Flies as Vectors of Microorganisms Potentially Inducing Severe Diseases in Humans and Animals


Agent of disease

Diseases

Type of the agents of disease

Authors

Polio

Poliomyelitis

Viruses

Greenberg (1965)

Shigella sp.

Dysentery

Bacteria

Levine and Levine (1991)

Vibrio cholerae

Cholera

Bacteria

Fotedar (2001)

EHEC O157:H7

Enteritis

Bacteria

Iwasa et al. (1999)

ETEC

Diarrhea

Bacteria

Jordi et al. (2000)

Campylobacter spp.

Diarrhea

Bacteria

Szalanski et al. (2004)

Helicobacter pylori

Enteritis

Bacteria

Grübel et al. (1997)

Salmonella spp.

Salmonellosis

Bacteria

Olsen and Hammack (2000)

Salmonella typhimurium

Typhus

Bacteria

Greenberg (1973)

Mycobacterium sp.

Tuberculosis

Bacteria

Fischer et al. (2001)

Staphylococcus aureus

Enteritis

Bacteria

Fotedar et al. (1992a, b)

Chlamydia trachomatis

Trachoma

Bacteria

Emerson et al. (2004)

Aspergillus, Penicillium

Multiorgan invasion

Fungi

Sales et al. (2002)

Cryptosporidium sp.

Diarrhea

Protozoa

Szostakowska et al. (2004)

Giardia lamblia

Giardiasis, diarrhea

Protozoa

Szostakowska et al. (2004)

Ancylostoma duodenale

Hookworm disease

Nematodes

Oyerinde (1976)


EHEC enterohemorrhagic Escherichia coli, ETEC enterotoxic Escherichia coli




Table 9.2
Reports on fly-transmitted agents of animal diseases in the literature (selection)










































































































Agent of disease

Diseases

Type of the agent of disease

Host

Authors

H5N1 and others

Bird flu

Virus

Birds/humans
 

Newcastle virus

Newcastle disease

Virus

Birds

Bram et al. (2002)

Herpes virus

Aujeszky’s disease

Virus

Pigs

Medveczky et al. (1988)

PRRSV

Respiratory syndrome

Virus

Pigs

Otake et al. (2004)

FMDV

Foot and mouth disease

Virus

Cattle, pigs

Greenberg (1973)

Bacillus anthracis

Anthrax

Bacteria

Cattle

Greenberg (1973)

Mycobacterium sp.

Tuberculosis

Bacteria

Cattle, pigs

Fischer et al. (2001)

Campylobacter jejuni

Diarrhea

Bacteria

Birds

Shane et al. (1985)

Streptococcus suis

Diarrhea

Bacteria

Pigs

Enright et al. (1987)

Corynebacterium pseudotuberculosum

Mastitis

Bacteria

Cattle

Yeruham et al. (1996)

Brucella species

Brucellosis

Bacteria

Cattle, pigs

Greenberg (1973)

Cryptosporidium species

Diarrhea

Protozoa

Birds, cattle, pigs

Graczyk et al. (1999)

Poultry tapeworm

Diarrhea

Cestodes

Birds

Abrams (1976)

Parafilaria species

Skin disease

Nematodes

Cattle

Bech-Nielsen et al. (1982)

Thelazia species

Eye worm disease

Nematodes

Cattle

O’Hara et al. (1989)


PRRSV Porcine reproductive and respiratory syndrome virus, FMDV foot-and-mouth disease virus


Thus, to obtain more recent data on the existing threat by microorganisms in industrial regions, the University of Düsseldorf initiated a long-term investigation (2006–2011) into the load of pathogens on flies close to stables/meadows used by chickens, pigs, cattle, horses, rabbits, and dogs and in addition checked the refinding rates after experimental exposure of flies to such agents of diseases (Förster et al. 2007, 2009; Förster 2009). In 2009, a Safeguard project (Campylobacter) was started by the governments of the Netherlands and North Rhine-Westphalia, which is the German state bordering the Netherlands. The aim of this project was to check the flies at selected downtown sites (with a huge number of restaurants) and recreation sites with respect to their load of agents of diseases in order to obtain basic data which may help to establish methods and better prophylaxis measures to interrupt transmission of agents of diseases. This chapter gives some of the results obtained with respect to bacteria and fungi which occurred on the surface of flies and/or in their intestine. Chapter 10 by Förster et al. (2012) deals with the transmission of different groups of parasites by various species of flies captured in the wild and reports from laboratory experiments showing the capacity of flies to transmit various parasites.



