Apstrakt
Background: The poultry industry is important in
boosting food security in a population; however, the
poultry environment and products can serve as
channels of antimicrobial resistant pathogens via the
food chain portending a health risk to humans and
the environment. This study investigated the
prevalence, antimicrobial resistance and virulence of
Proteus species from the feed, drinking water and
eggshells of four selected poultry farms in Lafia,
Nasarawa State.
Methodology: Farm samples (n =216) comprising
feed (64), drinking water (64) and swabs from
eggshells (88) were collected and processed for
isolation of Proteus species using standard
bacteriological methods. The antibiotics
susceptibilities of isolates to ten (10) commercial
antibiotics and carriage of three (3) virulence genes
(rsbA, ureC and luxS) were investigated using disc
diffusion test and Polymerase Chain Reaction,
respectively. Statistical significance difference among
the farms, sample types and Proteus species were
calculated using one-way ANOVA.
Results: Of the total samples studied, 34.26% (74/
216) were positive for Proteus species. Proteus
species were more prevalent in drinking water
samples (37.84%; 28/74) and feed samples (33.78%;
25/74) and least prevalent in eggshells (28.38%; 21/
74). Proteus species (n= 74) comprised P. mirabilis
78% (58/74) and Proteus vulgaris 22% (16/74) with
- mirabilis more predominant than P. vulgaris in
all the four farms sampled. The prevalence rate of
Proteus species was not statistically significantly
different (p > 0.05) among the farms, sample types,
and species. Isolates were 100% susceptible to
Amikacin and exhibited the highest resistance
(25.7%) to tetracycline. Molecular characterization
of the virulence genes of Proteus species revealed
the presence of luxS genes in P. vulgaris and rsbA
and ureC genes in P. mirabilis and P. vulgaris.
Conclusions: The overall prevalence rate of Proteus
species was low (34.26%) in the samples collected
and majority of the isolates were susceptible to the
antibiotics tested. Nonetheless, the level of resistance
to the antibiotics tested and carriage of virulence
genes is indicative of a significant health risk to the
consumers from transmission of Proteus species via
the food chain.
Reference
Bettridge JM, Lynch SE, Brena MC, et al.
Infection-interactions in Ethiopian village
chickens. Prev. Vet. Med. 2014; 117: 358–366.
https://doi.org/10.1016/j.prevetmed.2014.07.002.
Foti M, Rinaldo D., Guercio A., et al. Pathogenic
microorganisms carried by migratory birds
passing through the territory of the island of
Ustica, Sicily (Italy), Avian Pathol. 2011; 40 :405–
https://doi.org/10.1080/03079457.
588940.
Menghistu HT, Rathore R, Dhama KRK and
Agarwal K. Isolation, Identification and
Polymerase Chain Reaction (PCR) Detection of
Salmonella Species from Field Materials of
Poultry Origin. Int. J. Microbiol. Res. 2011. 2:
–142.
Lei CW, Zhang AY, Liu BH, et al. Molecular
characteristics of Salmonella genomic island 1
in Proteus mirabilis isolates from poultry farms
in China. Antimicrob. Agents Chemother. 2014;
: 7570–7572. https://doi.org/10.1128/
AAC.03992-14.
Ram P, Rao V, Rao S, Subramanyam KV and
Srinivas K. Prevalence and virulence gene
profiles of Proteus mirabilis isolated from
animal, human and water samples in Krishna
District, Andhra Pradesh, India, ~ 19 ~ Pharma
Innov. J. 2019; 8:19–23.
www.thepharmajournal.com (accessed
December 1, 2020).
Firildak G, Asan A and Goren E. Chicken
Carcasses Bacterial Concentration at Poultry
Slaughtering Facilities, Asian J. Biol. Sci. 2015;
:16–29. https://doi.org/10.3923/ajbs.2015.16.29.
Jambalang AR, Buys EM and F.S. Botha,
Bacterial species from retailed poultry eggs in
Tshwane, South Africa: Implication for
consumers, S. Afr. J. Sci. 113 (2017) 29–36.
Awad-Alla ME, Abdien HMF and Dessouki AA.
Prevalence of bacteria and parasites in White
Ibis in Egypt, 2010; Vet. Ital. 46: 277 - 286.
Tonkić M, Mohar B, Šiško-Kraljević K, et al.
High prevalence and molecular characterization
of extended-spectrum β-lactamase-producing
Proteus mirabilis strains in Southern Croatia, J.
Med. Microbiol. 2010; 59:1185–1190. https://
doi.org/10.1099/jmm.0.016964-0.
Barua H, Biswas PK, Olsen KEP, Shil SK and
Christensen JP. Molecular Characterization of
Motile Serovars of Salmonella enterica from
Breeder and Commercial Broiler Poultry Farms
in Bangladesh, PLoS One. 2013; 8 e57811. https:/
/doi.org/10.1371/journal.pone.0057811.
Lima-Filho JV, Martins LV, Nascimento de ODC,
et al. Evêncio-Neto J. Zoonotic potential of
multidrug-resistant extraintestinal pathogenic
Escherichia coli obtained from healthy poultry
carcasses in Salvador, Brazil, Brazilian J. Infect.
