Polytechnic Journal. 2019.

9(2): 86-92
ISSN: 2313-5727
http://journals.epu.edu.iq/index.php/polytechnic

RESEARCH ARTICLE

Isolation, Identification, and Antibiotics Susceptibility

Determination of Proteus Species Obtained from
Various Clinical Specimens in Erbil City
Treska Dh. Kamil1,2*, Sanaria F. Jarjes2
1
Department of Biology, College of Science, Cihan University - Erbil, Iraq, 2Department of Medical Laboratory Technology, Erbil Health
Technical College, Erbil Polytechnic University, Kurdistan Region - Iraq

*Corresponding author: ABSTRACT

Treska Dh. Kamil,
Department of Biology, Fifty-two Proteus isolates, (47) Proteus mirabilis, (4) Proteus vulgaris, and (1) Proteus hauseri are being
College of Science, Cihan isolated from (200) clinical specimens taken from patients admitted to different hospitals in Erbil city/
University - Erbil, Iraq. Kurdistan region of Iraq. Specimens were of urine, wounds swabs, burn swabs, vaginal swabs, ear swabs,
E-mail: treska.dhia95@ eye swabs, and sputum. All isolates were identified depending on cultural, morphological, biochemical
gmail.com
characteristics, and confirmatory VITEK 2 system. Furthermore, VITEK 2 (antibiotic susceptibility testing)
panel was used to determine the antibiotic susceptibility of Proteus isolates, and the results showed that
Received: 29 August 2019 all isolates were entirely resistant to tetracycline and tigecycline (100%), but sensitive to meropenem.
Accepted: 18 November 2019 Furthermore, the present study reported a case of rare Proteus species – P. hauseri – isolated from
Published: 01 December
a patient with urinary tract infection in Erbil City which characterized by no swarming on blood agar.
2019
Keywords: Antibiotic resistance; Erbil city; Proteus hauseri; Proteus species; VITEK 2
DOI
10.25156/ptj.v9n2y2019.pp86-92

INTRODUCTION The most defining microbiologic characteristic of Proteus

species is their swarming phenomenon, a multicellular
The genus Proteus is a Gram-negative rod-shaped bacterium differentiation process of short rods to elongated swarmer
belongs to the Enterobacteriaceae family, where it is placed cells. It allows the population of bacteria to migrate on
in the tribe Proteeae, together with the genera Morganella and a solid surface. Swarming appears macroscopically as
Providencia (Rosalski et al., 2012). Since this genus was first concentric rings of growth emanating from a single colony
described in 1885 by German microbiologist Gustav Hauser, or inoculum (Jacobsen et al., 2008).
Proteus, and in particular Proteus vulgaris, has undergone a
number of major taxonomic revisions (O’Hara et al., 2000a). Microorganisms belonging to genus Proteus are widely
distributed in the natural environment. They can be found
In1982, Hickman et al. separated P. vulgaris into three in polluted water, in soil, and manure, where they play an
biogroups on the basis of indole production. Biogroup one important role in decomposing organic matter of animal
was indole negative and represented a new species, Proteus origin. Besides, the saprophytic mode of life in the natural
penneri, while biogroups two and three remained together as environment and in the intestines of humans and animals,
P. vulgaris. The studies of O’Hara et al. (2000b) confirmed Proteus species, under favorable conditions, are able to cause
the existence of four genomospecies within P. vulgaris a variety of opportunistic nosocomial infections (Feglo et al.,
biogroup 3, which were called Proteus genomospecies 3, 4, 2010). This pathogen has a diverse mode of transmission and
5, and 6. These authors have proposed that genomospecies hence can cause infection in different anatomical sites of the
three be named Proteus hauseri. body (Nita et al., 2014), including those of the urinary tract
(causes complicated UTIs with a higher frequency compared
Currently, the genus Proteus consists of five species: Proteus to other uropathogens and formation of urinary stones),
mirabilis, P. vulgaris, P. penneri, P. hauseri, and Proteus myxofaciens, respiratory tract, ear, nose, skin, burns, and wounds, it may
as well as three unnamed Proteus genomospecies (O’Hara also cause gastroenteritis (Jacobsen et al., 2008).
et al., 2000b). P. myxofaciens is the only Proteus species
without any significance in the pathogenicity of humans The constant increase in the antibiotic resistance of clinical
(Janda et al., 2006). bacterial strains has become an important clinical problem