9.2 Methods and Targets



9.2.1 Fly Catching Close to Animal Houses


Flies were caught on warm and dry days (20–30°C) close to a dog meadow, poultry house, cattle barn, horse stable, pigpen, and rabbit cages in the surroundings of the small town of Dormagen near Düsseldorf in Germany. To avoid contamination by the tissues of typical insect catchers, the flies were first caught either with sterile vessels or with commercial sterile plastic bags and were immediately placed for 5–10 min in sterile petri dishes on blood agar. After this incubation, the flies were removed from the petri dishes, killed by CO2, and identified under a dissecting microscope. Later, larger numbers of flies were also caught with freshly washed butterfly nets. In these cases only the intestinal contents of these flies were examined.


9.2.2 Fly Catching at Recreation Sites


The catching sites at four selected recreation sites (often with crowds of people and where there were also numerous birds—geese, swans, ducks, and pigeons) were situated in larger towns or close by them. The following four sites were selected:

1.

The Old Town of Düsseldorf (Germany), with its many restaurants. The catching sites were meadows and bushes in the surroundings.

 

2.

A park in a suburb of Düsseldorf (at Castle Eller).

 

3.

A bathing lake close to Düsseldorf, which is crossed by the river Düssel, which gives its name to Düsseldorf. In summer thousands of people bathe there.

 

4.

The six-lakes-region close to the town of Duisburg (Germany), where the lakes are visited by huge numbers of people.

 

The flies were caught at intervals of 7–14 days (depending on the weather) with the help of butterfly nets, the opening of which had a diameter of 25 cm. The flies were transferred singly into sterile plastic vessels immediately after the catch.

The feces of the birds was collected in sterile, one-way plastic tubes and transported to the institutes for microbiological and/or parasitological investigations.


9.2.3 Determination of Microorganisms


The blood agar plates onto which the freshly caught flies had been placed were incubated at 37°C for 24 h. After the incubation, the petri dishes were checked for growth of microorganisms. For identification, the microorganisms were isolated and subcultured on blood agar and selective agar plates, and were finally incubated at 37°C for another 24 h. For identification of fungi, the microorganisms were isolated and were subcultured on Saboraud’s dextrose agar, and were then incubated at room temperature for 4 days. After the incubation period, the bacterial colonies were identified by standard bacteriological procedures (e.g., coagulase, oxidase test, Gram’s reaction, API®, Prolex®, VITEK®, etc.). Isolated E. coli bacteria were identified for their pathogenicity by in-house real-time polymerase chain reaction, differentiating enterotoxic E. coli, enteropathogenic E. coli (EPEC), EHEC, and enteroaggregative E. coli.


9.3 The Flies



9.3.1 Flies Around the Stables


The flies that were found close to the stables differed considerably with respect to their species relations from those found around dog meadows (Figs. 9.19.5). These differences are surely based on their different needs for different suitable breeding sites. Tables 9.3 and 9.4 summarize the occurrence of the different fly species at the different catching sites.

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Fig. 9.1
Motile Musca domestica larvae on their meat substrate


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Fig. 9.2
Adult Musca domestica fly


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Fig. 9.3
Stomoxys calcitrans. (a, b) Macrophotographs of adults. (c) Scanning electron micrograph of the head with the piercing/sucking apparatus


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Fig. 9.4
Fannia canicularis, adult and larva


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Fig. 9.5
Fannia canicularis, adult stage


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Fig. 9.6
Lucilia sericata, eggs


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Fig. 9.7
Lucilia sericata, larva


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Fig. 9.8
Lucilia sericata, pupae


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Fig. 9.9
Lucilia sericata, adult female


