Antimicrobial resistance trends from a hospital and diagnostic … · followed similar trends. AMR rates also largely agreed with the World Health Organization Global Antimicrobial

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Antimicrobial resistance trends from a hospital and diagnostic facility in Lahore, Pakistan: 6

A five-year retrospective analysis (2014-2018) 7

Carly Ching1, Summiya Nizamuddin2, Farah Rasheed2, R.J. Seager1, 8

Felix Litvak1, Faisal Sultan2, Muhammad Zaman1* 9

1. Boston University, Department of Biomedical Engineering, Boston, MA, USA 10

2. Shaukat Khanum Memorial Cancer Hospital & Research Centre, Lahore, Pakistan 11

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• * Muhammad H. Zaman 17

• Department of Biomedical Engineering 18

Boston University, 19

44 Cummington Mall 20

Boston, Massachusetts 02215 21

617-358-5881 22

[email protected] 23

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All rights reserved. No reuse allowed without permission. was not certified by peer review) is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity.

The copyright holder for this preprint (whichthis version posted November 22, 2019. ; https://doi.org/10.1101/19012617doi: medRxiv preprint

NOTE: This preprint reports new research that has not been certified by peer review and should not be used to guide clinical practice.

https://doi.org/10.1101/19012617

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Abstract 27

Objective: Observing antimicrobial resistance (AMR) trends is critical to identify emerging 28

pathogens and potential disease outbreaks. Determining these trends also allows for policy 29

evaluations and development of interventions. We performed a retrospective analysis of 30

microbiological testing results from a hospital and diagnostic facility in Lahore, Pakistan that 31

represents country-wide sampling. Within this analysis, data was disaggregated by nationality, as 32

it has been suggested that migration increases the burden of AMR. We sought to determine any 33

trends in AMR among populations, which are often at-risk, while contributing to AMR 34

surveillance in Pakistan, which currently does not have a national surveillance network. 35

Methods: Retrospective analysis of antimicrobial susceptibility records from 2014 to 2018 from 36

Shaukat Khanum Memorial Cancer Hospital & Research Centre (SKMCH&RC) in Lahore, 37

Pakistan was performed. All positive microbiological cultures from patients was analyzed to 38

assess antibiotic resistance rates of the most common bacterial isolates and incidence of 39

ESKAPE pathogens and emerging outbreaks among adults and children. 40

Results: For all years, data for a total of 12,702 and 78,130 bacterial and fungal isolates from 41

children and adults, respectively, with Pakistani nationality were analyzed. For all years, data for 42

597 and 2470 bacterial and fungal isolates for children and adults, respectively, with Afghan 43

nationality were analyzed. AMR rates largely did not vary between populations, but rather 44

followed similar trends. AMR rates also largely agreed with the World Health Organization 45

Global Antimicrobial Surveillance System results for Pakistan. 46

Conclusion: Pakistan requires increased AMR surveillance to identify emerging resistance 47

infections and outbreaks. 48

Keywords: Antimicrobial Resistance, Antibiotics, Surveillance 49



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1. Introduction 50

Antimicrobial resistance (AMR) is a major health concern worldwide. As of 2018, Pakistan was 51

the 5th most populous country in the world with 212.2 million people [1] . While Pakistan has a 52

national action plan to combat AMR[2], there is no national surveillance network, and global 53

reporting is done through the World Health Organization Global Antimicrobial Surveillance 54

System (GLASS) [3]. However, there is a voluntary coalition from major hospitals and 55

institutions that self-report antimicrobial resistance data, known as the Pakistan Antimicrobial 56

Resistance Network (PARN). A recent national situational report from 2018 highlighted the 57

burden and challenges of antimicrobial resistance in Pakistan[4]. Indeed, it has been recognized 58

as a national concern since 2014, however without comprehensive surveillance data it is difficult 59

to make accurate estimates of the burden of AMR throughout the country. 60

61

Adding to the complex situation in Pakistan is the influx of migrants and displaced populations. 62

The United Nations refugee agency estimates that Pakistan hosts more than 1.4 million registered 63

