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Excreta, Flies and Trachoma
Text by: Paul Emerson
Technical Editing by: Andrew Cotton
Quality assurance
by: Sandy Cairncross
This factsheet presents evidence on the
relationship between the common eye-seeking
fly musca sorbens, the eye disease
trachoma and the role that environmental
health factors (including habitat, climate
and sanitation) play in its transmission.
Introduction
Trachoma is an infectious
disease caused by Chlamydia trachomatis – a
micro-organism which spreads through contact with
eye discharge from the infected person and through
transmission by eye-seeking flies. Trachoma affects
about 84 million people of whom about 8 million are
visually impaired and repeated infection, if
untreated, can lead to blindness. Trachoma is the
leading cause of preventable blindness and continues
to be a major problem in many of the poorest and
most remote rural areas of Africa, Asia, Central and
South America. Active disease is most common in
pre-school children with prevalence rates as high as
60-90%. It often strikes the most vulnerable members
of communities--women and children, with adult women
at much greater risk of developing the blinding
complication of trachoma than are adult men. The key
environmental risk factors are water shortage,
flies, poor hygiene conditions, and crowded
households (WHO 2006).
The
Eye-seeking Fly Musca Sorbens
Adult Musca
sorbens feed directly from people or on
food gathered by people. They lay
their eggs on the faeces of people (and
their domestic livestock) and they rest at
night on the walls of human structures.
The close affinity of Musca sorbens
to man, coupled with aggressive feeding on
substances (ocular and nasal discharges)
that may contain Chlamydia trachomatis
by females, allow it to be a mechanical
vector of trachoma.
Musca sorbens is a
complex species with three members currently being
recognised, namely, M. sorbens, M. biseta
(Afrotropical and both referred to as the Bazaar
fly) and M. vetustissima (Asian /
Australasian referred to as the Australian bush fly)
(Pont 1991). M. sorbens is
frequently referred to as though it is a single
species; in what follows M. sorbens refers to
the two African species, rather than the specific
single species.
Relationship to man.
The species is known to be
domestic and is commonly referred to as being
synanthropic, meaning living in close proximity to
man. There is evidence that the closeness with man
is such that these flies can be termed euanthropic,
in that they have co-evolved with man and are not
only adapted to an environment which is shaped by
human activity, but are reliant on humans to provide
a suitable habitat. The species almost certainly
co-evolved with man in Africa and followed human
expansion across the world, limited in its
range only by its trophic requirements. Musca
sorbens did not follow the human migration into
the new world, (probably being unable to follow its
hosts over the transient northern land bridges) and
is absent from the Americas. This is likely why
flies have not been linked with trachoma
transmission in risk factor studies from Brazil and
Mexico (Taylor et al. 1985; Luna et al.
1992)
How many flies does a
fly produce? The theoretical ability for
population growth in M. sorbens is mind
bogglingly large. At a constant 28°C one adult
female emerging on August 1st could have
17.8 million progeny by mid-October. Thankfully,
this does not happen; the population is limited by
predators, parasites, disease, and most importantly
the availability of larval media. If a suitable
medium exists where M. sorbens lives, we can
presume that M. sorbens will find it and
breed in it.
Breeding in excreta.
Investigations into the preferred breeding media of
M. sorbens conclude that human faeces
available on the ground, but not in the full sun,
are the preferred breeding media of M. sorbens.
(Zimin 1948; Hafez and Attia 1958c; Peffly 1953). A
study from The Gambia (Emerson et al. 2001)
looked at the productivity in terms of numbers of
flies per hundred grams of faeces and also the
quality of the flies as measured by their
head-widths (bigger is better in the insect world,
it equates to greater longevity and fecundity).
Human faeces produced the most, and the biggest
flies. The study compared the distribution of
head-widths of flies caught from eyes with those
emerging from human and other animal faeces.
The mean head-width of the flies from human faeces
was similar to those caught from eyes, whilst the
flies from all other breeding media were
significantly smaller. We can reasonably
speculate that it is the presence of M. sorbens
and human faeces that is associated with trachoma
transmission.
Although human faeces are
clearly the preferred larval medium, a gravid female
M. sorbens will lay her eggs on the next best
thing, if human faeces are not available.
Young M. sorbens have been reported emerging
from pig, dog, milk-fed calf and cattle faeces in
addition to that of humans (Zimin 1948; Hafez and
Attia 1958c; Emerson et al. 2001) Musca
sorbens flies have not been reported from horse,
camel, donkey, sheep, goat or poultry faeces when
tested (Peffly 1953; Emerson et al. 2001).
Environmental factors and
Musca Sorbens
Temperature.
The duration of development from egg to adult is
temperature dependent, with lower temperatures
increasing development time and there being absolute
values below and above which development does not
take place (Hafez and Attia 1958a; Hafez and Attia
1958c). At ambient temperatures below 16°C and
above 40°C development of M. sorbens is very
slow. At a constant 28°C development from egg
to adult took 8.4 days; this was similar to field
conditions in the The Gambia (Emerson et al.
