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Research Article
Ulaanbaatar, Mongolia Rie Nakajima1, Takehito Takano2, Vaanchig Urnaa2, Nyambayar Khaliun1 Keiko Nakamura1 1International Health and Medicine, Graduate School of Tokyo Medical and Dental University, 1-5-45 Yushima, Bunkyo-ku Tokyo, Japan2Health Promotion, Graduate School of Tokyo Medical and Dental University, 1-5-45 Yushima, Bunkyo-ku Tokyo, Japan Address for Correspondence: Takehito Takano, Department of Health Promotion, Tokyo Medical and Dental University, 1-5-45 Yushima,
Bunkyo-ku Tokyo, Japan. E-mail: whocc.hlth@tmd.ac.jp
Citation: Nakajima R, Takano T, Urnaa V, Khaliun N, Nakamura K. Antimicrobial use in a country with insufficient enforcement of pharmaceutical
regulations: a survey of consumption and retail sales in Ulaanbaatar, Mongolia. Southern Med Review (2010) 3; 1:19-23
Abstract
Objective: To examine the inappropriate use of antimicrobials by investigating (1) actual utilization pattern and retail sales and (2)
antimicrobial resistant information provided by health professionals in Ulaanbaatar, Mongolia.
Methods: We investigated antimicrobial use in Ulaanbaatar, Mongolia by surveying 619 consenting customers who attended 250
randomly chosen pharmacies in December 2006. Pharmacy staff were also interviewed about antimicrobials purchased. In January
2007, we surveyed 117 consenting Ulaanbaatar medical doctors from seven local hospitals about their perceptions of treatment failure
due to antimicrobial resistance.
Results: Among 619 pharmacy customers, 48% of them had bought at least one type of antimicrobial medicine and, of these,
42% had a prescription to purchase antimicrobials. On average, 67% of the customers reported that a pharmacy worker had given
them information regarding the dose and timing at which the medicine should be used but only 9% reported that they had been
given information regarding possible adverse effects. The survey of medical doctors suggested that some antibiotics had become less
effective clinically between 2001 and 2006.
Conclusion: The study shows that less than half of all customers who purchased an antibiotic at a pharmacy had a prescription. This
shows that antimicrobials can be readily purchased without a prescription despite the existence of laws making such practices illegal.
There is a need to establish a vigilant drug regulatory authority to promote enforcement and regulation of medicines in Mongolia. To
create awareness regarding the dangers of antimicrobial resistance, educational campaigns for consumers are also necessary.
Keywords: antimicrobial utilization, antimicrobial resistance, developing country, Mongolia.
Organization (WHO) warns that the purchase of antimicrobials without a prescription leads to the misuse and overuse of During the past few decades, the number of antimicrobial- antimicrobials, resulting in the emergence of antimicrobial- resistant pathogens has increased rapidly in many parts of the world1. Of note, the rate of increase of antimicrobial-resistant pathogens in Asia is the highest in the world2-4. One Many developing countries have a limited ability to of the major reasons for the increase in antimicrobial-resistant manufacture antimicrobial medicines; therefore, they must pathogens in many developing countries is that antimicrobials obtain antimicrobial medicines from other countries. Numerous can be purchased without a prescription5. The World Health commercial dealers of pharmaceutical products compete with Southern Med Review Vol 3 Issue 1 Feb 2010
one another to extend sales in developing countries, providing conducted to train the interviewers, providing them with imported medicines to meet the demand for antimicrobials in knowledge and interviewing skills. Two interviewers visited these countries6. However, the control and regulation measures each of the pharmacies and interviewed the pharmacy staff. for the sale of pharmaceuticals in developing countries are often Following individual interviews with the pharmacy workers, insufficient. Mongolia is one such country where antimicrobials the study team spent one hour outside of the pharmacy and can be widely purchased without a prescription, despite the approached customers who had just left the pharmacy and existence of laws prohibiting this act. Penalties imposed on asked for their cooperation in completing a short interview. A offenders guilty of such acts include closure of a store where total of 619 pharmacy customers agreed to participate in the such a trade has been conducted7. Despite this, the measures to control and regulate the sale and purchase of antimicrobials The survey for practicing medical doctors was a self-administered in Mongolia are insufficient8, 9. This is a problem that not only affects Mongolia, but also impacts many developing countries report based on a structured questionnaire form: the reports were collected after a complete explanation of the purpose 10-12. In this context, the objectives of the present study were to explore the antimicrobial utilization of the survey and a step-by-step explanation of the questions pattern and retail sales; another objective was to explore the had been made by specially trained doctors. All queries were perceptions of clinicians regarding antimicorbial resistance.
