ARTICLES
Effect of fly control on trachoma and diar rhoea
Paul M Emerson, Steve W Lindsay, Gijs E L Walraven, Hannah Faal, Claus Bøgh, Kebba Lowe, Robin L Bailey
Summary
Background Domestic flies are accepted vectors of diarrhoea,
but their role in trachoma transmission has never been
quantified and no study has shown that fly control decreases
the prevalence of trachoma. We assessed the effect of fly
control on public health in a pilot study in Gambian villages.
Methods We studied two pairs of villages—one pair in the
1997 wet season, and one pair in the 1998 dry season. For
each pair, deltamethrin was sprayed for 3 months to control
flies in one village whilst the other was used as a control. Fly
populations were monitored with traps. We surveyed trachoma
at baseline and at 3 months, and collected daily data on
diarrhoea in children aged between 3 months and 5 years.
Findings Fly control decreased numbers of muscid flies by
around 75% in the intervention villages compared with
controls. Trachoma prevalence was similar at baseline (wet
season, prevalence in intervention village 8·8% vs control
12·2%; dry season, 18·0% vs 16·0%), but after 3 months of
fly control there were 75% fewer new cases of trachoma in the
intervention villages (wet season 3·7% vs 13·7%; dry season
10·0% vs 18·9%; rate ratio and relative risk of pooled data
0·25 [adjusted 95% CI 0·09–0·64], p=0·003). There was 22%
less childhood diarrhoea in the wet season (14% vs 19%,
period prevalence ratio 0·78 [0·64–0·95], p=0·01), and 26%
less diarrhoea in the dry season (6% vs 8%; 0·74
[0·34–1·59], p=0·60) compared with controls.
Interpretation Muscid flies are important vectors of trachoma
and childhood diarrhoea in The Gambia. Deltamethrin spray is
effective for fly control and may be useful for reducing
trachoma and diarrhoea in some situations, but further
research on sustainable fly-control methods is needed.
Lancet 1999; 353: 1401–03
See Commentary page 1376
Introduction
Flies act as mechanical vectors of many pathogens, but
they are commonly overlooked in public health
interventions. Childhood diarrhoea causes 3·3 million
deaths worldwide per year, with an estimated 1 billion
cases of diarrhoea annually in children under 5 years.1 Flies
are known vectors of diarrhoea-causing pathogens,
particularly those requiring a minute inoculum such as
shigella.2–5 Chlamydia trachomatis causes trachoma, and has
been found on flies fed on heavily infected laboratory
culture media.6 There is an association between flies and
trachoma,7–9 but as yet there are no field-based or
epidemiological studies that show that flies are direct
vectors of trachoma.
Trachoma is the main cause of preventable blindness
worldwide.10 Such blindness is more common in women
than men11 and results from repeated ocular C trachomatis
Medical Research Council, The Gambia (P M Emerson MSc,
G E L Walraven MD ); University of Durham, UK (S W Lindsay PhD);
National Eye Care Programme, The Gambia (H Faal FRCOphth,
K Lowe); Danish Bilharziasis Laboratory, Denmark (C Bøgh MSc,
S W Lindsay); and London School of Hygiene and Tropical Medicine,
UK (R L Bailey MRCP)
Correspondence to: Paul M Emerson, Medical Research Council
Laboratories, PO Box 273 Banjul, The Gambia
THE LANCET • Vol 353 • April 24, 1999
infections over many years. In less-developed countries,
young children are the reservoir of infection, and
transmission is clustered within villages,10–12 but the
mechanisms by which infection is spread are poorly
understood. An intervention that lowers the frequency of
transmission is likely to lower the prevalence of trachoma-
related blindness in the future.
The WHO initiative for the global elimination of
trachoma by the year 2020 (GET 2020) aims to control
trachoma by eyelid surgery, antibiotic treatment, facial
cleanliness, and environmental improvement (the SAFE
strategy). However, the implementation and sustainability
of antibiotic therapy is beset by poor compliance with
topical application of ophthalmic tetracycline eye
ointment13 and by the prohibitive cost of oral azithromycin.
