http://orcid.org/0000-0001-5032-7181
Figures
Abstract
Background
Antimicrobial resistance (AMR) has become an emerging issue in the developing countries as well as in Bangladesh. AMR is aggravated by irrational use of antimicrobials in a largely unregulated pluralistic health system. This review presents a ‘snap shot’ of the current situation including existing policies and practices to address AMR, and the challenges and barriers associated with their implementation.
Methods
A systematic approach was adopted for identifying, screening, and selecting relevant literature on AMR situation in Bangladesh. We used Google Scholar, Pubmed, and Biomed Central databases for searching peer-reviewed literature in human, animal and environment sectors during January 2010-August 2019, and Google for grey materials from the institutional and journal websites. Two members of the study team independently reviewed these documents for inclusion in the analysis. We used a ‘mixed studies review’ method for synthesizing evidences from different studies.
Result
Of the final 47 articles, 35 were primary research, nine laboratory-based research, two review papers and one situation analysis report. Nineteen articles on human health dealt with prescribing and/or use of antimicrobials, five on self-medication, two on non-compliance of dosage, and 10 on the sensitivity and resistance patterns of antibiotics. Four papers focused on the use of antimicrobials in food animals and seven on environmental contamination. Findings reveal widespread availability of antimicrobials without prescription in the country including rise in its irrational use across sectors and consequent contamination of environment and spread of resistance. The development and transmission of AMR is deep-rooted in various supply and demand side factors. Implementation of existing policies and strategies remains a challenge due to poor awareness, inadequate resources and absence of national surveillance.
Citation: Hoque R, Ahmed SM, Naher N, Islam MA, Rousham EK, Islam BZ, et al. (2020) Tackling antimicrobial resistance in Bangladesh: A scoping review of policy and practice in human, animal and environment sectors. PLoS ONE 15(1): e0227947. https://doi.org/10.1371/journal.pone.0227947
Editor: Eili Y. Klein, Johns Hopkins University, UNITED STATES
Received: March 31, 2019; Accepted: January 4, 2020; Published: January 27, 2020
Copyright: © 2020 Hoque et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All relevant data are within the paper
Funding: This work was supported by the UK Antimicrobial Resistance Cross Council Initiative supported by the seven research councils in partnership with the Department of Health, the Department of Environment, Food and Rural Affairs and the Global Challenges Research Fund (ES/P004563/1). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Introduction
The world is on the verge of sliding back to ‘pre-antibiotic era’ due to evolving resistance against life-saving antimicrobial drugs, with fundamental effect on individual and public health [1]. To combat this emerging global threat in a comprehensive manner, the World Health Organization (WHO) launched a Global Action Plan (GAP) in 2015 based on a ‘One Health’ approach—emphasizing the interdependence of human health, animal health, and the environment [2]. Recently, the interconnectedness of combating antimicrobial resistance (AMR) and achieving Universal Health Coverage (UHC) by 2030 has also been emphasized [3].
The southeast Asia is considered to have the highest risk of AMR among all the WHO regions [4]. Most of the countries in this region have some policy structure (either policy-in-place or policy-in-making) regarding the use of antimicrobials in food animals and fish. For example, the use of antimicrobials is banned as a food additive in some of these countries for rearing food animals, but implementation remains a problem due to the weak regulatory regime [5]. This is also true for policies to prevent contamination of the environment with antimicrobial residues from human and animal use [6].
In many of these countries, antimicrobials are widely available as over-the-counter (OTC) drug, Bangladesh is no exception [7]. The presence of a ‘pluralistic’ health system involving unqualified providers in the informal sector complicates the situation [8]. This is aggravated by the aggressive and unethical marketing practices of the pharmaceutical companies [9]. The regulatory regime in Bangladesh is weak concerning human, technical and logistic capacity to oversee this vast market [10].
Policies and regulations that support appropriate and rational use of antimicrobials are essential for effective interventions to contain the development and spread of AMR. Bangladesh has recently approved a National Action Plan (NAP) for containing AMR, in alignment with the WHO GAP guidelines [11]. For implementation of NAP, detailed information on the current AMR situation in Bangladesh in the human, animal and environment sectors is needed for concerted and coordinated actions across the sectors. Some small-scale studies reported patterns of antimicrobial prescription and use, non-compliance of dosage and development of resistance, and strategies to contain it in different sectors in Bangladesh; however, none so far has looked into the matter comprehensively. This scoping review aimed to fill-in this knowledge gap by examining the nature and extent of the problem in different sectors (human, animal, and environment) in Bangladesh, and exploring how the AMR issue is addressed in policy and practice and associated challenges and opportunities, and how it can be contextualized in the larger paradigm of ‘One Health’ for comprehensive tackling of this public health emergency.
Methods
To conduct this scoping review, we developed a protocol which specified the study objectives, research questions, inclusion/exclusion criteria, and data sources/search engines to be used (Google for unpublished/grey materials; Google Scholar, PubMed, and BioMed Central for peer-reviewed articles) (Table 1). We hand searched for relevant grey materials/unpublished documents from the institutional and journal websites. The key search terms were fixed, for all three sectors such as human, animal and environment (Table 2). A PRISMA extension for Scoping Reviews (PRISMA-ScR) checklist was filled-in to complete this report (S1 Table).
We followed the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) approach for selection of articles on current AMR situation and relevant policies and practices to be included in the analysis (Fig 1).
Data extraction and analysis
We used a ‘mixed studies review’ method for synthesizing evidence from qualitative, quantitative and mixed method studies which are useful in understanding complex public health interventions and programmes [12]. A data extraction matrix was used for organizing data, disaggregated into three key themes e.g., current antimicrobial situation (prescribing pattern, use and compliance); perception regarding irrational use of antimicrobials and emergence of AMR (providers, users); and current policies and practices related to antimicrobial use, including relevant sub-themes under each category (Table 3). The study team members critically appraised the selected articles under the guidance of principal investigator, as per PRISMA checklist. Studies that mainly focused on antimicrobial resistance in the human, animal and environment sectors in Bangladesh were included for analysis. Differences in thematic (or sub-thematic) categorization or interpretation of the evidences were resolved by discussion among the study team members under the supervision of the senior investigator to reach a consensus with additional revisions as deemed necessary.
