Environmental Influences on the Distribution of the Incidence of Cholera: A Case Study in Quelimane,...

Environmental Influences on the Distribution of the Incidence of Cholera: A Case Study in Quelimane, Mozambique

ANDREW COLLINS

Cholera continues to cause widespread suffering in many parts of the world. Previous research has mainly described modes of transmission and has correctly indicated the role of predisposing socio-economic conditions in affected areas. Little field research has been carried out, however, in endemic zones, on the contribution of physical characteristics in environmental resewoirs which prolong the survival time or increase the toxigeneity of Vibrio cholerae 01, despite substantial indication of their significance at laboratory scale. A study carried out in Quelimane, Mozambique, to test for such environmental influences on the spatial and temporal distribution of cholera incidence, is described. The role of population displacement in this relationship is also discussed. The practical implications of the results for prevention of prima y infection and subsequent reinfection are outlined.

The main aim of this study is to determine if physical environmental factors, relating to the extended survival time of Vibrio cholerue 01 or its increased toxigeneity, are influential in shaping the distribution of incidence of cholera. Laboratory experi- mentation carried out during the 1980s has indicated that survival times and toxigeneity of Vibrio cholerue 01 are affected by exposure to varying conditions of salinity and pH (Miller et al., 1984; 1986). This study examines the extent to which there were significant spatial patterns of incidence and association with key environmental factors during the course of a 12 month epidemic in Quelimane, Mozambique.

There is relevant application in

determining and identifying more favourable zones or areas of avoidance for communities at risk of recurring outbreaks in endemic regions. The testing of the physical environmental hypotheses outlined above also acts as a control against which specific non-environmental factors relating to the distribution of cholera incidence in Quelimane can be considered. Attention in this study is drawn in particular to the high densities of displaced persons that are located within some parts of the municipality.

THE PRESENT CHOLERA PANDEMIC

Cholera has been globally on the increase over the last three decades. The increase

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322 Andrew Collins

has been particularly big over the last three years with a rapid spread of the disease in South America and Africa (WHO, 1992a). The present strain of Vibrio cholerae 01 that is most responsible for this increase belongs to the El Tor subgroup which has been spreading from its origin in Indonesia since 1961. The World Health Organ- ization statistics show that the total reported infections in the world for 1991 were 594,694, approximately nine times the total figure of 70,084 for 1990 (WHO, 1991a; 1992b).

The bulk of media reports concentrated on the situation in South America despite the fact that, by the end of July 1991, 20 African countries had registered a total of 48,860 cases with 3,736 deaths representing a faster spread and increase than any other part of the world. By the end of 1991 statistics based on cases reported to WHO show that, whilst total infections from cholera in the Americas (391,220) were more than twice that of Africa (153,367), deaths were more than three times higher in Africa (13,998) than in the Americas (4,002). Mozambique was one of the most affected countries with reports for the first half of 1992 alone indicating 176 deaths in the provinces of Maputo, Gaza, Tete, Sofala, and Zambezia (Masungulo, 1992). By the end of 1992 the total for the whole country had risen to 30,802 cases with 726 deaths, by far the highest in Africa (WHO, 1993).

Precise definitions of endemic as opposed to epidemic cholera are difficult to formulate. However, as a guideline, Miller et al. (1985) have stated that cholera can be said to be endemic in an area where cases occur ‘not necessarily continuously, but regularly and without evidence of reimportation on each occasion, and a seasonal pattern is usually observed’. Studies on the epidemiology of cholera have broadly proposed four mechanisms for the maintenance of endemic cholera, as follows (Miller et al., 1985):

maintenance of Vibrio cholerae 01 in a non-human animal population; maintenance of Vibrio cholerae 01 in chronic carriers not necessarily excreting the organism; maintenance of Vibrio cholerae 01 by low- level continuous transmission through people with asymptomatic infection or mild disease; and maintenance of Vibrio cholerae 01 in an aquatic reservoir.

The fourth explanation, although regarded as impossible up until the mid-l970s, has attracted attention over the last 15 years (Merson et al., 1978; Miller et al., 1982; 1984; 1985; Siddique et al., 1991; Epstein, 1992; Colwell and Spira, 1992).

Shellfish have often been suspected of spreading cholera and several recent studies in coastal areas of the USA have served to reawaken the possibility of the non-human animal reservoir (Kaysner et al., 1987; Doran et al., 1989). It is interesting that the aquatic reservoir and the non-human animal reservoir theories would appear to be open to the possibility of convergence in that the feature of a brackish environment can be considered common to both circumstances. This has recently been emphasized further by the isolation of Vibrio cholerae 01 from the intestines and skin of fish in polluted coastal waters along the coastline of Peru (Tamplin and Parodi, 1991).

