A survey of veterinary hospitals in Nigeria for the presence of some bacterial organisms of nosocomial and zoonotic potential
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Veterinaria Italiana, 45 (2), 235‐241
© IZS A&M 2009 www.izs.it/vet_italiana Vol. 45 (2), Vet Ital
235
A survey of veterinary hospitals in Nigeria for the
presence of some bacterial organisms of nosocomial
and zoonotic potential
Faruk M. Tambuwal(1), Aminu Shittu(2), Mika’il B. Abubakar(1),
Mohammed D. Salihu(2), Abdulkadir U. Junaidu(2), Abdullahi A. Magaji(2),
Mohammed Lawal(2) & Mahmud Danyaro(1)
Summary
This study was undertaken to determine the
type and estimate the prevalence of bacterial
organisms on contact surfaces of five close‐to‐
patient facilities in three veterinary health care
settings within the Sokoto metropolis of north‐
western Nigeria. A total of 30 samples (10 from
each setting) were collected and analysed
using culture, microscopy and biochemical
testing. Bacterial species isolated from samples
in this study included the following: Bacillus sp.
(27.3%), Staphylococcus aureus (15.9%), Listeria
sp. (13.6%), Streptococcus sp. (11.4%), Salmonella
sp. (6.8%), Escherichia coli (4.5%), Staphylococcus
epidermidis (4.5%), Citrobacter sp. (2.3%),
Klebsiella sp. (2.3%), Lactobacillus sp. (2.3%),
Micrococcus sp. (2.3%), Pasteurella sp. (2.3%),
Proteus sp. (2.3%), and Yersinia sp. (2.3%). A
higher percentage (64.3%) of the total bacterial
isolates were zoonotic in nature and hence of
public health significance. Some pathogens
have the potential of nosocomial spread. In
this study, we seek to establish the first
evidence of bacterial presence in the major
veterinary health care settings in the Sokoto
region of north‐western Nigeria. Of particular
interest is the hypothesis, which has not
previously been formally
nosocomial infections are especially likely to
tested, that
be implicated in both animals and occupational
diseases in Nigeria. It was suggested that some
of these isolates were associated with the risk
of nosocomial and zoonotic infections and
hence draws attention to the need to
rigorously employ
precautions as part of the hospital’s infection
control programme in an attempt to protect
both patients and staff from infections.
standard veterinary
Keywords
Bacterium, Hospital, Nigeria, Nosocomial,
Veterinary, Zoonosis.
Un’indagine negli ospedali
veterinari in Nigeria sulla
presenza di alcuni organismi
batterici con potenziale
nosocomiale e zoonotico
Riassunto
Scopo di questo studio era determinare il tipo,
stimandone la prevalenza, di organismi batterici
sulle superfici di contatto di cinque sale per pazienti
in tre cliniche veterinarie della metropoli di Sokoto,
nella Nigeria nord‐occidentale. Sono stati raccolti
in totale 30 campioni (10 per ciascuna clinica) e
sottoposti ad analisi delle colture, esami
(1) Department of Microbiology and Pathology, Faculty of Veterinary Medicine, Usmanu Danfodiyo University,
P.M.B. 2254, Sokoto, Nigeria
ftmuhd@yahoo.co.uk
(2) Department of Public Health and Animal Production, Faculty of Veterinary Medicine, Usmanu Danfodiyo
University, P.M.B. 2254, Sokoto, Nigeria
ameen_vet@yahoo.com
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A survey of veterinary hospitals in Nigeria for the presence
of some bacterial organisms of nosocomial and zoonotic potential
Faruk M. Tambuwal, Aminu Shittu, Mika’il B. Abubakar,
Mohammed D. Salihu, Abdulkadir U. Junaidu,
Abdullahi A. Magaji, Mohammed Lawal & Mahmud Danyaro
236
Vol. 45 (2), Vet Ital www.izs.it/vet_italiana © IZS A&M 2009
microscopici e biochimici. Le specie batteriche
isolate dai campioni sono le seguenti: Bacillus sp.