Afghan refugees [5]. It has been postulated that migrant groups add to the burden of AMR due to 64

poor sanitation conditions and access to medicines and healthcare, however this sentiment is 65

often anecdotal or without supporting data which can cause unnecessary stigmas. A recent 66

comprehensive systematic review that looked at the pooled prevalence of AMR among migrant 67

groups in Europe found that AMR was higher in refugees and asylum seekers than other migrant 68

groups, but did not find evidence of higher rates of transmission of AMR from migrant to host 69

populations [6]. 70

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Here, we add to AMR surveillance data in Pakistan, broken down by nationality (either Pakistani 72

or Afghan nationals). The strength of this data set is the large sample size, much larger than 73

GLASS reporting sample sizes for Pakistan, and the ability to analyze temporal trends. 74

Limitations include that official migrant status of patients and patient medical history is 75

unknown, therefore interpretation of data should be done with caution. 76

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2. Methods 78

2.1 Sample collection 79

The retrospective descriptive study was conducted at Shaukat Khanum Memorial Cancer 80

Hospital & Research Centre (SKMCH&RC), Lahore, Pakistan, and comprised data related to all 81

microbiological cultures reported positive between 2014 and 2018. The hospital is a 195-bed 82

non-profit tertiary-care specialist cancer hospital with a referral base from all over the country 83

and adjoining regions. Additionally, the laboratory attached with the hospital runs through a 84

network of laboratory collection centers located in 50 major cities and towns of Pakistan. All 85

data was retrieved from the online records on the in-house information system database. 86

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2.2 Antimicrobial susceptibility testing/Bacterial identification 88

All bacterial isolates tested during the above time period were identified by standard techniques 89

and antimicrobial susceptibility testing was performed and interpreted according to Clinical 90

Laboratory Standards Institute (CLSI) criteria. 91

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2.3 Data Extraction 93

Migrants are defined as individuals born outside Pakistan; however, their patient history and 94

migrant status is unknown. Children were defined as individuals under the age of 18. Data was 95



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extracted from de-identified patient records stored in a standardized Excel format using a 96

purpose-built Python (version 3.7.3) script employing the Pandas package for data extraction and 97

analysis. Script is available upon request. Data for only registered patients has a low sample size 98

and is available upon request. 99

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3. Results 101

3.1 Study Population 102

Among all years, data for a total of 12 702 and 78 130 bacterial and fungal isolates from children 103

and adults, respectively, with Pakistani nationality were obtained. Among all years, data for 597 104

and 2470 bacterial and fungal isolates for children and adults, respectively, with Afghan 105

nationality were obtained (Table 1). 106

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3.2 Distribution of bacterial isolates 108

Among the top 5 most common bacteria isolated among adults for both populations were 109

Escherichia coli, Staphylococcus aureus, Pseudomonas aeruginosa and Klebsiella pneumoniae, 110

and this did not change between 2014 to 2018 (Table 2). In the adult Pakistani population 111

Enterococcus species filled out the top 5 most common bacterial isolate for each year, while for 112

the Afghan population it was Staphylococcus epidermidis. For Pakistani children, a similar 113

distribution including S. epidermidis is seen. For Afghan children, S. epidermidis, E. coli and S. 114

aureus are the most common bacteria across all years (Table 3). The full distribution of bacterial 115

infections for each year is provided in Supplemental File 1. 116

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3.3 Trends in incidence of ESKAPE pathogens and Salmonella typhi 118



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The ESKAPE pathogens are the leading cause of hospital acquired infections[7], and as such we 119

mapped the trends in incidence of these bacteria from 2014 to 2018. S. aureus is the most 120

prevalent ESKAPE pathogen in adults for both populations, followed by P. aeruginosa and K. 121

pneumoniae (Fig. 1A&B). This does not change between 2014 and 2018. Plotting this data for 122

children from Pakistan shows a similar trend and rates to adult (Fig. 1C). Similar analysis was 123

not performed for Afghanistan due to low numbers (Table S4). The incidence of Enterococcus 124

faecium, Acinetobacter baumannii and Enterobacter spp. remain low. 125

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While the incidence of A. baumannii did not increase dramatically (Fig. 1), we wanted to 127

determine if resistance to last-line antibiotics, carbapenem and colistin, changed. Carbapenem 128

resistant A. baumannii is an emerging infection in Pakistan[8]. We find that resistance to 129

imipenem and meropenem for both adults and children from Pakistan are within the reported 130

confidence intervals for data reported to GLASS in 2017 (53-72%)[9] and appear to be on a 131

downward trend from 2014 to 2018 (75.4% resistant to imipenem in 2014, 66.6% in 2018). 132