Results
We used Google, Google Scholar, Pubmed, and BiomedCentral databases for searching relevant literature from Bangladesh. Ultimately, 47 articles (AMR situation in human health = 36 and AMR situation in animal and environment = 11) were included for analysis. Of these, 35 were primary research, nine laboratory-based research, two review papers and one situation analysis report. Again, 19 of the articles on human health dealt with antimicrobial prescribing and/or use, five with self-medication, two on non-compliance of dosage, and 10 were on antibiotics sensitivity and resistance patterns. For AMR scenario in animals and environment, five papers focused on use in animals and six papers on environmental contamination. Besides, current health and drug-related policies and strategies for both humans and animals, and national action plan for containment of AMR in Bangladesh were included through hand search and grey literature search using Google. The findings from the review are described below according to key themes of the study.
AMR situation in humans: (Table 4)
Prescribing pattern, use.
Several small-scale studies reported on antimicrobial prescribing and its use, varying by factors such as age and sex. For example, children (66%) were prescribed more antimicrobials than adults (44%) [13], and the rate of prescribing antimicrobials was higher at the extremes of ages [14], and for males [15]. Higher-generationantimicrobials (e.g., ceftriaxone, ciprofloxacin, azithromycin) were prescribed quite frequently [14,16,28,31], especially by the physicians [16]. A study from a slum in Dhaka shows that awareness-building education may improve rational use of antimicrobials, by reducing prescription generation and/or its indiscriminate use [17]. Studies reveal two or more antimicrobials to be commonly prescribed at a time in Bangladesh [14,15,18,19,20,22,30,31], and more antimicrobials to be prescribed in hospital settings compared to community settings [21]. Prescribing antibiotics without laboratory tests was quite common in Bangladesh due to reported lack of testing facilities [18,19,22]. However, sometimes the qualified prescribers (e.g., in-service trainee doctors of medical college hospital) felt confident enough to select an appropriate antimicrobial and prescribe correct dose and duration based on clinical diagnosis [23]. This was also reiterated in a simulated patient study where antimicrobials were prescribed (71%) based on clinical acumen [24]. Qualified prescribers from some secondary and tertiary level hospitals were found to be aware of the treatment guidelines [25], but not those from the upazila (sub-district) hospitals [26]. Sometimes, standard treatment guidelines were not available [27]. Antimicrobials were commonly prescribed for fever, common cold, cough, diarrhea and ARI [16,19,26].
Non-compliance, self-treatment.
Patients’ non-compliance with scheduled dosage, and consequently facilitating the emergence of AMR, was a common phenomenon found in the literature reviewed [18,28,32,33]. This may be as high as 50% as patients used to stop taking antimicrobials as soon as the symptoms alleviated [18]. When prescribed antimicrobials did not work in the short-term, patients usually considered the doctors as incompetent [32,33].
The prevalence of self-treatment (taking medicine without consulting a qualified provider) in the reviewed studies was found to be quite high [33–38]. It was found to be common for illnesses such as dysentery, diarrhoea and food poisoning (36%); cold, cough and fever (28%); and presumed infection of some sort (13%) [34]. Reasons behind this self-treatment practice included advice from traditional healers (41%), prior experience with the particular antibiotic for the particular illness (33%), knowledge about antibiotics (17.5%), and waving doctors’ consultation fees (1%). Besides, practice of self-medication was also found to be associated with poverty [38].
Antimicrobials sensitivity and resistance.
Ten papers reported on antibiotic susceptibility testing and resistance patterns. Resistance against antibiotics like imipenem was found in uropathogens [39]. Susceptibility testing of clinical isolates demonstrated many of the common organisms such as E. coli, and S. typhi to be resistant to low-cost and commonly used antibiotics [40–43]. Mannan et al [40] collected 70 types of clinical isolates from samples of blood, sputum, urine and pus and found 64% of isolated S. typhi to be resistant to multiple antibiotics. Another study conducted in three tertiary level hospitals in Dhaka shows resistance against older and commonly used antimicrobials in E. coli, S. aureus, Pseudomonas and Klebsiella infections in 50% of the cases [41]. In 70% of cases, uncertainty about diagnosis was also a reason for prescribing excess antimicrobials. Antimicrobial sensitivity tests conducted on 2,016 culture positive urine samples from a tertiary medical college hospital in Bangladesh found E. coli in 84% of cases, which was resistant to amoxicillin in 82% of cases [42]. Similar results of low sensitivity of E. coli against amoxicillin were also observed in another study involving isolates from public and private hospitals, and clinics and diagnostic centres in Dhaka city [43].
In a recent study, Tarana et al [44] reported that Salmonella typhi was found sensitive to amikacin (70%), azithromycin (73%), ceftazidime (63%), ceftriaxone (67%) and ciprofloxacin (87%). Another study (2017) found E. coli in 86% of urine samples collected from a private medical college hospital in Dhaka which was highly resistant to amoxicillin (95%) [45]. More than 80% of MRSA isolates are also found to be sensitive to some macrolides (tobramycin, gentamycin) and carbapenem (meropenem) with resistant to ampicillin, amoxicillin, cefixime and azithromycin [46]. Antibiogram from a private sector tertiary hospital over three years (2016–2018) shows that the last resort antimicrobials (Polymyxin B and Colistin) retained their high sensitivity to Klebsiella, Psudomonos, and E. coli [47]. A review by GARP- Bangladesh National Working Group provided a descriptive analysis of the AMR situation in different sectors along with recommendations [48].