CHOLERA IN THE ENVIRONMENT

Although the role of faecally contaminated water as a means of transmission has been known about since the last century, when John Snow carried out his famous studies on the distribution of cholera cases in London (Snow, 1855), the theory of an environmental niche in which the vibrio survives remains largely unproven, much more attention being concentrated on the secondary modes of faecal-oral trans-

DISASTERS VOLUME 17 NUMBER 4 @ Basil Blackwell Ltd. 1993

Environmental Influences on the Distribution of Cholera 323

mission that develop as the disease spreads (WHO, 1986; 1991b; Pan American Health Organization, 1991a; World Bank, 1992).

Associative environmental studies on the transmission of cholera have been correct to highlight the importance not only of contaminated water supplies, but also underlying factors of poverty, congestion, socio-economic and behavioural disruption, and poor provision of appropriate health care. Ferguson (1975) highlights the importance of the prevalence of such conditions as an over- burdened medical service and poor communications, whilst Adesina (1977) pointed to a lack of commitment to maintaining a sanitary environment in post colonial areas, the maintenance of which was considered the sole respon- sibility of government. The Pan American Health Organization has reiterated the importance of personal hygiene and education in its bulletin on the chronic cholera situation in the Americas (Pan American Health Organization, 1991b). Donovan (1991) makes the connection between ’disease in the water supply and lack of liquidity in the economy’ and traces the cholera epidemic raging across Latin America to the ’policies of hard-nosed foreign financiers’. Robinson (1991) states that the breakdown of government infrastructure resulting in inadequate housing and sanitation, was the cause in Peru. The WHO points to overcrowding, lack of adequate and safe water supplies and insanitary disposal of excreta as the main factors in transmission. A rapid increase in the incidence of gastrointestinal infections, such as cholera, is also sometimes linked to the importation of pathogens by migrants from rural areas in which the disease is endemic (WHO, 1986), or amongst groups of newly arriving refugees to camps, such as has been described by Mulholland (1985) in an account of an epidemic in a refugee camp

in eastern Sudan in 1985. If there were no opportunities for

water or food to become contaminated with cholera vibrios, transmission of the disease would be very minor or would not occur at all. A brief resume of the state of the world’s water and sanitation supply, however, makes it clear that contamination is not likely to be eradicated in the immediate future. In 1980 WHO estimated that only 20 per cent of the world’s population had access to totally safe drinking water; that 80 per cent of all sick were suffering from diseases related to poor water and sanitation; and that 6 million children every year die from diarrhoea1 diseases primarily associated with bad water. Cholera is just one of the pathogens responsible. During the United Nations Drinking Water and Sanitation Decade of the 1980s, access to uncon- taminated water increased with WHO figures suggesting that between 1980 and 1990 more than 1.6 million additional people were provided with access to water of reasonable quality. But this has barely kept pace with population growth and about 1 billion people still lack an adequate water supply with 1.7 billion people lacking adequate sanitation facilities (Lloyd, 1992; World Bank, 1992). There is also the harsh reality that many of those registered as officially having access, still drink polluted water. The daunting scale of the effort required to eradicate these problems must mean that any additional preventative action that can be taken to reduce incidence should be explored with urgency.

The need for attention to be paid to the possibility of potential pools in nature of vibrios that are converted under appropriate conditions from innocuous water vibrios to toxigenic pathogens capable of epidemic spread has been outlined in relatively recent accounts (e.g., Miller et al., 1984; 1986) after laboratory investigation into the impact of physio-

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324 Andrew Collins

chemical stress on Vibrio cholerae 01. This has also been indicated by Greenough I11 (1990) and Colwell and Spira (1992) in resumCs of the ecology of Vibrio cholerue and its determinants of survival. Work by Miyaki et al., (1967), Pandit et al., (1967), and Prescott and Bhattacharjee (1969) suggests survival times dependent on factors such as temperature, pH, osmotic pressure, moisture content, salt or carbohydrate concentration, and the presence of organic matter and bacterial flora as key factors in determining survival times in different foodstuffs. Experimental studies have also shown that gastric acid is one of the body’s main lines of resistance against cholera (Cash et al., 1974) and vibrios are known to be unable to survive in carbonated water due to its low pH (WHO, 1986). Other investigations carried out on water suggested the key factors to be temperature, pH, salt, and bacterial and organic content (Singleton et al., 1982; Colwell and Spira, 1992).

