating to trachoma prevalence rates byage and sex and trachoma stage have been deposited in theWHO Library, from which single copies may be obtained onrequest.

2The term " mainland Chinese " is used to distinguishthose who arrived after the Second World War from theearlier immigrants here designated " Taiwanese Chinese

land Chinese were mostly encountered in 12 linsin which they formed the predominant part of thepopulation; the aborigines were restricted mainlyto 10 lins. Active trachoma prevalence rates differedmarkedly among the 3 groups and the differencecould not be attributed to a different age composi-tion:

Median age Active trachoma rate (%)(years) Crude Age-stan-

Taiwanese Chinese 15.3 20.9 20.9Mainland Chinese 19.1 12.4 12.9Aborigines 13.8 28.0 29.6

* On the basis of the Taiwanese Chinese examined population.

Age-specific rates (Fig. 4) depict well the discre-pancies among the 3 population groups.

FINDINGS

A progressively higher trachoma endemicity inthe 9 domains of study was marked by a steadyreduction in the proportion of healed (Tr IV) tototal trachoma cases from 92.5% in domain 1 to50.5% in domain 6 and 30.4% in domain 93 (Fig. 5).Within the cases of active trachoma a relative in-crease in Tr II from 4.2% in domain I to 16.3% indomain 9 was noted. The increase in Tr II wasapparently at the expense of Tr III which showed aproportionate decrease from 70.9% in domain 1 to56.4% in domain 9; Tr I showed only a smallincrease (from 25.0% in domain 1 to 27.3% indomain 9).The graphs of total and active trachoma pre-

valence by age (Fig. 6) show that the differencesamong the 9 domains were not limited to a certainage but extended to all age-groups (smaller differ-ences were seen in the older age-groups). Exceptfor domains 1 and 6, the age of peak prevalence ofactive trachoma was 15-19 years. The peak pre-valence of pre-cicatricial trachoma, stages I and II,shifted from 10-14 years, in domains 1-5, to 5-9 yearsin the domains of higher endemicity. In contrast,except for domain 6, cicatrizing trachoma, stage III,had a peak prevalence in the 15-19-year age-groupirrespective of endemicity.

Notwithstanding the adequate number examined,active trachoma was first diagnosed at the age of 6years in domain 1. In contrast it was first diagnosedin the 1-2-year age-group in domains 2 and 3 and in

3 The prevalence rates of Tr IV in the 9 domains arerestricted to the narrow range of 22.2 % (in domain 9) to29.2% (in domain 3).

F. A. ASSAAD, F. MAXWELL-LYONS & T. SUNDARESAN

TABLE 1

ACTIVE TRACHOMA PREVALENCE RATE AND SAMPLING STANDARD ERROR BY COMMUNITY

Sampled communitie

Name

Chang-huaMiao-liNan-touTai-peiTai-peiTai-nanPing-tungKao-hsiungHwa-lienNan-touPing-tungHwa-lienTao-yuanTai-chungChai-iHsin-chuTai-peiHsin-chuI-lanKao-hsiungTai-nanChang-huaTai-nanMiao-liTai-chungYang-ming-shanKao-hsiungKee-lungTai-tungI-lanYun-linTao-yuanTai-chungTai-tungChai-iPeng-huPeng-huYun-lin

~~ ~~~N.No.examined

atv

Type trachoma

Urban 1 361 110Rural 780 65Urban 845 91Urban 1692 238City 2 573 367Urban 814 124Urban 721 112Urban 537 85Urban 433 71Rural 570 95Rural 1650 277Rural 503 86Urban 644 111

Rural 1 001 180Urban 1 098 200Rural 719 135Rural 893 168Urban 619 121Urban 575 114City 1 518 305Rural 1844 378Rural 1 730 365City 1147 244Urban 807 174Urban 957 207Adm. 373 83Rural 1 711 386City 1175 268Urban 261 60Rural 664 157Urban 984 235Rural 835 204City d 696 171Rural 471 147Rural 1538 520Rural 147 53Urban 141 66Rural 1478 697

36 505 7 470

Prevalence of active trachoma

Rate(%)

8.1

8.310.814.114.315.215.515.816.416.716.817.117.218.018.218.818.819.519.820.120.521.121.321.621.622.322.622.823.023.623.924.424.631.233.836.146.847.2

20.5

PSE b Confidence limitsc

16.638.637.212.59.5

24.222.818.720.414.613.525.118.617.019.113.316.816.319.611.515.58.47.6

14.920.629.613.112.29.9

28.421.98.5

23.025.918.721.017.48.8

3.2

5.5 10.91.9 14.82.7 18.6

10.6 17.611.5 17.07.9 22.68.3 22.79.9 21.89.7 23.1

11.8 21.512.2 21.38.5 25.7

10.8 23.610.9 25.111.2 25.213.8 23.812.5 25.113.2 25.912.1 27.615.5 24.714.1 26.917.6 24.718.1 24.515.1 28.012.7 30.59.1 35.4

16.7 28.517.3 28.418.4 27.610.2 37.113.4 34.420.3 28.613.3 35.915.0 47.421.2 46.520.9 51.230.5 63.138.9 55.4

19.1 21.8

a In increasing order of active Tr rate.b Percentage standard error.c At the 95% probability level.d One lin in which only 2 persons were examined is excluded.