collected and answers and clarifications were given to the participating medical doctors before they submitted their completed questionnaire forms. The self-administered survey of the medical doctors was completed by 117 medical doctors who We conducted three surveys using structured questionnaires: agreed to participate in the study. These doctors were selected one for pharmacy workers, one for pharmacy customers, and from amongst 7 leading hospitals in Ulaanbaatar . one for practicing medical doctors. The study protocol was Face to face in depth interview of ten medical doctors were approved by the ethical review boards of the Tokyo Medical and Dental University and the Ministry of Health, Mongolia.
conducted. These doctors were randomly selected from participants of the medical doctor’s survey. These doctors Study area
answered questions regarding antimicrobial therapy. The questions were also asked regarding doctors’ knowledge on The study was carried out in Ulaanbaatar, the capital city Centre for Disease Control guidelines15. of Mongolia, where the general public’s accessibility to antimicrobials has been rapidly increasing in recent years as a Questionnaire items
result of the rapid economic development. The interview questionnaire for the pharmacy workers included Mongolia is a landlocked central Asian country, with a total area the following items: the names of all the antimicrobial medicines of 1.6 million square kilometers. Among the total 2.7 million sold at the pharmacy (regardless of strength), the average populations, 32% are living in Ulaanbaatar, the capital of number of customers who bought medicine per day, and Mongolia8. On the financial side, the Mongolian economy has the average number of customers who bought antimicrobial experienced positive GDP growth averaging 8.7 percent from medicine per day during the two week period prior to the study. The interview questionnaire for the pharmacy customers Mongolia’s current health system has been evolving for more included the following items: customer’s age, sex, educational than 70 years and is characterized by three levels of care: primary, background, purchase of antimicrobial and non antimicrobial secondary and tertiary care14. Although these health facilities still medicines, types and whether it was the oral or injectable form. do not meet the current needs of the country, 8 it is reported that The other questions were age, symptoms of the expected user for every 1000 Mongolians 2.7 physicians are available14. Health of the medicine, presentation of the prescription (to purchase insurance was introduced in 1994 and it is estimated that about antimicrobial medicines), and instructions given by the pharmacy 78% of the population is covered. However, it is still common staff regarding the use of the medicines. that patients have to pay out of pocket in private pharmacies to obtain the necessary medications8.
The self-administered questionnaire for the medical doctors asked for their professional estimates as to the current Subjects, sampling and questionnaire procedures
prevalence of antimicrobial resistance, their clinical experiences with antibiotics and the expected number of ineffective The pharmacies surveyed in the present study (both pharmacy treatments encountered during the application of each of the workers and customers) were selected from a list provided by the Mongolian Ministry of Health. A total of two hundred and fifty pharmacies were randomly selected from amongst the five Period of the survey
hundred pharmacies registered in Ulaanbaatar. Interviewers of the pharmacy and customer survey were clinical pharmacology The pharmacy staff and customer interviews were conducted professionals with sufficient knowledge of antimicrobials and in December 2006, while the survey of medical doctors was pharmaceutical practice. A three day training workshop was performed in January 2007. The study was performed during Southern Med Review Vol 3 Issue 1 Feb 2010
the winter season because the prevalence of acute respiratory Table 2. Number of customers who bought
infection is typically high during this time and thus a large antimicrobials per 50 customers who visited
number of antimicrobials are prescribed.
pharmacies to buy medicine.
