Bull. Org. nwnd.SantO 1968, 39, 547-566 Bull. Wid Hith Org.

Sampling Studies on the Epidemiology and Control of Trachoma in Southern

K. KUPKA,1 B. NIZETIt 2 & J. REINHARDS 3

Mass-treatment campaigns against trachoma and seasonal conjunctivitis, using chlor- tetracycline ointment, were started in 1952 in parts of southern Morocco. This paper reports the results ofa survey carried out between 1962 and 1965, under the auspices of the Moroccan Government, WHO and UNICEF, to evaluate the effects of the mass-campaign. The survey assessed the prevalence, gravity andfrequency ofcomplications of trachoma by ophthalmological examinations, conducted in the home, and the results are compared with data published elsewhere which were obtained before treatment started in the 1950s in parts ofthe study area. Additional studies were made ofthe relation between trachoma and the availability and use of water, and between the prevalence of trachoma in females and their exposure to infection. The over-allprevalence of trachoma was unaffected by the mass-treatment campaign but a larger proportion of the cases were at stage IV of the disease (healed). In one region, however, theprevalence ofactive cases (stagesI-III) in theyoungerage-groupshaddecreased considerably. The occurrence ofpannus decreased and while trichiasis decreased in children under 15 years of age, its prevalence increased in adults. This result may be important in planning future mass-campaigns.

INTRODUCTION 4 A few authors have reported increased prevalence Because of the high endemicity of trachoma and of trachoma in females (Bietti et al., 1962; Freyche, the regularly occurring seasonal epidemics of bac- 1958; Nakamura, 1957). Such differences may terial conjunctivitis in the south of Morocco collec- disappear in countries with very high endemicity tive treatment operations were commenced there in where everybody becomes infected. 1952, when broad-spectrum antibiotics became avail- Our observations in Morocco show that there is a able, and these have since been extended on an ever- higher prevalence of active trachoma, and particu- increasing scale. By 1960 almost the whole of the larly the grave cases, in women than in men and south had been covered. With the collaboration of that loss of vision shows a similar difference. This the Government, WHO and UNICEF, Reinhards et difference appears early in life and seems to increase al. (1959, 1968) conducted a series of clinical trials with age. which proved the efficacy of the " intermittent treat- Since sex difference in host sensitivity to infection ment" schedule.5 is unlikely, it would seem that environmental and behavioural factors are responsible. 1 Medical Officer, WHO Epidemiology and Health Statis- The following observations, made by us during tics Project, , Morocco; present address: Division many years of daily contact with the population in of Health Statistics, World Health Organization, Geneva, Switzerland. their normal environment, have a bearing on this 'Medical Officer, WHO Communicable Eye Diseases problem. They coincide with observations made by Project, Rabat, Morocco. other ophthalmologists who have also had long 3WHO Regional Office for Europe, Copenhagen, experience in Morocco (Pages, Decour, Trecolle and Denmark. infant often I For general data on Morocco, its population, the com- others). (1) The newborn female municable eye diseases problem and their control, as well receives less care than a boy, and thus may be more as for bibliography, see Reinhards et al. (1968). exposed to infection. (2) The young girl from about ' The " intermittent " schedule consists of the local application of chlortetracycline ointment (1 %) twice daily 5 years of age is often in full-time charge of her on 3-S5 consecutive days per month for 6 consecutive months. younger brothers or sisters whom she plays with and 2245 -547- 548 K. KUPKA, B. NI2ETIt & J. REINHARDS carries around on her back. Boys never have this undertaken of the reproducibility of the clinical duty and lead a more separate life. (3) The mother investigation procedures used. In addition, we tried carries her newborn child on her back for a year or to investigate the influence of water resources and until the next one is born; then the older child is their utilization on the gravity of trachoma as well given to the care of a girl in the family. as to assess the effect of repeated and prolonged The following observations about the eyes of contact with an infecting source on the number of young children have been made and confirmed in grave cases among females. several surveys (Reinhards et al., 1968). They were infected early in life with acute and sub-acute METHODS AND PROCEDURES bacterial conjunctivitis and remained infected for long periods throughout the year. All of them Sampling were also infected at an early age with an intensive For the trachoma survey a 2-stage sampling form of trachoma and they presumably had large method was chosen as the most practical way of quantities of the TRIC agent present in the obtaining a reasonable specimen coverage over a epithelium and in the discharge. scattered area with the minimal outlay of financial The eyes of young children, particularly if they resources and personnel. Using the 1960 census, a are full of purulent or mucopurulent discharge, are plan was drawn up establishing 4 homogeneous 2 constantly covered by a great number of flies and zones in the south, each consisting of about 100 000 the number of flies seems to increase the more the inhabitants, corresponding wherever possible with children are grouped. administrative divisions. The geographical location All this leads to the natural conclusion that the of these zones is shown in Fig. 1. Zone A corre- main source of bacterial and trachomatous eye in- sponded to the cercle 3 of (Province of Ksar- fections in the$e areas is in the eyes of the younger es-Souk), adjacent to the southern limit of the children (between the ages of 6 months and experimental sector of -; Zone B 5 years) and that- transmission by flies or otherwise corresponded to the cercle of Zagora (Province of occurs more easily to persons who are in a contin- ), west of zone A; Zone C included the uous and close contact with them. south-eastern parts of the cercies of Taroudant and Ouarzazate and was therefore partly in the Province Objectives of the study ' of and partly in the Province of Ouarzazate, It has been claimed recently that the evolution of west of Zone B; Zone D corresponded to the cercle trachoma is modified following a mass-campaign, of Goulimine, in the southern part of the Province resulting in a shortening of the course of the disease, ofAgadir between the Atlantic seashore and Zone C. a decrease in the prevalence of active cases, the The villages in each zone were listed following the earlier appearance of scarring and a decrease in the official village census list, and 10% (5% in Zone D complications and relative gravity of the disease. because of the large number of villages) of these These claims have been made largely on the grounds were selected at random. Owing to the wide varia- of hospital and dispensary records and on personal tion in size of the villages, care was taken to include impressions. Very few findings from the past can be a fair proportion of larger and smaller ones, by used as a base-line for comparison, however, as, making the selection separately from groups of large apart from the findings of geographically limited and groups of small villages. The official rural studies (Reinhards et al., 1968), reliable representa- census thus provided the basis for the first stage of tive data are lacking. the sample. The selected villages were thereafter The object of the present study was to describe mnarked on a map. the prevalence and gravity of trachoma and its An ad hoc census of the selected villages provided complications in the most seriously affected regions the basis for the selection of the second-stage samp- of south Morocco, to compare the results with ling units. In each sampled village 10% of the whatever data are available from the past and to 2 The criteria of homogeneity were based on the following evaluate the results of the control measures taken up factors: climate, altitude, and general way of life of the to this time. The data may also provide a basis for population. The climate is of the pre-Sahara type; altitude was estimated by typical vegetation. The characteristics evaluation of future evolution. A study was also shared by all 4 zones were that they were palm-tree oases with sedentary rural populations. I Kupka (1965). 8Administrative subdivision of a province. EPIDEMIOLOGY AND CONTROL OF TRACHOMA IN SOUTHERN MOROCCO 549