Situation in food animals, fisheries, and environment including spread of AMR (Table 5)
A high percentage of poultry meat and eggs meant for human consumption were found to have antimicrobial residues such as tetracycline, ciprofloxacin, enrofloxacin and amoxicillin [49,50]. The prevalence of antibiotic residues varied from >60% in liver, kidney, and eggs to around 50% in breast and thigh samples[49]. In Bangladesh, 3,079 metric tons of poultry manure is produced per day and 50% of this is directly used in aquaculture [51]. For example detectable amount of oxytetracycline residues was traced in 25% Pangas fish samples from Sylhet Sadar [52]. This has resulted in the presence of pathogenic bacteria resistant to commonly used antimicrobials in water resources and salad vegetables which are significant from a public health perspective [53–57]. The prevalence of Salmonella species was found to vary between 60% to 78% in different street foods in Chittagong while multidrug resistant Salmonella was found in each of the food items tested [58]. Besides, antimicrobials were found to be used routinely to increase food animal production, resulting in the spread of antibiotic resistant organisms from farms to environment to community [53]. Around 24% of goat farmers mentioned that they were familiar with the term antibiotic but none of them had any idea about antimicrobial resistance nor withdrawal period [58]. The hospitals of Dhaka city are also contributing to the process by discharging untreated medical wastes in the water, resulting in the presence of high-levels of resistant E. coli in the water [53]. This environmental contamination contributes to wild life infections from humans and animals e.g., the presence of multidrug resistance enterococcus in free-range wildlife and Shiga Toxin- producing E.coli in Buffalo faeces [59].
Current policies and strategies to contain AMR in Bangladesh
Quite a number of policies, guidelines, ordinances and laws relevant to containment of AMR in human, food animal, and environment sectors currently exist in Bangladesh (S1 Table). Of these, seven (human = 3; animal and environment = 4) addressed the AMR issue.
S1 Table: Table comparing different policies and regulations in the human, animal and environment sectors in Bangladesh.
Since the updated National Drug Policy 2016 [60], the government of Bangladesh (GoB) has developed three major policy documents/guidelines with direct implications on the prevention and control of AMR in human sector: i) Pharmacovigilance and Adverse Drug Reaction (ADR) Policy 2017 for monitoring the sale and dispensing of drugs without prescription; ii) Standard Treatment Guideline (STG) for appropriate use of antimicrobials in the sub-districts; and iii) a guideline for antimicrobial stewardship developed by the country’s premiere medical university (S1 Table). These policy documents dealt with different aspects of prevention and control of AMR in clinical settings.
In 2007, the Ministry of Fisheries and Livestock (MoFL) formulated the National Livestock Development Policy where they highlighted inadequate veterinary services and weak implementation of regulatory frameworks as barriers to address AMR in this sector (S1 Table). Specific laws on different aspects of food animals and fish were developed in 2010 where the use of antimicrobials, growth hormones, and pesticides were banned. For violating this law, a person might face up to one year's imprisonment or a fine of up to BDT 50,000 only (USD 650). These documents highlighted issues such as mandatory prescription for antibiotics sale, list of preferred antibiotics for illnesses of a particular system, and 1st and 2nd lines of choice of antibiotics for specific infecting organisms. Banning the general use of antibiotics as a growth factor is emphasized in documents pertaining to the animal sector. To prevent contamination of the environment, specific guidelines are advised for waste management e.g., Guideline for Assessment of Effluent Treatment Plant 2008, Medical Waste Management and Processing Rule 2008, and Environment Protection Act 1995. Interestingly, none of these made any specific reference to the problem of AMR (S1 Table).
Finally, a National Action Plan 2017–2022 for containing AMR in Bangladesh has been prepared by the Disease Control Unit of the Director General of Health Services, MoHFW with a road map for its implementation in alignment with the global plan [61]. The document emphasizes rational use of antibiotics in all sectors through the formulation of standard treatment guidelines, antibiotic stewardship, development of reference laboratories, Good Manufacturing Practice (GMP), Good Pharmacy Practice (GPP), infection prevention and control, and establishment of a comprehensive surveillance.
Discussion
This scoping review revealed widespread availability of antimicrobials without prescription in Bangladesh, a rising trend in its irrational use in humans and food animals and fisheries, and consequent spread of resistant strains through environmental contamination. The policies and strategies to contain AMR are at an early stage of development in the country and implementation remains a major challenge. This is due to poor awareness about AMR among the policy makers and practitioners, inadequate resources to implement measures to contain AMR, and absence of a comprehensive national surveillance system to monitor the emergence of AMR. The implications of these findings in the context of the emerging ‘One Health’ movement in the country is discussed, including some recommendations for tackling the problem urgently.
Supply and demand side factors facilitating the emergence of AMR
It is obvious from the findings that the factors underlying irrational and inappropriate use of antimicrobials, and consequent emergence of AMR in Bangladesh, have both supply and demand side perspectives. On the supply side, all categories of the allopathic practitioners whether qualified or not, are prone to use ‘excess’ antimicrobials due to poor awareness regarding its rational use. Other factors contributing to the emergence of AMR include lack of diagnostic facilities, burgeoning private practice and unreasonable demand for antibiotics from patients and ‘caregivers’, especially for children. Besides, there are aggressive marketing strategies of the pharmaceutical companies specifically aimed at generating prescriptions at the cost of patients. This scenario is not unlike that found in other countries of the region such as India [62], Indonesia [63], Malaysia [64], Nepal [65], and Laos [66] irrespective of specialties.
Encouragingly, attempts have been made to overcome the ‘gaps’ in knowledge and use of antimicrobials by these countries which have implication for Bangladesh. For example, the Indian Council of Medical Research (ICMR) brought a qualified group of prescribers in a workshop to enhance their knowledge on AMR and related issues, and involved them in preparing guidelines for rational prescription of antimicrobials [67]. GARP-Nepal is working to outline the components of national strategy for prevention of AMR in Nepal [65]. Indonesia and Malaysia have national level committees to monitor antimicrobial prescription and promote its rational use [68]. These countries hosted a dedicated website for consumer awareness and education regarding rational use of antimicrobials and included schools in the campaign. Besides, the ASEAN countries also included standard treatment guidelines, pharmacovigilence and problem-based pharmacotherapy in their core medical curriculum [68].