2001). Adult activity is also temperature
dependent. No published data exist
demonstrating this, but anecdotally adult Musca
sorbens in cages died at 40°C and above.
At 35°C and above, fly-to-eye contact is greatly
decreased with the flies being seen resting at the
top of walls where they are shaded by eaves, indoors
or on the underside of leaves.
There is a marked increase in
Musca sorbensfeeding activity in the relative
cool of the African morning and early evening
(Emerson et al. 2000). Anecdotally, the
greatest concentrations of Musca sorbens are
usually coupled with the greatest concentration of
people in tropical Afgrica, irrespective of the
temperature. "Clouds" of flies are commonly
seen around the faces of children in densely
populated villages in The Gambia, Tanzania, Kenya,
Ethiopia, Sudan, Mali, Niger, Ghana and Morocco
across the Berbers. Fewer flies are seen with
some of the nomadic people or those living in really
low population areas, such as the Kalahari and the
Sahel. However, in all probability M.
sorbens is quite likely to continue to transmit
trachoma (and be bothersome) during the African hot
seasons where temperatures creep beyond 45°C.
During these hot times the flies pester their hosts
in the shade.
Inside or outside the
house? In the Gambia there was statistically
no difference in fly-eye contact inside or outside a
house, (Emerson et al. 2000) although in
Ethiopia it was found that there were fewer indoors
(unpublished data). The Ethiopian data did not
record temperatures but it is likely that the
apparently inconsistent findings are actually linked
to temperature - in the relatively cool Ethiopian
highlands there is no reason for M. sorbens
to go into the shade.
Rainfall. Moisture
is probably the most important factor in what makes
faeces a suitable breeding medium; in very dry
environments human faeces desiccate rapidly and the
larvae developing within them die or migrate out of
them. Assuming that there is no loss of nutritional
value through the desiccation process, if water is
added to the stool, it may become a suitable
breeding media again, and will be utilized. This may
explain the conflicting reports of seasonal
variation in the density of adult M. sorbens.
No data exist on life expectancy of adult flies, but
it would be reasonable to assume that flies will
live longer when humidity is higher, which may also
be a contributing factor.
Seasonality.
The population of M. sorbens does not change
by orders of magnitude like that of the common house
fly M. domestica in the wet and dry seasons
(Emerson et al. 1999; Emerson et
al. 2000; Emerson 2004). The balance of
the evidence suggests that the adult M. sorbens
population is limited by the availability of
quality human faeces as a breeding media, and the
prime development of 'quality' in the human faeces
is the moisture content. In some places this
varies with season.
Altitude.
Data from Ethiopia (Alemayehu et al. 2005)
shows that at altitudes above 3,000m the prevalence
of signs of trachoma is greatly reduced from the
lower altitudes; this is consistent with the absence
of M. sorbens flies at the higher altitudes.
Collections of eye-seeking flies at different
altitudes found that the catches of M. sorbens
are basically zero above 3,000m.
Realistically, there are few places in the world
where people routinely live above 3,000m that are
also trachoma-endemic.
Musca sorbens does not breed in
latrine pits
Human faeces in pit latrines do not appear to be a
suitable breeding material. In a year-long
longitudinal study of 16 sentinel latrines in The
Gambia (Emerson 2005, only 65 M. sorbens were
ever caught emerging from latrine drop holes (from
192 catches). Of these 65 there was a
disproportionate number of females, which is not
consistent with the 1:1 ratio of males to females
always reported from breeding experiments. It is
suspected that most, if not all, of these 65 were
accidental captures of females attracted to the
latrine by the odour. Quite why M. sorbens
fails to breed in pit latrines is open to
conjecture. It is possible that that females are
attracted into the latrines and lay their eggs
there, but the larvae are out-competed by the larvae
of Calliphorid flies which may compete better for
oxygen in the moist conditions – and also eat
anything that doesn’t get out of their way, possibly
including the M. sorbens larvae.
It is therefore all the more important to strive for
isolation and containment of human excreta in
sanitary latrines.
Do other flies
contribute to Trachoma?
In experiments gathering
flies directly from the eyes of children conducted
in The Gambia, Tanzania and Ethiopia, only Musca
sorbens and Musca domestica (the common
housefly) have been caught (Emerson et al.
1999; Emerson et al. 2000; Emerson 2004;
Hafez and Attia 1958b; West (in press); Alemayehu
(unpublished data). Musca domestica
cannot be excluded as a potential vector of
trachoma; however, its broad feeding and ranging
habits make the possible vectorial capacity low to
absent. For a fly to act as mechanical vector
it must first pick up the bacteria from an infected
eye or nasal discharge and then transfer them to an
uninfected eye before the bacteria are either
dislodged in flight, killed by desiccation or ultra
violet light exposure, remove by the fly as it
grooms itself or stick to something else.
