Abbasi and Ghaznavi‑Rad BMC Gastroenterol (2021) 21:140

https://doi.org/10.1186/s12876-021-01719-3

RESEARCH ARTICLE Open Access

Quinolone resistant Salmonella species

isolated from pediatric patients with diarrhea
in central Iran
Elnaz Abbasi1 and Ehsanollah Ghaznavi‑Rad1,2,3*

Abstract
Background: This study aimed to investigate the frequency and the antibiotic resistance patterns of Salmonella spe‑
cies that were isolated from infectious diarrhea samples taken from pediatric patients in central Iran.
Methods: The study analyzed 230 stool specimens that were cultured on XLD, MacConkey agar and GN broth. Poly‑
merase chain reaction (PCR) assay was used to identify the Salmonella genus. The antibiotic resistance profiles and the
frequency of quinolone and integron genes were obtained.
Results: Out of 230 samples of infectious diarrhea, 21 (9.1%) cases of Salmonella spp. were identified using culture
methods. Another 28 (12.1%) samples had positive PCR results, with S. serovar Paratyphi B and C (9/21; 42.8%) and S.
Typhi (3/21; 14.3%) being the most recognized. The highest antibiotic resistance rates were found for nalidixic acid
(15/21; 71.4%), tetracycline (9/21; 42.8%). However, six (28.5%) of isolates were found resistant to cotrimoxazole, ampi‑
cillin and chloramphenicol. Among the plasmid-mediated quinolone resistance (PMQR) determinants, qnrS, qnrA, and
qnrB were positive in (9/15; 60%), (6/15; 40%) and (3/15; 20%) of the isolates, respectively. Class 1 and 2 integrons were
identified in 15 (71.4%) and 3 (14.3%) isolates, respectively.
Conclusion: High rates of quinolone resistant and low frequency of MDR Salmonella spp. isolates were identified in
central Iran, similar to findings in other parts of Asia. To prevent the spread of these resistant strains, the antimicrobial
resistance of Salmonella spp. isolates should be under constant surveillance, and empiric antibiotic therapy should be
adapted appropriately.
Keywords: Salmonella spp., Diarrhea, Antibiotic, Quinolone resistance, Iran

Background through enteric dysfunction and the impaired uptake of

Gastroenteritis remains a serious public health prob- macronutrients and micronutrients [2]. Salmonella is a
lem. This common human disease is the second leading common cause of infectious gastroenteritis among the
cause of morbidity and mortality in developing countries, pediatric age group in many developing countries [3].
including Iran, and has a particularly high morbidity in Globally, human salmonellosis causes 200 million to over
children younger than 5 years old (with an estimated 1 billion disease cases annually, with over 150 thousand
525,000 deaths per year worldwide) [1]. Diarrheal dis- of these cases resulting in death [4]. The S. enterica sero-
eases can negatively affect early pediatric growth both vars Typhi (S. Typhi) and Paratyphi (S. Paratyphi A, B
and C) are the most common causes of human salmonel-
*Correspondence: ghaznaviehs@yahoo.com; e.ghaznavirad@arakmu.ac.ir
losis worldwide [5]. Initially, the antimicrobial resistance
1
Department of Microbiology and Immunology, Faculty of Medicine, profiles of these Salmonella serovars were determined
Arak University of Medical Sciences, Arak, Islamic Republic of Iran against the antibiotics of ampicillin, co-trimoxazole
Full list of author information is available at the end of the article

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Abbasi and Ghaznavi‑Rad BMC Gastroenterol (2021) 21:140 Page 2 of 6