The work of Miller et al., (1984; 1986), involving extensive measurement of a variety of strains of Vibrio cholerue 01 under laboratory conditions, has suggested that optimal conditions of salinity, pH, nutrients and temperature are key factors in keeping them viable for more than 40 months. Particular attention was paid to the role of salinity and pH. Miller et al. (1984 p. 493) have stated (and others mentioned above have indicated) that their laboratory findings require the support of further investigation, such as ‘Detailed field studies to determine if reservoirs of Vibrio cholerue 01 really exist in such aquatic environments in the endemic areas of Asia and Africa’.

METHODOLOGY

The field study described in this paper focused on the issue of varying incidence of cholera rather than potentially spurious quantification of vibrios in and around

Quelimane.’ As an indication of faecal contamination of water, however, and conforming to standard practice, quantities of faecal coliforms were determined for all areas.

The practical objectives of the project relate to a range of interconnected factors, and attention is drawn to several areas of possible investigation relating to an epidemic, such as the one in Quelimane, displayed diagrammatically in Figure 1. The two main variables singled out for quantitative investigation in this study are the rate of incidence itself and relevant environmental factors, primarily linked to water supply. It is recognized, however, that there are other interrelating factors, not dealt with in detail here, that could provide the main focus for other studies relating to cholera incidence. The intention is to suggest that field measurement and findings relating to the interaction of these two elements may not only be the key to a better understanding of processes and patterns relating to cholera incidence, but also that they may provide a backdrop for a more informed inference about the other parts of the system.

QUELIMANE

Quelimane city, capital of Zambezia province and with a population of approximately 14O,OOO, has known cholera attacks in the past and was identified in early 1991 as suffering from a particularly bad outbreak (Mozambican Information Office, 1991).

The overall macro-scale geographical circumstances of the city, such as its estuarine location, high temperatures and humidity, heavy seasonal rainfall, and a vastly increased population (in this case due to an ongoing war of destabilization in the rural areas), are some of the characteristics that have been associated with endemic areas of cholera in the past (Adesina, 1975; Merson, 1980; Miller et al.,

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NATURE OF CHOLERA

SOCIOGEOGRAPHIC STRUCTURES AND BEHAVIOURAL PHENOMENA

FIGURE 1 A systems approach to an analysis of cholera incidence.

VIBRIO CHOLERAE

SEROTYPES NOT SUB-GROUP 01

/ \ BELONGING TO SUB-GROUP 01

BIOTYPE EL TOR CLASSIC BIOTYPE A\ SEROTYPE OGAWA SEROTYPE INABA

FIGURE 2 Details of cholera serotypes. That associated with Quelimane is boxed (Identification made by the Central Hospital, Quelimane 2992).

1982; 1985; Learmonth, 1988; WHO Features, 1990, WHO Technical Report Series, 1991). The case of Quelimane has added interest in that the particular serotype of the biotype El Tor (Figure 2) was identified as different from that associated with the main epidemic spreading through Africa at that time. This lends substantial weight to the understanding that the situation in Quelimane is endemic.

Physical background

As part of the sedimentary basin that occupies about 31 per cent of Mozambique, the zone is composed of

sands with fine sands at the surface, micas and layers of clay. In general it is characterized by prolonged sand dune ridges, known locally as ‘morundas’, shallow depressions between them and coastal plains, some areas of which are covered by mangroves (Figure 3). The estimated height of the sand dunes is between 5 and 10 metres above sea-level and they vary in dimension up to sizes of about 500 metres by 2000 metres. The low areas between the dunes are poorly drained, sandy but with a certain amount of organic and clay material, and are permanently flooded for the wet part of the year. The layers of clay or high clay content in the sand are relevant factors to


326 Andrew Collins

FIGURE 3 Quelirnane: main physical features.

note in the context of water borne disease as seepage may be prevented or restricted, causing stagnation of groundwater that might otherwise be undergoing a continuous process of filtration.

The coastal plain areas consist of some grasslands and a drainage network of streams, some of which are permanently in flood. This area is characteristically very saline. The mangrove areas beside river inlets and small lakes are flooded at high tide and are also high in salinity and clay content. The maximum monthly temperature varies between 27°C and 33"C, and the minimum, between 16OC and 24OC. (Direccao Nacional de Aguas, 1991 p. 5). The greater part of the rainfall comes in torrential rainstorms and the average per annum is 1428mm.

The salinizing influence of the ocean is known to remain up to a distance of 30 km inland in some cases. The presence of

fresh water in the area remains largely restricted to shallow lens-shaped water bodies with a limited regional extension. However, no detailed information on the locations of this water is known, the only recent hydrogeological survey concluding that;

Their extent does not obey the laws for a situation of hydraulic equilibrium due to the presence of clayey layers which hamper the groundwater flow, the variation of the groundwater level during the seasons, the tidal effect and occurrence of recent floods. (Direccao Nacional de Aguas, 1991 p. 2)

Land and water use

The main populated areas are on the morundus, habitation in other areas being restricted to small temporary fishing settlements. The principal local economic activity is agriculture, although some small



scale livestock production exists and fishing is common. The cultivation of palm groves, cassava and corn is restricted to the morundas, whilst rice and sweet potato are rotated on the lower areas between them, known locally as entredunas. Much of these more acidic and less saline areas are therefore not areas used for population settlement.

