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Original article

Prescribing patterns of antimicrobials in the Internal Medicine Department of Ibrahim Malik Teaching Hospital in Khartoum, 2016

Prescribing patterns of antimicrobials in the Internal Medicine Department of Ibrahim Malik Teaching Hospital in Khartoum, 2016

Salma Nasr Abdalla1, Bashir Alsiddig Yousef1,&

 

1Department of Pharmacology, Faculty of Pharmacy, University of Khartoum, Sudan

 

 

&Corresponding author
Bashir Alsiddig Yousef, Department of Pharmacology, Faculty of Pharmacy, University of Khartoum, Sudan

 

 

Abstract

Introduction: antimicrobials are among the most commonly prescribed therapeutic agents in hospitals. Irrational use of antimicrobials results in the development of antimicrobial resistance which could lead to life-threatening illnesses. Therefore, the assessment of antimicrobial prescribing and use is of utmost importance. This study aimed to examine the prescribing patterns of antimicrobials in the Internal Medicine Department of Ibrahim Malik Teaching Hospital in Khartoum, Sudan.

 

Methods: a descriptive, cross-sectional study was conducted using World Health Organization indicators for antimicrobial use in hospitals. Systematic random sampling was used to select 245 medical records from the 2613 medical records of patients admitted to the internal medicine department in 2016. Data were collected using a data collection form and a structured interview with the chief pharmacist in the hospital.

 

Results: of the 245 medical records examined, 201 (82%) patients were prescribed one or more antimicrobial drug. The average number of antimicrobials per patient was (2.1±1.1). The average duration of antimicrobial treatment was (4.9±3.8) days. The generic name was used in (35.6%) of antimicrobials, while (95.5%) of all antimicrobials were prescribed from the national essential medicines list. Overall, there were 421 courses of antimicrobials prescribed. The most frequently prescribed antimicrobials were ceftriaxone (131 courses) and metronidazole (89 courses). Among the documented infectious diseases, the most frequently encountered was pneumonia, followed by malaria. There was no drug and therapeutic committee, hospital formulary or essential medicines list, and standard treatment guidelines for infectious diseases in the hospital.

 

Conclusion: the results of the study revealed a high percentage of antimicrobial use in the Internal Medicine Department. Multifaceted interventions are urgently needed to promote rational prescribing of antimicrobials.

 

 

Introduction    Down

Antimicrobial drugs (AMD) are the most commonly prescribed medications in outpatient and inpatient settings [1,2]. While the rate of AMDs use in developed countries is around 30% [3], in developing countries, it ranges between 35% to 60% [4]. The burden of lower respiratory tract infections, diarrheal diseases, and tuberculosis (TB) represented 30% of the top ten causes of deaths globally in 2016 [5]. Infectious diseases are one of the major causes of mortality in developing countries [6]. In Sudan, 52.8% of diseases burden is attributable to infectious diseases [7]. This global burden on public health and the widespread use of antimicrobials necessitate their optimal use to reserve their efficacy. The irrational use of medicines is represented in different forms including polypharmacy, inappropriate indication, use of unnecessarily expensive drugs, and inappropriate use of antimicrobials [8]. The adoption of essential medicines list (EML) is a cornerstone of the rational use of medicines that helps in promoting the cost-effective use of drugs [9] and improving the quality of prescribing where drug information, prescribing training, and medical audit focus on a certain list of medicines [10]. Another essential element in rational prescribing is the use of the generic name, which contributes to safe prescribing and dispensing [11] and ensures the release of clear and unambiguous medication order [12], as well as containment of expenditure for drugs prescription. This is because generics are priced much less than the brand drugs [13,14]. Antimicrobial resistance (AMR) is a global problem that challenges public health by increasing morbidity, mortality, adverse drug effects, as well as the cost of treatment. The emergence of AMR is related to the consumption of antimicrobials. This is noticed with the positive correlation between antibiotics resistance (ABR) and consumption of antibiotics [15]. The highest consumption of AMDs at the hospital level is associated with the highest rate of resistance [16]. To ensure optimal and rational use of antimicrobials, information about antimicrobial prescribing patterns is very important since it helps in suggesting measures and interventions that improve AMDs prescribing practice. This study was carried out to investigate the use, and prescribing patterns of antimicrobials by using selected prescribing indicators in the Internal Medicine Department and to investigate the existence of EML or hospital formulary (HF) and standard treatment guidelines (STGs) for infectious diseases that regulate prescribing of antimicrobials in Ibrahim Malik Teaching Hospital in Khartoum, Sudan.