(trimethoprim-sulfamethoxazole) and chlorampheni- enterica subsp. enterica serovar Paratyphi B PTCC 1231
col, and bacteria with simultaneous resistance to all and S. Typhi PTCC 1609 were used as controls in each
three types of antibiotics were characterized as multi- assay (obtained from the Iranian Research Organization
drug resistant (MDR) [6]. Currently, MDR typhoid is in for Science and Technology). S. enterica subsp. enterica
decline in the Asian regions, where there is a high level of serovar Paratyphi C control strains were acquired from
resistance to second-line drugs, such as quinolones and the microbiology department of the Arak University of
fluoroquinolones [6]. This increased antimicrobial resist- Medical Sciences.
ance has decreased the number of effective treatment
options and, consequently, increased the treatment costs,
the risk of complications and the death rate, especially in Investigating Salmonella antibiotic resistance by disk
the pediatric age group [3]. diffusion
In the summer, diarrhea and dysentery are so common Using the Clinical and Laboratory Standards Institute
among the pediatric patients at central Iran [7–11]. It is (CLSI) 2017 guidelines [13], an antibiogram assay was
not efficient to identify typhoidal Salmonella in clinical performed on the isolated Salmonella spp. colonies.
detection labs, and specific information about the scale The antibiotic discs contained nalidixic acid (30 μg),
of typhoidal Salmonella in Iran’s central region is not tetracycline (30 μg), cotrimoxazole (25 μg), ampicillin
available. Therefore, this study has been conducted to (10 μg), chloramphenicol (30 μg), cefixime (5 μg), ceftri-
examine in depth the abundance, the phenotypic antimi- axone (30 μg), cefotaxime (30 μg), ceftizoxime (30 μg),
crobial resistance levels and the resistance gene content ceftazidime (30 μg), cefoxitin (30 μg), cefepime (30 μg),
of the region’s Salmonella species by examining diarrhea gentamicin (10 μg), azithromycin (15 μg), ciprofloxacin
samples from patients. (5 μg) and imipenem (10 μg) (Mast Diagnostics, United
Kingdom).
Materials and methods
Sample collection
Genotypic investigations
This study protocol was approved by the ethics com-
DNA extraction
mittee of the Arak University of Medical Sciences
DNA was directly extracted from the fecal samples and
(ARAKMU.REC. 93-176-30 and 1395.83). All methods
the reference Salmonella spp. isolates using the QIAamp
were performed in accordance with the relevant guide-
DNA stool mini kit (Qiagen GmbH, Hilden, Germany),
lines and regulations. For this cross-sectional, descriptive
according to the manufacturer’s protocol. The amount
study, 230 samples of diarrhea were gathered from pedi-
and purity of the extracted DNA were measured with
atric patients who were referred to the Children’s Educa-
a NanoDrop apparatus (Thermo Fisher Scientific,
tional-Therapeutic Center affiliated with Arak University
Waltham. Massachusetts, United States) and confirmed
of Medical Sciences (in the city of Arak, Iran) due to
using the universal primers for the bacterial 16S rRNA
diarrhea from May 2015 to May 2016. The parent/guard-
gene [8].
ian consent form was provided for participants under
16 years old.
The inclusion criteria for this study were as follows: a Genotypic identification
completed consent form and a questionnaire was filled PCR of the inlA gene was performed to confirm the Sal-
out by the patient or the patient’s parents and caregiv- monella genus [14]. PCR of the qnr determinant genes
ers; observation of more than five white blood cells per qnrS, qnrA, and qnrB was performed to amplify the
high-power field (HPF) in a stool specimen [12] and the plasmid-mediated quinolone resistance (PMQR) targets.
patient had not taken antibiotics for a week before con- Mutations in the gyrA and parC genes of the quinolone-
sultation at the hospital. resistant Salmonella spp. isolates were also identified
using DNA sequencing techniques [7]. Sul1,2 for sulfona-
Phenotypic investigation mide resistance and quartenary ammonium compounds
The fecal samples were cultured in Gram-negative (GN) (qac) resistance genes were investigated using PCR
broth, xylose lysine deoxycholate (XLD) and MacConkey method (Table 1) [15].
media (Merck, Hamburg, Germany); then biochemical
and serological tests were performed [7]. Application
programming interface (API) testing (Biomeriux, France) Integron detection
was used to confirm the presence of Salmonella spp. iso- To investigate class 1, 2 and 3 integrons, PCR assay
lated. S. enterica subsp. enterica PTCC 1709, S. enter- was performed as previously described in the literature
ica subsp. enterica serovar Paratyphi A PTCC 1230, S. (Table 1) [7].
Abbasi and Ghaznavi‑Rad BMC Gastroenterol (2021) 21:140 Page 3 of 6