570

Rank a

1234567891011121314151617181920212223242526272829303132333435363738

Total

_


TABLE 2

NUMBER OF LINS PER COMMUNITY ARRANGED IN CATEGORIES OF ACTIVE TRACHOMA PREVALENCE

Community a0

Chang-hua UrbanMiao-li RuralNan-tou UrbanTai-pei UrbanTai-pei CityTai-nan UrbanPing-tung UrbanKao-hsiung UrbanHwa-lien UrbanNan-tou RuralPing-tung RuralHwa-lien RuralTao-yuan UrbanTai-chung RuralChai-i UrbanHsin-chu RuralTai-pei RuralHsin-chu UrbanI-lan UrbanKao-hsiung CityTai-nan RuralChang-hua RuralTai-nan CityMiao-li UrbanTai-chung UrbanYang-ming-shan Adm.Kao-hsiung RuralKee-lung CityTai-tung UrbanI-lan RuralYun-lin UrbanTao-yuan RuralTai-chung City bTai-tung RuralChai-i RuralPeng-hu RuralPeng-hu UrbanYun-lin Rural

Total No. I

% 10.31

Categories of active trachoma prevalence (%)

5- 10- 15- 20- 25- 30- 35- 40- 45- 50- 55- 60- 65-<5 9.9 14.9 19.9 24.9 29.9 34.9 39.9 44.9 49.9 54.9 59.9 64.9 69.9 >70 Total

3 5 4 1 1 142 3 1 1 7

3 2 1 74 4 4 2 1 1 1617 10 6 1 1 262 2 1 2 71 4 1 1 81 1 2 2 61 3 1 151 1 3 1 6

2 3 4 1 4 1 1 161 2 2 1 6

1 2 1 41 1 3 2 3 1 11

2 2 3 1 1 91 1 2 1 2 73 2 2 2 1 1 2 1 514

3.71 6. 191 1 2 1 62 2 1 1 6

1 3 2 4 2 2 1 2 173 5 5 1 2 2 1 1 203 4 2 1 2 3 1 162 2 2 1 1 1 101 4 1 21 1 1 2 1 1 7

1 11 33 1 1 3 3 1 1 13

2 2 1 2 7

11

11

3

1 2 1 2 1 1 1 91 2 1 1 1 1 I7

1 ~~~~12 1 1 61 1 2 15

1 1 2 1 3 2 1 1 2 1 151 1 1 1 3

1 1 L3 3 2 1 1 1 11

13 59 67 62 41 35 26 22 7 9 3 2 2 1 1 351

3.7 16.8 19.1 17.7 11.7 10.0 7.4 6.3 2.0 2.6 0.9 0.6 0.6 0.3 0.3 100.0

a Arranged in order of increasing prevalence of active trachoma (see Table 1).b One lin in which only 2 persons were examined is excluded.

1


TABLE 3

NUMBER OF PERSONS PER COMMUNITY ARRANGED IN CATEGORIES OF ACTIVE TRACHOMA PREVALENCE

Categories of active trachoma prevalence (%)Community a -o 5 5- 10- 15- 20- 25- 30- 35- 40- 45- 50- 55- 60- 65- |70 Total no.