Some of the main parts of Quelimane, including much of the concrete city (i.e., the communal units of 24 de Julho, 1 De Maio cimento, Felipe San Magaia, Liberdade, A Luta Continua) are served by piped surface water from the river Licuari, 50km away. This supply is limited, however, to certain times of the day only, is poorly filtered and chlorinated, and ceases to function at times of drought. Consequently, the main supply for the population is from subterranean sources by means of wells, and it is therefore in connection with these that one might suspect to locate the most significant reservoirs of water contamination linked to the epidemic. There are a variety of types of well and this was taken into consideration in the sampling of sites in this study. They consist of the following categories.

Traditional wells, which are the most common and usually consist of bare earth holes that are deepened regularly by hand. Shallow concrete lined wells, many of which date back to colonial times. These vary from those which are open at the top to those which are covered and have a hand pump on top. This does not necessarily mean that they are totally protected, since there are often cracks in the concrete. Boreholes sunk in more recent years by specific projects. These have been restricted to a few areas, largely as a result of a lack of suitably thick fresh ground-water bodies. Some become

inactive not long after installation due to silting up with the fine sand. Their limited success has led to a recent reevaluation of the objectives of the main well water supply project in Quelimane . The municipal area of Quelimane is

divided into 5 Bairros, which are subdivided into the 39 smaller communal units displayed in Figure 4.

METHODS AND MATERIALS

Data collection and fieldwork

The data collection and fieldwork were carried out in Quelimane in August- September 1991. The scale chosen for the spatial representation of the incidence of cholera was by communal unit (Figure 4). Recently updated population figures for each of the communal units were provided by the City Health Department. The use of communal units for micro scale studies in Medical Geographical work has been appraised by Meade et al., (1979; 1983), Howe (1980), Giggs et al., (1980), and Learmonth (1986). Data for the recorded incidence of cholera during the epidemic was compiled by combining data for part of the period that were already in existence, with a detailed review of the provincial hospital records for the periods that were not covered. Cases were recorded for date of admittance and by the communal unit in which they resided. Also, an analysis of the age and sex of admitted cases, using this data, indicated that there were marginally more males and a higher proportion of children under 14. A stratified random sample was used to select sites for environmental observation and measurement in each of the 39 communal units and at least one example of each of the water source types, existing in any one, was sampled where possible.

Water tests to measure pH, residual chlorine, turbidity and faecal coliforms


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Environmental lnfluences on the Distribution of Cholera 329

were carried out using a DelAgua water tester with some additional tests, such as for ammonia and nitrate, being carried out separately. Soil pH at appropriate sites was measured using the barium sulphate and Munsell colour chart method. A list of the variables recorded at each site, justification for their inclusion in the survey and a more detailed indication of the measurement technique used is outlined below.

Variables measured at each survey site

Conductivity This gives a quick and easy comparative measure for salt concentrations in water by measuring positive ion content. For a full discussion see Mackereth et al., (1978), Chapman (1992), Talsma et al., (1971), Wilson (19741, and Cairncross (1983). On site measurements were taken using a calibrated 'Palintest' conductivity meter.

Water pH This was one of the key variables under investigation in the overall hypothesis. On site values were determined by the use of a colour comparator and phenol red tablets.

Turbidity This is caused primarily by suspended material, such as organic material, bacteria, algae, clay and minerals. Particles may include pathogens as well. On site values were determined by the use of a transparent turbidity tube.

Faecal colifomzs The faecal coliform count is widely accepted as a test for drinking water quality. The presence of faecal coliforms in water means that pathogens related to the human intestines are also likely to be present, given the circumstance of an epidemic. The tests were carried out using membrane filtration on site with apparatus

sterilized after each sample, incubation with lauryl sulphate nutrient at 44°C for 12-16 hours and a colony count carried out in a laboratory environment.

Temperature Temperature affects the rates of bacterial and chemical reactions in water. It was also necessary for the calibration of the conductivity meter. Measurements were carried out on site using a thermometer with subdivisions to 0.1 centigrade.

Ammonia Ammonia is commonly accepted as a good indicator of contamination by sewage. Tests were carried out using an ammonia test cube (comparator) and Nessler Reagent APHA.