Table 1 The primers used in this study

Target gene description Primer Sequence 5′ → 3’ Amplicon Annealing References
size (bp) temperature

Universal DNA bacterial 16s-rRNA-F16s-rRNA-R 5-AGG​AGG​TGA​TCC​AAC​CGC​A-35-ACC​TGG​AGG​ 367 55 [8]

AAG​GTG​GGG​AT-3
Salmonella spp. invA-FinvA-R 5- TTG​T TA​CGG​C TA​T TT​TGA​CCA-35- CTG​ACT​GCT​ 521 60 [14]
ACC​T TG​C TG​ATG-3
Fluoroquinolone gyrA-FgyrA-R 5-AAA​TCT​GCC​CGT​GTC​GTT​GGT-35-GCC​ATA​CCT​ 344 55 [7]
ACG​GCG​ATA​CC -3
parC-FparC-R 5-CTG​AAT​GCC​AGC​GCC​AAA​T T-35-GCG​AAC​GAT​ 168 55 [7]
TTC​GGA​TCG​TC-3
qnrS-FqnrS-R 5-TGG​AAA​CCT​ACA​ATC​ATA​CAT​ATC​G-3 5-TTA​GTC​ 656 60 [7]
AGG​ATA​AAC​AAC​AAT​ACC​C-3
qnrA-FqnrA-R 5-GAT​AAA​GTT​T TT​CAG​CAA​GAGG-35-ATC​CAG​ATC​ 593 60 [7]
GGC​AAA​GGT​TA-3
qnrB-FqnrB-R 5-GTT​GGC​GAA​AAA​ATT​GAC​AGAA-35-ACT​CCG​ 264 53 [7]
AAT​TGG​TCA​GAT​CG-3
Integrase1 Int1-FInt1-R 5-CAG​TGG​ACA​TAA​GCC​TGT​TC-35-CCC​GAG​GCA​ 160 55 [7]
TAG​ACT​GTA​-3
Integrase2 Int2-FInt2-R 5-TTG​CGA​GTA​TCC​ATA​ACC​TG-35-TTA​CCT​GCA​C TG​ 288 55 [7]
GAT​TAA​GC-3
Integrase3 Int3-FInt3-R 5-GCC​TCC​GGC​AGC​GAC​T TT​CAG-35-ACG​GAT​C TG​ 979 59 [7]
CCA​AAC​C TG​ACT-3
Sulfonamide resistance Sul1-FSul1-R 5-TCA​CCG​AGG​ACT​CCT​TCT​TC-35-CAG​TCC​GCC​ 331 65 [7]
TCA​GCA​ATA​TC-3
Sul2-FSul2-R 5-CCT​GTT​TCG​TCC​GAC​ACA​GA-35-GAA​GCG​CAG​ 435 58 [7]
CCG​CAA​T TC​AT-3
Quaternary ammonium compounds qac-Fqac-R 5-GCC​C TA​CAC​AAA​T TG​GGA​GA-35-CTG​CGG​TAC​ 370 55 [15]
CAC​TGC​CAC​AA-3