(27,3%), Staphylococcus
Listeria sp. (13,6%), Streptococcus sp. (11,4%),
Salmonella sp. (6,8%), Escherichia coli (4,5%),
Staphylococcus epidermidis (4,5%), Citrobacter
sp. (2,3%), Klebsiella sp. (2,3%), Lactobacillus
sp. (2,3%), Micrococcus sp. (2,3%), Pasteurella
sp. (2,3%), Proteus sp. (2,3%) e Yersinia sp.
(2,3%). Una percentuale più elevata (64,3%) degli
isolati batterici totali era di natura zoonotica e
pertanto significativa per la salute pubblica. Alcuni
patogeni presentano potenziale di diffusione
nosocomiale. In questo studio gli autori hanno
cercato di stabilire le prime evidenze di presenza
batterica nelle principali cliniche veterinarie della
regione di Sokoto, nella Nigeria nord‐occidentale.
Particolarmente interessante è l’ipotesi, non formal‐
mente verificata in precedenza, della probabilità che
in Nigeria le infezioni nosocomiali siano coinvolte
nelle malattie sia animali che occupazionali. È stato
proposto che alcuni di questi isolati siono associati
al rischio di infezioni nosocomiali e zoonotiche, il che
sottolinea la necessità di applicare rigorosamente
norme precauzionali veterinarie nell’ambito del
programma ospedaliero di controllo delle infezioni
allo scopo di proteggere sia i pazienti che il
personale.
aureus (15,9%),
Parole chiave
Batteri, Nigeria, Nosocomiale, Occupazionale,
Ospedale, Veterinario, Zoonosi.
Introduction
Field and laboratory veterinary work has been
associated with a wide variety of hazards for
many years (3). Nigerian veterinarians are
increasingly exposed to zoonotic diseases
through occupational exposure and contact
with animals, and only a few veterinary health
care settings employ the recommended
precautions as standard tools in infection
control.
Health is a high priority for any society and
infections remain a leading cause of disease
globally. Infections
hospitalised patients and become manifest
only after 48 h of stay are called ‘nosocomial’
(17). Such nosocomial or hospital‐acquired
infections lead to significant
that occur among
additional
morbidity, mortality and economic burdens
than should be expected from the patient’s
underlying disease alone.
Veterinary practices are unique environments
that bring humans into close contact with
many different species of patients. In the
practice environment, whether in a building or
in the field, veterinary
frequently exposed
unrecognised infectious pathogens, many of
which are zoonotic (11). Some of the
documented zoonotic infections that have
occurred in veterinary personnel include:
methicillin‐resistant Salmonella Typhimurium,
cryptosporidiosis, cat‐associated plague, cat‐
associated sporotrichosis, methicillin‐resistant
Staphylococcus aureus and dermatoplytosis.
Such zoonotic diseases that occur in veterinary
personnel as a result of being in contact with
infected animals are referred to as infectious
occupational hazards. Occupational hazards
are mainly caused by agents of zoonotic
infections such as Brucella sp., Mycobacterium
sp., Salmonella sp., Bacillus sp., Neisseria sp.,
Yersinia sp., Listeria sp., etc. (10, 11).
personnel
recognised
are
and to
During the career of a veterinarian, the
majority suffer an animal‐related injury
resulting in hospitalisation and/or significant
loss of work time (4, 6, 7, 8, 12). Most clinically
infected wounds from dog and cat bites are
mixed infections of aerobic and anaerobic
bacteria (16).
The aim and objective of this survey was to
establish preliminary evidence of the presence
of common aerobic or aero‐anaerobic bacteria
on five close‐to‐patient hospital facilities and
to determine their
emphasis on those with possible nosocomial
and zoonotic potential, to enable us to develop
a tailor‐made infection control programme for
each setting and to recommend possible
considerations on the need for further study.