 

 

Methods Up    Down

The study was a descriptive, cross-sectional, hospital-based study. It was conducted in the Internal Medicine Department of Ibrahim Malik Teaching Hospital, which locates in Khartoum locality and provides health services to all age groups. The Medical Department is divided into 44-bed short-stay ward and 30-bed long-stay ward. A systematic random sampling technique was used to select the sample (n= 245, calculated using OpenEpi) [17] from the medical records of all patients (N=2613) who were admitted to the Internal Medicine Department during the study period (January first 2016 - December 31 2016). As the medical records were arranged chronologically, the sample size was divided among the 12 months by proportion, based on the number of medical records in each month.

 

Inclusion criteria: the medical records of patients who were admitted to the Internal Medicine Department during the study period for whom at least one antimicrobial drug was prescribed were included in the study.

 

Exclusion criteria: patients who were prescribed only topical antimicrobial or were admitted for less than 48 hours were excluded from the sample.

 

Five prescribing indicators and two hospital indicators were used to achieve the objectives of the study. The WHO recommends these indicators in the manual "How to investigate antimicrobial use in hospitals: selected indicators" [1]. The prescribing indicators used in this study include the percentage of hospitalizations with one or more antimicrobials prescribed, the average number of antimicrobials prescribed per patient, percentage of antimicrobials prescribed by generic name, percentage of antimicrobials prescribed consistent with the EML and average duration of prescribed antimicrobial treatment. The hospital indicators include the existence of STGs for infectious diseases and existence of an approved HF list or EML. The data were collected by using two instruments adapted from the WHO [1]. The first instrument was a data collection form slightly modified to accommodate the objectives of the study. All data regarding the prescribing of AMDs were documented which include: the name of AMD, the diagnosis, the duration of treatment, the documentation of the dose, route of administration, frequency of administration, use of the generic name, use of AMD from EML and the request of culture. The final form was produced after performing a pilot test to refine the study instrument. The pilot data were excluded from the final results of the study. The second instrument was a questionnaire consisting of eight questions conducted with the chief pharmacist in Ibrahim Malik Teaching Hospital to obtain data regarding the hospital indictors. For the analysis of the medical conditions of patients who were prescribed AMD, the documented diagnosis (professional or medical) was classified firstly according to the International Classification of Diseases ICD-10 [18], into 8 groups of diseases, and then the indications for antimicrobial prescribing documented in the medical records were reported. When more than one diagnosis was documented for the patient, if it included infectious disease, only the infectious disease was reported. Data were entered into the Statistical Package for Social Sciences (SPSS, version 20) and Microsoft Excel 2010. Descriptive analysis was conducted. The chi-square test was used to examine the association between the number of AMDs prescribed and the age, comorbidity, length of hospital stay and diagnosis. For the statistical significance, a p-value (<0.05) was considered significant. The research protocol was approved by the Directorate of Research, Ministry of Health and Khartoum State. Only data relevant to the study were extracted from the patient medical records, identifiable data were never taken from the medical records or used in a way that harms the patient, so the privacy and confidentiality were maintained.

 

 

Results Up    Down

The interview with the chief pharmacist revealed that the hospital lack structures that regulate the prescribing of antimicrobials. There was no drug and therapeutic committee (DTC), HF or EML specifically designed to the hospital; accordingly, the national EML was used in this study. Also, there was no STGs for infectious diseases as separate or as a part of comprehensive treatment guidelines adopted by the hospital. A total of 201(82%) out of 245 medical records examined were enrolled in the study in which at least one AMD was prescribed. Table 1 shows the demographic and clinical characteristics of study patients. The mean age of the study patients was 53.9±20.4 years with the age group (>65) representing (39.4%). Among the 201 patients, males represented 116 (57.7%). The median length of hospital stay was 6 days. Infectious and parasitic diseases (35.3%), diseases of the circulatory system (23.4%), and diseases of the digestive system (10%) were the most common medical conditions for patients who were prescribed AMDs Table 1. Table 2 shows the prescribing indicators for antimicrobial use. The percentage of antimicrobial prescribing among the randomly selected sample was (201/245) (82%). A total of 421 courses of AMDs were prescribed with an average number of 2.1 ±1.1 AMD per patient. The generic name was used in (35.6%) of all AMDs prescribed. The description and frequencies of AMDs courses are summarized in Table 3. Of the 201 patients who received AMDs, (32.2%) received one AMD, (41.3%) two AMDs and (26.4%) three or more AMDs. Indication documentation for which the AMD was prescribed and the route of administration was omitted in (56%) and (35.1%) of the total courses prescribed respectively. The culture was requested in 12 (6%) out of the 201 medical records, with only one result documented. Under the chi-square test, the length of hospital stay (p <0.001) and the type of diagnosis (p = 0.02) were associated with the number of AMDs prescribed (Table 4). Among the 15 classes of AMDs prescribed cephalosporins (49.1%) and metronidazole (21.4%) were the most prescribed (Table 5). By agents, ceftriaxone and metronidazole were the most prescribed AMDs (Table 5). The most common infectious disease for which antimicrobials were prescribed was pneumonia followed by malaria, (viral hepatitis, sepsis), and urinary tract infections (UTI) as shown in Table 6.