FIG. I LOCATION OF SAMPLED ZONES AND EXPERIMENTAL SECTORS IN SOUTH MOROCCO

-o

------4 - -

C, / 2 ~~~~~~~~~~~~~Ouarzazate'f//Z4 - - _Ta -~~~~~~~~~~~

-.Agadir I -_-__ - - gor _- - z~~~~~- on_-_

g Sampled zone A g Sampled zone B 1 Exp. sector Goulmima-Tinjdad d Sampled zone C X Sampled zone D 2 Exp. sector households 1 in Zones A, B, C and 20 % of house- was attached to the medical team recorded the holds in Zone D'were randomly selected for exami- number of children with whom the women had lived nation. This resulted in a final sample of about in close contact during their childhood and their 200 households or 1000 persons, since the average adult life. All women 40-45 years of age were inter- size of a household was about 5 persons. viewed in all sampled households. The length of Teams consisting of 2 health agents under 1 male contact with each child, expressed in years, was public health nurse were sent to draw up simple estimated separately, as best we could, for child- street-maps of all the villages selected and to make a hood and for adult life, basing the estimates on census by households, recording the name of the current local child-rearing practices and paying due head and number of the members of each house- regard to new births and deaths occurring during hold. Each house door was marked in paint with its the period under investigation. There is always a census number, and this number was also marked tendency to underestimate rather than overestimate on the map and the census list. the number of children in the household, but these Family history omissions would add further weight to any conclu- During the examination of randomly chosen sions reached. The data were recorded on hand- households in Zone C, a trained interviewer who sorted cards together with clinical data of gravity, and tabulation was made after manual processing. IA household is defined as a group of people living The observations were divided into several exposure together under one roof and using common resources of livelihood and was used rather than a " family " because of classes by length of contact, separately for child- the very remote and complicated relationships often found. hood, adult life, and for the 2 combined, enabling 550 K. KUPKA, B. NIfETIt & J. REINHARDS us to determine the relative gravity of trachoma for recorded the clinical findings together with age and each exposure class. sex on IBM mark-sensing cards specially designed for such a purpose. Each card carried a code Water supply number to identify the person within the household, An administrative clerk attached to the ophthal- the household within the village, and the village mological team also collected information on the within the zone. The data were processed and distance of the households from the main supply of tabulated according to the model given in the third water used for drinking and other domestic pur- report of the WHO Expert Committee on Trachoma poses, and on the amount brought daily into the (1962). house in each sampled household. The distance was estimated by the clerk from the answers given and Observer variation the information divided into classes of < 500 m; Two ophthalmologists made the examinations in 500 m-1500 m; 1500 m-2500 m; and > 2500 m. all the field trials in Morocco, Dr J. Reinhards from All short distances and most medium distances were 1952 to 1958 and Dr B. Nizetic from 1960 onwards, verified. The volume of water brought daily into a and it was considered necessary to assess the obser- household was calculated from the number of con- ver variation both for the general measurements and tainers of a special type used in that area which for the clinical diagnoses. contained about 5 litres (their average volume was Our investigation concerned the observer varia- found in a preliminary study to vary by not more tion in (1) the estimation of the age of the examinees than half a litre). The per capita daily consumption and (2) the classification of trachoma cases in Mac- was obtained by dividing the total volume by the Callan's stages. For this purpose, the 2 ophthalmo- number of household members. The answers were logists, both with long experience of trachoma in first recorded on a questionnaire and later tran- Morocco, examined 100 children in a primary scribed on to hand-punched cards where coded school, in December 1964, as well as 100 adults in clinical results were also recorded to simplify the the village of , in Zone A. establishment of correlations. One observer examined each class according to Medical examination the usual procedure after the other had left. Later they both attended an assembly of the people to All members of the selected households were study a wider variety of ages and stages of the examined by the same ophthalmologist during a disease. Again each person was examined by both home visit. The households were notified of this ophthalmologists at 2 independent examinations visit beforehand, so that the maximum number of and the data were recorded on 2 cards. Thereafter, their members could be present. the observers re-examined the schoolchildren so that Age estimation. In the absence of civil registra- every child was examined 4 times during the same tion most people did not know their age, and this day. This procedure allowed the study of " intra- had to be estimated by the examining ophthalmolo- observer " as well as " inter-observer " variation. gist from the person's general appearance. Mothers Age estimation of the examinees. " Inter-obser- usually knew the age of their young children, even ver" variation in age estimation was studied in the in months for those under 1 year, but after that they village population rather than the school, because of had often forgotten the exact age. Estimations were the uniform age-group of the schoolchildren, and the not too difficult for children, but were obviously results are reproduced in Table 1. The degree of increasingly difficult for adults. agreement, expressed as the diagonal total divided Ophthalmological examination. The examinations by the total number of observations, was 68%. were made by means of a simple binocular loupe, By reducing the number of age-groups and thus using artificial light when necessary. Field condi- increasing their range (see Table 2), the proportion tions did not permit the use of a slit-lamp. Where of agreement is increased to 86%. The age-groups doubt existed, a second examination was made after used in this latter table are the ones which have been an interval of a few days, or if necessary after a recommended by the WHO Expert Committee on short period of treatment to eliminate bacterial Trachoma (1962) for the presentation of results and infections. The results of the examination were have been used throughout this study. The margi- classified according to the third report of the WHO nal totals exhibit greater agreement because many of Expert Committee on Trachoma (1962). A clerk the differences are compensated by similar under- EPIDEMIOLOGY AND CONTROL OF TRACHOMA IN SOUTHERN MOROCCO 551