Other sources of contamination that are
equally or more dangerous, such as anaerobic
bacteria, viruses and parasites have not been
demonstrated in this study.
prevalence, placing
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Faruk M. Tambuwal, Aminu Shittu, Mika’il B. Abubakar,
Mohammed D. Salihu, Abdulkadir U. Junaidu,
Abdullahi A. Magaji, Mohammed Lawal & Mahmud Danyaro
A survey of veterinary hospitals in Nigeria for the presence
of some bacterial organisms of nosocomial and zoonotic potential
© IZS A&M 2009 www.izs.it/vet_italiana Vol. 45 (2), Vet Ital
237
Materials and methods
Study area
This study covered three major veterinary
hospitals in the city of Sokoto, the capital of
Sokoto State, located in the north‐western zone
of Nigeria. The state is located between
longitudes 4°05´E and 6°40´E and latitudes
11°30´N and 14°00´N and shares common
borders with Niger to the north, Kebbi State to
the south‐west and Zamfara State to the east.
Materials used
All the glassware used were first washed and
sterilised in a hot air oven at a temperature of
160°C for 2 h and later stored in aseptic
conditions until required for use.
Sample collection
Samples
metropolitan veterinary premises, namely:
? the State Veterinary Clinic located at the
Sokoto North Local Government Area
? the Large Animal Clinic of the Usmanu
Danfodiyo University Veterinary Teaching
Hospital (UDUVTH)
? the Small Animal Clinic of the UDUVTH.
were collected from three
All three hospitals are located in the state
capital and receive cases from different areas
through visits from patients or through
ambulatory services. The State Veterinary
Clinic is owned by government and treats
ovine, caprine and avian cases. Most of the
canine and complicated cases in all species are
referred to the UDUVTH, due to the fact that it
is an institutionally based hospital with
improved facilities and better expertise. The
UDUVTH was divided into large animal, small
animal and avian clinics with each receiving
species‐specific cases that are handled by
specialists in each respective area. All three
hospitals perform bacterial disease diagnosis
on live animals admitted to the hospital.
Diagnoses of dead animals are performed in
post‐mortem rooms available on the premises
of each hospital. The Veterinary Microbiology
and Public Health Laboratories are owned by
the institution and receive clinical veterinary
samples from across the state.
The prepared sterile swabs were used to swab
the
various contact
considered to be the most proximal to patients.
Those surfaces include surgical tables, surgical
packs, examination tables, equipment trays
and surgical drapes/towels. The original
sample was collected in 5 ml of transport
medium after swabbing an area of 100 cm2 of
each surface. The samples were collected in
pairs, i.e. one in peptone water and the other in
selenite‐F broth media and transported to the
laboratory. All surfaces and equipment from
which samples were taken were assumed to be
cleaned and disinfected.
surfaces that are
Inoculation and isolation
A total of 1 ml per sample collected was
inoculated onto the respective media after a
serial (10‐fold) dilution, using a dilution factor
of 10–5. All samples in peptone water were
inoculated in two Petri‐dishes, with blood and
MacConkey agar, respectively. Samples in
selenite‐F broth were inoculated in Petri‐dishes
containing deoxycholate citrate agar (DCA).
All inoculated Petri‐dishes were incubated at
37°C for 24 h, after which the colonies were
observed and broth cultures were then sub‐
cultured in the corresponding media plates,
incubated at 37°C for 24 h, and observed for
characteristic colonies.
Each isolated colony was preserved in a
nutrient agar slant followed by smearing of
each isolate on microscopic glass slide for
staining.
A portion of each isolated colony was smeared
on a glass slide and stained with Gram
staining reagents and observed under a light
microscope using an oil immersion objective
(×100). Both the morphology and the Gram
reaction of the organisms were observed and
noted.
Biochemical tests
Biochemical tests were performed to confirm
the genus and/or species of the bacteria
associated with each sample. The catalase,
coagulase, triple sugar ion and indole tests
were performed in accordance with the
methods described in the Cowan and Steel
Manual (2).