Results boy. The clinical symptoms among the people suffering

Of the 230 analyzed samples, 21 (9.1%) and 28 (12.1%) from salmonellosis are given in Table 2.
were found to be positive for Salmonella spp. using the
exclusive culture and PCR methods, respectively. All Phenotypic and genotypic investigation
the culture-positive samples were identified as positive Of the 21 cultured Salmonella spp. isolates, 9 (42.8%)
using PCR; and seven of the samples that were culture- were identified as S. Paratyphi B, 9 (42.8%) were identi-
negative were also identified as positive using PCR. Of fied as S. Paratyphi C, and 3 (14.3%) was identified as S.
the 21 patients (9.1%) afflicted with Salmonella spp., 9 Typhi; no case of S. Paratyphi A was found.
(42.8%) were female and 12 (57.1%) were male, resulting
in a female-to-male infection ratio of 1:1.3. The aver- Phenotypic and genotypic antibiotic resistance
age age of the people afflicted with salmonellosis was determination
4 years and 5 months. The youngest diseased person Using the CLSI 2017 guidelines, the highest resistance
was an 8-month-old girl; the oldest was a 12-year-old rates in Salmonella spp. were observed against nali-
dixic acid (15/21; 71.4%), tetracycline (9/21; 42.8%),

Table 2 Frequency of clinical symptoms in pediatric patients with Salmonella spp.

Salmonella spp. Mucus in the stool Abdominal pain Vomiting Fever Blood in the stool

S. Paratyphi B 9/9 (100%) 9/9 (100%) 6/9 (66.6%) 5/9 (55.5%) 6/9 (66.6%)
S. Paratyphi C 9/9 (100%) 7/9 (77.7%) 3/9 (33.3%) 8/9 (88.8%) 8/9 (88.8%)
S. Typhi 3/3 (100%) 3/3 (100%) 1/3 (33.3%) 3/3 (100%) 3/3 (100%)
S. Paratyphi A – – – – –
Abbasi and Ghaznavi‑Rad BMC Gastroenterol (2021) 21:140 Page 4 of 6

cotrimoxazole (6/21; 28.5%), ampicillin (6/21; 28.5%), differences in climate and many other environmental
and chloramphenicol (6/21; 28.5%) (Table 3). All of the conditions, as well as age differences, and differences in
Salmonella isolates were susceptible to cefixime, ceftri- the level of economic development, the level of individual
axone, cefotaxime, ceftizoxime, ceftazidime, cefoxitin, hygiene, and contamination via food preparers who are
cefepime, gentamicin, azithromycin, ciprofloxacin, and chronic carriers of Salmonella [5].
imipenem. No cases of MDR were observed. All iso- In the present study, the most prevalent Salmonella
lates carrying PMQR contain similar mutations in parC enterica serovar isolates were S. Paratyphi B and S. Para-
at amino acid 80 (replacement of serine with isoleucine; typhi C (42.8%). In other studies, S. Typhi and S. Paraty-
GenBank accession no. HM068910) and gyrA at amino phi B were reported to be the predominant serogroup in
acid 83 (replacement of serine with leucine). The fre- Iran (Tehran) and Ethiopia, respectively [19, 20]. Gen-
quency of antibiotic resistance genes among Salmonella eral hygiene, socioeconomic conditions, and ecological
spp. was given in Table 4. conditions affect the frequency of Salmonella spp. sero-
groups [4].
Discussion Because salmonellosis is spread by food, any informa-
The frequency of salmonellosis, as determined by bacte- tion regarding the frequency and the antimicrobial resist-
rial culture and PCR, was 9.1% and 12.1%, respectively. ance of the isolates is a public health concern [21]. The
Of these two methods, the sensitivity of the PCR method antibiotic resistance properties of Salmonella spp have
was higher [16, 17]. Other studies conducted in Sudan, been reported to vary and be regionally distinct [22]. The
Iran (Tehran), Iraq reported frequencies of 4%, 7%, and present study is the first to report on the frequency of
14.8%, respectively [14, 18, 19]. These differences in salmonellosis and its associated resistance patterns for a
the frequency of salmonellosis may be related to a vari- panel of 16 antibiotics in central Iran.
ety of factors, including exposure to the natural reser- The traditional first-line drugs used to treat Salmo-
voirs of Salmonella species in these geographical areas, nella spp. are chloramphenicol, ampicillin, and cotri-
moxazole [6]. In Iran (Tehran) and Mexico, 11% and
33% of the strains have been reported to be resistant
Table 3 Phenotypic antibiotic resistance rates in Salmonella spp. to chloramphenicol, respectively [3, 23]. In Iran (Teh-
ran), Mexico, and Pakistan 13.5%, 20%, and 66.1% of
Antibiotic Salmonella S. Paratyphi B S. Paratyphi C S. Typhi the strains were found to be resistant to ampicillin
spp. n:9 n:9 n:3
n:21 [23–25]. In Iran (Tehran), Mexico, and Pakistan 23%,
28.8%, and 66.5% of the strains were resistant to cotri-
Nalidixic acid 15 (71.4%) 6 (66.6%) 6 (66.6%) 3 (100%) moxazole, respectively [23–25]. These differences indi-
Tetracycline 9 (42.8%) 5 (55.5%) 2 (22.2%) 2 (66.6%) cate that resistance to Salmonella first-choice agents
Cotrimoxa‑ 6 (28.5%) 2 (22.2%) 3 (33.3%) 1 (33.3%) may be related to presentation from different sources
zole
[26]. In Iran (Tehran), Sul1 was found to be resistant
Ampicillin 6 (28.5%) 4 (44.4%) 1 (11.1%) 1 (33.3%)
in 32% of the strains [3]. In India, Sul1 and Sul2 were
Chloram‑ 6 (28.5%) 3 (33.3%) 2 (22.2%) 1 (33.3%)
phenicol found to be resistant in 100% and 77.7% of the strains,