Colistin resistance in A. baumannii remains low ((highest percentage was 1.7% reported in 2016, 133

Table 4). For the population from Afghanistan, there were less than ten A. baumannii isolates, so 134

resistance rates were not calculated 135

136

We also looked at the incidence of multidrug-resistant Salmonella typhi which have recently 137

occurred in Pakistan. Since 2016, over 300 extensively drug resistant (XDR) typhoid cases 138

emerged in Sindh, Pakistan. These bacteria were resistant to fluoroquinolones and the third-139

generation cephalosporin ceftriaxone but typically still susceptible to azithromycin and 140

carbapenems [10]. Among the adult population from Pakistan, from 2014 to 2017 there were no 141



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cases of ceftriaxone resistant S. typhi , however in 2018, 20% of cases (n=45) were now 142

ceftriaxone resistant (Table 4). No resistant to carbapenems and low resistance to azithromycin 143

were observed (Table 4). In Pakistani children, low resistance to ceftriaxone was observed (0-144

5.9%) between 2014 to 2017. In 2018, 37.8% of S. typhi isolates (n=82) were resistant to 145

ceftriaxone but none were resistant to azithromycin. In 2017 however, 14.3% (n=35) of S. typhi 146

isolates from Pakistani children tested against azithromycin were resistant. There were no 147

detected cases of S. typhi in Afghan adults and only 1 case in 2018 in children which was 148

sensitive to all antibiotics tested. 149

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3.4 Antibiotic resistance profiles and temporal trends 151

We extracted the antimicrobial susceptibility data of the most common bacterial isolates 152

Escherichia coli, Staphylococcus aureus, Pseudomonas aeruginosa and Klebsiella pneumoniae 153

for each year. The full table of resistance of these bacterial is provided in the supplemental data 154

(Supplemental Tables S1-S4). 155

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For adults, we compared trends in % resistant for fluoroquinolones and carbapenems between the 157

two populations. We also looked at the % of oxacillin resistant S. aureus (MRSA) isolates 158

between the adult populations. Since the sample size for children from Afghanistan were very 159

low (below 10 and 20) we did not perform a comparative analysis. Looking at ciprofloxacin, % 160

resistance is similar between the two population, with the Afghan resistant rates being lower than 161

the population from Pakistan (Fig. 2), except for 2015 and 2016 for E. coli in which 162

ciprofloxacin resistance increases before decreasing (Fig. 2A). Interestingly, for S. aureus we see 163

that the upward trend follows each other (Fig. 2B). For imipenem, resistance is overall low for 164



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both populations (Fig. 3). Again for P. aeruginosa and K. pneumoniae resistance rates for the 165

Afghan population are overall lower than that of Pakistan. In K. pneumoniae, resistance to 166

carbapenems seems to be increasing for both populations (Fig. 3C). For P. aeruginosa for both 167

ciprofloxacin and imipenem, the % resistant for Pakistan appears to be stable while the % 168

resistant for the Afghan population is trending upwards but has not reached the levels of isolates 169

of those from Pakistan (Fig. 2C & 3B). For oxacillin resistance for S. aureus and S. epidermidis, 170

rates are very similar and strikingly follow a very similar trend (Fig. 4). It should also be noted, 171

that the sample size between the Pakistani and Afghan population differed by over 25-fold which 172

makes direct comparison complicated. 173

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Another important last-line antibiotic is colistin. Colistin resistance for E. coli, S. aureus, P. 175

aeruginosa and K. pneumoniae was detected at <1% for adults and children in Pakistan with the 176

exception of K. pneumoniae in 2018. In this year colistin resistant K. pneumoniae for adults rose 177

to 5.9% (n=222) and 2.2% for children (n=45) (Table S1-S4). It is important to track these types 178

of changes to see if this is an emerging phenomenon. Colistin resistance was only detected in P. 179

aeruginosa isolates at 1.4% (n=74) in 2016 in the adult population from Afghanistan. 180

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3.5 Comparison to WHO GLASS reporting 182

Data available from the WHO GLASS for 2017 as reported by the Center for Disease Dynamics 183

& Policy ResistanceMap[11] was compared to resistance rates reported here[9]. It should be 184

noted that both Pakistan and Afghanistan are enrolled in GLASS. There is currently no reported 185