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A survey of veterinary hospitals in Nigeria for the presence
of some bacterial organisms of nosocomial and zoonotic potential
Faruk M. Tambuwal, Aminu Shittu, Mika’il B. Abubakar,
Mohammed D. Salihu, Abdulkadir U. Junaidu,
Abdullahi A. Magaji, Mohammed Lawal & Mahmud Danyaro
238
Vol. 45 (2), Vet Ital www.izs.it/vet_italiana © IZS A&M 2009
Results
In general, bacteria of different genera/species
were isolated with varying frequencies among
all the sites sampled/examined. The occurrence
of common bacterial isolates from different
premises and sampling sites are presented in
Tables I and II, respectively.
Duplicate plates were used. Supposing the
dilution on a plate was 10–5, the average counts
were obtained using (12+10)/2 and the product
multiplied by the dilution factor. The
estimated number of organisms in 5 ml was
found to be 5.5 × 10–6 colony‐forming units
(cfu) and the total count per cm2 was found to
be 5.5 × 10–4 cfu/cm2. Bacterial counts exceed‐
ing 150 cfu/cm2 are an indication of inadequate
sanitation and call for improved sanitation.
The study was conducted to establish evidence
of presence of those bacterial isolates in
premises but the possible origin of pathogens
recorded in staff and in animals was not
determined.
Discussion
The results of this study are shown in Tables I
and II. The study revealed that facilities in
veterinary clinics in Sokoto are highly
contaminated with both pathogenic and non‐
pathogenic bacteria. Although the aim of this
survey was not to protect veterinarians as they
have to touch animals that are more
contaminated than the equipment, but rather
the staff who were not involved in caring for
the animals (those involved in maintenance
and cleaning activities), possibly the owners of
the animals and the healthy animals that were
examined on contaminated surfaces.
In this study, Bacillus sp. had the highest
prevalence (27.3%), with equipment trays
being the major source of infection. This may
be due to the ubiquitous nature of the bacillus
spores that are known to resist heat (high
temperatures), the organism germinates and
multiplies rapidly at room temperature (1).
Other reasons that may be responsible for the
high prevalence of Bacillus sp. may be the
ability of the organism to survive on dry
surfaces and the hygienic conditions under
which the veterinary clinics are being
managed.
S. aureus was the second most prevalent
organism in this study and constituted 15.9%
of the total isolates. Examination tables,
equipment trays and surgical drapes/towels
were the major source of infection by this
Table I
Prevalence of bacterial isolates from different premises
Bacterial isolates
State
veterinary
clinic
Large animal
clinic, UDUVTH
Small animal clinic,
UDUVTH
Total
Bacillus sp. 5 3 4 12 (27.3%)
Staphylococcus aureus 3 4 0 7 (15.9%)
Listeria sp. 1 2 3 6 (13.6%)
Streptococcus sp. 2 3 0 5 (11.4%)
Salmonella sp. 3 0 0 3 (6.8%)
Escherichia coli 0 2 0 2 (4.5%)
Staphylococcus epidermidis 1 0 1 2 (4.5%)
C itrobacter sp. 1 0 0 1 (2.3%)
Klebsiella sp. 0 1 0 1 (2.3%)
Lactobacillus sp. 0 1 0 1 (2.3%)
Micrococcus sp. 1 0 0 1 (2.3%)
Pasteurella sp. 0 0 1 1 (2.3%)
Proteus sp. 0 1 0 1 (2.3%)
Yersinia sp. 1 0 0 1 (2.3%)
Total 18 (40.9%) 17 (38.6%) 9 (20.5%) 44 (100%)
UDUVTH Usmanu Danfodiyo University Veterinary Teaching Hospital
Page 5
Faruk M. Tambuwal, Aminu Shittu, Mika’il B. Abubakar,
Mohammed D. Salihu, Abdulkadir U. Junaidu,
Abdullahi A. Magaji, Mohammed Lawal & Mahmud Danyaro
A survey of veterinary hospitals in Nigeria for the presence
of some bacterial organisms of nosocomial and zoonotic potential
© IZS A&M 2009 www.izs.it/vet_italiana Vol. 45 (2), Vet Ital
239
Table II
Prevalence of bacterial isolates from sampling sites
Bacterial isolates
Surgical
tables
Surgical
packs
