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Memórias do Instituto Oswaldo Cruz
Fundação Oswaldo Cruz, Fiocruz
ISSN: 1678-8060 EISSN: 1678-8060
Vol. 91, Num. 3, 1996, pp. 293-298
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Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 91(1), May/June
1996
The Associated Microflora to the Larvae of Human Bot Fly
Dermatobia hominis L. Jr. (Diptera: Cuterebridae) and its
Furuncular Lesions in Cattle
E Sancho, M Caballero*, I Ruiz-Martinez**/^+
Departamento de Parasitologia, Escuela de Medicina Veterinaria,
Universidad Nacional, 3000-Heredia, Costa Rica, America Central
*Laboratorio de Bacteriologia, Piet-UNA, Escuela de Medicina
Veterinaria, Universidad Nacional, Apartado 304-3000-Heredia,
Costa Rica, America Central **Departamento de Biologia Animal y
Ecologia, Area de Parasitologia, Facultad de Ciencias
Experimentales, Apartado 62, Universidad de Jaen,
E-23071-Jaen, Espana
Code Number: OC96058
Size of Files:
Text: 30K
No associated graphics files:
[TABLE AT END OF TEXT]
The microflora associated to furuncular lesions, larvae and
pupae of Dermatobia hominis, as well as the relationships
between parasite, host and microflora associated, as a
comprehensive microsystem, has been studied. One hundred and two
furuncular myiasis due to D. hominis larvae in several
breeds of cattle were studied and the following bacterial species
were significant: Staphylococcus aureus, S. epidermidis, S.
warneri, Bacillus subtilis and Escherichia coli.
Closely related, the microflora associated to 141 samples from
first, second, third instar larva and both external surface and
larval cavities has been studied. The representative associated
microflora to the larvae were: S. aureus, B. subtilis, S.
hycus and Moraxella phenylpiruvica, Moerella
wisconsiensis, Proteus mirabilis and P. vulgaris, M.
phenylpiruvica, M. wisconsiensis, P. mirabilis and P.
rettgeri were the representative microflora associated to 64
pupae of D. hominis.
Key words: Dermatobia hominis - associated bacterial
microflora - larvae - pupae - furuncular myiasis
Dermatobia hominis L. Jr. is a Neotropical fly
responsible for most prevalent myiasis in Central and South
America (from Mexico to Argentina) (Guimar es et al. 1983).
Myiasis due to D. hominis or dermatobiasis (Kasai et al.
1988) is easily identified by its characteristic furuncular
cutaneous lesions, characterized by a tumoration which involves
both epidermis and dermis. The larva is situated in a cavity
screened by a non-keratin flat epithelium that has a
communication orifice with the exterior (Neel et al. 1955). This
orifice is produced when the larva penetrates the host and is
maintained during the entire parasitic phase, about 35 to 47 days
(Sancho & Boschini 1985).
Their effects on the wild fauna are unknown, however the bot
fly maggots are a seriuos pest to livestock, specially on cattle
and humans (Steelman 1976). Though the literature on its
epidemiology is extensive (Guimar es & Papavero 1966), little
information about the D. hominis biology is available
(Neiva & Gomes 1917, Catts 1982, Sancho 1988).
The importance of the studies on the associated microflora to
myiasis-producing flies has been showed in Australian sheep
blowfly Lucilia cuprina Wied (Diptera: Calliphoridae)
(Guerrini et al. 1988), the new world screwworm Cochliomyia
hominivorax Coquerel (Diptera: Calliphoridae) (Bromel et al.
1983) and in the palearctic screwworm Wohlfahrtia
magnifica Schin (Diptera: Sarcophagidae) (Ruiz-Martinez &
Villa-Real 1995). The role of associated microflora in the
attraction, oviposition, larval culture and in the new tendences
of trapping flies are being intensely studied.
Adult bot fly D. hominis does not frequently visit the
hosts (Catts 1982) but, instead, they oviposit on a carrier,
usually a zoophilic fly or mosquito (Neiva & Gomes 1917, Sancho
1988). The carrier behaviour allows the larvae to reach the
host's skin. In another paper, we consider the possible
attractive factor for several primarily and secondarily myiasis
(Ruiz-Martinez & Villa-Real 1995). However, the possible role
and implications of bacteria associated to dermatobiasis for
in vitro culture of parasitic stage -larvae- (Zeledon &
Silva 1987) is clear and it is obviously important in the
knowledge of the pathogenicity or pathomorphology of the
furuncular lesions (Sancho 1988).