Trachoma is associated with poverty, and largely
disappears under improved environmental conditions and
access to better sanitation.14 Nonetheless, the prospect of
rapid global improvement remains bleak. The SAFE
strategy would be strengthened by the inclusion of realistic
and sustainable methods to reduce trachoma transmission.
We undertook a pilot study to investigate the role of
domestic flies in the transmission of trachoma and
diarrhoea.
Methods
Study population
Our study took place in four villages over 3 months in the Sanjal
area of The Gambia.15 One pair of villages was studied from
September, 1997, to December, 1997 (the wet season), the other
pair was studied from January, 1998, to April, 1998 (the dry
season). The two pairs of villages were selected from 23 available
small villages with populations of less than 400 in the Sanjal
district on the basis of trachoma prevalence, lack of immediate
access to primary health-care, homogeneous ethnic composition
(Wolof), and willingness to participate. The village pairs were
3 km and 12 km apart, respectively. One village from each pair
was arbitrarily assigned the study intervention (fly control), and
the other acted as a control. The study was approved by the joint
ethics committee of The Gambia government and the Medical
Research Council, and we obtained informed consent from the
villagers and guardians of children.
Fieldwork
Flies were controlled by ultra-low-volume application (Hudson
Portapac, Chicago, USA) of 0·175% volume to volume
deltamethrin (Aqua K-Othrine, Agrevo, UK) within and up to
20 m outside each village. Control began with an “attack” phase
of spraying every 2 days for 2 weeks, and continued with a
“maintenance” phase of spraying twice weekly in the wet season
when the fly population was largest, or once weekly in the dry
season when the fly population was smaller. No adverse effects of
spraying were recorded.
Fly populations were monitored by four fish-baited traps placed
in each village at an animal-tethering area, in a latrine, at the
centre of a domestic compound, and at the main meeting point for
24 h every 2 weeks. To measure fly-eye contact in the dry season,
hand-net collections of eye-seeking flies were made fortnightly
from ten seated children for 15 min. Flies that touched the
children’s eyes were collected and taken to the laboratory for
identification.
The whole of each village community was screened for
trachoma at baseline and at 3 months by the same community
ophthalmic nurse, who was unaware of the treatment status of
each village. Screening was done by everting the upper eyelid and
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ARTICLES

visually examining the tarsal plate with a torch and a 32·5 Wet season Dry season
binocular loupe. Eyes were graded according to the WHO Control Intervention Control Intervention
simplified scale,16 which classifies active trachoma as the presence village village village village
of follicular trachoma (five or more follicles >0·5 mm visible) or
Census population in 1993 285 334 185 217
intense trachoma (50% of tarsal plate obscured by inflammation). Number aged <10 years* 112 136 79 87
People with symptoms of trachoma were offered tetracycline eye Number aged 3–60 months 82 77 51 53
ointment, and those with trichiasis were referred to the district eye Number aged 3–60 months per family
clinic at which surgery was available. Mean 3·9 3·1 3·6 3·1
Median (range) 4 (1–11) 3 (1–7) 3 (1–7) 3 (1–9)
We collected data on diarrhoea for all children in the villages
Ocular examination
aged between 3 months and 5 years. Diaries were completed by At baseline 319 381 227 207
the mother or guardian of each child, who was asked to record At follow-up (%) 271 (85) 295 (77) 189 (91) 169 (74)
daily whether the child had had diarrhoea. We analysed the period % days diarrhoea data 90·9 91·6 93·7 90·3
prevalence (proportion of days on which diarrhoea reported) as a *In both ocular examinations.
measure of morbidity. Oral rehydration salts were given to Characteristics of study villages
children with diarrhoea, and any child with diarrhoea on
5 consecutive days was referred to the local health centre. 1993 census was 1020. 1124 people of all ages were
screened for trachoma at baseline, of whom 924 (82%)
Statistical analysis
were also screened at 3 months. Loss to follow-up, mainly
Our statistical analyses used EpiInfo (version 6) and SPSS
(version 6.1). Fly-count data, which were not normally owing to inclusion of temporary migrants in the baseline
distributed, were described by the median or adjusted geometric data, was similar for intervention and control groups (rate
mean. Counts from the four traps set on the same day were ratio for intervention vs control 1·13 [0·83–1·54]).
