Highlights
- •Gram-negative pathogens accounted for 280 (75%) of the total isolates among pilgrims.
- •Klebsiella Pneumoniae having the higher resistance to Augmentin 28(52%) and Ampicillins 55 (95%).
- •Most of the organisms were sensitive Tobramycin except A. Baumanni 3 (50%), E.Coli 4 (57%), and K. Pneumonia 6 (46%) respectively.
Summary
Objective
To identify commonly reported community-acquired organisms and antimicrobial resistance patterns exhibited by Gram-positive and Gram-negative pathogens among pilgrims visiting emergency care departments in Makkah.
Method
The study was designed as a retrospective audit of all patients (pilgrims) admitted to two hospitals and residing in the city of Makkah, Saudi Arabia.
Results
Among 374 isolates, Gram-negative pathogens accounted for 280 (75%), while the remaining 94 (25%) were Gram-positive organisms. Among all isolated pathogens, the highest resistance was observed for amoxicillin–clavulanic acid. Klebsiella pneumoniae had the highest resistance to amoxicillin–clavulanic acid and ampicillin. Most of the organisms were sensitive to tobramycin except Acinetobacter baumannii (n = 3, 50%), Escherichia coli (n = 4, 57%), and K. pneumoniae (n = 6, 46%).
Conclusion
Overall, a high resistance was observed for beta-lactam antibiotics. In addition, a high resistance was noted for ceftazidime with A. baumannii species (n = 16, 77%). However, for quinolones, the highest resistance to ciprofloxacin was observed for E. coli, A. baumannii, methicillin-resistant Staphylococcus aureus, and K. pneumoniae.
Keywords
1. Introduction
Antimicrobial resistance is an emerging problem worldwide. Makkah is a city of the utmost importance in the Muslim world, and millions of pilgrims from across the globe visit every year to perform religious rituals. These mass gatherings could potentially make Saudi Arabia a hot spot for the spread of multidrug-resistant (MDR) strains and the spread of antibiotic resistance around the world.
1
, 2
The aim of the current study was to develop a database on the most prevalent community-acquired organisms and their resistance pattern to commonly used antimicrobials in the city of Makkah, Saudi Arabia.2. Methods
The study was designed as a retrospective audit of electronic records from January to June 2015. The study was conducted at two hospitals in the city of Makkah with the availability of all major specialties in medicine that receive pilgrims with community-acquired exacerbations of chronic disorders. Infections were categorized as community-acquired in the case of a positive culture obtained within 72 h of admission, in accordance with the guidelines of the US Centers for Disease Control and Prevention (CDC).
3
All susceptibility testing was performed according to the Clinical and Laboratory Standards Institute (CLSI) performance standards (25th informational supplement, M100-S25).4
3. Results
Three hundred and seventy-four bacterial pathogens were isolated, the majority of which were from Al-Noor Specialist Hospital (n = 313, 83%). The most frequently isolated Gram-negative pathogen was Escherichia coli (n = 103, 27.5%), followed by Klebsiella pneumoniae (n = 71, 19%), Pseudomonas aeruginosa (n = 46, 12.3%), Acinetobacter baumannii (n = 26, 7%), and Proteus mirabilis (n = 17, 4.5%). Among Gram-positive pathogens, methicillin-resistant Staphylococcus aureus (MRSA) (n = 36, 9.6%) accounted for the highest proportion, followed by methicillin-sensitive Staphylococcus aureus (MSSA) (n = 21, 5.6%), Streptococcus spp (n = 20, 5.3%), Enterococcus spp (n = 11, 2.9%), and Staphylococcus epidermidis (n = 6, 1.6%). Most of the pathogens were isolated from urine samples (n = 139, 37.2%), followed by sputum (n = 95, 25.4%) and blood (n = 78, 20.9%). Details are shown in Table 1.