Analysis
Number of customers who bought antimicrobials per 50 customers All data were entered and analyzed using SPSS software (version 14.0). The average numbers of pharmacy customers who bought specific antimicrobial medicines per fifty customers (who bought both antimicrobial and non-antimicrobial medicines) from that pharmacy were calculated for each type of antimicrobial. This indicator was used to represent the retail sales of antimicrobials. Results and knowledge from pharmacy workers reveal the types of antimicrobials which has been sold to customers at pharmacies during the two weeks prior to the study (Table 1). Table 1. Types of antimicrobials sold to customers at
community pharmacies in Ulaanbaatar, Mongolia
* Average for 250 pharmacies located in Ulaanbaatar, Table 2 shows the number of customers who bought each type of antimicrobial medicine per 50 customers who visited pharmacies to buy medicine. Among the 619 pharmacy customers who agreed to participate in this study, 48.0% of them (297 customers) had bought at least one type of antimicrobial medicine. Among those who bought antimicrobials, 42.1% of them (125 customers) had a prescription for the antimicrobial medicine that was purchased. Antimicrobials commonly used by injection were benzylpenicillin (used by 90% of customers who bought antimicrobials), cefazolin (80%) and gentamicin (90%). The most common reasons for purchasing antimicrobials were acute respiratory disease (54.8%), genitourinary disease (15.5%), and gastrointestinal disease (10.7%). Among the pharmacy customers who suffered from acute respiratory disease, 45.1% of them bought oral penicillin, either amoxicillin (24.6%) or ampicillin (20.5%). The most common strength of these two antimicrobials was 500 mg (selected by 70% of Antimicrobials reported to have been sold during the 2 weeks customers who bought amoxicillin or ampicillin), and rest of prior to the interview day at community pharmacies.
them (30%) bought 250 mg which mainly used for children.
Southern Med Review Vol 3 Issue 1 Feb 2010
Table 3. Instructions given by pharmacy staff to
antimicrobials had a prescription, while the pharmacy customer customers regarding various parameters
survey showed that 42.1% of the customers who purchased antimicrobials had a prescription. These results are based on customers who visited community pharmacies in Ulaanbaatar. The pharmacy worker survey indicated that, amoxicillin and ampicillin, sulfamethoxazole-trimethoprim, and metronidazole were the most frequently sold antimicrobials in Ulaanbaatar pharmacies. The frequent sale of amoxicillin and ampicillin, both of which are oral penicillins, as over-the-counter drugs has also been reported in Vietnam and Mexico16, 17. The frequent use of these medications is most likely explained by their cost and availability: amoxicillin and ampicillin are generally less expensive than other antimicrobials, and over 70% of all pharmacies throughout the world sell amoxicillin18. All pharmacies in the present study sold both amoxicillin and ampicillin. Generally, variations in the types, frequency, and methods in which antimicrobials are used by the general public vary in countries according to disease patterns, patient characteristics, and the quantity and quality of care services at health facilities19. Variations in the general characteristics of antimicrobial use in developing counties also arise from the ability to purchase antimicrobials inexpensively and without a prescription. Among the pharmacy customers who bought over-the-counter medicines, more than half of the customers were seeking treatment for acute respiratory diseases; amoxicillin and ampicillin were sold to more than half of these customers. Antimicrobials were also frequently sold to patients suffering from genitourinary or gastrointestinal diseases. Table 3 shows the summary of instructions given by pharmacy Antimicrobials sold to these patients included not only workers to pharmacy customers. On average, 67.3% of the penicillins, but also a wide range of other antimicrobials customers reported that a pharmacy worker had given them including chloramphenicol and gentamicin. There is a concern information regarding the dose and timing at which the that the amount of antimicrobial use is related to the increase medicine should be used; 8.9% of them reported that they had in drug-resistant pathogens20. In fact, our survey of perception also been given information regarding adverse effects. of medical doctors showed that the antimicrobials which were frequently sold in community pharmacies were losing their The study reveals that the doctors feel that the medicines such effectiveness for the treatment of patients.