0 <5|9.9 14.9 19.9 24.9 29.9 34.9 I 39.9 44.9 49.9 95495 64.9 69.9 7 examined

Chang-hua Urban 256 496 523 59 27 1 361Miao-li Rural 287 348 97 48 780Nan-tou Urban 170 288 272 115 845Tai-pei Urban 644 448 298 190 40 72 1692Tai-pei City 66 651 888 761 89 118 2 573Tai-nan Urban 356 182 102 174 814Ping-tung Urban 56 87 304 145 129 721Kao-hsiung Urban 87 86 198 166 537Hwa-lien Urban 17 289 127 433Nan-tou Rural 23 85 351 111 570Ping-tung Rural 133 311 352 132 464 201 57 1650Hwa-lien Rural 100 147 180 76 503Tao-yuan Urban 154 294 196 644Tai-chung Rural 23 77 318 200 210 173 1 001Chai-i Urban 192 278 392 141 95 1 098Hsin-chu Rural 81 121 238 52 227 719Tai-pei Rural 189 256 107 125 47 45 80 44 893Hsin-chu Urban 88 135 132 186 78 619I-lan Urban 173 236 84 82 575Kao-hsiung City 65 219 141 365 224 243 98 163 1518Tai-nan Rural 174 497 464 132 132 165 225 55 1844Chang-hua Rural 267 333 318 73 274 363 102 1730Tai-nan City 34 166 249 455 75 41 127 1147Miao-li Urban 132 402 64 209 807Tai-chung Urban 98 264 128 211 174 82 957Yang-ming-shan Adm. 114 174 I 85 373Kao-hsiung Rural 411 166 142 505 403 63 21 1 711Kee-lung City 203 287 161 524 1175Tai-tung Urban 61 122 78 261I-lan Rural 60 109 67 307 58 63 664Yun-lin Urban 103 223 135 209 80 156 78 984Tao-yuan Rural 104 238 50 166 192 85 835Tai-chung City b 150 124 235 71 116 696Tai-tung Rural 85 83 159 144 471Chai-i Rural 135 91 236 94 355 199 86 106 145 91 1538Peng-hu Rural 49 43 55 147Peng-hu Urban 75 66 141Yun-lin Rural 545 346 204 64 162 157 1478

Total No. 34 1 144 5862 6887 6799 4468 4063 2675 2310 647 724 289 130 253 63 157 36505

% 0.1 3.1 16.1 18.9 18.6 12.2 11.1 7.3 6.3 1.8 2.0 0.8 0.4 0.7 0.2 0.4 100.0

a Arraniged in order of increasing prevalence of active trachoma (see Table 1).b One lin in which only 2 persons were examined is excluded.

CLINICAL AND EPIDEMIOLOGICAL ASPECTS OF TRACHOMA IN TAIWAN

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TABLE 4

GROUPING OF THE SAMPLE LINS INTO 9 DOMAINS OF PROGRESSIVELY HIGHER ENDEMICITY

|Prevalence of t Sample lins a Population examinedDomain active trachoma Taiwanese Chinese Mainland Chinese Aborigines

INo. % No. % No. % No. %

1 < 5 14 4.0 1129 3.4 49 1.9 - -

2 5-9.9 59 16.8 4 864 14.7 898 35.0 100 10.8

3 10-14.9 67 19.1 6 076 18.4 667 26.0 144 15.6

4 15-19.9 62 17.7 6 017 18.2 606 23.6 176 19.1

5 20-24.9 41 11.7 4 165 12.6 142 5.5 161 17.5

6 25-29.9 35 10.0 3 870 11.7 157 6.1 36 3.9

7 30-34.9 26 7.4 2 610 7.9 9 0.4 56 6.1

8 35-39.9 22 6.3 2 295 7.0 15 0.6 - -

9 >40 25 7.1 1 988 6.0 26 1.0 249 27.0

Total - 351 100.1 33014 99.9 2 569 100.1 922 100.0

a One lin in which only 2 individuals were examined is excluded.

FIG. 5RELATIVE FREQUENCY OF THE EVOLUTIVE STAGES OF TRACHOMA BY DOMAIN

19.5% 25.1% 5 27.2%

1 o53>5.13 %3.4%52.2%23.45I3 1 622

1.9% H~~~~~~~~~~~~)~~10.0%:I0.3% 5.3 7.6 %11692.5% 78.1%7.% 61.4%56%

Domain 1 2 3 4 5Trachoma evolutive

5 9% % 7.1 w- 8. 10 54 ~~~~~~~11.3% stages5.9%31.1% 71% 33.2% 8.9% ~ 5.319.0% Tr~Tn

12.6% 12.8%I2 12.1%, j 19.0%LeL _~~~~~~I1 1! _ 39.3%

Tr IJ

*0 Tr IV50.5% J 4.% \ 43.7% \30.4% _ * Trill

Domain 6 7 8 9WHO8B331

574


Z~ ~ ~ ~ ~~ ~ ~ ~ ~ ~ ~ ~~~~~~~~~~~1

0

U)<w~~~~~~~~~~~~~4u

0n

0

Ua.z

co W~~~~~%a:)uOIeA,3Jd )aOUa;eAaJd

0~~~~~~~~~~~~~~~~~~L LU

U0~~~~~~~~~~~~~~

LU ~~~ ~ ~~~~~~Lx~~~~~~~~~~~~~~~~~~~~~~~~~

> LU0

N~~~~~~~~~~~~~~~~~~~~~~~~ U~

U

U

UU -4

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5r_


FIG. 7PROPORTION OF HEALED TO TOTAL TRACHOMA BY DOMAIN FOR THE TAIWANESE CHINESE POPULATION

100

90

80

70

60

.50-

~40-30-

20-

10

0013 5 10 15 20 25 30 35 40 45 50 55 60 65 70 75

Age (years) WH81339

infants below the age of 1 year in the domains ofhigher endemicity.1Except for distinctly low Tr IV age-specific pre-