AMR data for Afghanistan and data from 6 surveillance sites (4 hospitals and 2 outpatient 186

facilities) from the 2018 call for data for Pakistan. For S. aureus, oxacillin for both populations 187



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levels were slightly below the confidence interval from GLASS for 2017 (63% (56-70%)), Table 188

4. For E. coli for both populations, ciprofloxacin resistance was ~15% higher outside the 189

confidence interval (56-62%) from GLASS. Carbapenem resistance was lower by ~5% lower 190

than the confidence interval reported (8-12%) (Table 5). Ampicillin and ceftriaxone were also 191

just below confidence intervals reported (Table 5). For K. pneumoniae, ciprofloxacin resistance 192

for the Pakistan population fell within GLASS values while that of the Afghanistan population 193

was lower. For both carbapenems and third generation cephalosporins, % resistance for both 194

populations were lower than reported by GLASS (Table 5). Our sample size, especially for the 195

Pakistani population, is between 5.5 to 13-fold greater than the number of isolates that make up 196

the resistance rates in GLASS. 197

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4. Discussion 199

Here, we present a situational report on antimicrobial resistance from a hospital and diagnostic 200

center in Lahore, Pakistan. We find that the resistance rates largely are within or close to the 201

range of previously reported values with a few notable differences (Table 5). However, national 202

reporting for all antibiotics and bacteria are still sparse and increased reporting would provide a 203

more comprehensive comparison. Notably, there were no striking difference in AMR rates for 204

the Afghan population compared to the Pakistani population. As discussed early, a recent 205

systematic review on AMR among migrant groups in Europe found AMR was higher in refugees 206

and asylum seekers than other migrant groups, but did not find evidence of high rates of 207

transmission of AMR from migrant to host populations [6]. Differences have been shown in the 208

type of AMR between migrant and host populations. For example a study comparing German 209

nationals to refugees shows differences in microbiome and prevalence of resistance genes [12]. 210

A study of AMR in Vibrio cholera stains from Afghan patients in Iran showed differences in 211



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resistance patterns. In Afghan patients resistance to erythromycin, sulfamethoxazole 212

trimethoprim and ampicillin was prevalent. In Iranian patients, resistance to tetracycline and 213

nalidixic acid was enriched, however the sample size for this study were low[13]. We do not 214

have genetic information to determine the underlying mechanisms of resistance. 215

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Overall, this report agrees with previously reported levels of antibiotic resistance in Pakistan and 217

does not demonstrate any strong differences among the AMR burden between national 218

populations from one hospital and research facility in Lahore, Pakistan that provides diagnostic 219

testing for locations around the county. This report, though, represents a specific clinical 220

situation and more standardized reporting is needed to generate more robust country-wide 221

estimates. Retrospectively, we observe the emergence of ceftriaxone resistant S. typhi (Table 3), 222

however real-time analysis is critical for preventing outbreaks as they first emerge. National 223

averages and baselines are important for hospitals to measure incidence of resistance and note 224

any unusual changes or up or downward trends. 225

226

Funding 227

None declared 228

229

Competing interests 230

None declared 231

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Ethical approval 233



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Boston University Institutional Review Board oversight was not required as research was 234

deemed not Human Subject Research. Exempt status for study was granted from the 235

SKMCH&RC Institutional Review Board. 236

Figure Captions 237

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Figure 1. Trends in incidence of ESKAPE pathogens isolated from 2014-2018 239

Incidence of ESKAPE pathogens from clinical isolates from SKCM&RC from 2014-2018 240

241

Figure 2. Trends in ciprofloxacin resistance in Adult patients, 2014-2018 242

Trends in resistance to ciprofloxacin for (A) E. coli, (B) S. aureus, (C) P. aeruginosa and (D) K. 243

pneumoniae isolates from adult populations with nationality from Pakistan or Afghanistan taken 244

from SKCM&RC, from 2014-2018 245

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Figure 3. Trends in imipenem resistance in Adult patients, 2014-2018 247

Trends in resistance to imipenem for (A) E. coli, (B) P. aeruginosa and (C) K. pneumoniae 248

isolates from adult populations with nationality from Pakistan or Afghanistan taken from 249

SKCM&RC, from 2014-2018 250

251

Figure 4. Trends in oxacillin resistance in Adult patients, 2014-2018 252

Trends in ciprofloxacin resistance for (A) S. aureus, and (C) S. epidermidis isolates from adult 253

populations with nationality from Pakistan or Afghanistan taken from SKCM&RC, from 2014-254