Nitrate Nitrate is also of interest in determining possible sewage contamination. Tests were carried out using a comparator and Nitra Ver 5 Nitrate reagent in a 5ml sample.

Water level Where there is a higher phreatic level, exposure of the ground water supply to sources of contamination, such as pit latrines, may be increased. Also, exposure of the water to the surrounding geology will vary at differing levels with different porosities allowing a variable degree of natural filtration of pathogens being transported laterally through the ground. Depths to water table from ground surface were therefore measured where possible.

Soil pH at surface and at water level Water pH alone was considered an incomplete indicator of the local environmental levels as there may be substantial non-environmental influence affecting it at certain times (e.g., cement from wells, metal influence of lifting mechanisms and one-off rainfalls). Soil pH was measured


330 Andrew Coffins

using the Barium sulphate and Munsel colour chart standard technique.

Soil type at surface and at water level Different soils allow different vertical and horizontal ground water transmissions and hence the rate of diffusion of pathogens is affected. Also, the varying porosity of different soils will cause a varying degree of the filtering of colloids (and removal of some pathogens). Analysis of samples was made at the site but restricted to fairly broad general terms, such as fine sand, sand and top soil, sand and clay, clay, and minerals such as mica.

At each site additional notes were made on predominant land use, type of sanitation available, distance to nearest latrine, use and amount of chlorine in water (generally not present and therefore not included in the main list of quantifiable variables) and the condition of the wells.

Data analysis

The Geographic Information System (GIS) ‘ARC INFO’ was used to create a database of original, transformed and statistically derived data. This facilitated the integra- tion and analysis of spatial features with the attributes for administrative areas and sample points.

Cross-sectional spatial analysis was carried out by first calculating rates of cholera per zone per 10,000 people. These have been represented in Figure 5. The density of population for each communal unit was calculated using areas measured by ARC INFO and have been represented in Figure 6. Significantly high areas of incidence were confirmed using a comparison with the Poisson distribution*. A correlation matrix for the 14 numerical variables was drawn up using correlation coefficients and significance testing at the 95 per cent and 99 per cent levels3. This process was repeated first excluding the tap water sites and then for the open earth

traditional sites only. Variables found to correlate significantly with the rate of incidence were selected for regression analysis by forward inclusion4. Residuals from variables surviving significantly in the regression equation were analysed and the positive and negative residuals from the main equation plotted on a map of the communal units to enable testing for spatial contiguity. Sites with significantly high values for particular variables were retrieved and superimposed on the residual plots to allow any spatially correlating patterns to be observed. Principal component analysis was also carried out on the matrix of variables on the basis that intercorrelations were suspected between variables.

Spatio-temporal analysis included calculating the epidemic curve, total number of communal units affected each month, standard deviation of the rate by month, and a close approximation of the rainfall for the same period. The rates per 1000 persons for each of the 14 months of the epidemic were also mapped. Poisson probabilities for rate of incidence per communal unit and per unit per month of epidemic were calculated and the significant outbreaks for each month mapped5. These maps were used to calculate

- the number of consecutive significant outbreaks in the same areas;

-outbreaks at time ’t + 1’ when outbreaks have occurred in a contiguous sublocation at time ’t’; and

- the number of non-consecutive and non-contiguous outbreaks.

The principal purpose of the time sequence maps and data generated from them was to assist in determining if the spread of the disease had been into those areas with sites already identified as being significant in terms of their environmental association with total rates of incidence of cholera.



RATE PER I0.000 PEOPLE

0 0 - 1 9 9

20 - 39 9 40 - 59 9 60 - 79 9 80 - 99 9 100 - 119 9

1111 120 - 139 9 140 - 159 9

> I60

0 3km - FIGURE 5 lncidence of cholera.

RESULTS

Cross-sectional survey results

The total number of registered cases of cholera for the full cycle of the epidemic in Quelimane covered by this study was 1,179. In the epidemic that followed in 1992, there was an even higher total. Figure 5 reveals a spatial pattern to higher and lower incidence of cholera. Unsur- prisingly, significant positive correlation existed between the rates of incidence for the communal units and the population densities (r=0.71 p>O.Ol). This strong positive correlation confirms the well known feature that, when the disease breaks out in a community, its transmission through the faecal oral route of contamination is likely to be multiplied under conditions of congestion.