valence rates in domain 9, no marked or sustaineddifferences were noted among the other domains(Fig. 6). However, the proportions of healed tototal trachoma by age (Fig. 7) show that there was:(1) very slow healing in domain 9, (2) very fasthealing in domain 1 and (3) an intermediate butdistinctly changing pattern among the other domains.The application of a weighted scoring system to

trachoma cases in the 9 domains (Assaad & Maxwell-Lyons, 1967a; see Annex 2) shows a rising average" total " score per case with rising endemicity(Table 5); an almost perfect correlation is obtainedbetween average " total " scores and active trachoma

1 With the exception of domain 8 in which active trachomahad a prevalence rate of 10.8% in the 1-2-year age-group.

prevalence rates (Fig. 8). Thus the 9 domains canbe arbitrarily divided into 4 groups:Group Domains Average " total" score per case

A 1, 2 and 3 3.47, 3.60 and 3.77, i.e., <4.0B 4, 5 and 6 4.15, 4.38 and 4.44, i.e., 4.0-<5.0C 7 and 8 5.19 and 5.28, i.e., 5.0-<6.0D 9 6.19, i.e., <6.0

The average intensity score (per case of activetrachoma) shows a markedly poorer correlationwith active trachoma prevalence rates. On the otherhand, except for domains 1, 2 and 3 the averagegravity score (per case of cicatricial trachoma)correlates well with endemicity; the first 3 domainshad nearly the same average gravity score. In linewith the above findings is the weak correlationbetween intensity and gravity scores on the one handand the markedly stronger correlation betweentotal and gravity scores on the other.


TABLE 5AVERAGE SCORES PER CASE OF TRACHOMA BY STAGE AND BY DOMAIN FOR THE

TAIWANESE CHINESE POPULATION

Stage of trachoma Average I Average AverageDomain total intensity gravity

Tr I Tr II Tr ilI Tr IV score score score

1 1.67 2.00 5.82 3.37 3.47 3.83 3.30

2 2.02 3.56 5.30 3.38 3.60 3.45 3.20

3 2.04 4.78 5.55 3.44 3.77 3.67 3.18

4 2.02 4.36 5.43 3.97 4.15 3.51 3.51

5 2.15 4.94 5.53 4.23 4.38 3.68 3.64

6 1.78 4.64 5.58 4.37 4.44 3.52 3.66

7 2.13 4.69 6.35 5.28 5.19 3.96 4.27

8 2.02 4.92 5.76 5.86 5.28 3.76 4.44

9 1.99 5.73 6.81 8.19 6.19 4.09 5.47

Total 2.01 4.89 5.81 4.29 4.48 3.72 3.75

I_ i_ l_ !_

Age-specific scores (Fig. 9) show frequent irregu-larities at successive ages. The grouping of domainsdemonstrates the differences in age-specific totaland gravity scores between groups-beyond theage of 9 years-among the 4 above-mentioneddomain groups (Fig. 10); the differences increasedas age advanced. Concerning the intensity scores,there was hardly any difference, irrespective of age,among the 3 groups A, B and C. On the other hand,beyond the age of 9 years, domain 9 gave consistentlyhigher scores.The apparent rather poor correlation between

intensity scores and endemicity is attributed to thevery mild character of the active signs of the disease.In the total' sample population examined, only 23cases of Tr I and 26 cases of Tr III were reported ashaving an F3 follicular involvement of the con-junctiva; nearly half of these cases, 10 and 12 casesrespectively, were diagnosed in domain 9. F1 casesaccounted for the majority of cases; the lowestpercentages-reported in domain 9-were 80.5 %of Tr I and 81.3 % of Tr III. Although, in contrast,Tr II cases show a distinct pattern of a shift fromF1 to F2 to F3 the higher the endemicity, theyaccount for only 12% of the total number of activetrachoma cases. The net result, therefore, is thatthe shift to a higher degree of follicular involvementthe higher the endemicity is masked by the over-whelming preponderance of F1 cases (Table 6).

In the case of pannus (Table 7), out of 1746 casesdiagnosed as Tr I in the total sample population,bnly 2 cases-one in domain 8 and the other indomain 9-presented an extension of vessels intothe cornea of 2 mm or more. Even among Tr IIcases only 48 (domain 9 accounting for 21 cases)were reported as having macropannus. The majorityof cases of macropannus were diagtiosed in Tr III-namely, 86.3% of the total of 364 cases.

