Volume 5, Number 1—February 1999
Socioeconomic and Behavioral Factors Leading to Acquired Bacterial Resistance to Antibiotics in Developing Countries
|Antimicrobial agent||Percentage of resistant isolates
|Urban (n = 30)||Rural/suburban (n = 44)|
aSignificant differences between the two groups at p < 0.05 (Chi-square test)
bSignificant differences between the two groups at p < 0.10 (Chi-square test)
- Kunin CM. Resistance to antimicrobial drugs a worldwide calamity. Ann Intern Med. 1993;118:557–61.
- Murray BE, Alvarado T, Kim KH, Vorachit M, Jayanetra P, Levine MM, Increasing resistance to trimethoprim-sulfamethoxazole among isolates of Eschericha coli in developing countries. J Infect Dis. 1985;147:724–8.
- Sack RB, Rahman M, Yunus M, Khan EH. Antimicrobial resistance in organisms causing diarrheal disease. Clin Infect Dis. 1997;24(Suppl 1):S102–5.
- Rahal K, Wang F, Schindler J, Rowe B, Cookson B, Huovinen P, Reports on surveillance of antimicrobial resistance in individual countries. Clin Infect Dis. 1997;24(Suppl 1):S169–75.
- Hoge CW, Gambel JM, Srijan A, Pitarangsi C, Echeverria P. Trends in antibiotic resistance among diarrheal pathogens isolated in Thailand over 15 years. Clin Infect Dis. 1998;26:341–5.
- Bennish ML, Salam MA, Hossain MA, Myaux J, Khan EH, Chakraborty J, Antimicrobial resistance of Shigella isolates in Bangladesh, 1983-1990: increasing frequency of strains multiply resistant to ampicillin, trimethoprim-sulfamethoxazole, and nalidixic acid. Clin Infect Dis. 1992;14:1055–60.
- Lima AA, Lima NL, Pinho MC, Barros Junior EA, Teixeira MJ, Martins MC, High frequency of strains multiply resistant to ampicillin, trimethoprim-sulfamethoxazole, streptomycin, chloramphenicol, and tetracycline isolated from patients with shigellosis in northeastern Brazil during the period 1988 to 1993. Antimicrob Agents Chemother. 1995;39:256–9.
- Bogaerts J, Verhaegen J, Munyabikali JP, Mukantabana B, Lemmens P, Vandeven J, Antimicrobial resistance and serotypes of Shigella isolates in Kigali, Rwanda (1983 to 1993): increasing frequency of multiple resistance. Diagn Microbiol Infect Dis. 1997;28:165–71.
- Dalsgaard A, Mortensen HF, Molbak K, Dias F, Serichantalergs O, Echeverria P. Molecular characterization of Vibrio cholerae O1 strains isolated during cholera outbreaks in Guinea-Bissau. J Clin Microbiol. 1996;34:1189–92.
- Mukhopadhyay AK, Garg S, Mitra R, Basu A, Rajendran K, Dutta D, Temporal shifts in traits of Vibrio cholerae strains isolated from hospitalized patients in Calcutta: a 3-year (1993 to 1995) analysis. J Clin Microbiol. 1996;34:2537–43.
- Githui WA, Kwamanga D, Chakaya JM, Karimi FG, Waiyaki PG. Anti-tuberculous initial drug resistance of Mycobacterium tuberculosis in Kenya: a ten-year review. East Afr Med J. 1993;70:609–12.
- el Baghdadi J, Lazraq R, Ibrahimy S, Bouayad Z, Guinet R, Benslimane A. Survey of primary drug resistance of Mycobacterium tuberculosis in Casablanca, Morocco. Int J Tuberc Lung Dis. 1997;1:309–13.
- Calva JJ, Sifuentes-Osornio J, Ceron C. Antimicrobial resistance in fecal flora: longitudinal community-based surveillance of children from urban Mexico. Antimicrob Agents Chemother. 1996;40:1699–702.
- Col NF, O'Connor RW. Estimating worldwide current antibiotic usage: report of Task Force 1. Rev Infect Dis. 1987;9(Suppl 3):S232–43.
- Kunin CM, Johansen KS, Worning AM, Daschner FD. Report of a symposium on use and abuse of antibiotics worldwide. Rev Infect Dis. 1990;12:12–9.