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 Kamil and Jarjes

(Adamus-Bialek et al., 2013). The evolution and spread of The isolates were processed as per the manufacturer’s
various mechanisms of antimicrobial resistance among instructions for ID and AST. The results were interpreted
common human pathogenic members of Enterobacteriaceae using VITEK 2 software version 08.01, and final results
are of increasing concern and lead to narrowing of available were obtained automatically.
therapeutic options (Boucher et al., 2009). However, the
multidrug-resistant strains of Proteus species have also been
RESULTS
reported worldwide (Singla et al., 2015). They have the ability
to resist several different types of antibiotics and called multi Isolation of Proteus Species
antibiotic resistant (Dadheech et al., 2015). Out of 200 clinical specimens of different infection
sources, 52 isolates (26%) were identified as Proteus spp.
Therefore, this study is concerned with isolation and They were isolated from 35  (28.45%) urine samples,
identification (ID) of Proteus species from various clinical 9 (36%) wound swabs, 5 (27.77%) burn swabs, 2 (33.33%)
samples taken from patients admitted to main hospitals vaginal swabs, and 1 (20%) sputum cultures, while results
in the Erbil City/Kurdistan region of Iraq, as well as showed complete absence of isolates from eye and ear
determination the susceptibility patterns of these isolates swabs [Table 1].
to different antibiotics.
The percentages of Proteus spp. isolated from various
MATERIALS AND METHODS clinical specimens are presented in Figure 1. Of (52) Proteus
isolates, Proteus mirabilis was the most common isolate
Samples Collection accounting for 47 (90.4%), followed by P. vulgaris 4 (7.7%)
Two hundred clinical specimens were collected aseptically and only one isolate (1.9%) of P. hauseri, were isolated.
from patients with symptomatic infections admitted to
different hospitals in Erbil City (Erbil Teaching Hospital, West Identification of Proteus Isolates
Erbil Emergency Hospital, CMC Hospital, and PAR Hospital) The isolates were first identified as related to the genus
during the period from October 1, 2018, to April 1, 2019. Proteus by swarming phenomenon on blood agar, the
Specimens were of urine samples (123), wounds swabs (25), cultures’ characteristic smell, and the pale appearance of
bacteria (non-lactose fermenting) on the MacConkey agar.
burn swabs (18), vaginal swabs (6), ear swabs (8), eye swabs
(15), and sputum (5). The specimens were directly inoculated in
Tryptone Soya Broth and streaked onto MacConkey agar and 1.90%
blood agar plates and incubated aerobically at 37°C for 24 h. 7.70%

Identification of the Isolates

P. mirabilis
Isolates were identified depending on cultural,
P. vulgaris
morphological, biochemical characteristics (Betty et al.,
2007), and confirmatory VITEK 2 system using (ID) GN 90.40% P. hauseri
cards (bioM´erieux Inc. USA).

Antibiotic Susceptibility Testing (AST)

AST-N326 panels (bioM´erieux Inc. USA) were used to Figure 1: Percentage of Proteus species isolated from different
determine the antibiotic susceptibility. specimens

Table 1: Isolation source and percentage of Proteus isolates

Isolation source Number of samples Number of Proteus spp. Isolated Total number of Proteus Percentage of Proteus
per source isolates per source isolates per source
P. mirabilis P. vulgaris P. hauseri
Urine 123 33 1 1 35 28.45
Wounds 25 6 3 0 9 36.00
Burns 18 5 0 0 5 27.77
Eye 15 0 0 0 0 0.00
Ear 8 0 0 0 0 0.00
Vagina 6 2 0 0 2 33.33
Sputum 5 1 0 0 1 20.00
Total 200 47 4 1 52 26.00
P. mirabilis: Proteus mirabilis, P. vulgaris: Proteus vulgaris, P. hauseri: Proteus hauseri