In the 3 active stages of the disease, the higherthe endemicity the smaller was the number of caseswhich failed, under field conditions, to show ademonstrable pannus. However, id stage I (and toa lesser extent in stage II) the higher the endemicitythe greater was the number of cases in which thelimbus could not be examined-because a largernumber of cases were in the very young age-groups(Assaad & Maxwell-Lyons, 1966).

In contrast to the above, the gravity scores,restricted only to cicatrizing lesions, correlate wellwith the proportion of total trachoma cases withdisabling or potentially disabling lesions 1 (Tables 5and 8, Fig. 8). Moreover, except for domain 1,the domains can be grouped, according to the pro-portion of cases with these lesions, into the same4 domain groups as by gravity scores. The correla-tion between gravity scores and the proportion of

As defined by the WHO Expert Committee on Trachoma(1962).


FIG. 8SCATTER DIAGRAMS SHOWING CORRELATION BETWEEN AVERAGE TOTAL, INTENSITY AND GRAVITY SCORES,PREVALENCE OF ACTIVE TRACHOMA AND PROPORTION OF CASES WITH DISABLING OR POTENTIALLY DISABLING

LESIONS FOR THE TAIWANESE CHINESE POPULATION IN THE 9 DOMAINS OF STUDY a

6.5r@ 6.0

5.5

0 5.05.0

4.5 -~ ~>-x 4.0

3.5 0

0 1 0 20 30 40 50Prevalence of active trachoma (%)

,5.5 0

- 5.0

> 4.0taO ~ 0

3.5 0

a,*< 3.0

0 10 20 30 40 50

Prevalence of active trachoma (%)

%,, 16.0

* 4! 14.0_ =

3 D 12.0

a, )10.0

_ 8.0

c- 6.0 a

3.0 3.5 4.0 4.5 5.0 5.5Average gravity score per case

Wm) 81340

4.1

O 4.0X) 0

@3.9o 0

f 3.8 -

~373. 6

<3.5

3.40 1 0 20 30 40 50Prevalence of active trachoma (%)

4.1

a 4.00O Q~~

@. 3.991o 0

- 3.8 -

, 3.7*

3.6

<, 3.5

3.43.0 3.5 4.0 4.5 5.0 5.5

Average gravity score per case

6.5

I 6.0

ac' 5.5-o0 *) 5.0

°4.5

> 4.0

3.5

3.0 3.5 4.0 4.5 5.0 5.5Average gravity score per case

a The open circles represent domain 1, where only 24 cases were diagnosed as active trachoma.

578


FIG. 9AVERAGE SCORE PER CASE BY AGE AND DOMAIN FOR THE TAIWANESE CHINESE POPULATION

TOTAL SCORE Domain

14

12

~10

> 4 .

0

01 3 5 10 15 20 25 30 35 40 45 50 55 60 65 70 75Age (years)

INTENSITY SCORE6

GRAVITY SCORE

14

12

cc

> 014-)

n0)

2-

579

01 3 5 10 15 20 25 30 35 40 45 50 55 60 65 70 75Age (years) WKO8131

li -

15U F. A. ASSAAD, F. MAXWELL-LYONS & T. SUNDARESAN

FIG. 10AVERAGE SCORE PER CASE BY AGE AND BY GROUP OF DOMAINS FOR THE TAIWANESE CHINESE POPULATION

Group ofTOTAL SCORE domains

14 ©

12-

l,0,~~~~~~~~~~~~~~~~~~~~~~~~

Ct:013 5 10 15 20 25 30 35 40 45 50 55 60 65 70 75Age (years)

INTENSITY SCORE0v) 6.*a

0 t

0a< 013 5 10 15 20 25 30O 35 4'0 45 50 55 60 65 70 75

Age (years)

GRAVITY SCORE14

CZ)

00~~~~~~~~~~~~~~~~~~~~~~~~~~~~~0

A,,, 66

5'

01 3 5 10 15 20 25 30 35 . 40 45 50 55 60 65 70 75Age (years)

WHO 81342-

on

CLINICAZL AND EPIDEMIOLOGICAL ASPECTS OF TRACHOMA IN TAIWAN 581

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cases with actual or potentially disabling lesionsextends throughout all the age-groups (Fig. 9, 10,11 and 12).