Since M domestica is attracted to a broad
range of substrates, and is not specifically
attracted to eyes, the likelihood that any bacteria
picked up will be transferred to a new host is
rather small. This is not to say that M.
domestica never plays a role in trachoma
transmission; when it is very abundant and crawling
over everything, it may be of transient importance.
References
-
Alemayehu W, Melese
M, Fredlander E, Worku A &
Courtright P (2005) Active trachoma in
children in central Ethiopia: association with
altitude. Trans R Soc Trop Med Hyg 99,
840-3
-
Emerson P, Bailey R,
Olaimatu M, Walraven G &Lindsay S (2000)
Transmission ecology of the fly Musca sorbens, a
putative vector of trachoma.
Trans R Soc Trop Med Hyg
94, 28-32.
-
Emerson
P, Lindsay S, Walraven G, et al.
(1999) Effect of fly control on trachoma and
diarrhoea. Lancet 353, 1401-1403.
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Emerson PM (2004) Role of
flies and provision of latrines in trachoma
control: cluster-randomised controlled trial.
Lancet 363, 1093–98.
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Emerson PM, Bailey RL,
Walraven GE &Lindsay SW (2001) Human and other
faeces as breeding media of the trachoma vector
Musca sorbens. Med Vet Entomol 15,
314-20.
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Emerson PM, Simms VM,
Makalo P & Bailey RL Household pit latrines as
a source of the fly Musca sorbens – a one
year longitudinal study from The Gambia (2005)
Tropical Medicine and International Health,
10; 706-709.
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Hafez M &Attia M (1958a)
On the developmental stages of Musca sorbens
wied., with special reference to larval behavior.
Bull Soc. Entomologique d'Egypte 42,
123-161.
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Hafez M &Attia M (1958b)
The relation of Musca sorbens wied. to eye
diseases, in Egypt. Bull Soc. Entomologique
d'Egypte 42, 275-283.
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Hafez M &Attia M (1958c)
Studies on the ecology of Musca sorbens wied. in
Egypt. Bull. Soc. Entomologique d'Egypte
42, 83-121.
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Luna EJ,
Medina NH, Oliveira MB, et al.
(1992) Epidemiology of trachoma in Bebdouro
State of Sao Paulo, Brazil: Prevalence and risk
factors. International Journal of
Epidemiology 21, 169-177.
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Peffly R (1953) The
Relative Importance Different Fly-Breeding
Materials in an Egyptian Village. The Journal
of the Egyptian Public Health Association,
165-180.
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Pont AC (1991) A review
of the fanniidae and muscidae (Diptera) of the
Arabian Penninsula. Fauna of Saudi Arabia
1991, 312-365.
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Taylor HR, Velasco F &Sommer
A (1985) The ecology of trachoma: an
epidemiological study in southern Mexico.
Bull World Health Organ 63, 559-567.
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West SK, Emerson PM,
Mkocha H, Mchiwa W, Munoz B, Bailey R & Mabey D
Effect of fly control following mass treatment
for trachoma in hyper-endemic setting: A
randomized trial in Tanzania (accepted)
Lancet
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WHO (2006)
http://www.who.int/blindness/causes/priority/en/index2.html
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Zimin, L. S. (1948). Key
to the third instar larvae of the synanthropic
flies of Tadzhikistan. Opred Fauna USSR,
28, 1-116 (in Russian).
Other
reference of interest:
-
Crosskey, R. W. &
Lane, R. P. (1993). House-flies, blow-flies and
their allies (calyptrate Diptera). In Medical
Insects and Arachnids. (R. P. Lane and R. W.
Crosskey eds.) London: Chapman and Hall:
403-428.
-
Curtis, C. F. & Hawkins,
P.M. (1982).
Entomological studies of on-site sanitation
systems in Botswana and Tanzania.
Transactions of the Royal Society of Tropical
Medicine and Hygiene, 76, 99-108.
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Legner, E.F, Sugerman,
B.B., Yu, H-s. & Lum, H. (1974). Biological and
integrated control of the Bush Fly, Musca
sorbens Wiedemann and other filth breedign
diptera in Kwajalein Atoll, Marshall Islands.
Bulletin of the Society of Vector Ecologists,
1, 1-14.
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Mau, R. F. L. (1978).
Larval development of Musca sorbens in
animal dung in Hawaii. Annals of the
Entomological Society of America, 71,
635-636.
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Meng, C. H. & Winfield,
G. J. (1944). Breeding habits of common West
China flies. Chinese Medical Journal,
62, 77-87.
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Sabrosky, C. W. (1952).
House Flies in Egypt. American Journal of
Tropical Medicine and Hygiene, 1,
333-336.
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Skidmore, P. (1985).
The biology of the Muscidae of the world.
Dordrecht, W. Junk Publishers.
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Tyndale-Biscoe, M. &
Hughes, R. D. (1968). Changes in the female
reproductive system as age indicators in the
bushfly Musca vetustissima Wlk.
Bulletin of Entomological Research, 59,
129-141.
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West, L. S. (1951).
The Housefly, its natural history, medical
importance and control. London, Constable
and Company.
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