obtained for each village, and we calculated the adjusted geometric Data on trachoma prevalence (figure) shows that there
mean for the catch from these traps by adding 1 to each count, was no difference in the community prevalence of active
calculating the geometric mean of the resulting four counts and trachoma at baseline in either village pair (wet season
then subtracting 1, to avoid the difficulty of a count score of zero. intervention 26/295 [8·8%] vs control 33/271 [12·2%]; dry
Variables that were not normally distributed were compared by the season 34/189 [18·0] vs 27/169 [16·0]). The prevalence of
non-parametric Kruskal Wallis H test and the Wilcoxon matched- trachoma after 3 months was lower in the intervention
pairs signed-ranks test. Categorical outcomes, such as prevalence
village than in the control village in both seasons (wet
rates, were initially compared by x2 with Yates’ correction. We
used Mantel-Haenzel estimates of relative risk and rate ratios for season intervention 11/295 [3·7%] vs control 37/271
stratified data. Trachoma cases and episodes of diarrhoea cannot [13·7%]; prevalence ratio 0·27 [adjusted 95% CI
be assumed to occur independently within households, so we 0·08–0·93], p=0·04; dry season 19/189 [10·0%] vs 32/169
adjusted confidence intervals and p values for these outcomes to [18·9%]; prevalence ratio 0·53 [95% CI 0·25–1·12],
allow for correlation within households by Miettinen’s test-based p=0·09). Overall, there was a 61% lower community
approach.17 The Kruskal Wallis H statistic derived from ranking of prevalence of active trachoma in the intervention villages
household or family disease rates was used in the adjustment. associated with fly control (relative risk=0·39 [95% CI
0·20–0·77], p=0·007).
Results The relative risk of becoming a new active trachoma case
Entomology at 3 months from baseline was lower in the intervention
Muscid flies (Musca sorbens—bazaar fly: M domestica— villages than the control villages (wet season relative
housefly) were more abundant in the wet-season control risk=0·20 [95% CI 0·05–0·82], p=0·026; dry season 0·33
village than in the dry-season control village: the median [0·1–1·06], p=0·064). Overall the risk was 75% lower in
(range) of the adjusted geometric mean numbers of flies per villages where fly control was practised than in control
trap per day was 9·80 (2·29–37·3) versus 5·98 (2·41–38·3), villages (relative risk=0·25 [0·09–0·64], p<0·003).
respectively, for M sorbens; and 10·2 (2·5–102·9) versus
4·24 (1·14–12·05) respectively, for M domestica. Spraying Diarrhoea
resulted in 76% fewer M sorbens (2·15 [0·19–5·62], p=0·02) All resident children aged between 3 months and 60
and 57% fewer M domestica (4·44 [1·21–36·25], p=0·04) in
the wet-season intervention village than in the control
village. In the dry-season intervention village, 75% fewer
M sorbens (1·51 [0–5·17], p=0·002) and 71% fewer
M domestica (1·21 [0–5·31], p=0·006) were caught during
the spraying period than in the control village.
Handnet collections of eye-seeking flies were virtually
100% efficient when there were few flies, but up to 5% of
flies escaped when there were more flies in total. In the dry
season during the spraying period, 96% fewer flies were
collected from the eyes of children in the intervention
village than from those in the control village (adjusted
geometric mean of number of flies per child in 15 min 0·06
vs 1·54, 4/54 fly positive catches vs 38/49, x2=49·8,
p<0·001). 92% of eye-seeking flies were M sorbens and 8%
were M domestica. Other fly species, predominantly
Chrysomyia albiceps, were caught in the traps, but were
never recorded on eyes or faces.
Trachoma
Village communities were of similar size, age composition Prevalence of active trachoma before and after fly control in
(table), and ethnicity (Wolof). The total population in the study villages in wet and dry seasons

1402 THE LANCET • Vol 353 • April 24, 1999


months were recruited for diarrhoea surveillance, 263
children in total. Data were obtained for over 90% of
possible child-days of observation, with no significant
differences between villages or age groups. The distribution
of numbers of children under 60 months per family was
not significantly different in the four villages (table).