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Fig. 9.10
Lucilia caesar, adult female and male


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Fig. 9.11
Muscina stabulans, adult female


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Fig. 9.12
Sarcophaga carnaria, adult and pupa


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Fig. 9.13
Pollenia rudis. These flies (6–12 mm) have square silver dots on their abdomen. They enter houses in autumn and winter


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Fig. 9.14
Mydaea ancilla, adult female. This species belongs to the family Muscidae


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Fig. 9.15
Muscina pabulorum, adult female


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Fig. 9.16
Calliphora vomitoria, adult stage and pupa


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Fig. 9.17
Helina reversio, the head of which has a frontal black line. The yellow-gray abdomen is characterized by two black dots


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Fig. 9.18
Phaonia errans. This 9–12-mm-sized fly has completely yellow legs and the tip of the abdomen of the male appears reddish-yellow



Table 9.3
Main fly species close to stables (most of them are also known for their ability to introduce myiasis in humans)

























Stable

Fly species

Cattle barns

Musca domestica (Figs. 9.1 and 9.2), Polietes lardaria, Stomoxys calcitrans (Fig. 9.3)

Horse stables

Musca domestica, Stomoxys calcitrans

Poultry houses

Mainly Musca domestica

Pigpens

Musca domestica, Fannia canicularis (Figs. 9.4 and 9.5)

Rabbit cages

Mainly Musca domestica, Stomoxys calcitrans



Table 9.4
Fly species on a meadow where dogs regularly deposit their feces (dog pond)








































Fly species

Percentage of total catches

Lucilia caesar, L. sericata (Figs. 9.69.10)

54%

Muscina stabulans (Fig. 9.11)

15%

Sarcophaga carnaria (Fig. 9.12)

11%

Pollenia rudis (Fig. 9.13)

4%

Mydaea urbana

4%

Mydaea ancilla (Fig. 9.14)

2%

Muscina pabulorum (Fig. 9.15)

2%

Calliphora vomitoria (Fig.9.16)

2%

Fannia canicularis (Figs. 9.4 and 9.5)

2%

Calliphora vicina, Helina reversio (Fig. 9.17), Phaonia errans (Fig. 9.18), Polietes lardaria

Each species appeared as 1% of the catches

Around the stables, Musca domestica was the absolutely dominant species. In all catches in 3 years it was always present in the same relations:



  • 44% of the catches in the pigpens


  • 30% of the catches in horse stables


  • 17% of the catches in rabbit cages


  • 9% of the catches in cattle barns

In several cases its occurrence in poultry houses reached approximately 90%, which coincided with several important and massive fly outbreaks which were investigated by our group:

(a)

In a valley with large poultry houses and chicken feces stored in the open air

 

(b)

After several field fertilizations with chicken feces close to villages

 

(c)

In a small town with a compost plant, the units of which were opened nightly by feral pigs and in the early mornings by crows

 

In all these cases the private houses up to a distance of 1 km were filled with hundreds of Musca domestica adults, which were apparently attracted by the dark interior of the houses when arriving from the surrounding fields, from the compost plant, and/or from badly stored chicken feces.

Practically in all cases the sex ratio of the flies caught was nearly 50:50 independent of whether the flies were caught close to the stables (i.e., outdoors) or inside houses.

The bloodsucking species Stomoxys calcitrans was an exception: only 42% of the flies caught outside were females. This might be attributable to the behavior of the females to suck blood and then to lay their eggs inside stables.

Tables 9.5 and 9.6 provide information on the life cycles of several important fly species, which of course primarily attack farm animals, but, however, also molest humans by often numerous touchdowns. During these contacts, agents of diseases (see Tables 9.1 and 9.2) may be placed on humans and their food too. In these cases the flies could become vectors of zoonotic agents of diseases (see also Sect. 9.5 and Chap. 10).