TABLE 1 CORRELATION TABLE SHOWING THE ESTIMATION OF THE AGE OF 100 VILLAGERS IN SOUTH MOROCCO, 1964, BY 2 DIFFERENT OBSERVERS

Observer Y Age- group < 1 1-4 5-9 10-14 15-19 20-29 30-39 40-49 > 50 Total (years)

< 1 5 1-4 10 10 5-9 6 4 10 Observer X 10-14 4 2 6 15-19 3 4 20-29 4 8 4 16 30-39 9 5 14 40-49 2 11 14 a 50 4 17 21

Total 0 15 6 8 9 9 15 20 18 100

or over-estimation by the observers. No significant For this, only the first examination done by each bias was observed. observer was taken into consideration. The varia- " Intra-observer " variation in age estimation was tion within observers was studied only among not studied because of the impossibility of each schoolchildren because the villagers were seen by observer seeing the same village people twice. each observer only once. The likelihood of the Diagnosis of clinical stages of trachoma. The examiners remembering individual cases was negli- variation between observers was studied among gible, as the village examination was made between 100 villagers as well as among 100 schoolchildren. the 2 school visits.

TABLE 2 CORRELATION TABLE SHOWING THE ESTIMATION OF THE AGE OF 100 VILLAGERS IN SOUTH MOROCCO, 1964, BY 2 DIFFERENT OBSERVERS USING A SMALLER NUMBER OF AGE-GROUPS

Observer Y

Age- group I1 1-4 5-14 15-24 25-44 > 45 Total (years)

< 1 5 5 1-4 10 10 5-14 14 2 16 Observer X 15-24 10 2 12 25-44 2 25 2 29 >45 27 28

29 100 Total 0 15 14 14 28 29 100 552 K. KUPKA, B. N]2ETIP & J. REINHARDS

TABLE 3 CORRELATION TABLE SHOWING VARIATIONS IN THE ESTIMATION OF THE CLINICAL STAGES OF TRACHOMA BY 2 DIFFERENT OBSERVERS AMONG 100 SCHOOLCHILDREN AND 100 VILLAGERS IN SOUTH MOROCCO, 1964

Observer X

Trachoma D Ill IV Total stageI I_

0 2 - 2

D - - 1

I 1 1 2 2 1 3 5 15

Observer Y IlI - - 3 5 7 15 14 11iFar |a 1 2 Illl 5 6 44 15 84

IV 7 6 15 52 81

Total 110 1 11 13 23 69 73 200

a In all clinical trials such cases were classified as Category " X " or " Probable cure ": Presence of fine papillary hypertrophy or follicles non-pathognomonic of trachoma, but with no active corneal lesions; need for further observation or investigation (Reinhards et al., 1959).

The results of variation between the 2 observers pared with 20 by observer Y. On only 15 cases was (Table 3) show that the agreement between the there agreement between both observers. The pro- 2 observers was 53 %. When stages 0 and D, and portion of agreement reached 80%, however, if stages II and III were combined the agreement was presented in the conventional way, i.e., diagonal 73.5%; when cases were merely divided into non- over marginal total. active (0+D+IV) and active (I, II and III), the Discussion of observer variation. From the above agreement reached 77 %. results it can be seen that the proportion of agree- " " The results of studies on intra-observer varia- ment between 2 examinations by the same observer tion are reproduced in Table 4. (intra-observer variation), as well as 2 examinations The degree of agreement between the 2 examina- by different observers (inter-observer variation) was tions by observer X amounted to 67%, and when very similar. Some disagreement is to be expected stages 0 and D, and stages I, II and III were in cases where the procedures depend more on combined, the proportion of agreement rose to personal judgement than on objective measurement, 77 %. For observer Y the respective results were but these results compare favourably with findings 64% and 81 %. By simplifying the classification into in other fields of clinical medicine. Comparisons of 2 groups, stages I, 1I and III (active cases) and marginal totals exhibit much smaller differences, stages 0, D and IV (trachoma free, doubtful and since over- and under-estimations at each examina- healed cases), the degree of agreement reached 82% tion compensate each other, thus demonstrating the and 81 % for observers X and Y respectively. This absence of important bias. The detailed classifica- last method of classification was used in estimating tion of the WHO Expert Committee on Trachoma the prevalence of trachoma in the sampled popula- (1962) may be more difficult to apply under field con- tion in this study. ditions than in a place with hospital facilities. So as Gravity and complications. Only the village popu- not to mask real differences it would seem prefer- lation was studied because the schoolchildren were able to simplify the classification of cases into too young to include severe cases in the sense of the broader groups, at least in mass surveys, to reduce nomenclature of the WHO Expert Committee on the observer variation to a minimum. The achieve- Trachoma (1962). Among 100 people examined, ment of better agreement in qualitative and quanti- 30 were classified as severe by observer X, com- tative estimation of symptoms is difficult and may EPIDEMIOLOGY AND CONTROL OF TRACHOMA IN SOUTHERN MOROCCO 553