Table 4 The frequency of antibiotic resistance genes among Salmonella spp.

Resistance Target gene Salmonella spp. S. Paratyphi B S. Paratyphi C S. Typhi

Sulfonamide Sul1 6/6 (100%) 2/2 (100%) 3/3 (100%) 1/1 (100%)
Sul2 3/6 (50%) 2/2 (100%) 1/3 (33.3%) 0%
Fluoroquinolone gyrA 15/15 (100%) 6/6 (100%) 6/6 (100%) 3/3 (100%)
parC 15/15 (100%) 6/6 (100%) 6/6 (100%) 3/3 (100%)
qnrS 9/15 (60%) 4/6 (66.6%) 2/6 (33.3%) 3/3 (100%)
qnrA 6/15 (40%) 2/6 (33.3%) 1/6 (16.6%) 3/3 (100%)
qnrB 3/15 (20%) 2/6 (33.3%) 0% 1/3 (33.3%)
Integrase Int1 15/21 (71.4%) 7/9 (77.7%) 6/9 (66.6%) 2/3 (66.6%)
Int2 3/21 (14.3%) 3/9 (33.3%) 0% 0%
Int3 0% 0% 0% 0%
Quaternary ammonium qac 9/21 (42.8%) 5/9 (55.5%) 3/9 (33.3%) 1/3 (33.3%)
compounds
Abbasi and Ghaznavi‑Rad BMC Gastroenterol (2021) 21:140 Page 5 of 6