Table 9.5
Development data of flies of central Europe






















































































































































Species

Size of adult (mm)

Eggs

Hatching of larvae

Larval development

Pupal rest

Life span of adults

Musca domestica

6–7

600–1,000 on feces (chicken, pig, horses, cattle) and other decaying organic matter

15°C: 50 h

15°C: 10–26 days

15°C: 18–21 days

60–70 days in stables

20°C: 23 h

20°C: 8–10 days

20°C: 10–11 days

30°C: 10 h

30°C: 4–7 days

30°C: 4–5 days

Musca autumnalis

5–7

600–900 on fresh feces

Temperature-dependent

4–7 generations per year

4–7 generations per year

Females of last generation hibernate

Fannia canicularis

4–6

Feces and putrescent material

25°C: 20–48 h

6 days

7–10 days

6–7 generations per year

Muscina stabulans

6–8

Eggs, larvae on chicken feces

Life cycle in summer about 2–3 weeks

Life cycle in summer about 2–3 weeks

Life cycle in summer about 2–3 weeks

4–5 generations per year

Stomoxys calcitrans

6–7

800 in groups of 25–50 in silage, in stables with urine and feces

1–2 days, temperature-dependent: 14 days up to months

6–8 days, temperature-dependent: 14 days up to months

6–8 days, temperature-dependent: 14 days up to months

Females live about 70–90 days

Haematobia irritans

4.5–5

In fresh cattle dung

Temperature-dependent: 24 days up to months, optimum 27–30°C

Temperature-dependent: 24 days up to months, optimum 27–30°C

Temperature-dependent: 24 days up to months, optimum 27–30°C

3–4 generations per year

Calliphora species

9–11

Eggs on feces with cadavers

Temperature-dependent

Temperature-dependent

10–40 days

1–2 months

10–14

Sarcophaga carnaria

10–19

Eggs on cadavers, agent of myiasis

Temperature-dependent

Temperature-dependent

10–40 days

1–2 months

Lucilia sericata, L. caesar

5–11

Eggs on feces, wounds, meat

24 h

4–7 days

1–2 weeks on the ground

1–2 months

Pollenia rudis

6–12

Eggs on feces, soil

Larvae parasitize in earthworms

4–8 days

1–2 weeks on carcasses

1–2 months

Phaonia errans

9–12

Eggs are placed on wood powder or dry feces

Temperature-dependent

4–5 generations per year

10–40 days

1–2 months

Hydrotaea dentipes

6–7

Eggs on human and animal feces

Temperature dependent

4–6 generations per year

10–40 days

2–3 months

Oestrus ovis

8–15

Larvae are deposited at the nose or eyes

Immediately after laying

Larvae hibernate in the nose

2–4 weeks on the ground

4 weeks

Hypoderma bovis

13–15

600–800 glued on hair of cattle

4–7 days, then invading the skin

Inside the body until March

14–65 days on the ground

3–5 days (up to 28 days in the cold)

Hypoderma lineatum

11–13

5–20 eggs per hair, in a row

3–6 days, then invading the skin

Inside the body until March

23–28 days on the ground

3–5 days



Table 9.6
Periods of activity of selected flies that attack cattle and sheep in central Europe





































































































































































































































Species

Breeding site

Jan

Feb

Mar

Apr

May

Jun

Jul

Aug

Sep

Oct

Nov

Dec

Musca domestica (housefly, typhoid fly)

Eggs and larva in and on animal feces, even in stables

+1

+1

+1

+1

+

+

+

+

+

+

+1

+1

Musca autumnalis (eye fly)

Eggs and larvae on animal feces outdoors, adults hibernate in buildings

02

02

02

+

+

+

+

+

+

+

02

02

Fannia canicularis (little housefly)

Eggs on feces of chicken and other animals, kitchen slops

02

02

02

02

+

+

+

+

+

+

02

02

Muscina stabulans (false stable fly)

Eggs, larvae often on chicken feces, predacious as well

+1

+1

+1

+1

+

+

+

+

+

+

+1

+1

Stomoxys calcitrans (stable fly; sucks blood every 3 days)

Oviposition on plant material in stables

+

+

+

+

+

+

+

+

+

+

+

+

Haematobia irritans (horn fly)

Eggs and larvae on fresh cow dung





+

+

+

+

+




Calliphora vicina, C. vomitoria (blowflies)