On the associated bacterial microflora of D. hominis
short reports are available (Sancho et al. 1986, Coronado 1989),
but they are not extensive and do not stablish correlations
between furuncular lesion and larvae or pupae. Theoretically, the
exposure of the wound to field environment and, mainly, bacterial
contamination resulting from numerous flies feeding on lesions,
could explain some associated bacterial microflora to larvae and
foruncular myiasis, but not all of them. There are some
interactions larvae-microflora, host body-microflora and furuncle
microflora-exogenous microflora that must be intensely
studied.
The main objective of this study is to isolate, identify and
analyze the bacterial microflora in the furuncular lesion,
larvae (first, second and third instars) and pupae of D.
hominis, and to discuss the role of these bacteria.
MATERIALS AND METHODS
The study has been carried out between April and October 1993.
Hides from slaughterhouse containing active furuncular myiasis
due to first, second and third instar larvae of D. hominis
were recovered as follows: the exterior surface of the wound was
shaved with alcohol-solution and a hot spatula was used to
eliminate any remaining bacterial contamination from surrounding
hide. With sterile forceps pressure was applied to the base of
each tumoration for extracting the larvae and removed from the
cavity with a cotton-swab in triplicate and were introduced in
vials Portagerm (41996 BioMerieux) with resazurine as ox-red
indicator (Barry et al. 1972, Yrios et al. 1975).
Larvae were placed in sterile vials and classified in instars
according with Jobsen and Mourier (1976). All samples were kept
in thermic plastic bags at 26-28 C, 80% RH at darkness for
analysis, within 24 to 48 hr, being the samples refrigerated at
4 C.
From six 1st instar larva, 43 2nd instar larva and 92 3rd
instar larva for associated bacterial microflora were studied.
For to obtain pupae, the mature 3rd instars larva were cultured
to pupae stage on a sterile filter paper in a climatic chamber
at 25+/-1 C, 60-65% of RH and photoperiode 12:12 hr. The pupae
(n= 64) were analyzed 20 days after (yellow pharate adult;
according to Siva-subramanian & Biagi 1983). Larvae and pupae
were washed with 5 ml of sterile saline solution and shaked in
Mixo-Tub during 5 min. The resulting fluid was analyzed for
external microflora. Then, the samples were homogenized in a
Potter (glass homogenizer) and a centrifugation was made. With
the supernatant as a sample for internal microflora, 0.2 ml
aliquots of each dilution were made and spread in triplicate on
identification media for statystical analysis.
Samples were processed following the technics recorded in
Sonnenwirth (1987). The plates were incubated at 30 C from 48 hr
to 5 days, with or without CO^2 and extend to 7 d for anaerobic
bacteria. Gram-negative proofs were made following the system
Pasco/mic/ID (Difco Lab., Detroit) with 30 substrates and 19
antibiotics. For Gram-positive and anaerobic bacteria the
criteria of Krieg and Holt (1987) was followed, using 10
substrates and antibiotics of Oxoid (Ltd., London), BioMerieux
(BM Lab, Paris) and Difco. The results were analyzed by API 20
E, Octals number of Difco and Micro-Scann computerized systems.
The criteria employed in bacterial taxonomy followed the
classification of Bergey's Manual of Systematic Bacteriology
(Krieg & Holt 1987). The percentages shown in the Tables were
referred to mean bacterial counts that were found in each wound
(3x10^6) and 100% is the maximum colony forming units (CFU). All
data were recorded on DB3 files and proccessed by Microstad Prog.
and BMDP statistical-packet.
RESULTS AND DISCUSSION
Of 102 furuncular lesions studied, on 97 bacteria were isolated
(95.1% of positive results, on five furuncular lesions none
bacterial species were isolated). Ten bacterial species were
identified and in decreasing order of importance (% from total)
were: S. aureus (41.00%), E. coli (10.33%), S.
warneri (9.00%), E. aerogens (8.66%), S.
epidermidis (8.50%), B. subtilis (6.00%), C.
freundii (2.50%), S. liquefaciens (1.50%), E.
cloacae (1.00%) and E. agglomerans (1.00%) (Table
I).