- Guyon AB, Barman A, Ahmed JU, Ahmed AU, Alam MS. A baseline survey on use of drugs at the primary health care level in Bangladesh. Bull World Health Organ. 1994;72:265–71.
- Bojalil R, Calva JJ. Antibiotic misuse in diarrhea. A household survey in a Mexican community. J Clin Epidemiol. 1994;47:147–56.
- Nizami SQ, Khan IA, Bhutta ZA. Drug prescribing practices of general practitioners and paediatricians for childhood diarrhoea in Karachi, Pakistan. Soc Sci Med. 1996;42:1133–9.
- Paredes P, de la Pena M, Flores-Guerra E, Diaz J, Trostle J. Factors influencing physicians' prescribing behavior in the treatment of childhood diarrhoea: knowledge may not be the clue. Soc Sci Med. 1996;42:1141–53.
- Hui L, Li XS, Zeng XJ, Dai YH, Foy HM. Patterns and determinants of use of antibiotics for acute respiratory tract infection in children in China. Pediatr Infect Dis J. 1997;16:560–4.
- Reyes H, Guiscafre H, Munoz O, Perez-Cuevas R, Martinez H, Gutierrez G. Antibiotic noncompliance and waste in upper respiratory infections and acute diarrhea. J Clin Epidemiol. 1997;50:1297–304.
- Rodolfo J, Lozano J, Ruiz J, Londono D, Rodriguez M, Ruiz A. Drug prescription patterns of recently graduated physicians in Colombia [abstract]. J Clin Epidemiol. 1997;50(Suppl 1):26S.
- Muhuri PK, Anker M, Bryce J. Treatment patterns for childhood diarrhoea: evidence from demographic and health surveys. Bull World Health Organ. 1996;74:135–46.
- Cash R. Inappropriate treatment for dysentery. BMJ. 1996;313:181–2.
- Lee MG, Henry GL. Drug availability in Jamaica. West Indian Med J. 1989;38:105–9.
- Williams RJ, Heymann DL. Containment of antibiotic resistance. Science. 1998;279:1153–4.
- Turnridge J. Epidemiology of quinolone resistance. Eastern hemisphere. Drugs. 1995;49:43–7.
- World Health Organization. The use of essential drugs: model list of essential drugs: fifth report of the WHO Expert Committee, 1992. World Health Organ Tech Rep Ser. 1992;825:1–75.
- Mabadeje AF, Akintonwa AA, Ashorobi RB. The value and effects of implementing an essential drugs list in the Lagos University Teaching Hospital. Clin Pharmacol Ther. 1991;50:121–4.
- Munishi GK. The development of the Essential Drugs Program and implications for self-reliance in Tanzania. J Clin Epidemiol. 1991;44(Suppl 2):7S–14S.
- Hogerzeil HV, Bimo , Ross-Degnan D, Laing RO, Ofori-Adjei D, Santoso B, . Field tests for rational drug use in twelve developing countries. Lancet. 1993;342:1408–10.
- Salako LA. Drug supply in Nigeria. J Clin Epidemiol. 1991;44(Suppl 2):15S–9S.
- Gonzalez Ochoa E, Armas Perez L, Bravo Gonzalez JR, Cabrales Escobar J, Rosales Corrales R, Abreu Suarez G. Prescription of antibiotics for mild acute respiratory infections in children. Bull Pan Am Health Organ. 1996;30:106–17.
- Sturm AW, van der Pol R, Smits AJ, van Hellemondt FM, Mouton SW, Jamil B, Over-the-counter availability of antimicrobial agents, self-medication and patterns of resistance in Karachi, Pakistan. J Antimicrob Chemother. 1997;39:543–7.
- Bexell A, Lwando E, von Hofsten B, Tembo S, Eriksson B, Diwan VK. Improving drug use through continuing education: a randomized controlled trial in Zambia. J Clin Epidemiol. 1996;49:355–7.
- Robles Y, Polack A. Continuing professional education in pharmacy in the Philippines 2. A current perspective. J Soc Adm Pharm. 1997;14:24–132.
- Ronsmans C, Islam T, Bennish ML. Medical practitioners' knowledge of dysentery treatment in Bangladesh. BMJ. 1996;313:205–6.