Examination
tables
Equipment
trays
Surgical
drapes/towels
Total
Bacillus sp. 1 3 2 5 1 12 (27.3%)
Staphylococcus aureus 1 0 2 2 2 7 (15.9%)
Listeria sp. 2 2 1 1 0 6 (13.6%)
Streptococcus sp. 0 2 1 2 0 5 (11.4%)
Salmonella sp. 1 1 1 0 0 3 (6.8%)
Escherichia coli 1 0 0 1 0 2 (4.5%)
Staphylococcus
epidermidis
0 1 0 0 1 2 (4.5%)
C itrobacter sp. 0 0 1 0 0 1 (2.3%)
Klebsiella sp. 0 0 0 0 1 1 (2.3%)
Lactobacillus sp. 0 1 0 0 0 1 (2.3%)
Micrococcus sp. 1 0 0 0 0 1 (2.3%)
Pasteurella sp. 1 0 0 0 0 1 (2.3%)
Proteus sp. 0 1 0 0 0 1 (2.3%)
Yersinia sp. 0 1 0 0 0 1 (2.3%)
Total 8 (18.2%) 12 (27.3%) 8 (18.2%) 11 (25.0%) 5 (11.4%) 44 (100%)
organism. This prevalence observed might be
due to the fact that the organism is
comparatively stable in the environment and
in certain conditions, such as improper
cleaning and disinfection
facilities. The organism occurs as a commensal
on the skin and mucous membrane of animals
and is the causative agent of staphylococcal
gastroenteritis in animals and humans through
the production of enterotoxins. Worldwide,
S. aureus is the leading cause of gastroenteritis
resulting from the
contaminated food (9). The organisms can be
spread on the hands and clothes of veterinary
personnel during clinical procedures that
involve animal handling
examination or surgery, or cleaning of hospital
premises by workers.
of veterinary
consumption of
for
medical
Listeria sp. was responsible for approximately
13.6% of the bacterial isolates and was most
often isolated from surgical tables and packs.
The organisms can be recovered from animal
faeces and can grow and replicate in the
environment at a wide range of temperatures
(from 4°C to 45°C). This contributes to the
strong presence of the organism in our hospital
premises. The organism is the causative agent
of listeriosis, a disease characterised by
abortion, septicaemia and endopthalmitis (15).
Streptococcus sp. constituted 11.4% of isolates,
with a higher prevalence on surgical packs and
equipment trays. Streptococci
commensals of mucous membranes, are
known to cause pyogenic infection in many
species of animals and in humans and are
associated with abscess formation, suppurative
conditions and septicaemia (15).
are often
Salmonella sp. constituted 6.8% of isolates and
was frequently identified on surgical tables,
surgical packs and
Salmonella sp. belongs
Enterobacteriacae which inhabits the gastro‐
intestinal tract of humans and animals. It is of
public health importance in that 1 cfu/g of its
isolates has been incriminated in food poisoning
(1). Improper cleaning and disinfection of
contact surfaces in veterinary clinics contribute
to the proliferation of the organism, even at
high levels, because it can grow and multiply
at a wide range
temperatures. Infection is characterised by an
incubation period that varies between 6 h to
7 days (1).
examination
to
tables.
family the
of environmental
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A survey of veterinary hospitals in Nigeria for the presence
of some bacterial organisms of nosocomial and zoonotic potential
Faruk M. Tambuwal, Aminu Shittu, Mika’il B. Abubakar,
Mohammed D. Salihu, Abdulkadir U. Junaidu,
Abdullahi A. Magaji, Mohammed Lawal & Mahmud Danyaro
240
Vol. 45 (2), Vet Ital www.izs.it/vet_italiana © IZS A&M 2009
Escherichia coli constituted 4.5% of the bacterial
isolates and its highest prevalence was
observed on surgical tables and equipment
trays. E. coli also belongs to the family
Enterobacteriacae. It is a normal component of
the flora in the large intestine of warm‐
blooded animals including humans. This
organism occurs in appreciable numbers of
veterinary clinics of which its source is the
faecal material of animals being presented for
one treatment or another, coupled with the
unhygienic condition of the environment.