2018 255

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Table 1. Characteristics of Study Population, 2014-2018 261

Nationality : Pakistan Identified bacterial isolates, n

Year Children Adults

Male Female Total Male Female Total

2014 1375 1074 2449 7511 6970 14481

2015 1092 932 2024 7000 6753 13753

2016 1341 1058 2399 7541 7737 15278

2017 1408 1383 2791 8188 8891 17079

2018 1594 1445 3039 8472 9067 17539

Total 6810 5892 12 702 38 712 39 418 78 130

Nationality: Afghanistan Identified bacterial isolates, n

Year Children Adults

Male Female Total Male Female Total

2014 54 8 62 164 165 329

2015 66 69 135 253 154 407

2016 73 54 127 332 244 576

2017 106 31 137 305 206 511

2018 94 42 136 371 285 656

Total 393 204 597 1425 1054 2479 262

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Table 2. Top 5 Most Frequent bacteria isolated in adults, 2014-2018 271

Nationality: Pakistan Nationality: Afghanistan

Bacteria Adults, n (%) Bacteria Adults, n (%)

2014 Escherichia coli 4475(30.9)

2014 Pseudomonas aeruginosa 49 (14.9)

Staphylococcus aureus 2261(15.6)

Escherichia coli 49 (14.9)

Pseudomonas aeruginosa 1555(10.7)

Staphylococcus aureus 48 (14.6)

Enterococcus species 892(6.2)

Klebsiella pneumoniae 31 (9.4)

Klebsiella pneumoniae 885(6.1)

Staphylococcus epidermidis 22 (6.7)

Other 4413(30.5)

Other 130(39.5)


2015 Escherichia coli 85 (20.9)


Staphylococcus aureus 78 (19.2)


Pseudomonas aeruginosa 63 (15.5)


Klebsiella pneumoniae 31 (7.6)


Staphylococcus epidermidis 28(6.9)

Other 3809(27.7)

Other 122(30.0)


2016 Staphylococcus aureus 142(24.7)


Escherichia coli 100(17.4)







Other 4453(29.1)

Other 163(28.3)











Other 4896(28.7)

Other 169(33.1)





Pseudomonas aeruginosa 1559(8.9) Pseudomonas aeruginosa 88(13.4)





Other 5132(29.3) Other 197(30.0) 272

n=number of isolates, % refers to % of all isolates 273

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Table 3. Top 5 Most Frequent bacteria isolated in children, 2014-2018 282

Nationality: Pakistan Nationality: Afghanistan

Bacteria Children, n1 (%2) Bacteria Children, n (%)

2014 Escherichia coli 497 (20.3) 2014 Staphylococcus epidermidis 20(32.3)




Diphtheroid species 4(6.5)


Micrococcus species 3(4.8)

Klebsiella pneumoniae 139(5.7) Staphylococcus aureus 3(4.8)

Other 899 (36.7)


Other 14(22.6)

2015 Escherichia coli 491(24.2) 2015 Staphylococcus epidermidis 31(23.0)









Other 665(32.9)

Other 49(36.3)









Micrococcus species 5(3.9)

Other 778(32.4)

Other 21(16.5)









Diphtheroid species 5(3.6)

Other 881(31.6)

Other 45(32.8)

2018 Escherichia coli 751(24.5) 2018 Escherichia coli 27(19.9(









Other 1088(35.8)

Other 42(30.9)

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1n=number of isolates 284 2 % of all isolates 285

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Table 4. Selected Antibiotic Resistance Profile for Salmonella typhi and Acinetobacter 291