S. aureus is common in piogenic proccesses but also on
animal skins, as well as S. warneri, S. epidermidis and
E. coli (Jansen & Hayes 1987). The other bacteria species
with enteric characteristics, probably appeared by contamination
due to flies visiting-wounds, as we can usually see on furuncular
lesions of Dermatobia, looking for nutritive sources (such
as Stomoxys calcitrans, Musca domestica, Muscina
stabulans, personal observations). It may explain the lower
isolation percentages for these species obtained in our study.
Whereas only in 66.7% samples of L-I bacteria were recorded (4
bacteria species) (Table II), in the 79% samples of L-II (8
bacteria species) and 97.8% of L-III (19 bacteria species)
samples positive isolations were recorded. The associated
microflora to larvae (L-I to L-III) in the external surface were:
S. aureus, S. epidermidis, B. subtilis (all of these
corresponding with frequent microflora isolated in the furuncular
myiasis), S. hycus, S. sciuri and M.
phenylpiruvica. On the other hand, the main associated
bacteria microflora to larvae in the internal cavities were:
M. phenylpiruvica, M. wisconsiensis, P. mirabilis,
P.vulgaris and B. subtilis (Table II).
Only bacteria species belonging to wounds were isolated on the
external surface of larvae, increasing the number and relative
importance rate of isolation from second to third instar larvae
(from only one bacteria species isolated -S. aureus- in
L-I, to four bacteria isolated in L-II and ten bacteria species
isolated in L-III) (Table II). When we tried to measure the
statistical similitude within samples from wounds and from
external surface of larvae by Sorensen's coeficient, the
percentages obtained were 85.0% (for L-II) and 96.0% (For L-III)
respectively. These facts show that the microflora associated
with larval surface was only a draging product from wounds.
On the contrary, the results obtained from internal body
(digestive and respiratory tracts) of larvae indicates that these
bacteria were not significant and S. aureus was never
isolated in significant levels from the internal body of the
larvae, whereas other bacteria such as M. phenylpiruvica,
M. winconsiensis, P. mirabilis, P. vulgaris and B.
subtilis are the dominant ones (Table II) and were never
isolated significantly from wounds. It is very probable that
these bacteria species stablish a competence against those from
wounds (Greemberg et al.1970) and they may constitute
endosymbionts of the larvae of D. hominis, that contain
a bactericide or bacteriostatic substance against foreign
microflora (Baba et al. 1987). Our results seem to point out
in this direction: the larvae contains their proper bacteria
microflora (this phenomenon is clear in L-II and L-III) and these
bacteria reject the foreign one ingested by the larval
nutrition.
Probably, this phenomenon will be common in myiasis-producing
flies: similar results have been obtained on Australian sheep
blowfly Lucilia cuprina (Emmens & Murray 1982), in new
world screwworm Cochliomyia hominivorax (De Vaney et al.
1973) and in palearctic screwworm fly Wohlfahrtia
magnifica (Ruiz-Martinez & Villa-Real 1995).
As a whole, the number of bacteria species isolated increased
from instar I to instar III (from 4 to 19) (Table II) and
decreased from instar III to pupae (from 19 to 7) (Table II).
Obviously, the increasing size of the furuncular hole (due to
larval growth) and its exposed surface to the environment
produces a correlative increase of microflora associated or
imported (from environment). Moreover, the infestation itself
increased the microflora coming from feeding fly visiting-wounds.
In this way, the high number of flies feeding on wound exudates
may be the major cause of foreing contamination of the furuncles
under natural conditions (Hawley et al. 1951). The larger
development time of third instar larvae (Sancho & Boschini 1985)
could favour the continuous contamination throughout the field
environment and wound-visiting flies.
On the other hand, although one bacteria capable of producing
piodermitis as S. aureus was isolated from the wound-
samples, no secondary bacterial infection was recorded.
Noticeably there have been no cases of acute secondary bacterial
infection in human skin parasitized by warble flies (Brenes &
Maezerville 1963). Nevertheless, when the parasite attacks other
host tissues a secondary bacterial infection is recorded (such
as a meningo-encephalitis, case reported by Cespedes et al.