- Hartog R. Essential and non-essential drugs marketed by the 20 largest European pharmaceutical companies in developing countries. Soc Sci Med. 1993;37:897–904.
- Lee PR, Lurie P, Silverman MM, Lydecker M. Drug promotion and labeling in developing countries: an update. J Clin Epidemiol. 1991;44(Suppl 2):49S–55S.
- Pearson CA. The role of district hospitals and the action in international medicine network. Infect Dis Clin North Am. 1995;9:391–405.
- Thamlikitkul V. Antibiotic dispensing by drug store personnel in Bangkok, Thailand. J Antimicrob Chemother. 1988;21:125–31.
- Kigotho AW. Ugandan doctors request antibiotic moratorium. Lancet. 1997;350:1014.
- Dua V, Kunin CM, White LV. The use of antimicrobial drugs in Nagpur, India. A window on medical care in a developing country. Soc Sci Med. 1994;38:717–24.
- Singh J, Raje N. The rise of Western medicine in India. Lancet. 1996;348:1598.
- Haak H. Pharmaceuticals in two Brazilian villages: lay practices and perceptions. Soc Sci Med. 1988;27:1415–27.
- Kafle KK, Gartoulla RP, Pradhan YM, Shrestha AD, Karkee SB, Quick JD. Drug retailer training: experiences from Nepal. Soc Sci Med. 1992;35:1015–25.
- Rahman F, Andersson R, Svanstrom L. Medical help seeking behaviour of injury patients in a community in Bangladesh. Public Health. 1998;112:31–5.
- Fagbule D, Kalu A. Case management by community health workers of children with acute respiratory infections: implications for national ARI control programme. J Trop Med Hyg. 1995;98:241–6.
- Van der Geest S. Marketplace conversations in Cameroon: how and why popular medical knowledge comes into being. Cult Med Psychiatry. 1991;15:69–90.
- Wolff MJ. Use and misuse of antibiotics in Latin America. Clin Infect Dis. 1993;17(Suppl 2):S346–51.
- Obaseiki-Ebor EE, Akerele JO, Ebea PO. A survey of antibiotic outpatient prescribing and antibiotic self- medication. J Antimicrob Chemother. 1987;20:759–63.
- Lansang MA, Lucas-Aquino R, Tupasi TE, Mina VS, Salazar LS, Joban N, Purchase of antibiotics without prescription in Manila, the Philippines. Inappropriate choices and doses. J Clin Epidemiol. 1990;43:61–7.
- Okeke I, Lamikanra A. Quality and bioavailability of tetracycline capsules in a Nigerian semi-urban community. Int J Antimicrob Agents. 1995;5:245–50.
- Hossain MM, Glass RI, Khan MR. Antibiotic use in a rural community in Bangladesh. Int J Epidemiol. 1982;11:402–5.
- Goel P, Ross-Degnan D, Berman P, Soumerai S. Retail pharmacies in developing countries: a behavior and intervention framework. Soc Sci Med. 1996;42:1155–61.
- Calva JJ, Ceron E, Bojalil R, Holbrook A. Antibiotic consumption in a community of Mexico City. II. Survey of purchases at pharmacies. Bol Med Hosp Infant Mex. 1993;50:145–50.
- Abosede OA. Self-medication: an important aspect of primary health care. Soc Sci Med. 1984;19:699–703.
- Shahid NS, Rahaman MM, Haider K, Banu H, Rahman N. Changing pattern of resistant Shiga bacillus (Shigella dysenteriae type 1) and Shigella flexneri in Bangladesh. J Infect Dis. 1985;152:1114–9.
- Yang YH, Fu SG, Peng H, Shen AD, Yue SJ, Go YF, Abuse of antibiotics in China and its potential interference in determining the etiology of pediatric bacterial diseases. Pediatr Infect Dis J. 1993;12:986–8.
- Catalano M, Almiron MA, Romeo AM, Caruso E, Murtagh P, Harisiadi J. Comparison between parental report and results of microbiologic agar assay for presence of antibiotic in urine of Argentinian children with acute lower respiratory tract infection. Rev Infect Dis. 1990;12(Suppl 8):S998–1000.
- Kunin CM, Lipton HL, Tupasi T, Social, behavioral, and practical factors affecting antibiotic use worldwide: report of Task Force 4. Rev Infect Dis. 1987;9(Suppl 3):S270–85.