Dis. 2013; 17 54–61. https://doi.org/10.1016/
j.bjid.2012.09.004.
Armbruster CE, Smith SN, Yep A and Mobley
HLT. Increased incidence of urolithiasis and
bacteremia during Proteus mirabilis and
Providencia stuartii coinfection due to
synergistic induction of urease activity, J. Infect.
Dis. 2014; 209 1524–1532. https://doi.org/
1093/infdis/jit663.
Moosavy M, Esmaeili S, Amiri F, et al. Detection
of Salmonella spp in commercial eggs in Iran.
; 7: 50 -54.
Al Momani W, Janakat S and Khatatbeh M.
Bacterial contamination of table eggs sold in
Jordanian markets. Pakistan J. Nutr. 2017; 17
–20.
Salihu YIMD. Evaluation of microbial contents
of table eggs at retail outlets in Sokoto metropolis,
Nigeria, Sokoto J. Vet. Sci. 2015;13: 22–28.
Ebringer A and Rashid T. Rheumatoid arthritis is
caused by a Proteus urinary tract infection,
APMIS. 2014; 122: 363–368. https://doi.org/
1111/apm.12154.
MC Owoseni, O Oyigye, B Sani, J Lamin and A Chere
Jacobsen SM, Stickler DJ, Mobley HLT and
Shirtliff ME. Complicated catheter-associated
urinary tract infections due to Escherichia coli
and Proteus mirabilis. Clin. Microbiol. Rev.
; 21: 26–59. ttps://doi.org/10.1128/
CMR.00019-07.
Food And Agriculture Organization (Fao), Drivers,
Dynamics And Epidemiology Of Antimicrobial
Resistance In Animal Production, Fao, 2016.
www.fao.org/publications (accessed December
, 2020).
Nahar A, Siddiquee M, Nahar S, et al. Multidrug
Resistant-Proteus Mirabilis Isolated from
Chicken Droppings in Commercial Poultry
Farms: Bio-security Concern and Emerging
Public Health Threat in Bangladesh, J. Biosaf.
Heal. Educ. 2014; 2: 120.
Pathirana HNKS, De Silva BCJ, Wimalasena
SHMP, Hossain S and Heo GJ. Comparison of
virulence genes in Proteus species isolated from
human and pet turtle. Iran. J. Vet. Res. 2018;
: 48–52. https://doi.org/10.22099/
ijvr.2018.4768.
Trivedi MK, Banton A, Trivedi, D, et al.
Phenotyping and Genotyping Characterization of
Proteus vulgaris After Biofield Treatment. Int.
J. Genet. Genomics. 2015; 3 (6): 66 -67.
Mohamed T, Zhao S, White DG and Parveen S.
Molecular characterization of antibiotic resistant
Salmonella Typhimurium and Salmonella
Kentucky isolated from pre- and post-chill whole
broilers carcasses, Food Microbiol. 2014 38: 6–
https://doi.org/10.1016/j.fm.2013.08.002.
Aboh EA, Giwa FJ and Giwa A. Microbiological
assessment of well waters in Samaru, Zaria,
Kaduna, State, Nigeria, Ann. Afr. Med. 2015;
: 32. https://doi.org/10.4103/1596-3519.148732.
Taga ME, Semmelhack JL and Bassier BL. The
LuxS-dependent autoinducer AI-2 controls the
expression of an ABC transporter that functions
in AI-2 uptake in Salmonella typhimurium. Mol.
Microbiol. 2001; 42 (3): 777 -793.
Różalski A, Torzewska A, Moryl M, et al.
Proteus sp. – an opportunistic bacterial pathogen
– classification, swarming growth, clinical
significance and virulence factors, Folia Biol.
Oecologica. 2012; 8:1–17. https://doi.org/
2478/fobio-2013-0001.
Esther Chat M and John Dadah A, Uba A.
Isolation of Enteric Bacteria from Various
Sources in Selected Poultry Farms in Kaduna
State, Bioprocess Eng. 2019; 3 1. https://doi.org/
11648/j.be.20190301.11.
Naing L, Winn T and Rusli BN. Practical Issues
in Calculating the Sample Size for Prevalence
Studies. Archives of Orofacial Sciences. 2006;
:9-14.
Suresh T, Hatha AAM, Sreenivasan D, Sangeetha
N and Lashmanaperumalsamy P. Prevalence and
antimicrobial resistance of Salmonella
enteritidis and other salmonellas in the eggs and
egg-storing trays from retails markets of
Coimbatore, South India, Food Microbiol. 2006.
: 294–299. https://doi.org/10.1016/
j.fm.2005.04.001.
Office International des Epizooties (OIE), Manual
Of Diagnostic Tests And Vaccines For Terrestrial
Animals, 7th ed., Paris, 2012. www.oie.int
(accessed December 1, 2020).
Cheesbrough M. District Laboratory Practice in
Tropical Countries, Part 2 Second Edition, 2006.
Clinical and Laboratry Standards Institutes.