Table 1Descriptive characteristics of the study group
| Characteristics | Frequency (n) | Percentage (%) |
|---|---|---|
| Gender Male Female | 191 183 | 51.0 49.0 |
| Nationality Saudi Pakistani Egyptian Bangladeshi Yemeni Burmese Nigerian Indonesian Indian Other | 177 30 24 15 25 20 8 13 13 49 | 47.3 8.0 6.4 4.0 6.7 5.3 2.1 3.5 3.5 13.1 |
| Hospital Ajyad Emergency Hospital (primary care hospital) Al-Noor Specialist Hospital (tertiary care hospital) | 61 323 | 16.3 86.3 |
| Pathogens isolated Acinetobacter baumannii ESBL-producing Escherichia coli Escherichia coli Enterobacter cloacae Enterococcus spp Klebsiella pneumoniae MRSA Streptococcus spp MSSA Pseudomonas aeruginosa Proteus mirabilis Staphylococcus epidermidis Salmonellae | 26 4 103 9 11 71 36 20 21 46 17 6 4 | 7.0 1.1 27.5 2.4 2.9 19.0 9.6 5.3 5.6 12.3 4.5 1.6 1.1 |
| Specimen type Blood Urine Sputum Swab Other | 78 139 95 54 8 | 20.9 37.2 25.4 14.4 2.1 |
ESBL, extended-spectrum beta-lactamase; MRSA, methicillin-resistant Staphylococcus aureus; MSSA, methicillin-sensitive Staphylococcus aureus.
3.1 Resistance pattern to beta-lactam antibiotics
The resistance rates were high among Gram-negative bacteria. E. coli (n = 38, 59%), K. pneumoniae (n = 28, 52%), and MRSA (n = 15, 75%) strains showed resistance to amoxicillin–clavulanic acid (Table 2) . A high resistance to ampicillin was recorded for E. coli (n = 66, 84%), as well as for K. pneumoniae (n = 55, 94%), MRSA (n = 17, 78%), and P. mirabilis (n = 14, 88%). In addition, P. aeruginosa (n = 9, 36%) also showed resistance to ceftazidime. Both Gram-positive and Gram-negative bacteria showed high resistance to ceftazidime, with A. baumannii species having the highest rate (n = 16, 77%). However, Gram-negative bacteria, with the exception of Enterobacter spp, were noticed to have high resistance to penicillin.
Table 2Resistance patterns of different pathogens to different antibiotics
| Drugs | A. baumannii | ESBL E. coli | E. coli | E. cloacae | K. pneumoniae | MRSA | Streptococcus spp | MSSA | P. aeruginosa | P. mirabilis | Salmonella |
|---|---|---|---|---|---|---|---|---|---|---|---|
| Amox/Clav | NR | NR | 38 (59%) | 5 (84%) | 28 (52%) | 15 (75%) | 0 | 4 (29%) | NR | 6 (50%) | 0 |
| Ampicillin | 3 (100%) | NR | 66 (84%) | 6 (75%) | 55 (94%) | 17 (78%) | NR | 10 (91%) | 3 (75%) | 14 (88%) | NR |
| Aztreonam | NR | NR | 16 (49%) | NR | 4 (23%) | 5 (72%) | NR | 0 | NR | NR | NR |
| Cefazolin | NR | NR | 8 (40%) | NR | 8 (43%) | 5 (84%) | NR | 0 | NR | NR | NR |
| Cefepime | 13 (77%) | NR | 16 (41%) | NR | 8 (27%) | 3 (60%) | NR | NR | 13 (34%) | 4 (58%) | 0 |
| Cefoxitin | NR | 0 | 16 (24%) | 7 (100%) | 10 (20%) | 3 (30%) | 3 (75%) | 0 | 0 | 3 (23%) | NR |
| Cefuroxime | NR | NR | 10 (45%) | 0 | 8 (35%) | 4 (80%) | NR | 0 | NR | NR | 0 |
| Ceftazidime | 16 (77%) | NR | 20 (34%) | NR | 11 (24%) | 4 (50%) | NR | NR | 9 (36%) | 7 (70%) | 0 |