A significant positive correlation was also found between the conductivity of the sites and the rate of incidence for the corresponding area. This was particularly strong when tapped water sites (water pumped from the river) were excluded from the calculations (r = 0.82 p > 0.01). The regression equation of rate with density and with the inclusion of conductivity remained significant (P = 40.6 F=26.6 p>O.Ol using all water source types, and r2=62.0 F=21.2 p>O.O1 using bare earth wells only). The regression equation could not be extended to include, satisfactorily, other variables except soil- pH when the data for open-earth wells only were used (P=64.2 F112.5 p>O.Ol). The residuals from the regression equation of density on rate of incidence displayed an expected characteristic of autocor-


332 Andrew Collins

OF P E O P L E PER SQUARE

[1111 1 - 2 4 9

25 - 74 9

75 - 124 9

125 - 174 9

I 175 - 224 9

I 225 - 274 9

> 27s

0 3km -

K I L O M E T E R

FIGURE 6 Population density.

relation, as confirmed by Durban Watson statistics (DW = 0.28 p >0.05 using all water source sites; and DW-0.70 p>O.O5 using bare earth wells only). Figure 7 represents the spatial analysis of the same residuals, which reveals a non-random pattern with a distinctly contiguous block of communal zones on the western flanks of Quelimane. Comparison of the positive residuals from density on rate of incidence with sites of significantly high conductivity values at the 99 per cent confidence level (also represented in Figure 7) display a spatial correlation. There are therefore initial grounds to suggest from these results that, although population density dominates as a key associating factor, water sources with higher salinities also significantly correlate to the pattern of incidence in the study area.

Faecal coliform contamination of water was found to be present in all of the zones and at the majority of sites. The count for tap water supply was generally low, most typically in ones and twos per 100m1, but sometimes exceeding this. Faecal contamination is spatially widespread and spatially random over the area and did not correlate significantly with rate of incidence in any of the six correlation matrices drawn up. This indicates that, although faecal coliform counts were indicating locations where Vibrio cholerue might be able to exist, it fell short of explaining the pattern of incidence, given the situation of widespread faecal contamination that was found in Quelimane.

Principal components analysis illumin- ated the presence of several groups of variables that may be considered as



‘t

STANDARDIZED RESIDUAL

> *3 00

+2 0E - *3 08

* I 00 - +2 00

0 EE - +I 00

E 00 - -I 00

-I 00 - -2 00 0

YELLS YITH SIGNIFICANTLY HIGH (S9XI.v.l) CONDUCTIVITY READINGS

+ YELLS UITH SIGNIFICANTLY LOYER (99XL.u.I) CONDUCTIVITY READINGS

FIGURE 7 Standardized residuals from regression of population density on rate of incidence and locations of wells with significantly high and low conductivity readings.

possible ‘factors’ relating to the distribution of incidence of cholera6. Factor 1, in addition to confirming the relationship already suggested between rate of incidence and conductivity, also included water pH and the lower level soil pH. There is a suggestion here, therefore, that pH levels are to some extent represented in the overall associative analysis if considered in the context of the principal component analysis. Factor 2 was made up of turbidity, ammonia and faecal coliforms. This appears a logical grouping in that ammonia is commonly associated with human waste and turbid water is likely to be the medium they end up in.

Spatio-temporal results

The epidemic curve of cholera incidence over the 14 months is displayed in Figure 8. The number of localities affected over time follows a similar pattern at first but the two curves become more separated in the last 5 months of the epidemic indicating that, although the disease was on the decline, it had become relatively more dispersed. This is to some extent also reflected by the curve for the standard deviation of the rate of incidence between the communal units.

The curve indicating average monthly rainfall at Quelimane (Figure 9) indicates that the outbreak occurred as the driest


334 Andrew Collins

MONTH

FIGURE 8 The temporal relationship between recorded incidence, number of areas affected and the standard dmiations of the mean rate per 1000 persons.

part of the year was approaching and that the peak of the epidemic was in the driest month. High incidence was maintained during the rainy months but drops off dramatically with the end of the rains.

The spread of the disease could be appreciated with regard to environmental variables by use of the time sequence mapping part of this project. In its initial stages the main focus of incidence moved from one side to the other of the main city area. The shift was, at this stage, in favour of areas already identified as environmentally preferable to the longevity of Vibrio cholerue. The disease spread from the location of the initial reported incidents in Chirangano, with the densest population, to the opposite side of the main urban area

of Quelimane. It was this north-west facing flank of the city, Manhawa A + B, that had the higher rate of incidence throughout the rest of the epidemic.