TABLE 4 INTRA-OBSERVER VARIATION IN THE ESTIMATION OF THE CLINICAL STAGES OF TRACHOMA AMONG 100 SCHOOLCHILDREN FOR 2 DIFFERENT OBSERVERS IN SOUTH MOROCCO, 1964

Observer X Trachoma 0 D 11 III F. III IV Total stage L I_e _

I 0 4 2 6

D 2 1 II Observer X 5 2 7 2 3 5 10

III 3 27 3 35

IV 3 2 6 27 39

Total 7 7 38 38 100

Observer Y Trachoma stage 0 D 11 III F. III IV Total 0 D 1 6 8 Observer Y II 1% 5 8 III F. 1

III 4 38 3 45 IV 1 _ 14 23 38

Total 1 8 - 64 27 100

depend on how long the examiners have been the civil authorities. The replacements were selected trained together for this specific purpose. Investiga- at random from villages of comparable size. tions into this problem should be pursued. In general, attendance was very good; but in order to obtain this high attendance, all villages had RESULTS AND DISCUSSION to be visited twice and some of them several times. Most of the non-attendance was due to permanent Census of sampled zones or seasonal migration. Results of both the official and the ad hoc census, The discrepancies observed in the population as well as sampling data pertaining to the 4 zones, figures between the official census and the ad hoc are shown in Table 5. census may be due either to errors in the official Of the 41 selected villages 3 had to be replaced in census or, more likely, to changes that had occurred zone B, 1 because it could not be reached at the between the 1960 official census and the ad hoc time owing to floods, and 2 others because they census. A comparison of the sex and age distribu- could not be located. One village in zone C was tion of the sample in all 3 zones with that given by replaced because of the uncooperative attitude of the 1960 official census shows that, apart from 554 K. KUPKA, B. NIIETI1 & J. REINHARDS

TABLE 5 TOTAL POPULATION IN THE 4 SURVEYED ZONES AND DETAILS OF THE SAMPLE EXAMINED IN SOUTH MOROCCO, 1962-65 Number of villages No. of No. of No. absent Zone Zonewith > 100 with < 100 households inhabitants atexamination households households Total

Zone A Total population (official census) 59 203 262 18 945 104 604 1st stage sample (official census) 6 20 26 1 850 10 679 1st stage sample (ad hoc census) - - - 1 784 10 495 2nd stage sample (ad hoc census) - _ _ 178 988 - Examined _ _ _ 178 964 24 (2.5 %)

Zone B Total population (official censys) 51 363 414 22 084 124 348 1st stage sample (official census) 5 36 41 1 968 11 491 1st stage sample (ad hoc census) - - _ 1 637 10 537 2nd stage sample _ _ - 166 940 - Examined - _ _ 166 936 4 (0.4 %)

Zone C Total population (official census) 35 308 343 18 519 89163 1st stage sample (official census) 4 32 36 1 757 9 082 1st stage sample (ad hoc census) - - - 1 788 9 333 2nd stage sample _ - _ 182 877 - Examined _ _ _ 182 870 7 (0.8 %)

Zone D Total population (official census) 29 897 926 21 186 100 275 1st stage sample (5 %) (offlcial census) 2 46 48 1 313 6111 - 1st stage sample (ad hoc census) - - - 1 337 6 356 - 2nd stage sample (20 %) _ _ _ 269 1 277 - Examined _ _ _ 269 1 243 32 (2.6 %) differences due to the inaccurate estimation of age, young males into urban areas for temporary work, most differences appear in the under-representation and also to the tendency of males to wish to appear of persons under the age of 1 year, due to the older than they really are: females usually wished to reluctance of many parents to show young children appear younger. to outsiders. The same discrepancy was also ob- served in the official census when compared with the Prevalence of trachoma United Nations model (United Nations, 1955). The Four zones have been investigated so far. Clinical under-representation of males between 15 and 44 findings on prevalence in zones A and B are shown years of age might be due partly to the migration of in Table 6 and in zones C and D in Table 7. EPIDEMIOLOGY AND CONTROL OF TRACHOMA IN SOUTHERN MOROCCO 555

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. . ., 0 0o 6 6 \. .\ o. 6 0X Z6 o0 Z6

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- - >0) 0 = 0= 0 - = = -a >- 0 0 0- - - %- co 0 0= 0- O+ L-. .. I I_- EPIDEMIOLOGY AND CONTROL OF TRACHOMA IN SOUTHERN MOROCCO 557