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 Kamil and Jarjes

Also by microscopic examination of the bacteria, which For confirmation of the results, VITEK 2 system (ID) GN
appeared as straight rods and Gram negative when it stained cards were used and the results are indicated in Table 3.
with Gram stain.
Antibiotic Susceptibility Determination of Proteus
Several conventional biochemical tests were done to Isolates
characterize the suspected Proteus isolates. The results The susceptibility patterns of the Proteus isolates are
indicated that these isolates were belonged to three Proteus presented in Table 4. It was found that the more effective
species; P. mirabilis, P. vulgaris, and P. hauseri. All the (52) antibiotic against isolates was the Meropenem, where all
Proteus isolates showed positive results to the catalase, Proteus isolates were sensitive to it. Adversely, the less
urease, and motility, but were negative to citrate and oxidase effective antibiotics were tetracycline and tigecycline
test. Forty-seven of the (52) Proteus isolates gave clearly when they were resisted by all isolates. However, the
negative results for indole and salicin fermentation tests and effect of other antibiotics was variable among the Proteus
considered as P. mirabilis. On the other hand, P. vulgaris was isolates.
represented by (4) isolates when such isolates gave positive
results to indole and salicin fermentation tests. However, Antibiotic resistance profile [Figure  2] revealed that
only one isolate gave a positive result for the indole test generally a vast of resistance was detected among
and negative for the salicin fermentation test and P. hauseri the P. mirabilis isolates against the antibiotics used. It
was suspected [Table 2]. was found that out of (47) P. mirabilis isolates, 100%
resistance property was found to piperacillin, aztreonam,
Table 2: The biochemical identification results of Proteus tetracycline, and tigecycline; more than 90% resistance to
isolates obtained by conventional tests piperacillin\tazobactam, ceftazidime, cefepime, imipenem,
Test Proteus isolates
ciprofloxacin, and trimethoprim/sulfamethoxazole; and
P. mirabilis* P. vulgaris P. hauseri
(n=47) (n=4) (n=1)
about 70% or less resistance pattern was identified to
Oxidase − − − netilmicin, tobramycin, and levofloxacin.
Catalase + + +
Urease + + + This study also observed resistance of P. vulgaris isolates
SIM test to tetracycline and tigecycline (100%), aztreonam and
H2S Production + + + netilmicin (75%), cefepime and levofloxacin (50%),
Indole − + + cefotaxime, amikacin, and ciprofloxacin (25%), while all
Motility + + + P. vulgaris isolates were sensitive to other tested antibiotics.
Salicin fermentation − + −
Citrate − − − On the other hand, P. hauseri isolate was found to be
*n: Number of isolates, −: A negative result, +: A positive result.
P. mirabilis: Proteus mirabilis, P. vulgaris: Proteus vulgaris,
resistant to piperacillin, ceftazidime, aztreonam, imipenem,
P. hauseri: Proteus hauseri tetracycline, and tigecycline, as illustrated in Figure 2.

100
90
Resistance percentage (%)

80
70
60
50
40
30
20
10
0

p. mirabilis

p. vulgaris

P. hauseri

Antibiotics

Figure 2: Antibiotic resistance profile of isolated Proteus species

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 Kamil and Jarjes

Table 3: The biochemical identification results of Proteus isolates obtained with (ID) GN cards of VITEK 2 system
Well No. Symbol/Test P. mirabilis P. vulgaris P. hauseri
2 Ala‑Phe‑Pro‑ARYLAMIDASE − − −
3 ADONITOL − − −
4 L‑Pyrrolidonyl‑ARILAMIDASE − − −
5 L‑Arabitol − − −
7 D‑CELLOBIOSE − − −
9 BETA‑GALACTOSIDASE − − −
10 H2S PRODUCTION + + +
11 BETA‑N‑ACETYL‑GLUCOSAMINIDASE − − −
12 GlutamylArylamidase pNA − − −
13 D‑Glucose + + +
14 GAMMA‑GLUTAMYL‑TRANSFERASE + − +
15 FERMENTATION‑GLUCOSE − + +
17 BETA‑GLUCOSIDASE − − −
18 D‑MALTOSE − + +
19 D‑MANNITOL − − −
20 D‑MANNOSE − − −
21 BXYL (BETA‑XYLOSIDASE) − − −
22 BETA‑ALANINEARYLAMIDASE pNA − − −
23 L‑Proline ARYLAMIDASE − − +
26 LIPASE − − −
27 PALATINOSE − − +
29 Tyrosine ARYLAMIDASE − − +
31 UREASE + + +
32 D‑SORBITOL − − −
33 SACCHAROSE/SUCRALOSE − + +
34 d‑TAGATOSE − − −
35 D‑TREHALOSE + − −
36 CITRATE (SODIUM) − − −
37 MALONATE − − −
39 5‑KETO‑D‑GLUCONATE − − −
40 L‑LACTATE alkalinization − − +
41 ALPHA‑GLUCOSIDASE − − +
42 SUCCINATE alkalinization − − +
43 Beta‑N‑ACETYL‑GALACTOSAMINIDASE − − −
44 ALPHA‑galactosidase − − −
45 PHOSPHATASE + − +
46 Glycine Arylamidase − − −
47 ORNITHINE DECARBOXYLASE + − −
48 LYSINE DECARBOXYLASE − − −
49 DECARBOXYLASE bASE − − −
53 L‑HISTIDINE assimilation − − −
56 COUMARATE + + +
57 BETA‑GLUCORONIDASE − − −
58 O/129 RESISTANCE + − +
59 Glu‑Gly‑Arg‑ARYLAMIDASE − − −
61 L‑MALATE assimilation − − +
62 ELLMAN − − +
64 L‑LACTATE assimilation − − −
Other well numbers between 1 and 64 not designated in this table are empty. (−) a negative result, (+) a positive result. P. mirabilis: Proteus mirabilis,
P. vulgaris: Proteus vulgaris, P. hauseri: Proteus hauseri