Other bacterial isolates incriminated in this
study include: Staphylococcus
(4.5%), Citrobacter sp. (2.3%), Klebsiella sp.
(2.3%), Lactobacillus sp. (2.3%), Micrococcus sp.
(2.3%), Pasteurella sp. (2.3%), Proteus sp. (2.3%)
and Yersinia sp. (2.3%). These are also very
important organisms that survive in the
practice environment as a result of improper
hygienic practices.
epidermidis
This study also revealed that the degree of
contamination varies between the premises
sampled (Table I). The highest prevalence of
bacterial isolates (40.9%) was observed in the
State Veterinary Clinic; this is followed by the
Large Animal Clinic of the UDUVTH which
had a prevalence of 38.6%. The Small Animal
Clinic of the UDUVTH was observed to have
the lowest prevalence (20.5%), which may be
due to the fact that in the Small Animal Clinic,
more sterilisation/disinfection measures are
employed in comparison with the Large
Animal Clinic and the State Veterinary Clinic.
The frequency of infectious agents in the
facilities was also recorded (Table II). It was
observed that surgical packs and equipment
trays, with a prevalence of 27.3% and 25%,
respectively, are the two major sources of
infection to both patients and personnel. This
is then followed by surgical tables and
examination tables, each of which had a
prevalence rate of
drapes/towels revealed the lowest prevalence
(11.4%).
18.2%. Surgical
To minimise and control the risk of contracting
and disseminating zoonotic
practitioners and nosocomial infections to
diseases to
visiting animal patients, we recommended the
following:
? all clinicians should strictly adhere to the
standard veterinary precautions at all times
? each setting should formulate an infection
control plan tailored for its practice
? adequate hospital disinfectants, necessary
safety equipment and a clean water supply
should be standardised in all hospitals
? staff education and training, especially on
the appropriate use of hospital disinfectants
and cleaning procedures,
implemented
? public health veterinarians
encouraged to implement client education
programmes that will contribute to the
protection of clients and their children from
contracting zoonoses
? since both patients and veterinarians are at
increased risk of contracting nosocomial and
zoonotic infections, respectively, specific
guidelines, both
veterinarians, infection control and general
guidelines with protocols for reporting
accidents should be instituted in every
health care setting
? further studies and the use of improved
methodologies for
antibiograms and molecular characterisation
of isolates should be conducted to lead to a
better understanding of their biology which
may help in developing more effective
infection control measure(s).
should be
should be
for animals and
bacterial speciation,
Conclusion
In conclusion, samples collected and analysed
in this study showed that the veterinary
hospitals in Sokoto are heavily contaminated
with bacteria, among which most are zoonotic
and hence are of serious public health
significance and can be considered nosocomial
hazards.
Further studies on the acceptable contamin‐
ation thresholds per ingestion for each of the
different pathogens isolated, together with
their antibiogram to determine possible
resistance, are recommended. The latter is
required due to the fact that the presence of
resistant pathogens in hospital premises has
Page 7
Faruk M. Tambuwal, Aminu Shittu, Mika’il B. Abubakar,
Mohammed D. Salihu, Abdulkadir U. Junaidu,
Abdullahi A. Magaji, Mohammed Lawal & Mahmud Danyaro
A survey of veterinary hospitals in Nigeria for the presence
of some bacterial organisms of nosocomial and zoonotic potential
© IZS A&M 2009 www.izs.it/vet_italiana Vol. 45 (2), Vet Ital
241
implications for animal husbandry and the
transfer of antibiotic‐resistant bacteria to
humans (13) and other visiting patients. The
evidence of the presence and prevalence of
other non‐bacterial pathogens should be
studied, especially in practices involved in the
handling of pets as they offer significant
benefits to our society and ownership of pets is
associated with health hazards due to close
companionship (5, 14).