 

 

Discussion Up    Down

In this study, analysis of the demographic data showed that the majority (39.4%) of study patients were elders (>65 years). This may explain the high percentage of comorbidities (40.8%) among the study patients. In accordance with results reported elsewhere [19-22], out of the total of 201 patients (57.7%) were male. Among the 245 medical records that were randomly selected, the percentage of patients who were prescribed one or more antimicrobial was 201 (82%), comparable to a Ugandan study [23] which reported (79%), and lower than results observed in Pakistan [24] (89%,91%), but higher than those reported in Nepal, [19] Nigeria, [22] and one study conducted in the medicine ward in Elobeid teaching hospital in Sudan, [25] which were (29.5%), (40%), and (58%) respectively. Although there is no standard value for this indicator, this value (82%) is alarming because as the use of the antimicrobials is increased the development of AMR will increase too [26]. This finding indicates the need for further studies to assess the appropriateness of antimicrobial use. The average number of antimicrobials per patient was 2.1 which was in accordance with the results in Nepal study, [27] but higher than the results reported by Elfaki [25] and Deshmukh et al. [28] In the absence of standard values for the prescribing indicators which should be developed according to the local patterns of diseases, policies and treatment guidelines; this value should be kept as low as possible. However, it might be considered acceptable in hospital settings where the cases are more complicated. During the hospital stay (26.4%) of patients received 3 or more AMDs which was higher than the result observed in a study from Nepal, [19] but lower than the finding from an Indian study [28] in which the percentages were (15%) and (50.5%) respectively. This study revealed a significant relationship between the number of antimicrobials prescribed and the length of hospital stay. Patients who spent longer duration (>6 days) in the hospital received more than two AMDs in comparison to those who spent less than 6 days. This finding is consistent with a study carried out in India [29]. This association might be explained by the high risk of acquiring nosocomial infections with more prolonged exposure to the hospital environment [30]. We also expect that patients with longer hospital stay are more likely to be undergoing invasive and surgical procedures which increase the risk of infections [31]. Another significant relationship was found between the number of AMDs and the type of diagnosis. Patients whose primary diagnosis was infectious disease or diseases of the digestive system were more likely to receive more than two AMDs compared to patients with other types of diagnosis. Thus more attention is needed to these groups of patients.

 

The adjustment of antimicrobial therapy, according to the culture and sensitivity test results, is important to optimize the course of treatment and decrease the selection pressure by using antimicrobial drugs with a narrower spectrum [32]. Almost all prescriptions were empiric. The specimens for culture were requested for only 12(6%) patients; this indicates that the multiple prescribing of antimicrobials (three or more) was not due to change in regimen according to the sensitivity test result, but might be due to frequent unjustified changes in the regimen. The average duration of antimicrobial treatment was 4.9 days. To minimize the development of AMR, the clinical guidelines should guide the duration of antimicrobial therapy [1]. Concerning the documentation of the dose and frequency of administration they were reported in (93.1%) and (98.8%) of the prescribed AMDs, respectively. However, the route of administration was poorly documented, only in (64.9%) of the 421 prescribed courses of AMDs. The documentation of these elements is essential for optimizing patient care since it ensures the release of clear medication order while avoiding incorrect dose, route of administration, and dose frequency. The generic name was used in (35.6%) of the prescribed AMDs; this is comparable to Elfaki [25] result which was (37%). However, it was lower than those reported in Nigeria [22] and Nepal [27]. This result is obviously far away from the standard value advocated by the WHO (100%). Although in Sudan, the generic drugs in the market are much less than the brand, the use of the generic name in prescribing should be encouraged to avoid dispensing errors and duplication of treatment. Almost all (95.5%) of antimicrobials were prescribed from the national EML. The documentation of indication is one of the most critical standards for good practice, [33] that decreases inappropriate prescribing of antimicrobials [34]. Among the 201 reviewed medical records, the indication was documented in only 82 (40.8%) records. In the remaining 119 (59.2%) cases, there is a possibility of concomitant infectious disease which was not documented in the patient record in addition to the primary diagnosis on admission. However, this low percentage of documentation questions the rationale behind prescribing the AMDs. In Australia, the last national antimicrobial prescribing survey (NAPS) report revealed that the indication for antimicrobial prescription was documented in (72.5%) of the total prescription which was considered below the best practice of (>95%) [35].