In the demand side, rising trend of antimicrobials use resulting from poor consumer awareness on dangers of inappropriate use, use as a stop-gap measure, non-compliance with dosage, and self-medication as observed in Bangladesh are also common in India [69–71], Sri Lanka [72], Nepal [73], Pakistan [74], Indonesia [75,76], and Vietnam [77]. Due to poor level of awareness, sometimes the physicians are pressurized by the patients and/or their caregivers to prescribe antimicrobials especially in urban areas, without any proper indication. In many instances, antibiotics are used as a 'quick & cheap' alternative by both the patients/caregivers and the providers, including use for self-medication [78].
In this review, we found a large proportion of medical practitioners and students in Bangladesh unaware about the guidelines on the use of antimicrobials. The urgency of including this in the graduate curriculum cannot be overemphasized. Coupled with stringent implementation of regulatory measures in the production and distribution of antimicrobials, with appropriate incentives (‘carrot and stick’ approach), will go a long way in mitigating the AMR problem.
Policies and strategies are there, but implementation remains a challenge
There is no dearth of policies and strategies especially since 2014, but operationalization of these remains a challenge which is true for implementing any public policy in general in Bangladesh [79], including the SDGs [80]. Bangladesh is one of the 100 countries with National Action Plan for containment of AMR developed (as of March 2018), however, a recent review of the Action Plans identified some challenges for its implementation in LMICs like Bangladesh [81]. These include lack of functional mechanism for implementation or coordination, lack of adequate financial and institutional resources for relevant capacity and means for infection prevention and control (e.g., through WASH activities), and building awareness and political commitment. To address these challenges, measures such as mainstreaming of the AMR containment process across sectors, adequate resourcing through national budgets and annual development plans, and inter-sectoral coordination for infection prevention and control are suggested [81].
The way forward?
The importance of building awareness among the policy-makers for coordinated action across the sectors, updating medical and allied health sciences curriculum for rational use of medicines including antimicrobials, and adequate resourcing with budget and human resources cannot be overemphasized. Again, for the very fundamental task of infection prevention and control in LMICs like Bangladesh, the implementation of WASH activities has an important role to play by reducing the transmission of resistant strains in the environment [82–84]. This is plausible as factors such as poor sewage system; poor infection prevention and control in the hospitals, clinics, education institutions and workplaces; and poor sanitation facilities, and hygiene practices contribute to the spread of resistant strains from environment to food chain. The percentage of resistant isolates may be higher in humans compared to the environment (e.g., animal stool and water sample), but the load (number of resistant isolates/sample) is higher in environment which acts as a reservoir of resistant genes [85]. Though Bangladesh has travelled a long way in controlling open defaecation through much lauded Community Led Total Sanitation (CLTS), the environment remains highly contaminated with faecal matter [86]. In the transition, Bangladesh moved to primitive pit latrines instead of household improved latrine; 60% of the population have onsite sanitation facilities including pit latrines, but onsite sludge management is lacking. In Dhaka, 22% of the households are connected to a sewer system, but only 2% of faecal sludge is estimated to be properly treated. Though majority of the people have access to better quality water for drinking, contamination with microbes, arsenic or salts in pockets is alarming. For example, 80% of piped water is found to be contaminated with E. coli [86]. The situation is exacerbated by the absence of good hygiene practices which multiplies the effects of unsafe water and sanitation. This importance of WASH interventions is highlighted by a recent Chatam House review of the progress of the AMR situation where the author emphasized the need for more investments in WASH for sustainable containment of AMR over long run in the LMICs [87]. This should alert the policy-makers as provision of sustainable WASH services to the population has implications on overall human development (e.g., stunting, educational attainment) and long-term poverty reduction strategy in Bangladesh.
The problem of AMR is multi-sectoral, multi-disciplinary, and multi-institutional and thus need a coordinated response of the three sectors, adopting a comprehensive approach such as that of One Health. The outbreak of avian influenza in Bangladesh in 2007 exposed the vulnerability of the country to transmission of infection from animals and environment. In 2008, stakeholders in the human, animal and environmental sectors came together to promote the concept of ‘One Health’ in Bangladesh [88]. As a consequence of this movement, the GoB came up with the ‘National One Health Strategy’ in 2012 [89]. In 2016, a One Health Secretariat was established at the IEDCR with staff from three ministries (human health, animal health and environment) and support from the development partners [90]. However, improving awareness among professionals and practitioners across the sectors for consensus actions, and coordination among different sectors and ministries remain a major challenge to move forward. Given the poor state of Bangladesh to ‘prevent-detect-respond’ to health emergencies (i.e., outbreaks of epidemics and pandemics including AMR) as revealed by Global Health Security Index (Bangladesh occupying 113/195 position, scoring 35/100), there is little time to waste [91].
Limitations
In this scoping review of AMR situation in Bangladesh, we tried to gather maximum available information. However, due to restricted access to some of the databases, the search may not be exhaustive. Besides, there was dearth of published materials on this topic in general, and particularly in some sectors such as the contribution of environmental contamination in initiating and propagating AMR. The included articles were critically appraised but the weighted ratings were not done.
Conclusion
The factors for the development and transmission of AMR in Bangladesh are deep-rooted in various supply and demand side factors. However, irrational use of antimicrobials in, and beyond, human health sector (e.g., animal health and environment) is aggravating the situation and posing a threat to human health. To address this comprehensively, multi-sectoral and multi-stakeholder efforts are needed based on the strategy of ‘One Health.’ For this, critical awareness of the problem across the sectors and professionals, high level political commitment, intra and inter-ministerial coordination among relevant sectors, and enforcement of regulatory regime are urgently warranted.