1962). These may suggests that the skin has an immunological
function with an inhibitory effect on bacteria present in the
wound (Patterson & Edelson 1982). Another possibility is the
larval substance with bactericide properties in D. hominis
(as suggested the data of Picado 1935) and in other warble flies
(Bennett 1955, Beesley 1968) as Baba et al. (1987) showed with
the antibacterial effect of "sarcotoxins I, II and III" from
flesh flies. In this way, Coronado (1989) observed the
bactericide effect of larval extracts from D. hominis
against S. aureus, S. epidermidis, S. caprae and
Streptococcus spp. Independently or together, showed the
absence of acute secondary bacteria infection on human skin and
bovine cattle hides as facts for intensive studies in the future,
but with one noteworthy difference: the hypothesis on
antibacterial properties of D. hominis's larval extracts
working on living tissues (not in carcases, decayed or dead
tissues as flesh-flies and "sarcotoxins").
A group of 64 pupae of D. hominis was studied (Table
II) and in 44.75% positive results were obtained. This relative
sterility was observed by Greemberg et al. (1970) for pupae of
several flies. Seven bacteria species were isolated and only four
with relative importance: M. winconsiensis, M. phenylpiruvica,
P. mirabilis and P. rettgeri. These bacteria species
were isolated from internal body of first, second and third
instar larvae (Table II) and never isolated in the furuncular
myiasis.
Observing the bacteria microflora associated to different
studied samples (Table II), we conclude that M.
phenylpiruvica, M. wisconsensis and P. mirabilis,
plus B. subtilis constitute the microflora proper of
larvae and pupae of Dermatobia, and secondarily P.
vulgaris and P. rettgeri. Curiously, these bacterial
species are commonly found in other myiasis producing-flies
(Emmens & Murray 1982, Bromel et al. 1983, Ruiz-Martinez & Villa-
Real 1995) with different life-habits. This is the first record
about the presence of M. wisconsensis (Hickman et al.
1984) in animal tissues.
As stated above, we assumed that the antibacterial properties
of some bacteria species (Baba et al. 1987, Coronado 1989), alone
or added to the skin immunological factors (Patterson & Endelson
1982) for explain the results of Tables I and II. Nevertheless,
another idea suggests the role of specific bacteria associated
to the larvae of D. hominis (Table II). Recently Guerrini
et al. (1988) showed that some bacteria create a double effect.
First, to produce smells attractive to gravid females (perhaps
for the carriers?), that explain the prevalence of furuncular
myiasis (Thomas, 1988). Moreover, faty acids coming from wounded
tissues and other decomposed tissues would justify the attraction
for this wounds (Mulla et al. 1977). Second, to maintain a pH
coinciding with the maximum rates of larval survival. Certainly,
the pH rates observed over 419 foruncular lesions due to D.
hominis were very constant (6.88+/-0.05) and its variations
for samples of second and third instars larvae and pH from the
outer or inner part of the cattle hides were very small (personal
observations) and coincides with the optimal pH for S.
aureus (Tables I, II).
In our opinion the furuncular lesion, the larvae and its
associated microflora must be considered as a whole micro-
habitat. It is possible that the external microflora would be
essential for maintaining the pH. The optimal pH and bacteria
would be neccesary for an adequate larval development. The wound
and larvae metabolism would be probably adequate for attractions
of new carriers (with egg mass adhered). The larvae associated
microflora would help this process and provide an adequate inner-
habitat to larvae. The understanding of this complex situation
may lead to succes for in vitro culture of larval instars,
to better undestand of the larval development, the development
of traps and to comprehensive studies about biology of D.
hominis.
ACKNOWLEDGMENTS
To Mr Gustavo Chinchilla and Dr Frederic A Poudevigne (USDA-
ARS-Screwworm Program), Dr M Miranda and Dr B Badilla
(Montecillos Slaughterhouse), Dr C Boschini and Dr L Torres
(National University of Costa Rica) for sampling and research
facilities. To Dr R Villa-Real and Dr L Extremera for manuscript
corrections and methodological designs from Bacteriological
Research Unit of Jaen University. To Spanish Airlines Iberia for
care, transport assistance and effectiveness. To Mr JJ Richmond,
Mr JB Granados and Mr F Corrales (USDA-ARS-Screwworm Program) for
technical assistance in field trials and Mr J Gonzalez Soto, Ms
G Hernndez Gomez and Ms L Lang from Bacteriological Department
of Universidad Nacional, Costa Rica. To Ms G Bolanos from U.S.