 

Cephalosporins are still one of the most prescribed antibiotics in hospitals due to their wide spectrum and safety. In the current study, cephalosporins were the most prescribed class of antimicrobials constituting (49.1%) of all prescribed courses of AMDs. This is similar to what was reported in a one-day antibiotic usage audit conducted in Soba university hospital in Khartoum in 2011, in which (76%) of all prescribed antibiotics were cephalosporins [36]. Other studies from Nigeria [21] and Uganda [23] showed similar results. The third-generation cephalosporins constituted the majority of the total courses of AMDs prescribed in this study. This raises a concern regarding its impact on the development of ABR because of the collateral damage caused by this class of antibiotics [37], which favors the propagation of resistant bacteria [38]. Ceftriaxone and metronidazole were the most prescribed antimicrobial drugs. They were most likely used for the treatment of aspiration pneumonia, which is one of the complications of a cerebrovascular accident, a condition that is most frequently encountered among the diseases of the circulatory system. At the study time, the hospital lacks the structures that regulate the prescribing of antimicrobials like DTC, HF or EML, and STGs for infectious diseases. These structures have a leading role in the promotion of rational prescribing and reflect the commitment of the hospital towards the high quality of patient care [1]. One of the limitations of this study is that the findings cannot be generalized to other hospitals in Khartoum state. Also, the study did not assess the appropriateness of antimicrobial use which should be addressed by other studies in the future.

 

 

Conclusion Up    Down

The findings of this study showed a high percentage of antimicrobials prescribing among the random sample studied. Most of the antimicrobials were prescribed from the national EML. However, prescribing using the generic name was a matter of concern. The study revealed a problem of suboptimal documentation of route of administration and the indication for antimicrobials prescribed, both of them compromise the rational prescribing of antimicrobials. The third-generation cephalosporins were the most commonly prescribed class which may contribute to the emergence of AMR. The empiric therapy predominated in this study, which was indicated by a very low request of culture. Finally, the study revealed the lack of structures that regulate the prescribing of antimicrobials and promote its rational use in the hospital, like DTC, HF or EML, and STGs for infectious diseases. Several measures and strategies are needed to promote rational prescribing of AMDs like the introduction of the antimicrobial stewardship program, implementation of continuous educational programs for prescribers about rational prescribing of antimicrobials, as well as continuous supervision, audit and feedback.

What is known about this topic

  • Antimicrobial drugs are one of the most prescribed medicines;
  • The rational use of antimicrobial drugs includes prescribing when only indicated, use of the generic name, prescribing from the EML or HF, and adoption of STGs.

What this study adds

  • Antimicrobial drugs were highly prescribed in the internal medicine department;
  • The indication and route of administration were poorly documented;
  • The hospital lacks measures and structures that regulate the prescribing of antimicrobials like DTC, HF or EML and STGs for infectious diseases.

 

 

Competing interests Up    Down

The authors declare no competing interests.

 

 

Authors’ contributions Up    Down

Yousef B supervised all steps of the research and participated in study design. Abdalla S did the research from the design to data collection, analysis, and interpretation. All the authors have read and approved the final version of the manuscript.