Eggs on feces and cadavers



+

+

+

+

+

+

+

+

+


Sarcophaga carnaria (flesh fly)

Eggs and larvae on meat, cadavers, earthworms




+

+

+

+

+

+

+



Lucilia sericata (gold fly)

Eggs in wounds, cadavers, feces





+

+

+

+

+

+



Lucilia caesar (carrion fly)

Eggs and larvae in feces, cadavers





+

+

+

+

+

+



Oestrus ovis (nose botfly)

Larvae are extruded into the nose of sheep and goats

Larvae in nose

Larvae in nose

Larvae in nose

Pupae on ground

+

+

+

+

+

+

+

Larvae in nose

Hypoderma bovis (large skin botfly)

600–800 eggs adhere to hair of cattle

Larvae in body

Larvae in body

Larvae in body

Pupae on ground

+

+

+

+

+

Larvae in body

Larvae in body

Larvae in body

Hypoderma lineatum (small botfly)

5–20 eggs per hair of cattle

Larvae in body

Larvae in body

Larvae in body

Larvae in body

+

+

+

Larvae in body

Larvae in body

Larvae in body

Larvae in body

Larvae in body


+, activity of adult flies in the wild and in stables; +1, activity of fly stages in stables; 02, overwintering in buildings or stables; , in winter rest

Tables 9.5 and 9.6 in addition show the periods when the flies are most active at the in general moderate temperatures of central Europe. In warmer regions they are active for practically the whole year, so the potential transmission of agents of diseases may occur throughout the year. This makes it clear that only strict prophylaxis measures will protect animals and as a consequence also humans who live in the close neighborhood of animals.

All flies caught in the surroundings of human dwellings and/or different animal houses or recreation sites are so-called synanthropic species (Sukopp and Wittig 1998). The definition of the term “synanthropy” characterizes plant or animal species which have adapted their life cycle to human housing areas. There they may reproduce in such high numbers that they do not need additions from outside to maintain their population at a constant level. In cases of an increase in food, many other individuals of this species might be attracted and this may lead to real plagues. Eusynanthropy and hemisynanthropy are subgroups of synanthropy. In the first case, the occurrence and reproduction of a certain species is obligatory because of the co-occurrence with human houses. Members of the genus Drosophila are examples of flies in Europe. Examples of other insects are the bedbug (Cimex lectularius), the bread beetle (Stegobium paniceum), and imported cockroaches (Blatta orientalis, Blattella germanica, Supella longipalpa, Periplaneta americana), which can only exist in human houses, whereas forest cockroaches (e.g., Ectobius silvestris) enter human dwellings only occasionally. “Hemisynanthropy” (the facultative form) covers species which find an optimum amount of food and facilities for survival inside or around human dwellings, but these species also survive easily outside human settlements. For example, Lucilia caesar is such an species as is the Eurasian swift (Apus apus), which likes to use human buildings as a starting point for its magnificent flights, although it may also start from natural rocks, etc.

With respect to these definitions of synanthropy, many flies are hemisynanthropic animals, which use the facilities of human settlements with all their garbage, superfluous food, and protected places for their—often immense—reproduction. They may, however, survive easily far away from human settlements, since dead animals, their carcasses, and their degrading feces offer practically unlimited food and propagation facilities. Therefore, even the best fly control measures cannot prevent the constant influx of flies from outside into human houses and into the stables of farmed animals. However, eusynanthropy and hemisynanthropy of most flies make it necessary for humans to control fly propagation by minimizing the breeding sites in and around human buildings of any kind. This can be done simply by reduction of garbage, removing remnant food, removing feces, changing straw, etc. In addition—especially in monocultures of many animals—chemical treatment of animals, of the stable walls, and/or of the straw might become necessary to prevent feeding farm animals from being disturbed or even to avoid infections with agents of diseases as listed in Tables 9.1 and 9.2.

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Aug 31, 2016 | Posted by in GENERAL | Comments Off on Flies as Vectors of Microorganisms Potentially Inducing Severe Diseases in Humans and Animals

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