Maps recording significantly higher- than-expected numbers of cholera cases for each month (using the modified version of Fergusson’s Poisson method and a 97.5 per cent probability level) revealed that the majority of outbreaks were non-consecutive and non-contiguous. (Consecutive outbreaks in same location = 30.4 per cent; outbreaks at time ’t + 1’ in contiguous sublocation = 13.1 per cent; outbreaks in non-consecutive and non-contiguous sublocations = 52.2 per cent; initial stage of epidemic = 4.3 per cent.) These results may reflect the



MONTH

FIGURE 9 The relationship between recorded incidence of cholera and rainfall at Quelimane.

limitations of using an inappropriate time period (1 month is too long, given that the incubation period for cholera may be only a few days), but may also to some extent reflect the increasing dispersion already indicated by the relationship of the epidemic curve to the number of localities affected (Figure 8). What remains a key finding of this particular study, however, is that the percentage of total significant outbreaks, subsequent to the initial one, in areas recording significantly higher salinity in the aquatic environment from which people drink, was 87 per cent. This was calculated by combining the monthly 'significant outbreak mapping' for communal units with well sites recording significantly high conductivities.

DISCUSSION

This study suggests an association between rate of incidence of cholera and areas recording higher conductivity, which in this context can be regarded as a measure of greater or less saline water sources. Existing knowledge lends substantial weight to many of the results. Without doubt other less clear associations between the measured variables could also be pointed to in a survey of this type, and of particular interest is the indication of groups of variables indentifiable as factors. Some of the main findings of the research would therefore also support the possibility of synergistic effects, where several variables working together may be producing results which are more than the


336 Andrew Collins

sum of their parts. Precipitation is the main climatic

feature of interest, as it effects the rate at which contamination is washed into the water supplies. This relationship has also been suggested by Lindskog and Lindskog (1988) and Moren et al. (1991) in studies of contamination of wells in Malawi, and is commonly understood to be important by water analysts looking at well water supplies. Also, residents in Quelimane described how, at the peak of the rainy season, wells may overflow, the poor sanitation in many cases causing the water supply to be particularly vulnerable at that time. The rainfall pattern, however, suggests the epidemic taking off in a drier period. This may be due to the other circumstances associated with water borne 'disease epidemics, namely shortage of water. The dipping of collection utensils into fewer functioning water supplies, at reduced levels and thus with concentrated levels of contamination, helps to transmit Vibrio cholerue from one collecting utensil to another. The water may also become more brackish when, at these low levels, there is a saline intrusion from neighbouring areas.

The particularly high and persistent incidence of cholera in Manhawa A + B, a communal unit on the worst affected flank of the city which suffers from occasional flooding in the wet season, must also be considered within the context that people in that Bairro are to a large extent displaced persons from the rural areas and may therefore represent an especially suscept- ible community. Some of the rural areas they came from are not known to have been cholera zones and they would therefore be equipped with little immunity. Their reduced socio-economic status is also likely to have made them vulnerable to infection. It should be pointed out that the three zones displaying the lowest standard residuals from the regression of incidence on density of population (Figure 7) are historically established areas where

the population is largely indigenous to the City of Quelimane.

The relationship between cholera and malnutrition is a further factor that should be considered in this context. Mulholland (1985) and Moren et al. (1991) both point to its significance. Hypochlorhydria through loss of gastric acids, which are one of the body's main lines of resistance against cholera, predisposes to higher incidence (Cash et al., 1974). If the evidence of Thomason et al. (1981), that acute malnutrition predisposes to hypochlorhydria is correct in this particular circumstance, then it is reasonable to suspect that this is the mechanism by which cholera selectively attacks the malnourished (Nalin et al., 1978). The sociogeographic factors, suggested in this survey as being particularly relevant to further understanding epidemics of this kind, are therefore likely to relate partly to the relationship of people to their place of normal residence. Attention is drawn to the unstable demographic circumstances in which this outbreak occurred and which were primarily related to the destabilization of rural areas due to war, resultant displacement and subsequent settlement in Quelimane.

Another major factor relating to the findings of the Quelimane study, however, is that the zone of Manhawa A + B is largely denuded of vegetation and, as the results of the survey show, provides highly saline water. The relationship between high quantities of displaced persons and a degraded environment, where compacted and exposed soils become alkaline and saline and where the saline intrusion from the estuary is extensive (possibly enhanced by degrada- tion), is presented here as being synonymous with a significantly higher and sustained rate of incidence. The starting point of the cycle of causation is not, however, entirely clear, as the area may already have been environmentally



poor. Newcomers may have subsequently been allocated the least desirable zones to settle in. Areas with a low rate of incidence, or no incidence at all, are one or two of the concrete central zones of the city, but more markedly the heavily planted outer zones of Gogone, Bazar and Migano. These are zones recording lower population densities but people are concentrated into parts of these areas and density values may therefore be mis- leading. Of more interest to this study is that these zones typlfy areas of vegetation, more acidity and a less saline environment. Contamination of wells in terms of faecal coliforms is still present but the incidence of cholera is lower, a strong point lending support to the hypothesis of environmental zones favourable to the survival time of Vibrio cholerue 01. It may be concluded that, although the Quelimane study goes some way to determine the existence of a relationship between the physical environment and cholera incidence in terms of water quality and land, the particular combinations of environmental and demographic factors that relate to the health of displaced people remain to be empirically identified.