DISCUSSION AN D CONCLUSIONS

In 2 previous studies use was made of the groupingof the sample population by stratum (the sampled38 communities) in developing a scoring system andin assessing observer variation (Assaad & Maxwell-Lyons, 1967a, 1967b). In the present study use ismade of the marked local differences in the endemi-city of the disease in forming homogeneous domainsof study by grouping the sample units, the lins, byactive trachoma rate ' rather than by administrativedivision. The within-group homogeneity thtusachieved unmasks some of the minor variations inthe disease picture among the domains.2 Becauseof this the study was further limited to the pre-dominant population group on the island-theTaiwanese Chinese.A striking feature of the study is that peak pre-

valence of Tr III was persistently reached, irrespec-tive of endemicity, in the 15-19-year age-group.3In contrast with higher endemicity Tr I and Tr IIshowed a distinct shift in peak prevalence to youngerage-groups. One can, therefore, presume that therelation between peak prevalence of Tr III and ageis independent of endemicity, while the risk ofinfection (denoted by Tr I and Tr II) is not. It hasbeen suggested (Assaad & Maxwell-Lyons, 1966)that the cohort born or passing its infancy and earlychildhood during the war years suffered a higherrate of infection than earlier or later cohorts. Thiscohort is represented in the age-group which was15-19 years old at the time of the 1960-61 survey.It is of interest to note that in a limited small-scalefollow-up survey of control communities, late in1966, a shift of peak prevalence of Tr III to an olderage was reported (Table 9).As would be expected, the reduction in the risk

of infection in recent years is more marked the lowerthe endemicity. The lower the endemicity the olderthe age of peak prevalence of Tr I and Tr II and thehigher the proportion of cases of healed to totaltrachoma.

I In domain 9 the lins give an active trachoma rate rangingfrom 44.20% to 72.6%.

2 The grouping of lins by active trachoma prevalence rateand not by administrative division precludes the possibility ofassigning confidence limits to the sample estimates.

3 In domain 6 the peak is manifested in the age-group20-24 years. Nevertheless the curve in Fig. 6 for thisdomain shows a distinct break in the 15-19-year age-group.


TABIEXTENT OF PANNUS IN ACTI%

No. of trachoma cases diagnosed

Domain Tr I Tr II Tr IilULNE a No Micro- Macro- Total ULNE a No Micro- Macro- Total ULNE No

pannus pannus pannus pannus pannus pannus pannus

1 1 ~~~~32 6 1122 12 34 39 85 1 14 10 25 36

3 31 72 88 191 1 23 30 1 55 1 66

4 51 97 132 280 4 41 49 1 95 81

5 45 79 123 247 11 29 64 6 110 2 54

6 66 113 94 273 14 42 66 5 127 2 78

7 33 76 97 206 9 31 68 6 114 2 44

8 44 62 74 1 181 12 29 84 8 133 1 47

9 107 64 105 1 277 27 23 94 21 165 3 15

Total 390 600 754 2 1746 79 233 465 48 825 11 423

a Upper limbus not examined.

FIG. 11

PROPORTION OF THE TOTAL NUMBER OF TRACHOMA CASES WITH DISABLING OR POTENTIALLY DISABLINGLESIONS BY AGE AND DOMAIN FOR THE TAIWANESE CHINESE POPULATION

352

Domain60

50

Be- 401-

0- 300

a_ 20

10

01 0 1 5 20 25 30 35 40 45 50 55 60 65 70 75

Age (years) WHO 81

582


TRACHOMA BY DOMAIN

Total active trachoma cases

Tr III

Micro- 'IMacro-pannus !pannusI~~~~~~~~~~~~~~~~~~~~~~~~~~~~

13 2

197 10

391 30

575 37

476 45

562 32

447 40

454 27

463 91

3 578 314

Total

17

243

488

693

577

674

533

529

572

ULNE a

No. %

1 4.2

13 3.7

33 4.5

55 5.1

58 6.2

82 7.6

44 5.2

57 6.8

137 13.5

4326 480 7.0

No pannus Micropannus Macropannus Total

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

6 25.0 15 62.5 2 8.3 24 100.0

84 23.8 246 69.7 10 2.8 353 100.0

161 21.9 509 69.3 31 4.2 734 99.9

219 20.5 756 70.8 38 3.6 1 068 100.0

162 17.3 663 71.0 51 5.5 934 100.0

233 21.7 722 67.2 37 3.4 1 074 99.9

151 17.7 612 71.7 46 5.4 853 100.0

138 16.4 612 72.6 36 4.3 843 100.1

102 10.1 662 I 65.3 113 11.1 1 014 100.0

1 256 18.2 4 797 69.6 364 5.3 6 897 100.1

FIG. 12PROPORTION OF THE TOTAL NUMBER OF TRACHOMA CASES WITH DISABLING OR POTENTIALLY DISABLING

LESIONS BY AGE AND GROUP OF DOMAINS FOR THE TAIWANESE CHINESE POPULATION

Group of60 domains60

5040

cL2Oc- 200 - -= /10 ~ ~ ~~ ~ ~ ~ ~ ..W~~~~~eeeS @o ~ ~ ~ 010 0

I0 @00.,

01 3 5 10 15 20 25 30 35 40 45 50 55 60 65 70 75Age ( years ) WHfRlq.,.. , - -j .j

583


TABLE 8PROPORTION OF TRACHOMA CASES WITH DISABLING OR POTENTIALLY DISABLING

LESIONS BY DOMAIN

F3C1, F2C2or C3

No. %

11 3.4

72 4.5

90 3.6

137 5.0

98 4.6

112 5.2

112 7.0

126 8.4

189 13.0

7Tric

No.