Supporting information
S1 Table. Policies and regulations in Bangladesh relevant to prevention and control of AMR.
https://doi.org/10.1371/journal.pone.0227947.s001
(DOCX)
S2 Table. PRISMA-ScR checklist for “Tackling antimicrobial resistance in Bangladesh: A scoping review of policy and practice in human, animal and environment sectors” (PONE-D-19-07275).
https://doi.org/10.1371/journal.pone.0227947.s002
(DOCX)
Acknowledgments
This study forms part of a larger study titled ‘Pathways of antibiotic use in humans and animals in Bangladesh (PAUSE)’ funded by the Economic and Social Research Council and the Global Challenge Research Fund (ES/P004563/1) and we acknowledge our partners Loughborough University, UK, and icddr,b, Bangladesh for their encouragement and cooperation to take this forward.
References
- 1.
AMR Review (2016), Tackling Drug-Resistant Infections Globally: final report and recommendations, London: AMR Review, https://amr-review.org/sites/default/files /160525_Final%20paper_with%20cover.pdf.
- 2.
WHO. Global action plan on antimicrobial resistance. Geneva, Switzerland: World Health Organization, 2015. Available from: http://www.wpro.who.int/entity/drugresistance/resources/globalactionplaneng.pdf.
- 3. Bloom G, Merrett GB, Wilkinson A, Lin V, Paulin S. Antimicrobial resistance and universal health coverage. BMJ Global Health. 2017;2(4):e000518. pmid:29225955
- 4. Chereau F, Opatowski L, Tourdjman M, Vong S. Risk assessment for antibiotic resistance in South East Asia. BMJ. 2017;358:j3393. pmid:28874338
- 5. Goutard FL, Bordier M, Calba C, Erlacher-Vindel E, Gochez D, de Balogh K, et al. Antimicrobial policy interventions in food animal production in South East Asia. BMJ. 2017;358:j3544. pmid:28874351
- 6. Lundborg CS, Diwan V, Pathak A, Purohit MR, Shah H, Sharma M, et al. Protocol: a ‘One Health’ two year follow-up, mixed methods study on antibiotic resistance, focusing children under 5 and their environment in rural India. BMC Public Health. 2015;15(1):1321.
- 7. Ahmed SM, Hossain MA. Knowledge and practice of unqualified and semi-qualified allopathic providers in rural Bangladesh: implications for the HRH problem. Health Policy. 2007;84(2–3):332–43. pmid:17618702
- 8. Ahmed SM, Hossain MA, Chowdhury MR. Informal sector providers in Bangladesh: how equipped are they to provide rational health care? Health Policy and Planning. 2009;24(6):467–78. pmid:19720721
- 9. Mohiuddin M, Rashid SF, Shuvro MI, Nahar N, Ahmed SM. Qualitative insights into promotion of pharmaceutical products in Bangladesh: how ethical are the practices? BMC Med Ethics. 2015;16(1):80. pmid:26625723
- 10. Ahmed SM, Naher N, Hossain T, Rawal LB. Exploring the status of retail private drug shops in Bangladesh and action points for developing an accredited drug shop model: a facility based cross-sectional study. J Pharma Pol Prac. 2017;10(1):21. pmid:28702204
- 11.
Ministry of Health and Family Welfare (MoHFW), Government of Bangladesh. National Action Plan: Antimicrobial Resistance Containment in Bangladesh 2017-’22. Available from: https://www.flemingfund.org/wp- content/uploads/ d3379eafad36f597500cb07c21771ae3.pdf.
- 12. Pluye P, Hong QN. Combining the power of stories and the power of numbers: mixed methods research and mixed studies reviews. Ann Rev Pub Health. 2014;35:29–45.
- 13. Datta SK, Paul TR, Monwar M, Khatun A, Islam MR, Ali MA, et al. Patterns of prescription and antibiotic use among outpatients in a tertiary care teaching hospital of Bangladesh. Int J Pharm Pharm Sci. 2016;8(11):54.
- 14. Fahad B, Matin A, Shill M, Asish K. Antibiotic usage at a primary health care unit in Bangladesh. Australasian Medical Journal (Online). 2010;3(7):414.
- 15. Begum MM, Uddin MS, Rahman MS, Nure MA, Saha RR, Begum T, et al. Analysis of prescription pattern of antibiotic drugs on patients suffering from ENT infection within Dhaka Metropolis, Bangladesh. Int J Basic Clinic Pharmacology. 2017;6(2):257–64.
- 16. Sayeed MA, Iqbal N, Ali MS, Rahman MM, Islam MR, Jakaria M. Survey on Antibiotic Practices in Chittagong City of Bangladesh. Bangladesh Pharmaceutical Journal. 2015;18(2):174–8.
- 17. Chowdhury F, Sturm-Ramirez K, Al Mamun A, Iuliano AD, Chisti MJ, Ahmed M et al. Effectiveness of an educational intervention to improve antibiotic dispensing practices for acute respiratory illness among drug sellers in pharmacies, a pilot study in Bangladesh. BMC Health Serv Res. 2018;18(1):676. pmid:30170573
- 18. Haque MA. Antimicrobial use, prescribing, and resistance in selected ten selected developing countries: A brief overview. Asian J Pharm Clin Res. 2017;10(8):37–45.
- 19. Biswas M, Roy DN, Rahman MM, Islam M, Parvez GM, Haque MU et al. Doctor’s prescribing trends of antibiotics for out-patients in Bangladesh: A cross-sectional health survey conducted in three districts. Int J Pharma Sciences Res. 2015;6(2):669–75.
- 20. Ahmed S, Korpe P, Ahmed T, Chisti MJ, Faruque AS. Burden and Risk Factors of Antimicrobial Use in Children Less Than 5 Years of Age with Diarrheal Illness in Rural Bangladesh. Am J Trop Med Hyg. 2018 Jun 6;98(6):1571–6. pmid:29714159
- 21. Rashid MM, Chisti MJ, Akter D, Sarkar M, Chowdhury F. Antibiotic use for pneumonia among children under-five at a pediatric hospital in Dhaka city, Bangladesh. Patient Prefer Adherence. 2017;11:1335. pmid:28831244
- 22. Ata M, Hoque R, Biswas RS, Mostafa A, Hasan FU, Barua HR. Antibiotics prescribing pattern at outpatient department of a tertiary medical college hospital. Chattagram Maa-O-Shishu Hospital Medical College Journal. 2018;17(2):36–9.