Embassy of San Jose (Costa Rica) for english corrections.
To United States Department of Agriculture (USDA), Agricultural
Research Services (ARS), Screwworm Program for Research
facilities, specially to Research-Leaders Dr FD Parker and Dr JB
Welch and the Administrative-Program Mr R Aguirre.
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This project was funded by Universidad Nacional and CONICIT of
Costa Rica (Central America). Postdoctoral grant from Ministerio
de Educacion y Ciencia/Fulbright Comission of Spain.
^+Corresponding author.
Fax: +34-53-212141.
Email: iruiz@piturda.uja.es
Received 5 June 1995
Accepted 7 February 1996
TABLE I
Microflora associated to furuncular lesions due to Dermatobia
hominis in cattle
Bacterial Presence/ % / Mean % Relative
species sample total of isol- importance
ation index
---------------------------------------------------------------
Staphylococcus aureus 85 83.33 41.00 34.16
Staphylococcus epidermidis 43 42.16 8.50 3.58
Staphylococcus warneri 32 31.37 9.00 2.82
Bacillus subtilis 50 49.02 6.00 2.94
Escherichia coli 60 58.82 10.33 6.08
Enterobacter agglomerans 5 4.90 1.00 0.05
Enterobacter aerogens 17 16.67 8.66 1.44
Enterobacter cloacae 10 9.80 1.00 0.10
Citrobacter freundii 9 8.82 2.50 0.22
Serratia liquefaciens 6 5.88 1.50 0.09
# isolated species= 10
Bacterial absence 5 4.90
The 'relative importance index' is defined as the result of the
mean percentage of isolation x the presence by sample and / by
the total observations (in this case 102 furuncular lesions).
TABLE II
Discriminative analysis of microflora associated to furuncular
lesions, larvae and pupae of Dermatobia hominis
Type of sample
Bact. species
--------------------------------------------------------------
Furunc- Larvae - I Larvae - II Larvae - III Pupa
ular Ext. Int. Ext. Int. Ext. Int.
lesions
--------------------------------------------------------------
Staphylococcus aureus
34.16 6.00 1.25 14.88 0.84 30.44 0.72 -
Staphylococcus epidermidis
3.58 - - - - 2.17 0.04 -
Staphylococcus hycus
- - 3.39 5.21 - 1.60 0.44 -
Staphylococcus hominis
- - - - - 0.16 - -
Streptococcus haemolyticus
- - - - - 0.26 - -
Streptococcus sciuri
- - - - - 2.20 - 0.11
Streptococcus similaris
- - - - - - 0.08 -
Streptococcus warneri
2.82 - - - 1.77 - - -
Streptococcus xylosus
- - 1.10 - - - - -
Bacillus subtilis
2.94 - - 3.06 3.72 4.96 1.56 0.51
Escherichia coli
6.08 - - - 0.51 0.69 0.11 -
Aeromonas salmonicida
- - - - - - 0.18 -
Proteus mirabilis
- - - - 8.62 - 4.45 4.22
Proteus vulgaris
- - - - - - 4.21 -
Proteus rettgeri
- - - - - - 0.90 2.25
Providencia stuartii
- - - - - - 0.11 -
Enterobacter aerogens
1.44 - - - - - - -
Enterobacter agglomerans
0.05 - - - - - - -
Enterobacter cloacae
0.10 - - - - - - -
Moerella wisconsiensis
- - - - 13.92 - 4.79 9.38
Moraxella phenylpyruvica
- - 11.80 0.66 10.05 - 9.54 10.00
Citrobacter freundii
0.22 - - - - 0.08 - -
Serratia sp.
- - - - - - - 0.07
Serratia liquefaciens
0.09 - - - - - 0.07 -
Serratia marscescens
- - - - - 0.08 - -
Total = 25
10 1 4 4 7 10 14 7
(#): positive isolation reffering to relative importance index
in each sample-kit; (-): negative isolation
Copyright 1996 Fundacao Oswaldo Cruz
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