Acknowledgments
This first phase of the study was conducted to
establish evidence of bacterial organisms after
complaints had been received from local
veterinarians who contracted infections from
their practice premises. The aim was to
develop guidelines for infection control on
those premises. We
Professor Otor J. Uko and Dr Abdulkadir U.
Junaidu, the former and current Directors of
the UDUVTH, respectively, for their support
of this study.
are grateful to
References
1. Abram S.B. 1990. Staphylococcal food poisoning, Bacillus cereus food poisoning: control of
communicable disease in man, 15th Ed. An official report of the American Public Health Association
(APHA). APHA, Washington, DC , 171, 177.
2. Barrow G.I. & Feltham R.K.A. (eds) 1993. C owan & Steel’s Manual for the identification of medical
bacteria, Third Ed. C ambridge University Press, C ambridge, 26, 27, 31, 32, 36.
3. Elliotson J . 1930. On the glanders in the human subject. Medico-C hirurgical Transactions, 16, 171-218.
4. Gabel C .L. & Gerberich S.G. 2002. Risk factors for injury among veterinarians. Epidemiology, 13 (1),
80-86.
5. Geffray L. 1999. Infections associated with pets [in French]. Rev Med Interne, 20 (10), 888-901.
6. J eyaretnam J ., J ones H. & Phillips M. 2000. Disease and injury among veterinarians. Aust Vet J , 78,
625-629.
7. Landercasper J ., C ogbill T.H., Strutt P.J . & Landercasper B.O. 1988. Trauma and the veterinarian.
J Trauma, 28, 1255-1259.
8. Langley R.L., Pryor W.H. & O’Brien K.F. 1995. Health hazards among veterinarians: a survey and
review of the literature. J Agro Med, 2, 23-52.
9. Loir Y.L., Baron F. & Gautier M. 2003. Staphylococcus aureus and food poisoning. Genet Mol Res,
2 (1), 63-76.
10. Marcus L. 1998. Nosocomial zoonoses. New Engl J Med, 338 (11), 757-759.
11. National Association of State Public Health Veterinarians, Inc. (NASPHV) 2005. C ompendium of
measures to prevent diseases associated with animals in public settings. MMWR, 25 March 2005,
54 (RR04), 1-12 (www.cdc.gov/mmwr/preview/mmwrhtml/rr5404a1.htm accessed on 26 May 2009).
12. Neinhaus A., Skudlic C . & Seidler A. 2005. Work-related accidents and occupational diseases in
veterinarians and their staff. Int Arch Occup Environ Health, 78 (3), 230-238.
13. Piddock L.J .V. 1996. Does the use of antimicrobial agents in veterinary medicine and animal
husbandry select antibiotic-resistant bacteria that infect man and compromise antimicrobial
chemotherapy? J Antimicrob C hemother, 38, 1-3.
14. Plaut M., Zimmerman E.M. & Goldstein R.A. 1996. Health hazards to humans associated with
domestic pets. Annu Rev Public Health, 17, 221-245.
15. Quinn P.J ., Markey B.K., C arter M.E., Donnelly W.J . & Leonard F.C . 2002. Veterinary microbiology and
microbial disease. Blackwell Science Ltd, London, 49, 73.
16. Talan D.A., C itron D.M., Abrahamian F.M., Moran G.J . & Goldstein E.J .C . 1999. Bacteriologic analysis
of infected dog and cat bites. N Engl J Med, 340, 85-92.
17. Wenzel R., Bearman G., Brewer T. & Butzler J .-P. 2008. A guide to infection control in the hospital,
4th Ed. International Society for Infectious Diseases, Boston, Massachusetts, 1.