16

71

98

129

97

87

99

98

107

947 5.8 802

-hiasisI P

% No.

5.0 4

4.4 19

3.9 25

4.7 45

4.6 33

4.0 34

6.2 34

6.5 35

7.3 46

5.0 275

annus4 mm

1.3

1.2

1.0

1.6

1.6

1.6

2.1

2.3

3.2

Otheropacities

No. % No.

11 3.4 25

44 2.7 109

72

89

71

76

70

67

60

2.9

3.2

3.3

3.5

4.4

4.5

4.1

153

201

159

161

163

158

224

1.7 560 3.5 1 353

The markedly mild character of signs of activityof the disease, whether conjunctival or corneal,irrespective of endemicity, suggests that a reductionin the risk of infection is first reflected in a loweringof the intensity of clinical signs, to be followed laterby a reduction in incidence, and hence in the longrun in prevalence of the diseas

TABLE 9PREVALENCE OF Tr III 11

COMMUNITIES IN

Age-group Total no.(years) examined

< 5

5-14

15-24

25-34

35-54

> 55

Total

176

374

169

154

212

67

1 152

The rather rapid reduction in the intensity of theactive disease renders a forecast from intensity togravity possible only within wide ranges. Further-more when endemicity has been reduced over a

relatively short period-judged by the differencebetween active and healed trachoma-to the level

se. of domains 1, 2 and 3, gravity, defined in terms ofthe proportion of cases with disabling or potentiallydisabling lesions or presented in the form of average

N CONTROL scores, ceases to serve as a distinguishing feature of1966 the disease.Cases of Tr III Under the conditions prevailing in Taiwan at the

time of the survey- namely, a rapid change in theNo. % risk of infection manifested in lower incidence of

0 0o. the disease (reduced number of new infections), amild form of active disease and a high rate of

5 1.3 spontaneous cure (reduced rate of reinfection)-15 8.9 the " total " score gives a better indication of46 29.9 differences in the disease pattern under the various54 25.5 degrees of endemicity. The average " total " score15 22.4 includes components relating to the intensity of the

active disease and to the gravity of cicatricial135 11.7 lesions and also takes in account the ratio of cases

in the healed and active stages of the disease.

RESUME

En 1960-1961, une vaste enquete sur la prevalence dutrachome, preludant a la mise en aeuvre d'un programme

de traitement de masse, a et menee A Taiwan pour faire le

point de la situation epidemiologique. On a examine autotal 36 507 personnes, le lin, quartier habite par 125 per-sonnes environ, etant pris comme unite d'echantillonnage.

Total no.Domain trachoma

cases

2

3

4

5

6

7

8

9

Total

320

1 612

2 508

2 766

2 122

2 170

1 607

1 497

1 456

16058

Total

i %

7.8

6.8

6.1

7.3

7.5

7.4

10.1

10.6

15.4

8.4

584


On a note, entre lins contigus, de nettes variations del'endemicite trachomateuse. Leur analyse a permis defaire ressortir certaines diff6rences dans les aspectscliniques et epidemiologiques du trachome en fonctiondu degre d'endemicite. Cette analyse a et limitee augroupe de population le plus important, compose deChinois immigres avant la deuxieme guerre mondiale.On a en outre constitue des secteurs d'etude homogenesen groupant des lins d'endemicite analogue.

L'enquete a montre que plus l'endemicite est elevee,plus la proportion des cas de trachome gueri par rapporta l'ensemble des cas est faible. La prevalence maximaledu trachome actif (Tr III) est toujours observee, quel quesoit le degre d'endemicite, dans le groupe d'Age de 15 A19 ans. Au contraire, la frequence maximale du trachomeprecicatriciel se manifeste dans des groupes d'age de plusen plus jeunes au fur et A mesure que croit l'endemicite.On peut en conclure que l'exposition A l'infection a ete

tr6s forte 15 a 19 ans auparavant, mais que le risque aconsiderablemeht diminu6 depuis quelques ann6es etdans une proportion d'autant plus grande que l'end6mi-cite est faible.Le caractere benin des signes cliniques d'activite du

trachome - qu'il s'agisse des 1lsions conjonctivales oucorneennes - donne A penser que la diminution durisque d'infection se marque d'abord par une attenuationde I'intensite relative du trachome, puis par une baisse del'incidence et enfin par une chute des taux de prevalence.