There were some inevitable limitations in the selection of variables in the initial stages of this analysis, due to the still largely unresolved complexities which remain in the field of pathogenesis. The balance between what should and should not be attempted in Medical Research is well put by Feachem et al., (1989).

Models of the larger system must, at this stage in our understanding, operate in broad conceptual terms that are both specific enough to be useful as a guide to data collection, analysis and policy formation, but general enough to preserve clarity in the face of potentially limitless detail. The trees are important but they must not obscure the wood.

Other limitations were the lack of a record

of the environmental variables over time and of adequate health data. An even more detailed study might aim to monitor changes in the environmental variables at each part of the epidemic. Processes requiring attention in that case might include changes in water pH with rainfall, surface run-off effects on turbidity and conductivity and, in particular, factors relating to decreased levels of sanitary hygiene at times of flood.

The main practical implication of this study is that guidelines for helping to reduce the incidence of cholera should take into account the physical environment in which vulnerable communities are located. More specifically, consideration should be given to the risk of local environments serving as a reservoir for Vibrio cholerue 01. The identification of risk areas could be vitally important for planning purposes, in determining whether or not there are more favourable zones or areas of avoidance for communities suffering from recurring epidemics. In already settled areas, the identification of, and intervention in, processes of environmental change leading to the creation of physical conditions favourable to Vibrio cholerue 01, such as salinization and alkalinization, could be a major factor in preventing the primary transmission and subsequent persistence of cholera.

Notes Many thanks are due to the following govem- mental departments, non-governmental organ- izations, institutions and individuals who have contributed in various ways to this study. In Mozambique Instituto National de Saude (National Institute of Health), Maputo, for quickly realizing the relevance of the project and giving approval to field work being carried out in Quelimane; Direccao Provincial de Saude de Zambezia (Provincial Directorate of Health for Zambezia Province), for giving official approval of the


338 Andrew Collins

work in Quelimane and assisting with transport; Direccao de Saude de Cidade de Quelimane (City Health Department in Quelimane), for providing logistical assistance in Quelimane; and Laboratorio Provincial de Agua (Provincial Water Laboratory), for providing a base from which to work in Quelimane. In England Quaker Peace and Service, for a contribution of f500 in the form of a ‘Study Travel Bursary’; Skillshare Africa (formerly International Voluntary Service), for the contribution of a f500 bursary; Oxfam Technical Department, for the loan of one DEL AGUA portable laboratory for water testing, a new conductivity meter and the supply of disposables at a nominal fee; Robins Institute of Surrey University, for brief and essential instruction in the use of the DEL AGUA equipment, which was originally designed there; Nigel Trodd (Kingston Univer- sity) for guidance on methodology; Teresa Conolly (Kingston University and Birkbeck College) and Ed Parsons for ARC INFO instruction; Richard Black (King’s College, London) for essential advice and comments on drafting this paper; Roma Beaumont for help with figures; and Professor B. Drasar (London School of Hygiene and Tropical Medicine) for comments on drafts. 1.

2.

3.

4.

Though isolation and testing of Vibrio cholerae 01 may be a worthwhile pursuit at laboratory scale, the centrifuging and analysis of large quantities of environmental media is considered inappropriate. This distribution has been suggested as appropriate for disease distributions of this kind by Giggs et al., (1980) and Jones (1988). Matrices were created using Pearson’s Product Moment and Spearman’s Rank correlation coefficients. Both techniques were employed so as to cover for a lack of normality in some variables, a requirement when using Pearson’s alone, or for confir- mation (using a stronger test) when using Spearman’s alone (Shaw and Wheeler, 1985). All data were tested for normality and transformations attempted where appropriate using the square root, log and loge of the values. The order in which variables were included into the equation was also carried out using

5.

6.

the partial correlation coefficients for each of the significant variables, as outlined by Johnston (1980). Stepwise regression using MINITAB was performed on the entire data set to confirm the results. This technique has been adapted from that used by Ferguson (1975) in his mapping of the 1975 cholera epidemic in Kisumu District, Kenya. A maximum of three factors could be extracted if using an eigenvalue of 1.00, as suggested by Shaw and Wheeler (1985). The nature of the groupings themselves suggested a maximum of 3 factors, or 2 for the most convincing analysis bearing in mind some of the results already established in this study. The loadings for variables in factor 1 were rate of incidence -0.367, Water pH -0.372, Conductivity -0.371, Soil pH near to water level -0.416.

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Andrew Collins Department of Geography King’s College London Strand London WC2R 2LS


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