- 23. Hoque R, Mostafa A, Haque M. Intern doctors’ views on the current and future antibiotic resistance situation of Chattagram Maa O Shishu Hospital Medical College, Bangladesh. Therapeutics Clinic Risk Management. 2015;11:1177. pmid:26316762
- 24. Islam MS. Irrational Use of Drugs, Healthcare Level and Healthcare Expenditure in Bangladesh. Int J Health Econ Policy. 2017 Oct 11;2(4):152.
- 25. Afreen S, Rahman MS. Adherence to treatment guidelines in a university hospital: Exploration of facts and factors. Bangladesh J Pharmacol. 2014;9(2):182–8. https://doi.org/10.3329/bjp.v9i2.18537
- 26. Ahmed SM, Islam QS. Availability and rational use of drugs in primary healthcare facilities following the national drug policy of 1982: is Bangladesh on right track? J Health Popul Nutr. 2012;30(1):99. pmid:22524126
- 27. Faiz MA, Basher A, editors. Antimicrobial resistance: Bangladesh experience. Regional Health Forum. 2011;15(10: 1–8. Available from: http://origin.searo.who.int/publications/journals/regional_health_forum/media/2011/V15n1/rhfv15n1p1.pdf
- 28. Chouduri AU, Biswas M, Haque MU, Arman MS, Uddin N, Kona N, et al. Cephalosporin-3G, Highly Prescribed Antibiotic to Outpatients in Rajshahi, Bangladesh: Prescription Errors, Carelessness, Irrational Uses are the Triggering Causes of Antibiotic Resistance. J Appl Pharm Sci. 2018;8(06):105–12.
- 29. Paul TR, Hamid MR, Alam MS, Nishuty NL, Hossain MM, Sarker T et al. Prescription Pattern and Use of Antibiotics Among Pediatric Out Patients in Rajshahi City of Bangladesh. Int J Pharm Sci Res. 2018;9(9):3964–70.
- 30. Shamsuddin AK, Rahman MS, Sultana N, Islam MS, Shaha AK, Karim MR, et al. Current Trend of Antibiotic Practice in Paediatric Surgery in Bangladesh. IOSR Journal of Dental and Medical Sciences (IOSR-JDMS) 2019;18(4):28–32.
- 31. Al Rasel Bin Mahabub Zaman M, Hasan M, Rashid HA. Indication-based use of antibiotic in the treatment of patients attending at the primary health care facility. Cough. 2018;44:22–0.
- 32. Sutradhar KB, Saha A, Huda NH, Uddin R. Irrational use of antibiotics and antibiotic resistance in southern rural Bangladesh: perspectives from both the physicians and patients. Annu Res Rev Biol. 2014;4(9):1421–30.
- 33. Saha MR, Sarwar S, Shill MC, Shahriar M. Patients' Knowledge and Awareness towards Use of Antibiotics in Bangladesh: A Cross-sectional Study Conducted in Three Tertiary Healthcare Centers in Bangladesh. Stamford J Pharmaceutical Sciences. 2010;3(1):54–8.
- 34. Biswas M, Roy MN, Manik MIN, Hossain MS, Tapu STA, Moniruzzaman M, et al. Self- medicated antibiotics in Bangladesh: a cross-sectional health survey conducted in the Rajshahi City. BMC Public Health. 2014;14(1):847.
- 35. Nishat C, Rashedul M. Prevalence of self-medication of antibiotics among people in Bangladesh. Ind J Pharma Prac. 2012;5(4):65–72.
- 36. Haque MU, Kumar A, Barik SMA and Islam MAU. Prevalence, practice and irrationality of self-medicated antibiotics among people in northern and southern region of Bangladesh. Int J Res Pharm Biosciences 2017;4(10): 17–24.
- 37. Rana MM, Karim MR, Islam MR, Mondal MNI, Wadood MA, Bakar SMA et al. Knowledge and Practice about the Rational Use of Antibiotic among the Rural Adults in Rajshahi District, Bangladesh: A Community Clinic Based Study. Human Biology Review 2018;7 (3):259–271.
- 38. Saha T, Saha T. Awareness Level of Patients Regarding usage of Antibiotics in a Slum Area of Dhaka City, Bangladesh. SSRG Int J Med Science 2018;5(9):10–16.
- 39. Begum N, Shamsuzzaman S. Emergence of carbapenemase-producing urinary isolates at a tertiary care hospital in Dhaka, Bangladesh. Tzu Chi Medical Journal. 2016;28(3):94–8. pmid:28757733
- 40. Mannan A, Shohel M, Rajia S, Mahmud NU, Kabir S, Hasan I. A cross sectional study on antibiotic resistance pattern of Salmonella typhi clinical isolates from Bangladesh. Asia Pac J Trop Biomed. 2014;4(4):306–11.
- 41. Rahman MS, Huda S. Antimicrobial resistance and related issues: An overview of Bangladesh situation. Bangladesh J Pharmacol. 2014;9(2):218–24.
- 42. Ahmed B, Akhter M, Hasan M, Alam MK. Sensitivity pattern of urinary tract pathogens to anti-microbial drugs at a tertiary level hospital in Bangladesh. Journal of Dhaka National Medical College & Hospital. 2011;17(1):18–21.
- 43. Shahriar M, Hossain M, Kabir S. A Survey on Antimicrobial Sensitivity Pattern of Different Antibiotics on Clinical Isolates of Escherichia coli Collected from Dhaka City, Bangladesh. J Appl Sciences Env Management. 2010;14(3).
- 44. Tarana MN, Shumu SJ, Khanam RA, Jahan H, Sarker S, Bhowmic D, et al. Antimicrobial susceptibility pattern for Salmonella Typhi isolated from blood in Shaheed Suhrawardy Medical College, Dhaka. Journal of Shaheed Suhrawardy Medical College. 2018;10(2):96–8.