 

 

Tables Up    Down

Table 1: demographic and clinical characteristics of study patients

Table 2: prescribing indicators for antimicrobial use in the Internal Medicine Department (N=201)

Table 3: description and frequencies of antimicrobial drugs prescribed for the study patients

Table 4: factors associated with prescribing multiple antimicrobial drugs

Table 5: frequencies of the antimicrobial drugs prescribed for the study patients by class and agents (N=421)

Table 6: frequencies of infectious diseases for which antimicrobials were prescribed

 

 

References Up    Down

  1. World Health Organization. How to Investigate Antimicrobial Use in Hospitals: Selected Indicators. 2012. Accessed 13 April 2017.

  2. Krivoy N, El-Ahal WA, Bar-Lavie Y, Haddad S. Antibiotic prescription and cost patterns in a general intensive care unit. Pharm Pract. 2007; 5(2): 67-73. PubMed | Google Scholar

  3. Trostle J. Inappropriate distribution of medicines by professionals in developing countries. Soc Sci Med. 1996; 42(8): 1117-20. PubMed

  4. Van der Meer JW, Gyssens IC. Quality of antimicrobial drug prescription in hospital. Clin Microbiol Infect. 2001; 7(Suppl 6): 12-5. PubMed | Google Scholar

  5. World Health Organization. The top 10 causes of death. Accessed 15 September 2019.

  6. World Health Organization. Sudan health profile 2015. 2017. Accessed 5 July 2017.

  7. Ambrus JL Sr, Ambrus JL Jr. Nutrition and infectious diseases in developing countries and problems of acquired immunodeficiency syndrome. Exp Biol Med (Maywood). 2004; 229(6): 464-72. PubMed | Google Scholar

  8. World Health Organization. Promoting rational use of medicines: core components. 2002. Accessed 23 July 2017.

  9. Couper MR. Strategies for the rational use of antimicrobials. Clin Infect Dis. 1997;24(Suppl 1): S154-6. PubMed | Google Scholar

  10. Hogerzeil HV. The concept of essential medicines: lessons for rich countries. BMJ. 2004;329(7475):1169-72. PubMed | Google Scholar

  11. World Health Organization. Guidance on the use of international nonproprietary names (INNs) for pharmaceutical substances. 1997. Accessed 1 July 2017.

  12. ASHP guidelines on preventing medication errors in hospitals. Am J Hosp Pharm. 1993; 50(2): 305-14. PubMed

  13. Haas JS, Phillips KA, Gerstenberger EP, Seger AC. Potential savings from substituting generic drugs for brand-name drugs: medical expenditure panel survey, 1997-2000. Ann Intern Med. 2005;142(11): 891-7. PubMed | Google Scholar

  14. Hellerstein JK. The importance of the physician in the generic versus trade-name prescription decision. Rand J Econ. 1998; 29(1): 108-36. PubMed | Google Scholar

  15. Sumpradit N, Chongtrakul P, Anuwong K, Pumtong S, Kongsomboon K, Butdeemee P et al. Antibiotics Smart Use: a workable model for promoting the rational use of medicines in Thailand. Bulletin of the World Health Organization. 2012; 90(12): 905-13. PubMed | Google Scholar

  16. Shlaes DM, Gerding DN, John JF, Craig WA, Bornstein DL, Duncan RA et al. Society for Healthcare Epidemiology of America and Infectious Diseases Society of America Joint Committee on the Prevention of Antimicrobial Resistance: guidelines for the prevention of antimicrobial resistance in hospitals. Clin infect Dis. 1997; 25(3): 584-99. PubMed | Google Scholar

  17. Dean AG, Sullivan KM, Soe MM. Open Source Epidemiologic Statistics for Public Health. Version 3.01. Accessed 1 February 20.

  18. World Health Organization. Classifications: ICD-11 is here! 2016. Accessed 4 April 2017.

  19. Shankar RP, Partha P, Shenoy NK, Easow JM, Brahmadathan KN. Prescribing patterns of antibiotics and sensitivity patterns of common microorganisms in the Internal Medicine ward of a teaching hospital in Western Nepal: a prospective study. Ann Clin Microbiol Antimicrob. 2003; 2: 7. PubMed | Google Scholar

  20. Ahmad A, Revanker M, Haque I, Pravina A, Ivan R, Dasari R et al. Study the Prescription Pattern of Antibiotics in the Medicine Department in a Teaching Hospital: A Descriptive Study. International Journal of Toxicological and Pharmacological Research. 2014; 6(2): 43-46.