baumannii, 2014-2018 292

% resistant

S. typhi n

AMP1 n2 CHL n CIP n CEFX n IMI n MER n AZT n

Adult 26 2014 69.2 26 68.0 25 100.0 26 0 26 -

-

- Pakistan 21 2015 42.9 21 45.0 20 95.2 21 0 21 -

-

-

22 2016 50.0 22 45.5 22 55.6 9 0 21 0 1 0 1 14.3 7

30 2017 40.0 30 51.9 27 60.0 10 0 30 0 1 0 1 10 20

46 2018 66.7 45 64.4 45 100.0 15 20 45 0 11 0 11 0 42

Children 15 2014 57.1 14 61.5 13 80.0 15 0.0 15 -

-

- Pakistan 17 2015 64.7 17 64.7 17 88.2 17 5.9 17 0 1 0 1 -

36 2016 66.7 36 63.6 33 37.5 8 0.0 35 0 1 0 2 0 16

41 2017 52.5 40 56.1 41 69.2 13 5.0 40 -

-

14.3 35

82 2018 73.8 80 66.3 80 82.1 28 37.8 82 0 31 0 31 0 80

293

% resistant

A. baumannii n

CIP n IMI n MER n COL n

Adult 338 2014 84.62 338 75.4 338 77.8 334 0.3 326

Pakistan 312 2015 80.13 312 77.9 312 78.1 311 0.0 307

391 2016 78.96 385 72.9 388 73.1 387 1.8 271

306 2017 67.00 297 60.6 302 61.8 304 1.7 174

332 2018 73.11 331 66.6 332 66.9 332 0.4 235

Children 64 2014 70.31 64 65.6 64 65.6 64 0 60

Pakistan 54 2015 79.63 54 81.5 54 81.5 54 0 54

73 2016 69.86 73 70.8 72 72.6 73 0 50

54 2017 65.38 52 66.0 53 66.0 53 0 34

64 2018 64.52 62 63.5 63 63.5 63 0 36

294

1AMP= ampicillin, CHL= chloramphenical, CIP=ciprofloxacin, CEFX=ceftriaxone, 295

IMI=imipenem, MER=meropenem, AZT=azithromycin, COL=colistin 296 2 The n beside each antibiotic represents the number of isolates that were tested for that antibiotic 297

and which the % resistant was calculated from. 298

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Table 5. Comparison of resistance rates to GLASS averages for 2017 303

304

1The n beside each antibiotic represents the number of isolates that were tested for that antibiotic 305

and which the % resistant was calculated from. 306

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315

316

Pakistan (GLASS)

Pakistan (SKMCH&RC)

Afghanistan (SKMCH&RC)

Antibiotic

% resistant (average (95% CI))

n1 Antibiotic % resistant n % resistant n

S. aureus Oxacillin 2017 63 (56-70) 193 Oxacillin 47 2390 49.6 115

E. coli Aminopenicillins 2017 97 (95-98) 427 Ampicillin 91.4 5566 93.8 96

Fluoroquinolones 2017 59(56-62) 866 Ciprofloxacin 79.5 5578 77.6 98

Carbapenems 2017 10(8-12) 814 Imipenem 3.7 5528 2.1 97

Third Generation Cephalosporins

2017 86(83-89) 458 Ceftriaxone 79.5 5290 86.7 98

K. pneumoniae Fluoroquinolones 2017 58(51-65) 189 Ciprofloxacin 56.2 1280 24.1 29

Carbapenems 2017 43(36-50) 181 Imipenem 13.6 1275 0 29

Third Generation Cephalosporins

2017 84(79-88) 227 Ceftriaxone 65.3 1290 48.3 29



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Pakistan. National AMR Action Plan for Pakistan 2017:1–64. 324

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resistance: translating ideas into reality. Lancet Infect Dis 2018;18:1066–7. 326

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[9] World Health Organization. Global Antimicrobial Resistance Surveillance System 341

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92-4-151344-9. 343

[10] Klemm EJ, Shakoor S, Page AJ, Qamar FN, Judge K, Saeed DK, et al. Emergence of an 344

extensively drug-resistant Salmonella enterica serovar typhi clone harboring a 345

promiscuous plasmid encoding resistance to fluoroquinolones and third-generation 346

cephalosporins. MBio 2018;9:1–10. https://doi.org/10.1128/mBio.00105-18. 347

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(accessed October 31, 2019). 350

[12] Häsler R, Kautz C, Rehman A, Podschun R, Gassling V, Brzoska P, et al. The antibiotic 351

resistome and microbiota landscape of refugees from Syria, Iraq and Afghanistan in 352

Germany. Microbiome 2018;6:1–11. https://doi.org/10.1186/s40168-018-0414-7. 353

[13] Tabatabaei SM, Salimi Khorashad A. Antimicrobial Resistance Patterns of Vibrio cholera 354

Strains Isolated From Afghan and Iranian Patients in Iran. Int J Infect 2015;2:5–10. 355

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Antimicrobial resistance trends from a hospital and diagnostic … · followed similar trends. AMR rates also largely agreed with the World Health Organization Global Antimicrobial