respectively [27]. The difference in frequency of sul- Conclusion

fonamide-resistant in different regions mainly relates To reduce and prevent outbreaks of quinolone resistance,
to different antibiotic usage patterns [5]. However, and prevention of the emergence of MDR Salmonella spp.,
MDR Salmonella spp. are a worldwide concern but is a coherent program needs to be developed for the control
not very common [6]. and surveillance of antimicrobial resistance in the long
In Iran (Tehran), Malaysia, and Nigeria, 51.8%, 42%, run. Further, empiric antibiotic therapy should be adapted
and 65.9% of the strains were resistant to tetracycline, appropriately, and Salmonella carriers should be identified
respectively [28–30]. and given specific treatment in order to prevent this trans-
Although quinolone/fluoroquinolones are intended mission route.
to be appropriate drugs against resistant isolates, the
enhancement in antimicrobial resistance is a burden in
Abbreviations
controlling infections caused by Salmonella spp. [31]. PCR: Polymerase chain reaction; DNA: Deoxyribonucleic acid; XLD: Xylose
In the present study, 71.4% of the Salmonella strains lysine deoxycholate; PMQR: Plasmid-mediated quinolone resistance; MDR:
were found to be resistant to nalidixic acid, and none Multi-drug resistant; HPF: High-power field; BLAST: Basic local alignment
search tool.
of the strains was resistant to ciprofloxacin. In Iran
(Tehran), Nigeria, and India, 66.6%, 59%, and 96% of Acknowledgements
the strains were resistant to nalidixic acid, respectively The authors gratefully acknowledge the educational assistance of Arak Uni‑
versity of Medical Sciences due to its financial contributions to and support of
[32–34]. this study.
In this study, qnrS, qnrA, and qnrB were found at
60%, 40%, and 20%, respectively, in nalidixic acid- Authors’ contributions
EGR conceptualized and designed the study. EA were involved in the data
resistant Salmonella strains. In Iran (Tehran), qnrS, collection, generation, and performed data analysis. All authors have read and
qnrA, and qnrB were found at 56.5%, 30.4%, and 1.1% in approved this version of the manuscript.
the strains, respectively [32]. In Brazil, qnrS, qnrB, and
Funding
qnrA were found at 53.3%, 40%, and 0% in the strains, This work was financially supported by the Arak University of Medical Sciences
respectively [31], while in India, qnrB was at 70% and (Grant Number 1395.83 and ARAKMU.REC. 93-176-30). The funder had no role
none of the strains showed resistance to qnrA and qnrS in the design of the study and collection, analysis, and interpretation of data
and in writing the manuscript. This funding is only for purchasing materials in
[35]. Quinolones, and especially fluoroquinolones, are this study. No additional external funding was received for this study.
widely used in poultry farms and in the treatment of
companion animals in Iran, and this contributes to the Availability of data and materials
All data pertaining to this study are within the manuscript in sections sample
risk of resistant zoonotic bacterial agents being spread collection and results. The datasets analyzed and/or used during the current
via the food chain [36]. Generally, studies have deter- study are available from the corresponding author on reasonable request.
mined a direct relationship between quinolone usage
in poultry and the frequency of nalidixic acid-resistant Declarations
Salmonella spp. isolates from humans [37]. Fluoro-
Ethics approval and consent to participate
quinolone resistance is prevalent across Asia, in part This study received ethical approval from the Arak University of Medical
because of the widespread consumption of this class of Sciences (Numbers: 2137 and 2571). Informed consent was obtained from a
antimicrobials [6]. parent and/or guardian for participants under 16 years old. A signed consent
form was obtained from each patient. There was no access to any information
In the current study, qac were found at 42.8% in Sal- that enabled authors to identify individual patients.
monella isolates, while in Iran (Tehran) and Iraq, qac
were found at 31% and 60% in the strains, respectively Consent for publication
Not applicable.
[3, 38].
In Iran (Tehran), int1 (32%), int2 (13%), and int3 (0%) Competing interests
were found in the strains [3], while in Hong Kong, int1 The authors stipulate that they have no conflict of interest in regard to this
study.
was found in 13% of the strains but none showed resist-
ance to int2 and int3 [39]. Of the three categories of Author details
1
integrons pertinent to antimicrobial resistance, the class Department of Microbiology and Immunology, Faculty of Medicine, Arak
University of Medical Sciences, Arak, Islamic Republic of Iran. 2 Molecular
I integron is the most frequently obtained in Gram-neg- and Medicine Research Center, Faculty of Medicine, Arak University of Medical
ative bacteria [40]. The prevalence of integrons in the Sciences, Arak, Islamic Republic of Iran. 3 Department of Medical Laboratory
enterobacteriacae family has been varied and has played Sciences, School of Allied Medical Sciences, Arak University of Medical Sci‑
ences, Arak, Iran.
a significant role in the development of drug-resistant
bacteria [41]. Thus, the high prevalence of antibiotic Received: 30 September 2020 Accepted: 15 March 2021
resistance probably relates to the high prevalence of class
I and II integrons.
Abbasi and Ghaznavi‑Rad BMC Gastroenterol (2021) 21:140 Page 6 of 6

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