  21. Khan FA, Singh VK, Sharma S, Singh P. A prospective study on the antimicrobial usage in the medicine department of a tertiary care teaching hospital. J Clin Diagn Res. 2013; 7(7): 1343-6. PubMed | Google Scholar

  22. Iliyasu G, Dayyab FM, Bolaji TA, Habib ZG, Takwashe IM, Habib AG. Pattern of antibiotic prescription and resistance profile of common bacterial isolates in the internal medicine wards of a tertiary referral centre in Nigeria. J globl Antimicrob Resist. 2015; 3(2): 91-4. PubMed | Google Scholar

  23. Kiguba R, Karamagi C, Bird SM. Extensive antibiotic prescription rate among hospitalized patients in Uganda: but with frequent missed-dose days. J Antimicrob Chemother. 2016; 71(6): 1697-706. PubMed | Google Scholar

  24. Atif M, Azeem M, Saqib A, Scahill S. Investigation of antimicrobial use at a tertiary care hospital in Southern Punjab, Pakistan using WHO methodology. Antimicrob Resist Infect Control. 2017; 6: 41. PubMed | Google Scholar

  25. Elfaki ASM. Assessment of Antibiotics prescription in Hospitalized Patients at Elobeid Hospital, Sudan. Sudan Journal of Medical Sciences. 2009; 4(3): 269-72. Google Scholar

  26. Ventola CL. The Antibiotic Resistance Crisis: Part 1: Causes and Threats.PT. 2015; 40(4): 277-83. PubMed | Google Scholar

  27. Paudel KR, Sharma M, Das BP. Prevalence of antimicrobial chemotherapy in hospitalized patients in the department of internal medicine in a tertiary care center. Nepal Med Coll J. 2008; 10(2): 91-5. PubMed | Google Scholar

  28. Deshmukh V, Khadke V, Patil A, Lohar P. Study of prescribing pattern of antimicrobial agents in indoor patients of a tertiary care hospital. Int J Basic Clin Pharmacol. 2013; 2(3): 281-5.

  29. Bansal D, Mangla S, Undela K, Gudala K, D'Cruz S, Sachdev A et al. Measurement of Adult Antimicrobial Drug Use in Tertiary Care Hospital Using Defined Daily Dose and Days of Therapy. Indian J Pharm Sci. 2014; 76(3): 211-7. PubMed | Google Scholar

  30. Weber DJ, Rutala WA, Miller MB, Huslage K, Sickbert-Bennett E. Role of hospital surfaces in the transmission of emerging health care-associated pathogens: norovirus, Clostridium difficile, and Acinetobacter species. Am J Infect control. 2010; 38(5 Suppl 1): S25-33. PubMed | Google Scholar

  31. Jeon CY, Neidell M, Jia H, Sinisi M, Larson E. On the Role of Length of Stay in Healthcare-Associated Bloodstream Infection. Infect Control Hosp Epidemiol. 2012; 33(12): 1213-8. PubMed | Google Scholar

  32. Leekha S, Terrell CL, Edson RS. General Principles of Antimicrobial Therapy. Mayo Clin Proc. 2011; 86(2): 156-167. PubMed | Google Scholar

  33. Vercheval C, Gillet M, Maes N, Albert A, Frippiat F, Damas P et al. Quality of documentation on antibiotic therapy in medical records: evaluation of combined interventions in a teaching hospital by repeated point prevalence survey. Eur J Clin Microbiol Infect Dis. 2016; 35(9): 1495-500. PubMed | Google Scholar

  34. Yeo JM. Antimicrobial stewardship: Improving antibiotic prescribing practice in a respiratory ward. BMJ Qual Improv Rep. 2016 5(1): u206491.w3570. PubMed | Google Scholar

  35. National Centre for Antimicrobial Stewardship and Australian Commission on Safety and Quality in Health Care. Antimicrobial prescribing practice in Australian hospitals: Results of the 2015 National Antimicrobial Prescribing Survey. Sydney; 2016.

  36. Yousif MMA. The prevalence of Extended Spectrum β-lactamase and AmpC- Producing Bacteria in a Sudanese Tertiary Hospital. Sudan Med J. 2015; 50(3): 10-17. Google Scholar

  37. Elhag K. Diversification of antibiotics as a means to control antimicrobial resistance and improve treatment options in Sudan. Sudan Med J. 2013; 49(3): 128-135. Google Scholar

  38. Kheder S. Cephalosporin Usage and Resistance Trend in a Sudanese Hospital Surgical Wards. J Pharm Biomed Sci. 2011; 11(3): 1-6. Google Scholar