- Haak H, Hardon AP. Indigenised pharmaceuticals in developing countries: widely used, widely neglected. Lancet. 1988;2:620–1.
- Abellanosa I, Nichter M. Antibiotic prophylaxis among commercial sex workers in Cebu City, Philippines. Patterns of use and perceptions of efficacy. Sex Transm Dis. 1996;23:407–12.
- Strang JK. Tracing patients in rural Africa. Lancet. 1996;348:1083–4.
- Esezobo E, Offiong E. In vitro studies on some brands of oxytetracycline capsules available in Nigeria. Nigerian Journal of Pharmacology. 1986;17:24–8.
- Agom JK, Akanni AO, Dawodu TO. Quality of ampicillin/cloxacillin preparations on the Nigerian market. Nigerian Journal of Pharmacology. 1990;21:36–8.
- Taylor RB, Shakoor O, Behrens RH. Drug quality, a contributor to drug resistance? Lancet. 1995;346:122.
- Ballereau F, Prazuck T, Schrive I, Lafleuriel MT, Rozec D, Fisch A, Stability of essential drugs in the field: results of a study conducted over a two-year period in Burkina Faso. Am J Trop Med Hyg. 1997;57:31–6.
- Hogerzeil HV, Battersby A, Srdanovic V, Stjernstrom NE. Stability of essential drugs during shipment to the tropics. BMJ. 1992;304:210–2.
- Shakoor O, Taylor RB, Behrens RH. Assessment of the incidence of substandard drugs in developing countries. Trop Med Int Health. 1997;2:839–45.
- Gustafsson LL, Wide K. Marketing of obsolete antibiotics in Central America. Lancet. 1981;1:31–3.
- Ali HM, Homeida MM, Abdeen MA. Drug dumping in donations to Sudan. Lancet. 1988;333:538–9.
- Berckmans P, Dawans V, Schmets G, Vandenbergh D, Autier P. Inappropriate drug-donation practices in Bosnia and Herzegovina, 1992 to 1996. N Engl J Med. 1997;337:1842–5.
- Guidelines for drug donations. Geneva: World Health Organization; 1996. Report No.: WHO/DAP/96.2.
- Adjepon-Yamaoah K. Drugs for the tropicstheir uses and abuses. Afr Health. 1980;:14–6.
- Land T. Combating counterfeit drugs. Nature. 1992;355:192.
- McGregor A. Counterfeit drugs flood developing world. Lancet. 1997;350:1690.
- Alubo SO. Death for sale: a study of drug poisoning and deaths in Nigeria. Soc Sci Med. 1994;38:97–103.
- Couper MR. Strategies for the rational use of antimicrobials. Clin Infect Dis. 1997;24(Suppl 1):S154–6.
- Huang WF, Wen KC, Hsiao ML. Adulteration by synthetic therapeutic substances of traditional Chinese medicines in Taiwan. J Clin Pharmacol. 1997;37:344–50.
- Michel JM. Why do people like medicines? A perspective from Africa [letter]. Lancet. 1985;1:210–1.
- Ogungbamila FO, Ogundaini AO, eds. Traditional healing methods in the control and treatment of infectious diseases: report of a workshop on traditional healing methods in the control of infectious diseases. 1993 Jan 21-23; Obafemi Awolowo University, Ile-Ife, Nigeria.
- Ogunbona FA, Akanni AO. Comparative bioavailability studies on some brands of ampicillin capsules. Pharmazie. 1985;40:479.
- Ali HM. Reduced ampicillin bioavailability following oral coadministration with chloroquine. J Antimicrob Chemother. 1985;15:781–4.
- Ogunbona FA, Oluwatudimu OO. Effect of a non-European (Nigerian) diet on the bioavailability of nitrofurantoin in man. Int J Pharmaecutics. 1985;29:191–3.
- Attef OA, Ali AA, Ali HM. Effect of Khat chewing on the bioavailability of ampicillin and amoxycillin. J Antimicrob Chemother. 1997;39:523–5.
- Johri RK, Zutshi U. An Ayurvedic formulation `Trikatu' and its constituents. J Ethnopharmacol. 1992;37:85–91.