Performance Standards for Antimicrobial
Susceptibility Testing CLSI supplement M100S,
Abbas KF, Al Khafaji JK and Al-Shukri MS.
Molecular Detection of Some Virulence Genes
in Proteus mirabilis Isolated from Hillaprovince,
Int. J. Res. Stud. Biosci. 2015; 3: 85–89.
www.arcjournals.org (accessed December 1,
.
Barbour EK, Hajj ZG, Hamadeh S, et al.
Comparison of phenotypic and virulence genes
characteristics in human and chicken isolates of
Proteus mirabilis, Pathog. Glob. Health. 2012.
: 352–357. https://doi.org/10.1179/
Y.0000000042.
Ubiebi C. Isolation And Identification Of Bacterial
Isolates From Poultry And Fish Feeds Sold In
Abraka, Delta State, Nigeria, J. Ind. Technol. 2017;
Oyinloye JMA, Amiolemhen OI and Ibitayo AO.
Antibiotic profile of some bacteria from poultry
feed and faeces in Ado Ekiti, J. Microbiol.
Biotech. Res. 2015; 5 (5): 1-6.
Kuznetsova MV, Afanasievskaya EV, Pokatilova
MO, Kruglova AA and Gorovitz ES. Diversity
and antibiotic resistance of enterobacteria isolated
from boilers in a poultry farm of Perm Krai: A
-year study, Agric. Biol. 2019; 54: 754–766.
Ponce-de-Leon A, Rodriguez-Noriega E, MorfinOtero R, et al. Antimicrobial susceptibilty of
gram-negative bacilli isolated from intraabdominal amd urinary tract infections in Mexico
from 2009 to 2015: Results from the study for
Monitoring Antimicrobial Resistance Trends
(SMART). PLoS ONE 2018; 13 (6): e0198621.
https://doi.org/10.1371/journal.pone.0198621.
Ayandiran T O, Falgenhaur L, Schmiede J,
Chakraborty T and Ayeni FA. High resistance
to tetracycline and ciprofloxacin in bacteria
isolated from poultry farms in Ibadan, Nigeria.
The J. Infec. Dev. Ctries. 2018; 12 (6): 462 –
doi:10.3855/jidc.9862.
Tesfaye H, Alemayehu H, Desta AF and Eguale
T. Antimicrobial susceptibilty profile of selected
enterobacteriaceae in wastewater samples from
health facilities, abbatoir, downstream rivers and
a WWTP in Adiss Ababa, Ethopia. Antimicrob
resis Inf Cont. 2019; 8 (134): 2 - 11.
Dadheech T, Vyas R and Rastog V. Antibiotic
resistance of aerobic bacterial isolates of Proteus
mirabilis from sick layer chickens infected with
septicaemia and salpingitis in Ajmer region of
Rajasthan. World J. Pharm. Pharm. Sci. 2015;
: 2002–2011.
Nair MS, Upadhyaya I,. Amalaradjou MAR and
Venkitanarayanan K. Antimicrobial Food
Additives and Disinfectants, in: Foodborne
Pathog. Antibiot. Resist., John Wiley & Sons,
Inc., Hoboken, NJ, USA, 2017: pp. 275–301.
https://doi.org/10.1002/9781119139188.ch12.
Landers TF, Cohen B, Wittum TE. and Larson
EL. A review of antibiotic use in food animals:
Perspective, policy, and potential, Public Health
Rep. 2012; 127 4–22. https://doi.org/10.1177/
Okonko I, Nkang A, Eyarefe O, et al. Incidence
of Multi-Drug Resistant (MDR) Organisms in
Some Poultry Feeds Sold in Calabar Metropolis,
Br. J. Pharmacol. Toxicol. 2010; 1:15–28.
Hasan B, Faruque R, Drobni M, et al. High
Prevalence of Antibiotic Resistance in Pathogenic
Escherichia coli from Large- and Small-Scale
Poultry Farms in Bangladesh, Avian Dis. 2011;
: 689–692. https://doi.org/10.1637/9686-
-Reg.1.
Mohammed SO, Ahmed ES, Hafez EE, Khalid A
and Elshahaby OA. Characterization and
Purification of Urease Enzyme From New
Proteus mirabilis Strain, J. Adv. Sci. Res. 2014;
(4): 8 -11.
Alatrash AKM and Al-Yassen AK. Detection of
urer and urec among Proteus mirabilis. Asian
Journ. Pharm. Clin. Res. 2017; 10(8). DOI: http:/
/dx.doi.org/10.22159/ajpcr.2017.v10i8.18987.
Sun Y, Wen S, Zhao L, et al. Association among
biofilm formation, virulence gene expression, and
antibiotic resistance in Proteus mirabilis isolates
from diarrhetic animals in Northeast China, BMC
Vet. Res. 2020; 16: 176. https://doi.org/10.1186/
s12917-020-02372-w.
Różalski A, Torzewska A, Moryl M, et al. Proteus
sp. – an opportunistic bacterial pathogen –
classification, swarming growth, clinical
significance and virulence factors. Folia Biol.
Oecologica 2012; 8, 1–17. https://doi.org/
2478/fobio-2013-0001.