Trachoma was found to be almost universal in all TABLE 8 4 zones and in zones A, B and C the small fraction PREVALENCE ESTIMATES OF ACTIVE CASES a OF TRACHOMA IN THE 4 of trachoma-free (Tr 0) persons was in the very SAMPLED ZONES IN SOUTH MOROCCO, 1962-65 young age-groups; in zone D some trachoma-free people were also found among older children and |Zone Al Zone BI Zone C Zone D adults. Everywhere the disease was acquired very early in life and its prevalence increased very rapidly Active cases (%) 63 57 55 41 with age. The first cases were found in 2- and 3- month-old infants (younger infants were rarely 95 % confidence limits (%) 59-67 54-61 51-59 38-44 seen), usually earlier among girls than boys. Before were 1 year were they old 50% already infected and a Stages 1, 11 and 111. 95% were infected in the 1-4-year age-group; these proportions were generally reached somewhat sooner by girls than by boys (except in zone D). and the true unknown prevalence in the population The greater frequency of cases among female infants lies between 59% and 67%, with 95% confidence. might be ascribed either to differences inherent in As can be seen from the confidence intervals, sex or to sampling errors, but most probably it was zone A had a significantly higher -prevalence than due to the adfliitted neglect of girls in some tribes. zones C and D. While most of the physical factors Boys have a more privileged position in the family, of environment of the first 3 zones, such as climate, and would be more readily treated if treatment were soil, etc., appear to be generally extremely similar, difficult to obtain. In zones A, B and C the as are also the way of life, race and religion of the prevalence of active cases was somewhat higher inhabitants, there is one geographical feature which, among females than among males in all age-groups. with its ecological consequences, differentiates zones In zone D the opposite was found in children up to C and D and might explain the differences in 4 years of age. trachoma. Whereas in zones A and B the villages The beginning of the scarring process (stage III) are clustered quite close together along the principal occurred at about 3-6 years of age, in both males river running though each area, in zones C and D and females. At about 10 years of age 50% of the there are various smaller streams, each with a few children had reached stage III, still with no villages strung out along them; the villages tend to significant difference between the sexes in any zone. be smaller as well as more widely scattered. Also, From then up to the age of 45 years, active the proximity of zone D and a few parts of zone C trachoma was more frequent in females than in to the Atlantic Ocean may improve the climatic males in each age-group. This could have been due conditions. to the fact that females remain in closer contact with Although the prevalence of trachoma in the infants and thus become frequently reinfected and 4 zones might have been different before the mass- are prevented from reaching stage IV (healed) (see campaigns, the observed zone variation might also pp. 562-564). be due to the different impact of treatment during Stage IV was first observed between the ages of the mass-campaigns. There might have been differ- 5 and 11 years in zones A, B and C and earlier in zone ences in emphasis in the campaigns in the 4 zones, D; it was usually seen earlier among boys than in their acceptance by the population or in the girls, and 50% of the sample reached this stage at regularity of self-treatment within the family. about 25 years of age, again earlier in zone D and Unfortunately, the few data available on the past earlier for males than females. By 45 years of age, are of questionable reliability and comparison with about 96 % of males and 87 % of females had reached the results of the present survey is difficult. The stage IV. methods used in most of the previous work were not The proportion of active cases (stages I, II and always indicated, geographical situations were often III) in the total population was calculated according vague, and results were usually published as to the method of Cochran (1963). The estimates, estimated ranges of prevalence, which could not be together with their 95 % confidence intervals for the used to explain zone differences. The only studies 4 zones, are presented in Table 8. described by Reinhards et al. (1968) which might Thus, in zone A, for instance, the estimate of eventually be used for comparison, are those from prevalence of active cases (stages I, II, III) was 63 %, Skoura in 1952, adjacent to the north-east of our 558 K. KUPKA, B. NI2ETI' & J. REINHARDS sampling Zone C, and from Ouarzazate in 1953 earlier than before. A more detailed cohort study included in our sampling Zone C. Even those would possibly be needed to answer this question. studies are difficult to compare, but we may assume Stage IV starts to appear in the school age-group that units next to each other are likely to be similar, (5-14 years). The surveys in the 1960s showed that especially when ethnic as well as environmental stage IV was relatively much more important than conditions appear identical. The claim by most in the earlier surveys. In the recent surveys 50% of authors that trachomatous conditions were very the population reached stage IV at about the age of much the same in all areas before mass-treatment 25 years, a percentage never reached in any age- started is of little value in comparative studies. group in earlier surveys. The prevalence of trachoma in the present survey is different from that found in the previous surveys Relative gravity of trachoma in the sampled zones of Reinhards et al. (1968). A number of children An important distinction has been made between now escape infection for some time, particularly in the relative intensity of trachoma-defined as the Zone D. Unfortunately the under-representation of degree of activity of the disease in an individual case very young children in the sample prevents an accurate at a given time-and the relative gravity of comparison with those observed recently in Skoura trachoma-defined as the degree of disabling and Goulmima (Reinhards et al., 1968). complications and sequelae, or of active lesions The total of active cases was also lower in our which, if untreated, will lead to disabling survey, varying from 41 % to 63%, compared with consequences.' 87% in Skoura and 92% in Ouarzazate in 1952 and Data on relative gravity, grouped separately by 1953 respectively. This crude figure for prevalence the characteristics of the lesions, are given in may obviously be affected by sex and age Tables 9 and 10 for the 4 zones, and summarized in distribution and may also vary with the prevalence Table 11. Graphical presentation of the prevalence of trachoma-free and healed cases (stagesO and of grave cases by age and sex is attempted in Fig. 2. IV). Here, the difference appears mainly in the The number of grave cases was consistently marked increase in the number of healed cases higher among females, and increased with age. The observed in the recent surveys. In the previous first severe cases appeared from 3 to 14 years earlier studies, only 8% (Ouarzazate) and 13% of healed among females. cases (Tr IV) were registered as spontaneous cures As shown in Tables 9 and 10, in zones A and B compared with our finsdings of 35 %-42 % (first more than 7 % and in zones C and D more than 2 % 3 zones) in 1960-64. of the total population suffered from trichiasis. An The observed approximately 3-fold increase in the increase in prevalence with age was observed in all number of cured cases may be considered as one of zones and in persons aged 45 years and over the the most important features of the improvement in rates reached between 6 % and 26 % for both sexes the situation, thanks to the mass-treatment effect. combined. Among females, trichiasis occurred This finding is even more remarkable if con- earlier and about twice as frequently as in men, in sideration is given to the fact that the higher the all age-groups and in all 4 zones (Fig. 3). endemicity, the greater the difficulty of obtaining a noticeable treatment effect; a possible reason being Loss of vision the increased likelihood of reinfection or the more The recording of loss of vision and blindness is of pronounced degree of the infiltrative lesions. great importance in any survey of communicable Unhappily in such conditions the intensity and eye diseases. The presentation of data has to be regularity of treatment suffers; because of lack of made by age-groups and by sex. In all surveys )ersonnel, only self-treatment could be organized in made, loss of vision was recorded only in those Morocco. cases with pathological signs which could have been A study of the scarring process shows that the caused by eye infections. However, it was virtually first cases of stage III start to appear at the time impossible to decide what proportion of the cases of when the prevalence of active cases reaches its maximum (age-group 1-4 years) as found in earlier 'Thygeson, P. & Maxwell-Lyons, F. (1961) Trachoma: surveys. However, because a certain number of assessment of intensity and gravity. In: Report on the conference on the control of communicable eye diseases, children now escape infection for a year or more it Istanbul (Unpublished document EURO-158.3, from the is possible that in some the cicatrization now starts WHO Regional Office for Europe). EPIDEMIOLOGY AND CONTROL OF TRACHOMA IN SOUTHERN MOROCCO 559