| Cefotaxime | 18 (100%) | NR | 8 (31%) | 0 | 6 (23%) | 3 (60%) | NR | 0 | 18 (95%) | NR | 0 |
| Ceftriaxone | NR | NR | NR | 0 | 0 | 4 (67%) | 0 | NR | NR | 0 | NR |
| Cephalothin | NR | NR | 29 (97%) | 4 (100%) | 12 (67%) | 13 (87%) | 5 (36%) | 0 | NR | 6 (100%) | NR |
| Ertapenem | 0 | 0 | NR | 0 | 3 (13%) | 0 | NR | 0 | NR | NR | 0 |
| Imipenem | 9 (90%) | 0 | 3 (3.0%) | NR | 5 (82%) | 10 (50%) | 0 | 3 (43%) | 5 (11%) | 0 | 0 |
| Meropenem | 9 (64%) | 0 | NR | 0 | 3 (10%) | NR | 0 | 0 | 3 (17%) | 0 | 0 |
| Oxacillin | NR | NR | NR | NR | NR | NR | NR | 4 (24%) | NR | NR | NR |
| Penicillin G | NR | NR | NR | NR | NR | 10 (91%) | 3 (20%) | 8 (89%) | NR | NR | NR |
| Pip/Taz | 0 | NR | NR | 0 | 3 (17%) | NR | NR | NR | 4 (33%) | 0 | NR |
| Ticarcillin | NR | NR | NR | NR | NR | NR | NR | NR | 10 (59%) | NR | NR |
| Mezlocillin | 6 (100%) | NR | 3 (100%) | NR | NR | NR | NR | NR | 3 (100%) | NR | NR |
| Amikacin | 16 (67%) | 3 (75%) | 6 (7%) | NR | 3 (5%) | NR | 0 | NR | 5 (12%) | 5 (34%) | NR |
| Gentamicin | 11 (46%) | 3 (75%) | 22 (28%) | 3 (50%) | 24 (38%) | 10 (42%) | NR | NR* | 9 (21%) | 12 (75%) | NR |
| Tobramycin | 3 (50%) | NR | 4 (57%) | 0 | 6 (46%) | NR | NR | NR | 0 | 0 | NR |
| Ciprofloxacin | 19 (83%) | 3 (75%) | 57 (60%) | 4 (45%) | 26 (41%) | 15 (63%) | NR | 4 (40%) | 13 (49%) | 9 (60%) | 0 |
| Levofloxacin | 4 (67%) | NR | 4 (100%) | NR | 4 (44%) | 0 | NR | 0 | 0 | NR | 0 |
| Moxifloxacin | NR | NR | 19 (6 3%) | NR | 16 (55%) | 5 (42%) | NR | 4 (40%) | 3 (100%) | NR | 0 |
| Nalidixic acid | NR | NR | 9 (75%) | 0 | NR | NR | NR | NR | NR | NR | NR |
| Norfloxacin | NR | NR | 8 (44%) | 0 | 0 | NR | 3 (100%) | 0 | 0 | 0 | NR |
ESBL, extended-spectrum beta-lactamase-producing; MRSA, methicillin-resistant Staphylococcus aureus; MSSA, methicillin-sensitive Staphylococcus aureus; Amox/Clav, amoxicillin–clavulanic acid; Pip/Taz, piperacillin–tazobactam.
a Only resistant culture numbers and percentages are presented in the table; when only one or two samples are resistant then the results are not reported (NR).
3.2 Resistance among isolated pathogens to aminoglycosides and fluoroquinolones
With regard to the three most commonly used aminoglycoside antibiotics (amikacin, gentamicin, and tobramycin), E. coli (extended-spectrum beta-lactamase (ESBL)-positive) was observed to have the highest resistance to amikacin (n = 16, 67%). For gentamicin, P. mirabilis (n = 12, 75%) was noted to have high resistance. Details are given in Table 2. Most Gram-negative organisms were highly resistant to quinolones, except Salmonella Typhi. The highest resistance to ciprofloxacin was observed for E. coli (n = 57, 60%), A. baumannii (n = 19, 83%), MRSA (n = 15, 63%), and K. pneumoniae (n = 26, 41%), as shown in Table 2. Interestingly, A. baumannii, E. coli and K. pneumoniae were noticed to be highly resistant to levofloxacin.