DISCUSSION Bassam and Al-Kazaz (2013) who indicated that the total
isolation percentage of Proteus spp. from different clinical
Two hundred clinical specimens were screened for specimens was 28.57%, whereas the results were higher
Proteus spp. It was found that 52 isolates (26%) were than those obtained by Feglo et al. (2010); Naz and Rasool
identified as Proteus spp. A near result was recorded by Al- (2013); Ahmed (2015); and Latif et al. (2017) who mentioned

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 Kamil and Jarjes

Table 4: Antibiotic susceptibility patterns of Proteus isolates obtained with AST‑N326 cards of VITEK 2 system
Antibiotics Number of Proteus isolates with susceptibility
P. mirabilis (n=47) P. vulgaris (n=4) P. hauseri (n=1)
S I R S I R S I R
Piperacillin 0 0 47 4 0 0 0 0 1
Piperacillin\tazobactam 2 0 45 4 0 0 1 0 0
Ceftazidime 0 1 46 3 0 1 0 0 1
Cefepime 3 1 43 2 0 2 1 0 0
Aztreonam 0 0 47 1 0 3 0 0 1
Imipenem 2 0 45 4 0 0 0 0 1
Meropenem 47 0 0 4 0 0 1 0 0
Amikacin 44 0 3 3 0 1 1 0 0
Gentamicin 11 35 1 4 0 0 1 0 0
Netilmicin 23 0 24 1 0 3 1 0 0
Tobramycin 19 0 28 4 0 0 1 0 0
Ciprofloxacin 3 1 43 3 0 1 1 0 0
Levofloxcain 13 1 33 2 0 2 1 0 0
Tetracycline 0 0 47 0 0 4 0 0 1
Tigecycline 0 0 47 0 0 4 0 0 1
Trimethoprim/sulfamethoxazole 3 0 44 4 0 0 1 0 0
*n: Number of isolates, S: Sensitive, I: Intermediate, R: Resistant. P. mirabilis: Proteus mirabilis, P. vulgaris: Proteus vulgaris, P. hauseri: Proteus hauseri

that Proteus spp. from clinical specimens represented (8.4%), with many results. This result agreed with similar studies
(12.6%), (19%), and (12.6%), respectively. The reason for conducted by Yah et al. (2001); Jones et al. (2003); Newman
the difference in isolation percentages may be due to the et al. (2006); Feglo et al. (2010); and Pandey and Tyagi
differences in the size of samples, isolation sources, and (2013). In contrast with studies performed by Orett (1999);
number of hospitals surveyed. Reslinski et al. (2005); and Al-Bassam and Al-Kazaz (2013),
which showed Proteus spp. to be more commonly in urine
Of (52) Proteus isolates, 47 isolates (90.4%) of different than in other clinical specimens.
clinical specimens were identified as P. mirabilis. This result
was agreed with Gonzalez and Bronze (2018) who reported In addition, high vaginal swabs from women with
that P. mirabilis causes (90%) of Proteus infections and can symptomatic vaginitis showed an isolation percentage of
be considered a community-acquired infection; Feglo et al. 33.33%. However, the picture is not clear in the case of
(2010) and Al-duliami et al. (2011), who mentioned that Proteus in women with vaginitis due to small numbers of
P. mirabilis is more widespread than P. vulgaris in clinical infected women involved in this study.
infections. Furthermore, Auwaerter (2008) declared that
P. mirabilis is the species most commonly recovered from Furthermore, results showed a complete absence of isolates
humans, especially from urinary and wound infections. It from the eye and ear swabs. This may be due to the season
accounts for 90% of all infections caused by the Proteus of collecting samples and the possible medication taken
species. before sampling.