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FIG. 2 TABLE 11 DISTRIBUTION AND FREQUENCY OF GRAVE CASES PREVALENCE OF GRAVE CASES (%) BY AGE AND SEX BY AGE AND SEX IN THE 4 ZONES, IN THE 4 SURVEYED ZONES IN 1962-66 1962-65 1 Age-groups (years) Zone Sex 1-4 5-14 15-24 25-44| > 45 Total

A Males - 2 8 15 33 10 Females - 8 20 36 45 18

B Males - 3 8 21 24 10 Females - 2 20 28 52 19

C Males - 2 3 6 13 5 Females 3 6 10 11 26 12

D Males 1 2 8 7 11 6 Females 2 4 10 13 24 12

50 loss of vision were due to trachoma and what ZONE B / proportion to conjunctivitis. A number of typical 40 pannus cases exist in which no circumscribed leucomata can be detected. Even in such cases the 30 t_/// role of bacterial infection in the determination at of the loss of corneal transparency cannot be cn /~ < 20 / /~ evaluated. Also the presence of trachoma may play / 0,.0 / 1 1 10 /I FIG. 3 PREVALENCE OF TRICHIASIS, INCLUDING ENTROPION, a 1 10 20 30 40 50 6( BY AGE AND SEX IN THE 4 ZONES, 1962-65 n1 3u1. 11 B ZONE C - 0 / 20 30 F ZONES A AND B / _ A

10 20k t 1 v0 n */ AB V o l0 20 30 40 50 60 10- .-2 JU

.0 ZONE D .000 20

10

Un _, 0 10 20 30 .40 50 60 Age (years) 30 WHO 81200 Age (years) WHO 81201

____ Female ____ Female Male - Male 562 K. KUPKA, B. NIIETI6 & J. REINHARDS a role in the origin of a leucoma but often this maintained suppression of conjunctivitis in the cannot be established with certainty. whole population since 1953-55. Because definitions of blindness vary greatly from author to author and from country to country, it is Difference in severity of trachoma in relation to sex difficult to compare differences or evaluate changes We are aware that the method, described earlier, which may occur. The easiest group to delimitate of collecting data by interrogation and linking this includes the cases of total blindness, which can be with clinical findings has many shortcomings when defined as having no vision or not more than faulty applied in a primitive community. light projection. The term " economic blindness " We are also aware of difficulties which arise in has been used for any degree of vision less than comparing data obtained in such " exposure 20/200-5/200, but strict criteria cannot be followed classes" very different in numerical size. (In fact in the examination of primitive communities in there were very few females in our sample who had these natural conditions. had little or no contact with young children during In this survey the finger-counting test was used their lives.) where gross corneal opacities were present. The Similar surveys are being continued and for the limit for economic blindness was taken to be 5/200. above reasons we propose to give the results of this Unfortunately this makes the comparison with rstudy only to indicate the trends. older data impossible when 10/200 was set as the limit Interviews were obtained with 130 females or only cases of complete blindness were counted. between 40 and 45 years of age. The relation Several other facts make comparability difficult: between the length of contact with an infected (1) In some southern tribes it is very difficult to see source of one or more young children during the all blind adults for examination, even if they are woman's childhood, as well as during her adult life, known to be present in the household. (2) The and the prevalence of grave cases is reproduced in survival rate of blind people may be lower than for Table 12. the rest of the population of the same age. This has As can be seen from the column totals, the been observed even in developed countries and prevalence of grave cases increases with the number would make evaluation of changes in the blind rate of years of contact during childhood, being 30% and the rate of yearly new additions to the blind with no contact, 36 % after 1-4 years' contact, and group extremely difficult. 45% after contact of 5-14years. The linear trend In the zones A, B, C and D the number of was significant (at the I % level) using the test economic blind in the sample was recorded as 1.1 %, procedure suggested by Yates (1948). 1.7%, 0.5%, and 0.5% respectively, with higher Similarly, an increase in the percentage of grave rates among females than males in the first 2 zones cases was observed with increased contact during and increasing with age (in retrospect we feel that motherhood as shown by the row totals. With no the sample might have been too small to evaluate contact, 15 % of grave cases was \observed, the blind rate correctly). Tables 9 and 10 show that increasing to 41 % with contact of 15 years or more. those with one eye completely blind amounted to Here, the increase in the percentage of grave cases 1 %-3 % of the total with lowest rates in zones C was predominantly between those cases with no and D. Here also the rates in females were higher contact and those with 1-4 years' contact. than in men and increased with age. If the childhood and motherhood years of contact Much higher rates of economic blindness were are combined (diagonal), the correlation is very found in 1954 in the Goulmima experimental similar for obvious reasons, increasing from 12% sector. This can be explained by the different for no contact (either in childhood or motherhood) standards applied to obtain a rough estimate of to 50% for maximum contact reQeived in childhood residual vision (in 1954, 10/200 was considered as and in motherhood. the borderline). A detailed analysis of the joint effect of childhood A most striking feature was the almost complete and motherhood contact on gravity would require absence of economic blindness in the younger age- greater numbers of observations and further studies groups in the 1962-65 surveys. may be useful. The relative absence of leucomata in younger In general, the data reported here have shown persons who had lived most of their lives with self- earlier onset and constantly higher prevalence of treatment available may be explained by a I Kupka (1965). EPIDEMIOLOGY AND CONTROL OF TRACHOMA IN SOUTHERN MOROCCO 563