as benzyl penicillin, gentamicin, metronidazole, ampicillin, phenoxymethyl penicillin, and ciprofloxacin are no longer very High consumption of antimicrobials among patients with effective in treatment as they may have a problem of antibiotic common diseases such as acute respiratory disease and gastrointestinal disease were frequently reported in several countries16, 17 and the same has been observed in Mongolia. Especially the patients who are suffering from genitourinary disease are on rise in Mongolia and these patients frequently The results of the pharmacy worker and pharmacy customer surveys were consistent, with about half of the pharmacy There is a tendency in developing countries to take antimicrobials customers purchasing antimicrobial medicines: the pharmacy even when their symptoms are not serious or even when worker survey indicated that an average of 4.6 (SD = 1.8) out there are no signs of infection21. One such medicine is of 10 customers purchased antimicrobial medicines, while the chloramphenicol, which is widely used in developing countries, pharmacy customer survey showed that 48.0% of the pharmacy primarily because it is cheap and broad spectrum. However, this customers purchased antimicrobial medicines. The results of medicine is now rarely used in developed countries because of the pharmacy worker and pharmacy customer surveys also its serious adverse effects, such as the development of aplastic consistently showed that 40% of the customers who purchased anemia22. The present survey shows that chloramphenicol is antimicrobials had a prescription: the pharmacy worker survey commonly used in Mongolia, especially for the treatment of reported that 4.0 (SD = 2.3) out of 10 customers who purchased gastrointestinal disease. However, the present study shows that Southern Med Review Vol 3 Issue 1 Feb 2010
only 4% of the customers, who purchased chloramphenicol, received information regarding side effects. 1. World Health Organization Global Strategy for Containment of To date, there have been limited laboratory studies conducted Antimicrobial Resistance. World Health Organization, 2001. WHO/ on antimicrobial sensitivity in Mongolia and it is difficult to CDS/DRS/2001.2 http://www.who.int/csr/resources/publications/ establish whether antimicrobial resistance has increased or not. drugresist/en/EGlobal_Strat.pdf (Accssed 17/11/ 2009) 2. Lee NY et al. Carriage of antibiotic-resistant Pneumococci among Hence, promoting the use of an antimicrobial sensitivity test Asian children: A multinational surveil ance by the Asian Network before prescribing antimicrobials is an important approach to for Surveil ance of Resistant Pathogens. (ANSORP). Clin Infect Dis monitor and to control the further emergence of antimicrobial 3. Song JH et al. High prevalence of antimicrobial resistance among clinical Streptococcus pneumoniae isolates in Asia (an ANSORP Although it is a crude measure of changes in resistance, study). Antimicrob Agents Chemother 2004; 48:2101-2107. 4. Akita H. Penicil in resistant Streptococcus pneumoniae: Actual this survey of experienced medical doctors in Ulaanbaatar condition of overseas. Shonika Rinsho 2002; 55:2291-2296. [in also suggested that based on their clinical experience some antimicrobials are losing their effectiveness for the treatment of 5. Hoban D et al. Demographic analysis of antimicrobial resistance among Streptococcus pneumoniae: worldwide results from PROTEKT 1999-2000. Int J Infect Dis 2005:9; 262-273. There are no specific antibiotic guidelines in Mongolia and it 6. WHO. Priority medicines for Europe and the world. In: World is necessary to promote and establish best practice clinical Health Organization. 2001. http://archives.who.int/prioritymeds/report/index.htm ( Accssed 17/11/2009) guidelines. These guidelines should not be limited to medical 7 Ministry of health Mongolia. Drugs act of 1998. Ulaanbaatar, doctors, but should also target and include pharmacists and Mongolia, 1998. http://moh.mn/moh%20db/Healthreports.nsf/ pharmacy workers. The knowledge of pharmacy workers about antimicrobials play a key role in promoting the rational use 8. Bolormaa T et al. Mongolia: Health system review. Health Systems of antimicrobials, considering the fact that many consumers 9. Ministry of health Mongolia. Mongolia Pharmaceutical sector purchase directly in Ulaanbaatar. Hence, the education of assessment report. Ulaanbaatar, Mongolia, 2004.