- 45. Nahar A, Hasnat S, Akhter H, Begum N. Evaluation of antimicrobial resistance pattern of uropathogens in a tertiary care hospital in Dhaka city, Bangladesh. South East Asia J Public Health. 2017;7(2):12–8.
- 46. Ahmed AA, Salam MA, Hossain MS, Aktar MB, Juyee NA, Hasan SA. Trends in antibiotic resistance patterns of methicillin resistant and methicillin sensitive Staphylococcus aureus in Khwaja Yunus Ali Medical College Hospital. KYAMC Journal. 2018 May 9;9(1):6–10.
- 47. Hasan MJ, Hosen MS, Bachar SC. The resistance growing trend of common gram-negative bacteria to the potential antibiotics over three consecutive years: a single center experience in Bangladesh. Pharm Pharmacol Int J. 2019;7(3):114–9.
- 48.
Global Antibiotic Resistance Partnership- Bangladesh- GARP- Bangladesh National Working Group. Antibiotic Use and Resistance in Bangladesh- Situation Analysis & Recommendations. January 2018. Washington DC and New Delhi: Centre for Disease Dynamics, Economics & Policy (CDDEP).
- 49. Islam A, Saifuddin A, Al Faruq A, Islam S, Shano S, Alam M, et al. Antimicrobial residues in tissues and eggs of laying hens at Chittagong, Bangladesh. Int J One Health. 2016;2(11):75–80.
- 50. Sattar S, Hassan MM, Islam S, Alam M, Al Faruk MS, Chowdhury S, et al. Antibiotic residues in broiler and layer meat in Chittagong district of Bangladesh. Veterinary World. 2014;7(9).
- 51. Hossen MS, Hoque Z, Nahar BS. Assessment of poultry waste management in Trishal upazila, Mymensingh. Research in Agriculture Livestock and Fisheries. 2015;2(2):293–300.
- 52. Hossain MM, Barman AA, Rahim MM, Hassan MT, Begum M, Bhattacharjee D. Oxytetracycline residues in Thai pangas Pangasianodon hypophthalmus sampled from Sylhet sadar upazila, Bangladesh. Bangladesh Journal of Zoology. 2018 Jul 26;46(1):81–90.
- 53. Islam MA, Islam M, Hasan R, Hossain MI, Nabi A, Rahman M, et al. Environmental spread of NDM-1-producing multi-drug resistant bacteria in Dhaka, Bangladesh. Appl Environ Microbiology. 2017:AEM. 00793–17.
- 54. Rashid M, Rakib MM, Hasan B. Antimicrobial-resistant and ESBL-producing Escherichia coli in different ecological niches in Bangladesh. Infec Ecology Epidemiol. 2015;5(1):26712.
- 55. Neela FA, Banu MNA, Rahman MA, Rahman MH, Alam MF. Occurrence of antibiotic resistant bacteria in pond water associated with integrated poultry-fish farming in Bangladesh. Sains Malays. 2014;44:371–7.
- 56. Haque A, Yoshizumi A, Saga T, Ishii Y, Tateda K. ESBL-producing Enterobacteriaceae in environmental water in Dhaka, Bangladesh. Journal of Infection and Chemotherapy. 2014;20(11):735–7. pmid:25103169
- 57. Ahmed T, Urmi NJ, Munna MS, Das KK, Acharjee M, Rahman MM, et al. Assessment of microbiological proliferation and in vitro demonstration of the antimicrobial activity of the commonly available salad vegetables within Dhaka metropolis, Bangladesh. Am J Agri Forestr. 2014;2(3):55–60.
- 58. Bhowmik P, Ahaduzzaman M, Hasan RB. A Cross Sectional Anthropo-Clinical Study on Antimicrobials Prescription Pattern in Goat Patients at Chittagong, Bangladesh. Bangladesh Journal of Veterinary Medicine. 2017;15(2):119–26.
- 59. Hassan MM, Begum S, Al Faruq A, Alam M, Mahmud T, Islam A. Multidrug Resistant Salmonella Isolated from Street Foods in Chittagong, Bangladesh. Microbiology Research Journal International. 2018:1–8.
- 60.
MoHFW, GoB. National Drug Policy 2016. English version. Available from: http://www.dgda.gov.bd/index.php/laws-and-policies/261-national-drug-policy-2016-english-version
- 61.
DGHS/MoHFW, Government of Bangladesh. National Action Plan 2017–2022: Antimicrobial Resistance Containment in Bangladesh. Available from: https://www.flemingfund.org/wp-content/uploads/d3379eafad36f597500cb07c21771ae3.pdf
- 62. Kotwani A, Wattal C, Joshi P, Holloway K. Knowledge and perceptions on antibiotic use and resistance among high school students and teachers in New Delhi, India: A qualitative study. Indian Journal of Pharmacology. 2016;48(4):365. pmid:27756945
- 63. Hadi U, van den Broek P, Kolopaking EP, Zairina N, Gardjito W, Gyssens IC. Crosssectional study of availability and pharmaceutical quality of antibiotics requested with or without prescription (Over The Counter) in Surabaya, Indonesia. BMC Infectious Diseases. 2010;10(1):203. https://doi.org/10.1186/1471-2334-10-203.
- 64. Fatokun O. Exploring antibiotic use and practices in a Malaysian community. Int J Clin Pharm. 2014;36(3):564–9. pmid:24700341
- 65. Basnyat B, Pokharel P, Dixit S, Giri S. Antibiotic use, its resistance in Nepal and recommendations for action: a situation analysis. J Nepal Health Res Counc. 2015;13:102–11. https://doi.org/10.33314/inhrc.632. pmid:26744193
- 66. Quet F, Vlieghe E, Leyer C, Buisson Y, Newton PN, Naphayvong P, et al. Antibiotic prescription behaviours in Lao People's Democratic Republic: a knowledge, attitude and practice survey. Bull World Health Organ. 2015;93:219–27. pmid:26229186
- 67. Chandy S.J., Michael J.S., Veeraraghavan B., Abraham O.C., Bachhav S.S. and Kshirsagar N.A., 2014. ICMR programme on antibiotic stewardship, prevention of infection & control (ASPIC). The Indian J Med Res. 2014;139(2):226. pmid:24718396
- 68.