TABLE 12 RELATION BETWEEN CHILDHOOD AND MOTHERHOOD CONTACT WITH AN INFECTIVE SOURCE AND PERCENTAGE OF GRAVE CASES OF TRACHOMA a

Childhood contact (years) Contact during 0 1-4 5-14 Total No. % No. % No. % No. % (ytears)o exa- Grave exa- Grave exa- Grave exa- Grave mined cases mined cases mined cases mined cases

0 8 12 5 20 - - 13 15 1-4 10 40 6 33 1 0 17 35 5-14 49 33 28 36 6 50 83 35 > 15 8 25 5 60 4 50 17 41

Total 75 30 44 36 11 45 130 34

a Among females 40-45 years of age in Zone C 1964-65. active trachoma in females, with delayed healing and environmental differences are particularly evident in a markedly higher frequency of grave cases and Morocco; not only are young girls less cared for complications (Vozza et al., 1964). Two factors than boys, but females usually have constant close seem to be involved in shaping the frequency and association with young children throughout much of severity of trachoma: susceptibility and exposure. their lives. The risk of exposure is thus very high. Difference in susceptibility of the sexes was Although the mother may at first be the source of suggested by Bietti et al. (1962) who claimed that infection to very young children (WHO Expert the conditions of exposure are similar for both Committee on Trachoma, 1956) 2 with a prevalence sexes. However, a greater inherent susceptibility in of active cases among children close to 100%, one the female sex would be somewhat exceptional, can easily speculate on the possibility of the mutual considering the findings in other diseases. Greater intensification of infection between mother and female susceptibility has been found in only a few child reaching a vicious circle. In the absence of infectious diseases such as whooping-cough, scarlet adequate acquired immunity the mother is unable fever, diphtheria, dysentery, mumps and the to achieve spontaneous healing and remains in common cold. Even then, the bias towards the stage III of the disease. Higher rates of reinfection female sex appears only in some age-groups, being among females (Freyche, 1958) 3 and thus a non-existent or even reversed in others (Taylor & prolonged course of the disease, increase the risk of Knowelden, 1957). severe lesions 4 such as conjunctival or comeal In view of the observations presented, we are complications, and an early age of onset of more inclined to favour the hypothesis of Freyche trichiasis. (1951). He ascribes the higher prevalence in females The results of our studies are consistent with the to greater and more frequent exposure to infection, hypothesis that gravity of trachoma among females due to social habits, at least in most of the countries is mainly determined by the increased risk of where trachoma is prevalent. If differences in reinfections; there were no indications whether susceptibility do exist, they would be to a great extent confounded with large sex differences in way 'See also: WHO Regional Office for Europe (1961) Report of the conference on the control of communicable eye of life and environmental conditions ". These diseases, Istanbul (Unpublished document EURO-158.3). 3See also: WHO Regional Office for Europe (1958) 1 Savic, D. & Popovic, M. (1958) Epidemiological survey Report of the European conference on trachoma control, of trachoma conducted in the village of Martinci. In: Report Dubrovnik (Unpublished document EURO-158). of the European conference on trachoma control, Dubrovnik, 'See: WHO Regional Office for the Eastern Medi- October 1958 (Unpublished document EURO-158, from the terranean (1960) Report of the conference on trachoma, WHO Regional Office for Europe). Tunis (Unpublished document EM/Trach.Conf./26). 564 K. KUPKA, B. NI2ETIt & J. REINHARDS

TABLE 13 RELATION BETWEEN THE DISTANCE OF THE HOUSEHOLD FROM THE WATER SOURCE AND THE INCIDENCE OF TRACHOMA BY AGE-GROUPS IN ZONES A AND B, 1962-63 Age-group (years) Distance from < 1 1-14 > 15 Total water _1 oa source No. % No. % No. % No. % (m) exa- Inci- exa- Inci- exa- Inci- exa- Inci- mined dence mined dence mined dence mined dence

Active cases <500 20 60 524 92 538 35 1082 58 501-1 500 3 100 108 87 100 15 211 53 1 501-2 500 5 60 75 100 61 26 141 67 > 2500 14 71 242 96 210 28 466 65

Total 42 67 949 93 909 25 1 900 60

Grave cases < 500 20 0 524 2 538 27 1 082 15 501-1 500 3 0 108 2 100 29 211 14 1 501-2 500 5 0 75 3 61 26 141 13 > 2 500 14 0 242 3 210 28 466 16

Total 42 0 949 3 909 27 1 900 14

superinfection or associated infections were to Daily per capita use of water. The relation of blame. The frequency of grave cases observed water use to the prevalence of active cases, as well as among females who have had no contact with the prevalence of grave cases, is shown in Table 14. siblings or their own children is 12.5% compared The prevalence of active cases was lower in the to the expected frequency of grave cases (by age-group 1-14 years with increased use of water. interpolation) in males of the same age-group, of For the other age-groups no such evidence was 10% in zone C. This comparison strongly suggests found. However, because the age-group 1-14 years that the susceptibility hypothesis is incorrect. was numerically the most important one, the lower frequency of active cases with increased use of water A study of the correlation between water supply and was also found for the total population. trachoma A higher prevalence of grave cases was associated Distance of household from the water source. An with the lowest water consumption in all age-groups investigation was made of 343 families, out of 344, in which grave cases were found. randomly selected in the first 2 zones. The relation The proportion of water used for drinking and between the distance from the water source and the cooking purposes was not investigated but it was frequency of active trachoma cases, as well as the assumed that the amount consumed as intake was prevalence of grave cases, is presented in Table 13. fairly constant in a given area and in a given Little correlation was found in the study of season. It is very likely therefore that any prevalence of active cases, but somewhat higher additional amount would be used mostly for prevalence rates were observed for distances above hygiene purposes and therefore would result in 1500 m. The percentage of grave cases was very increased cleanliness. The information from little higher for the households with the longest Table 14 suggests some correlation between the distance (>2500 m) to the water source. water use and disease. EPIDEMIOLOGY AND CONTROL OF TRACHOMA IN SOUTHERN MOROCCO 565