C'est la gravite du trachome, et non son intensite, quireflete le mi-ux le degre d'endemicite, sauf lorsque cedernier atteint des valeurs tres faibles. L'emploi d'unenotation globale moyenne, basee sur la mesure del'intensite et de la gravite de la maladie et tenant comptedu rapport entre les cas de trachome gueri et les cas detrachome actif, est la methode la plus scire pour evaluer1'endemicite.

REFERENCES

Assaad, F. A. & Maxwell-Lyons, F. (1966) Bull. Wld HlthOrg., 34, 341-355

Assaad, F. A. & Maxwell-Lyons, F. (1967a) Amer. J.Ophthal., 63, 1327-1356

Assaad, F. A. & Maxwell-Lyons, F. (1967b) Bull. WldHlth Org., 36, 885-900

Deming, W. E. (1950) Some theory of sampling. NewYork, John Wiley & Sons.

Siegel, S. (1956) Nonparametric statistics for the beha-vioural sciences, New York, McGraw-Hill

WHO Expert Committee on Trachoma (1962) Wld HilthOrg. techn. Rep. Ser., 234

Annex I

SAMPLING PROCEDURE

The Province of Taiwan is administratively dividedinto 5 shihs (big cities), 16 hsiens (counties) and 1kuanli chu (administration). Further subdivisionfollows a definite pattern. A city is subdivided intochus (districts), which in turn are subdivided intolis (sub-districts). Each county comprises a numberof chens (towns, forming the county urban com-munity) and hsiangs (townships, forming the countyrural community). Each chen is subdivided intoa number of lis, while each hsiang is formed of anumber of tsuns (villages). The lis and the tsunsare further subdivided into lins (neighbourhoods),which form the smallest administrative units, eachcomprising an average of 23 households.The sampling procedure entailed the designation

of 38 strata-5 big cities, 16 county-urban and16 county-rural communities and 1 administra-tion--and the multi-stage sampling of every stratumindependently. The primary (first-stage) samplingunits comprised the administrative divisions, thechus, the chens and the hsiangs. In every city, half

the chus were selected, while in every county, halfthe chens and a quarter of the hsiangs were selected.The selection was done at random using the popu-lation figures as weights. The exact sampling frac-tion for each stratum was calculated on the basis ofDecember 1958 inter-census figures as follows:

population in first-stage sampling unitstotal population in stratum

The number of houses to be included in the surveywas computed as follows:

(1) the average number of persons per house wasfirst calculated:

population in first-stage sampling unitnumber of houses in first-stage sampling unit

(2) the sampling fraction for the lower stages wasobtained:

over-all sampling fractionfirst-stage exact sampling fraction'


(3) the sample size in the first-stage sampling unitwas determined by multiplying the populationin the first-stage sampling unit by the samplingfraction beyond first stage;

(4) the number of houses to be visited was esti-mated:

sample populationaverage number of persons per house

The number of lins to be examined in each of the

Anm

first-stage sampling units was then determined asfollows:

number of houses to be included in sampleaverage number of houses per lin

In each of the first-stage sampling units (chu,chen or hsiang) a number of lis or tsuns equal tothe above-determined number of lins was drawnat random without application of weights. Fromeach of the selected lis or tsuns one lin was drawnat random, again without the application of weights.

nex 2

WEIGHTED SCORES ACCORDING TO PHYSICAL SIGNS

Score

Physical sign Symbol Degree of involvement Imma- Matureture follicles

follicles

Conjunctival follicles F a, b Involving less than 1/3 of the surface area I 2Upper tarsal Involving 1/3-2/3 of surface area 2 4

conjunctiva Involving the entire surface area 3 6

Conjunctival scars C a, c Deviation of upper tarsal conjunctival vessels, and/orfine scattered superficial scars in upper tarsal conjunc-tiva, or scars of any severity or extent in other con-junctival sites

Moderate readily recognizable scarring with no shorten-ing or distortion of the upper tarsus 4

Dense scarring of the upper tarsal conjunctival tissue 9Trichiasis and/or entropion 16

Limbus and cornea:Pannus

Vessels (measured V a, bc < 1.0 mm extension Ifrom the upper 1.0 -<2.0 mm extension 2limbus) 2.0 -<4.0 mm extension 3

4.0 -<6.0 mm extension 4> 6.0 mm extension 5

Infiltration just I a, b Minimal (seen only with monocular loupe) Ibeyond corneal Barely recognizable by naked eye 2vessels Dense opacification 3

Comeal scars kop a, c Pupillary area involved, moderate visual loss d 4Resulting in gross visual loss in one eye 9Resulting in gross visual loss in both eyes (economic

blindness) 16

a Physical sign taken into account in computing " Total " score.b Physical sign taken into account in computing " Intensity" score.c Physical sign taken into account in computing " Gravity" score.d Assessed by objective examination.

586

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