ASEAN. Rational use of medicines in the ASEAN region. Jakarta: ASEAN Secretariat, 2017.
- 69. Kotwani A, Holloway K. Trends in antibiotic use among outpatients in New Delhi, India. BMC Infectious Diseases. 2011;11(1):99. https://doi.org/10.1186/1471-2334- 11–99.
- 70.
Sahoo KC. Antibiotic resistance and environmental factors: focusing on the situation in Odisha, India: Inst for folkhalsovetenskap/Dept of Public Health Sciences; 2012.
- 71. Kotwani A, Wattal C, Joshi P, Holloway K. Irrational use of antibiotics and role of the pharmacist: an insight from a qualitative study in New Delhi, India. J Clin Pharm Therapeutics. 2012;37(3):308–12.
- 72. Patabendige C, Chandrasiri N, Karunanayake L, Karunaratne G, Somaratne P, Elwitigala J, et al., editors. Antimicrobial resistance in resource-poor settings—Sri Lankan experience. Regional Health Forum; 2011.
- 73. Shankar P, Partha P, Shenoy N. Self-medication and non-doctor prescription practices in Pokhara valley, Western Nepal: a questionnaire-based study. BMC Family Practice. 2002;3(1):17. https://doi.org/10.1186/1471-2296-3-17.
- 74. Shaikh BT. Anti-microbial resistance in Pakistan: a public health issue. Journal of Ayub Medical College Abbottabad. 2017;29(2):184–5.
- 75. Widayati A, Suryawati S, Crespigny Cd, Hiller JE. Beliefs about the use of nonprescribed antibiotics among people in Yogyakarta City, Indonesia: a qualitative study based on the theory of planned behavior. Asia Pacific J Pub Health. 2015; 27(2):NP402–NP13. https://doi.org/10.1177/1010539512445052.
- 76. Hadi U, Duerink DO, Lestari ES, Nagelkerke NJ, Werter S, Keuter M, et al. Survey of antibiotic use of individuals visiting public healthcare facilities in Indonesia. Int J Inf Diseases. 2008;12(6):622–9. Available from: https://doi.org/10.1016/i.iiid.2008.01.002.
- 77. Van Nguyen K, Do NTT, Chandna A, Nguyen TV, Van Pham C, Doan PM, et al. Antibiotic use and resistance in emerging economies: a situation analysis for Viet Nam. BMC Public Health. 2013;13(1):1158.
- 78. Nair M, Tripathi S, Mazumdar S, Mahajan R, Harshana A, Pereira a et al. “Without antibiotics, I cannot treat”: A qualitative study of antibiotic use in Paschim Bardhaman district of WestBengal, India. PLoS One 2019; 14(6):e0219002. Available from: pmid:31247028
- 79.
Rahman S. OR modelling and public policies in Bangladesh: implementation challenges. Available from: https://pdfs.semanticscholar.org/9a11/19d587930f4acb18ab48d6a15470e9103208.pdf
- 80.
Sabbih MA. Implementation Challenges of SDGs Country Study: Bangladesh. Presented at Research-Policy meeting on Interpreting SDGs for South Asia: In Search of a Regional Framework, Dhaka, 20 Nov. 2018. Available from: https://bit.ly/2WlfIIV
- 81.
Antimicrobial resistance: national action plans. Interagency Coordination Group on Anti-microbial Resistance (IACG) Discussion Paper. Available from: https://www.who.int/antimicrobial-resistance/interagency-coordination-group/IACG_AMR_National_Action_Plans_110618.pdf
- 82. Rainey R, Weinger M. The role of water, sanitation and hygiene (WASH) in healthcare settings to reduce transmission of antimicrobial resistance. AMR Control [Online Edition]. 2016; 65–8.
- 83. Macintyre A, Wilson-Jones M, Velleman Y. Prevention First: Tackling AMR through Water, Sanitation and Hygiene. AMR Control, 2017.
- 84. Alvarez-Uria G, Gandra S, Laxminarayan R. Poverty and prevalence of antimicrobial resistance in invasive isolates. International Journal of Infectious Diseases. 2016;52:59–61. pmid:27717858
- 85. Susanne A. Kraemer SA, Ramachandran A, Gabriel G. Perron GG. Antibiotic Pollution in the Environment: From Microbial Ecology to Public Policy. Microorganisms. 2019;7: 180. pmid:31234491
- 86.
World Bank. Promising Progress: A Diagnostic of Water Supply, Sanitation, Hygiene, and Poverty in Bangladesh. WASH Poverty Diagnostic. Washington, DC: World Bank.; 2018.
- 87.
Clft C. Review of progress on antimicrobial resistance. Centre on Global Health Security, Chatham House, The Royal Institute of International Affairs. Available from: https://www.nih.org.pk/review-of-progress-on-antimicrobial-resistance
- 88.
Flora MS. One Health journey in Bangladesh: from advocacy to action (abstract). 9th One Health Bangladesh Conference: Achieving sustainable development goals (SDGs) through One Health approach. Abstract Book. Dhaka: Institute of Epidemiology, Disease Control & Research (IEDCR); 2017.
- 89.
Institute of Epidemiology, Disease Control & Research (IEDCR). Strategic framework for One Health approach to infectious diseases in Bangladesh. Dhaka: Bangladesh; 2012 Available from: https://bit.lv/2VOZgPB. Cited 24 Feb 2019.
- 90. Dahlal R, Upadhyay A, Ewald B. One health in south Asia and its challenges of implementation from stakeholder perspective. Vet Record. 2017;181(23):1–6. pmid:29084821
- 91.
Global Health Security Index: Building collective action and accountability. October 2019. Available from: https://www.ghsindex.org.