TABLE 14 RELATION BETWEEN THE PER CAPITA DAILY USE OF WATER, ESTIMATED IN LITRES, AND THE INCIDENCE OF TRACHOMA BY AGE-GROUPS IN ZONES A AND B, 1962-63

Age-group (years) Volume <1 1-14 > 15 Total of water (litres) No. % No. % No. % No. % exa- Inci- exa- Inci- exa- Inci- exa- Inci- mined dence mined dence mined dence mined dence

Active cases < 5 10 70 228 95 183 26 421 64 5-10 29 62 628 94 584 24 1 241 60 > 10 3 100 93 87 142 26 238 51

Total 42 67 i949 93 909 25 1 900 60

Grave cases < 5 10 i 0 228 4 183 30 421 15 5-10 29 0 628 2 584 28 1 241 14 > 10 3 0 93 2 142 23 238 15

Total 42 0 949 3 909 27 1 900 15

Strangely enough, no correlation was found any conclusions from this study, because of some between the per capita use of water and the distance confusing factors not taken into account in planning of the water source. One might conclude that the the study. For instance, we now realize that the average amount used is a family characteristic, transmission rate of communicable eye diseases in dependent more on the habits of cleanliness, and southern Morocco is usually higher in the larger and apparently unaffected by the distance the water has more crowded villages. In general such villages to be carried. Possibly, unless water is immediately have developed only where a water supply is readily available within the house, from a tap or a well, the available near by. These and other factors should distance from the house is not important. be taken into consideration in any future study of Great caution should be applied in trying to draw this type.

RESUME

Un programme de traitement de masse du trachome observations faites aux quelques donnees recueillies vers a e lanc6 au Maroc en 1952; des 1960, les operations 1950, avant le traitement. On a egalement'recherche l'in- s'etaient etendues a la quasi-totalite du sud du pays. fluence de certains facteurs de milieu, specialement des Pendant cette campagne, on a utilise le traitement local ressources en eau et de leur utilisation, et les rapports intermittent, consistant en l'application locale d'une existant dans le sexe feminin entre la prevalence et la pommade a la chlortetracycline a 1 %, deux fois par gravite du trachome et les risques accrus d'exposition a jour, pendant 3 a 5 jours consecutifs par mois durant l'infection. 6 mois. On a procede par sondage a deux degres, l'unite du Au cours d'une enquete menee dans la region, de 1962 premier ordre etant le village, l'unite du second ordre la a 1965, sous les auspices du Gouvemement marocain, de famille, au sens large du terme. L'echantillon de popu- l'OMS et du FISE, on s'est attache a determiner la pre- lation final comprenait environ 4000 personnes, soit 1 % valence du trachome, sa gravite et la frequence des com- de la population totale de la region. La collaboration des plications et a comparer, dans la mesure du possible, les habitants a ete tres satisfaisante (99% de participation) 566 K. KUPKA, B. NIZET1 & J. REINHARDS et on peut considerer 1'echantillon comme representatif sexe feminin, la gravite relative du trachome est toujours en ce qui concerne la repartition par sexe et par groupes plus marquee et elle s'accroit avec l'age; les cas graves d'age. Les resultats des examens ophtalmologiques ont apparaissent 3 a 14 ans plus tot chez que les hommes. e analyses pour faire ressortir les variations du diag- L'infiltration corneenne importante (pannus > 4 mm) nostic chez un meme examinateur ou entre deux exami- s'observe dans 0,1 a 1% des cas et le trichiasis atteint, nateurs. De meme I'age des habitants a ete evalue par selon les zones, 2 a 7 % de la population. Le pourcentage deux enqueteurs differents et les resultats de cette estima- des cas de cecite (vision reduite a 5/200) varie selon les tion ont e't compares. Dans tous les cas, une concordance endroits de 0,05 a 1,7 %. satisfaisante a et notee. L'etude de l'influence du sexe montre qu'en general les Les examens ont montre que la pr6valence globale du sujets de sexe feminin sont exposes a contracter l'infection trachome 'a tous les stades (I a IV) etait tres elevee, plus pr6cocement, ils presentent une plus forte prevalence atteignant selon les zones des taux de 84,9 'a 98,9%. de trachome actif, un taux moindre d'evolution vers la L'atteinte semble tres precoce et la frequence de I'affec- guerison et une tendance plus nette 'a la gravite et ah l'appa- tion augmente rapidement avec l1'age: 50% des infections rition de complications. Selon les auteurs, ce phenomene surviennent avant I an et 95 % des enfants de 1 'a 4 ans est du1 a un taux de reinfection beaucoup plus eleve chez sont trachomateux. L'apparition des cicatrices (stade III) les femmes et a des contaminations croisees a repetition se fait vers l'age de 3 a 6 ans et 50% des enfants ages de entre les meres et les enfants. On n'a pu etablir de corr6- 10 ans sont au stade III. Vers I'age de 45 ans, environ lation nette entre la prevalence du trachome et la distance 96% des hommes et 87 % des femmes ont atteint le stade separant l'habitation de la source d'approvisionnement IV. La proportion des cas actifs par rapport a l'ensemble en eau; cependant les indices de gravite sont generalement des cas varie de 41 a 63 %. La comparaison avec les rares plus eleves lorsque cette distance est considerable. On a donnees recueillies en 1952 et 1953 indique une proportion note un plus grand nombre de cas de trachome actif ou moindre de cas actifs et un taux de trachome gueri pres grave si la consommation d'eau pour les soins d'hygiene de trois fois plus eleve pour 1'enquete actuelle. Dans le etait basse.

REFERENCES

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