4. Discussion
Three hundred and seventy-four pathogenic bacteria were isolated in two different hospitals in the city of Makkah. Gram-negative bacteria accounted for 280 (75%) of the total isolates, while the remaining 94 (25%) were Gram-positive organisms. Among Gram-negative bacteria, E. coli was the most frequently occurring organism, followed by K. pneumoniae and P. aeruginosa. There are several possible reasons for the development of resistance.
To date this is the perhaps the first study to address antibiotic susceptibility in relation to pilgrims within the first 72 h of admission to emergency departments. Overall it was noted that among the Gram-positive strains, MSSA and Enterococcus spp were the most commonly found organisms in the present study; this is somewhat in line with the results of other studies reporting antibiotic resistance in the Saudi region.
5
In contrast, MRSA was the second most prevalent organism in this study and its resistance pattern against many beta-lactam and non-beta-lactam antibiotics was variable. The resistance pattern is correlated with that of a previous study, in which the author reported a 40% resistance rate to oxacillin.5
Moreover, a higher resistance rate to gentamicin and tetracycline was observed. Overall, the pattern of susceptibility to antibiotics in the present study revealed that most of the commonly reported organisms were resistant to beta-lactam antimicrobials, suggesting a dire need to optimize and scrutinize the usage of antibiotics at the emergency centres when managing community-acquired infections among pilgrims from different parts of world.2
In conclusion, E. coli and MRSA were two common isolates resistant to most of the antibiotics. Overall, a high resistance was observed for beta-lactam antibiotics. In addition, a high resistance to ceftazidime was seen for A. baumannii species (n = 16, 77%). However, for quinolones, the highest resistance to ciprofloxacin was observed for E. coli, A. baumannii, MRSA, and K. pneumoniae.
Funding: The Deanship of Scientific Research and the Institute of Scientific Research and Revival of Islamic Heritage at Umm Al Qura University, Kingdom of Saudi Arabia, funded this study.
Ethics approval: This study was initially approved by the Ethics Committee of the Faculty of Medical Sciences at Umm Al Qura University with reference number AMSEC 15-26-12. Further approval was obtained from the Directorate General of Health, Ministry of Health, Makkah region with reference number 47/300/43149 based on ethical approval from the Al-Noor Specialist Hospital Ethics Review Board.
Conflict of interest: The authors have no conflicts of interest.
References
- Antimicrobial resistance among Gram-positive pathogens in Saudi Arabia.J Chemother. 2012; 24: 125-136
- Potential risk for drug resistance globalization at the Hajj.Clin Microbiol Infect. 2015; 21: 109-114
- CDC/NHSN surveillance definition of health care-associated infection and criteria for specific types of infections in the acute care setting.Am J Infect Control. 2008; 36: 309-332
- Performance standards for antimicrobial susceptibility testing; twenty-fifth informational supplement (M100-S25).CLSI, Wayne, PA2015
- Profile of bacterial pneumonia during Hajj.Indian J Med Res. 2011; 133: 510-513
Article info
Publication history
Published online: June 13, 2016
Accepted:
June 7,
2016
Received in revised form:
June 6,
2016
Received:
May 20,
2016
Corresponding Editor: Eskild Petersen, Aarhus, Denmark.Identification
Copyright
© 2016 The Author(s). Published by Elsevier Ltd on behalf of International Society for Infectious Diseases.
User license
Creative Commons Attribution – NonCommercial – NoDerivs (CC BY-NC-ND 4.0) | How you can reuse 
Elsevier's open access license policy
Creative Commons Attribution – NonCommercial – NoDerivs (CC BY-NC-ND 4.0)
Permitted
For non-commercial purposes:
- Read, print & download
- Redistribute or republish the final article
- Text & data mine
- Translate the article (private use only, not for distribution)
- Reuse portions or extracts from the article in other works
Not Permitted
- Sell or re-use for commercial purposes
- Distribute translations or adaptations of the article
Elsevier's open access license policy