As per our knowledge, only two articles have been The effect of different antibiotics on Proteus isolates
published regarding the isolation of P. hauseri. The first was investigated. Interestingly, these isolates showed
article was by O Hara et al. (2000b), in which only two cases different susceptibility toward antibiotics used in this
of P. hauseri out of 52 isolates were isolated, and they have study [Table 4]. It has been found that the majority of the
not mentioned whether swarming was present or not. In isolates were multidrug-resistant since they were resistant
the second article, Ostwal et al. (2016) isolated the third to three antibiotics or more. Proteus species can harbor
case of P. hauseri from the stool; there was no swarming numerous plasmid and integron-mediated determinants
on blood agar so that these isolates may be misdiagnosed. of antimicrobial resistance (Hall and Collis, 1998). In
Our P. hauseri isolate also did not show swarming. line with the findings of this study, resistance of Proteus
species (P. mirabilis and P. vulgaris) against antibiotics has
Results showed that the highest percentage of Proteus been reported by Newman et al., 2006; Mordi and Momoh,
isolates from clinical specimens was isolated from wound 2009; Feglo et al., 2010; Bahashwan and El Shafey, 2013;
swabs specimens representing about 36%. Being wound Kibret and Abera, 2014; and Ahmed, 2015. Although
isolates were the highest percentage in the same trend some antibiotics to which Proteus species are known to be

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 Kamil and Jarjes

sensitive, now they appear to be resistant or less effective. Boucher, H. W., G. H. Talbot, J. S. Bradley, J. E. Edwards, D. Gilbert
According to De Francesco et al. (2007), etiology and and L. B. Rice. 2009. Bad bugs, no drugs: No ESKAPE! An
update from the Infectious Diseases Society of America. Clin.
drug resistance change through time as well as may be Infect. Dis. 48(1): 1-12.
due to random and improper use of these antibiotics. Our Dadheech, T., R. Vyas and V. Rastogi. 2015. Antibiotics Resistance
P. hauseri isolate was sensitive to meropenem, amikacin, of aerobic bacterial isolates of Proteus mirabilis from sick layer
ciprofloxacin, gentamicin, trimethoprim/sulfamethoxazole, chickens infected with septicemia and salinities in Ajmer region
and some other antibiotics, whereas the P. hauseri isolate of Rajasthan. World J. Pharm. Pharm. Sci. 4(7): 2002-2011.
of Ostwal et al. (2016) was only sensitive to meropenem. De Francesco, M. A., G. Ravizzola, L. Peroni, R. Negrini and
N. Manca. 2007. Urinary tract infections in Brescia, Italy: Etiology
O’Hara’s P. hauseri isolates were sensitive to amikacin,
of uropathogens and antimicrobial resistance of common
ciprofloxacin, gentamicin, as well as trimethoprim/ uropathogens. Med. Sci. Monit. 13: BR136-BR144.
sulfamethoxazole and resistant to tetracycline, which are Feglo, P. K. S., Y. Gbedema, S. N. A. Quay, Y. Adu-Sarkodie and C. O.
close to some extent with our findings. Okrah. 2010. Occurrence, species distribution and antibitics
resistance of Proteus isolates: A case study at the Komfo
Anokye teaching hospital in Ghana. Int. J. Pharm. Sci. Res. 1(9):
CONCLUSIONS 347-352.
Gonzalez, G. and M. S. Bronze. 2018. Proteus Infections:
In this study, P. mirabilis, P. vulgaris, and P. hauseri are the Background, Pathophysiology, Epidemiology. Available from:
species implicated in Proteus infections in Erbil City. http://www.emedicine.medscape.com/article/226434-overview.
[Last accessed on 2018 Sep 13].
P. mirabilis was predominant species among patients
Hall, R. M. and C. M. Collis. 1998. Antibiotic resistance in gram-
with Proteus infections and wounds recorded the highest negative bacteria: The role of gene cassettes and integrons.
percentage of Proteus isolation. Furthermore, a case of rare Drug Resist. Updat. 1: 109-119.
Proteus species – P. hauseri – isolated from a patient with Hickman, F. W., A. G. Steigerwalt, J. J. 3rd Farmer and D. J. Brenner.
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