prescribers and dispensers (including drug sellers) is important 10. Borg MA, Scicluna EA. Over-the-counter acquisition of antibiotics for appropriate antimicrobial use and for the containment of in the Maltese general population. Int J Antimicrob Agents 2002; 20:253-257. 11. Al Bakri AG et al. Community consumption of antibacterial drugs within the Jordanian population : sources, pattrns and This study provides an understanding of the sale and use of appropriateness. Int J Antimicrob Agents 2005; 26: 389-395. antimicrobials by a sample of the general public in Ulaanbaatar, 12. Mitsi G et al. Patterns of antibiotic use among adults and parents Mongolia. At present, the public can purchase antimicrobials for in the community: A questionnaire-based survey in a Greek urban the treatment of common diseases, such as acute respiratory population. Int J Antimicrob Agents 2005; 25: 439-443. 13. UNDP. Employment and poverty in Mongolia. In: United Nations infection, without requiring a prescription and without receiving Development Programme.2007.http://hdr.undp.org/en/reports/ proper instructions regarding the use of such medicines. The nationalreports/asiathepacific/mongolia/name,3392,en.html development of comprehensive and consistent control measures at national level to regulate the medicine quality and distribution 14. WHO Regional Office for the Western Pacific. Country health information profiles. In: World Health Organization Regional is urgently needed in Mongolia. Also, antimicrobials should not Office for the Western Pacific. 2007. http ://www.wpro.who.int/ be available as over-the-counter drugs.
countries/2007/mog/ (Accessed 17 Nov 2009).
15. CDC. Infectious Disease guidelines. In: Centers for Disease Control and Prevention. http://www.cdc.gov/ncidod/guidelines/guidelines_topic.htm (Accessed 10 Aug 2009).
16. Duong DV et al. Availability of antibiotics as over-the-counter The present study is first of its kind and it explores the use of drugs in pharmacies: a threat to public health in Vietnam. Trop antimicorbials in Mongolia. The study reveals that antibiotics are commonly available in Mongolia and the consumers have 17. Calva J. Antibiotic use in periurban community in Mexico: a easy access to these medicines. Establishing a drug regulatory household and drug store survey. Soc Sci Med 1996; 8: 1121-1128. authority could improve the enforcement and also can aid to 18. Cameron A et al. Medicines prices, availability, and affordability improve the quality use of antimicrobials. Mass educational in 36 developing and middle-income countries: a secondary campaigns could also create awareness regarding the use of 19. Dong H et al. Association between health insurance and antibiotics prescribing in four counties in rural China. Health Policy 1999; 48:29-45. 20. Albrich WC et al. Antibiotic selection pressure and resistance in Streptococcus pneumoniae and Streptococcus pyogenes. Emerg The authors report no conflicts of interest. 21. Okumura J et al. Drug utilization and self-medication in rural communities in Vetnam. Soc Sci Med 2002; 54:1875-1886.
22. Duke T, et al. Chloramphenicol versus benzylpenicil in and gentamicin for the treatment of severe pneumonia in children in This study was supported by Grants-in-Aid of Scientific Studies Papua New Guinea: a randomized trial. Lancet 2002; 359:474- of the Japan Society for the Promotion of Science.
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