- Lamikanra A, Fayinka ST, Olusanya OO. Transfer of low level trimethoprim resistance in faecal isolates obtained from apparently healthy Nigerian students. FEMS Microbiol Lett. 1989;50:275–8.
- Murray BE, Mathewson JJ, DuPont HL, Ericsson CD, Reves RR. Emergence of resistant fecal Escherichia coli in travelers not taking prophylactic antimicrobial agents. Antimicrob Agents Chemother. 1990;34:515–8.
- Woolfson A, Huebner R, Wasas A, Chola S, Godfrey-Faussett P, Klugman K. Nasopharyngeal carriage of community-acquired, antibiotic-resistant Streptococcus pneumoniae in a Zambian paediatric population. Bull World Health Organ. 1997;75:453–62.
- Lamikanra A, Okeke IN. A study of the effect of the urban/rural divide on the incidence of antibiotic resistance in E. coli. Biomedical Letters. 1997;55:91–7.
- Implementation of the global strategy for health for all by the year 2000, second evaluation; and eighth report on the world health situation. Geneva: World Health Organization; 1992.
- Korte R, Rehle T, Merkle A. Strategies to maintain health in the Third World. Trop Med Parasitol. 1991;42:428–32.
- Horton R. The infected metropolis. Lancet. 1996;347:134–5.
- Rosas I, Salinas E, Yela A, Calva E, Eslava C, Cravioto A. Escherichia coli in settled-dust and air samples collected in residential environments in Mexico City. Appl Environ Microbiol. 1997;63:4093–5.
- Meers PD. Infection control in developing countries. J Hosp Infect 1988;11 Suppl A:406-10.
- Okello D, Konde-Lule J, Lubanga R, Arube-Wani J. Waste disposal in private medical clinics in Kampala, Uganda [abstract]. J Clin Epidemiol. 1997;50(Suppl 1):45S.
- ARI Program for the control of acute respiratory infections. Geneva: World Health Organization; 1994.
- Shann F. The management of pneumonia in children in developing countries. Clin Infect Dis. 1995;21(Suppl 3):S218–25.
- Brown RC. Antibiotic sensitivity testing for infections in developing countries: lacking the basics [letter]. JAMA. 1996;276:952–3.
- Ringertz S, Muhe L, Krantz I, Hathaway A, Shamebo D, Freij L, Prevalence of potential respiratory disease bacteria in children in Ethiopia. Antimicrobial susceptibility of the pathogens and use of antibiotics among the children. Acta Paediatr. 1993;82:843–8.
- Mastro TD, Ghafoor A, Nomani NK, Ishaq Z, Anwar F, Granoff DM, Antimicrobial resistance of pneumococci in children with acute lower respiratory tract infection in Pakistan. Lancet. 1991;337:156–9.
- Andrews JM, Brown D, Wise R. A survey of antimicrobial susceptibility testing in the United Kingdom [letter]. J Antimicrob Chemother. 1996;37:187–8.
- Mutanda LN, Omari AM, Wamola IA. Adaptation of a method of measuring zone diameters of bacterial growth inhibition by antibiotics to suit developing countries. East Afr Med J. 1989;66:441–7.
- Shah VP. Trends in health, nutrition, and socio-economic status in Nigeria, India, and Brazil (1960-1990). J Trop Pediatr. 1993;39:118–27.
- Summerfield D. Health in the developing world. Health loses out to the arms trade. BMJ. 1993;307:387.
- Murray CJ, Lopez AD. Global mortality, disability, and the contribution of risk factors: Global Burden of Disease Study. Lancet. 1997;349:1436–42.
- Dodge CP. Health implications of war in Uganda and Sudan. Soc Sci Med. 1990;31:691–8.
- Goma Epidemiology Group. Public health impact of Rwandan refugee crisis: what happened in Goma, Zaire, in July, 1994? Lancet. 1995;345:339–44.
- Marfin AA, Moore J, Collins C, Biellik R, Kattel U, Toole MJ, Infectious disease surveillance during emergency relief to Bhutanese refugees in Nepal. JAMA. 1994;272:377–81.
- Cornwall J. Tuberculosis: a clinical problem of international importance. Lancet. 1997;350:660–1.
Page created: December 10, 2010
Page updated: December 10, 2010
Page reviewed: December 10, 2010
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.