Children in the dry season had 58% less diarrhoea than
those studied in the wet season (period prevalence
ratio=0·42 [0·23–0·76], p=0·003). The proportion of days
on which diarrhoea was reported was significantly lower
with increased age (p for trend <0·001) in all the villages,
but there was no association with family size. Period
prevalence of diarrhoea was lower in the intervention
village than the control village in both seasons (wet season
14% vs 19%, relative risk=0·78 [95% CI 0·64–0·95],
p=0·01; dry season 6% vs 8%, 0·74 [0·34–1·59], p=0·60).
Overall, in the villages with fly control there was 22% less
childhood diarrhoea in the wet season and 26% less in the
dry season than in the control villages.
Discussion
In our pilot study the control of muscid flies lowered the
transmission of trachoma and the period prevalence of
diarrhoea in children. However, our study was done in
only four small settlements and may have been affected by
bias—for example, realisation that there were fewer flies at
certain times might have made the mothers report less
diarrhoea and led the nurse to make differential
observations of trachoma. We cannot exclude this
possibility, but it does not seem likely to have affected our
findings, since the diarrhoea data show similar age trends
in all villages and the nurse worked consistently at
validation sessions.
Collections of flies directly from children’s eyes
confirmed that despite comprising less than 10% of the
total fly population, M sorbens made over 90% of fly-eye
contacts and is therefore the most likely insect vector of
trachoma. M domestica made the remainder of the eye
contracts and must be considered a potential vector. We
tested 395 flies caught from the eyes of swab-positive
children by PCR for the C trachomatis common cryptic
plasmid,18 and we identified successfully two M sorbens
carrying the bacteria—supporting evidence of their role as
vectors. Our field records of fly behaviour show that M
domestica and M sorbens are strongly attracted to human
faeces and prepared food, and are probably mechanical
vectors of diarrhoea in The Gambia.
Ultra-low-volume spraying with deltamethrin decreased
fly-eye contacts by 96%, although if fly-catching was less
efficient in control villages with more flies, this proportion
may be an underestimate. Fly control resulted in 75%
fewer new cases of trachoma in intervention villages than in
control villages, and a 61% (95% CI 23–80) decrease in
point prevalence of trachoma in intervention villages,
which compares favourably with supervised face-washing.19
However, fly control with insecticides is unlikely to be a
sustainable routine public-health measure in countries in
which trachoma prevalence is highest. Spraying would be a
useful adjunct to trachoma-elimination strategies or during
trachoma outbreaks, and our study suggests that spraying
would also decrease morbidity from diarrhoea. A definitive
study on the role of flies in the transmission of trachoma
would need to include external assessment of trachoma,
perhaps with photographs, a larger study population, and a
larger number of villages. Such a study would need to run
THE LANCET • Vol 353 • April 24, 1999
ARTICLES
for a whole year. The development and assessment of other
sustainable and cost-effective methods for the control of
muscid flies, such as the provision of latrines, identification
and clearance of breeding sites, and assessment of the
feasibility of locally made traps, should be a research
priority.
Contributors
All investigators contributed to design and implementation of the study.
Paul Emerson and Kebba Lowe did the fieldwork. Analyses were done by
Robin Bailey, Steve Lindsay, and Paul Emerson. Paul Emerson and
Steve Lindsay wrote the paper, which all investigators edited.
Acknowledgments
We thank Keith McAdam for his support and for use of MRC facilities in
The Gambia; the people of Kumbija, Sinchu Palen, Pasi Mut, and
Samba Sotor for their willingness to participate; Dawda Joof and the North
Bank Division District Health Team for their support; and Shabbar Jaffar
and Linda Williams at the London School of Hygiene and Tropical
Medicine for statistical advice. Deltamethrin was donated by Agrevo
Environmental Ltd. The study was funded by the UK Department for
International Development (DFID).
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