Skip directly to site content Skip directly to page options Skip directly to A-Z link Skip directly to A-Z link Skip directly to A-Z link
Volume 5, Number 1—February 1999
Perspective

Socioeconomic and Behavioral Factors Leading to Acquired Bacterial Resistance to Antibiotics in Developing Countries

Iruka N. Okeke*, Adebayo Lamikanra*, and Robert Edelman†Comments to Author 
Author affiliations: *Obafemi Awolowo University, Ile-Ife, Nigeria;; †University of Maryland School of Medicine, Baltimore, Maryland, USA

Main Article

Table 2

Source and quality of tetracycline capsules in a Nigerian suburban town (compiled with data from [53])

Sample Source Tetracycline content (% of label claim) Content of ATCa (%) Bioavailability (%)b
C1 Manufacturerc 105.9 None detected 100
C2 Hospital 107.5 5.3 63.4d
C3 Roadside stall 104.5 1.1 80.5d
C4 Pharmacy 66.1 2.4 65.2d
C5 Patent medicine stall 84.5 1.9 87.6d
C6 Roadside stall 67.8 1.5 Not tested
C7 Patent medicine stall 89.6 1.8 Not tested

aAnhydrotetracycline, one of four tetracycline degradation products.
bMeasured from cumulative excretion of tetracycline in the urine of five volunteers.
cReference standard obtained from the manufacturer.
dSignificantly different from C1 (p = 0.01, Wilcoxon signed rank test).

Main Article

References
  1. Kunin  CM. Resistance to antimicrobial drugs a worldwide calamity. Ann Intern Med. 1993;118:55761.PubMed
  2. 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;147:7248.
  3. Sack  RB, Rahman  M, Yunus  M, Khan  EH. Antimicrobial resistance in organisms causing diarrheal disease. Clin Infect Dis. 1997;24(Suppl 1):S1025.PubMed
  4. 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):S16975.PubMed
  5. 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;26:3415. DOIPubMed
  6. 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;14:105560.PubMed
  7. 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;39:2569.PubMed
  8. 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;28:16571. DOIPubMed
  9. 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;34:118992.PubMed
  10. 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;34:253743.PubMed
  11. 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;70:60912.PubMed
  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;1:30913.PubMed
  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;40:1699702.PubMed
  14. Col  NF, O'Connor  RW. Estimating worldwide current antibiotic usage: report of Task Force 1. Rev Infect Dis. 1987;9(Suppl 3):S23243.PubMed
  15. Kunin  CM, Johansen  KS, Worning  AM, Daschner  FD. Report of a symposium on use and abuse of antibiotics worldwide. Rev Infect Dis. 1990;12:129.PubMed
  16. 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;72:26571.PubMed
  17. Bojalil  R, Calva  JJ. Antibiotic misuse in diarrhea. A household survey in a Mexican community. J Clin Epidemiol. 1994;47:14756. DOIPubMed
  18. Nizami  SQ, Khan  IA, Bhutta  ZA. Drug prescribing practices of general practitioners and paediatricians for childhood diarrhoea in Karachi, Pakistan. Soc Sci Med. 1996;42:11339. DOIPubMed
  19. 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;42:114153. DOIPubMed
  20. 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;16:5604. DOIPubMed
  21. 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;50:1297304. DOIPubMed
  22. 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.
  23. Muhuri  PK, Anker  M, Bryce  J. Treatment patterns for childhood diarrhoea: evidence from demographic and health surveys. Bull World Health Organ. 1996;74:13546.PubMed
  24. Cash  R. Inappropriate treatment for dysentery. BMJ. 1996;313:1812.PubMed
  25. Lee  MG, Henry  GL. Drug availability in Jamaica. West Indian Med J. 1989;38:1059.PubMed
  26. Williams  RJ, Heymann  DL. Containment of antibiotic resistance. Science. 1998;279:11534. DOIPubMed
  27. Turnridge  J. Epidemiology of quinolone resistance. Eastern hemisphere. Drugs. 1995;49:437. DOIPubMed
  28. 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;825:175.PubMed
  29. 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;50:1214.PubMed
  30. Munishi  GK. The development of the Essential Drugs Program and implications for self-reliance in Tanzania. J Clin Epidemiol. 1991;44(Suppl 2):7S14S. DOIPubMed
  31. 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;342:140810. DOIPubMed
  32. Salako  LA. Drug supply in Nigeria. J Clin Epidemiol. 1991;44(Suppl 2):15S9S. DOIPubMed
  33. 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;30:10617.PubMed
  34. 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;39:5437. DOIPubMed
  35. 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;49:3557. DOIPubMed
  36. Robles  Y, Polack  A. Continuing professional education in pharmacy in the Philippines 2. A current perspective. J Soc Adm Pharm. 1997;14:24132.
  37. Ronsmans  C, Islam  T, Bennish  ML. Medical practitioners' knowledge of dysentery treatment in Bangladesh. BMJ. 1996;313:2056.PubMed
  38. Hartog  R. Essential and non-essential drugs marketed by the 20 largest European pharmaceutical companies in developing countries. Soc Sci Med. 1993;37:897904. DOIPubMed
  39. Lee  PR, Lurie  P, Silverman  MM, Lydecker  M. Drug promotion and labeling in developing countries: an update. J Clin Epidemiol. 1991;44(Suppl 2):49S55S. DOIPubMed
  40. Pearson  CA. The role of district hospitals and the action in international medicine network. Infect Dis Clin North Am. 1995;9:391405.PubMed
  41. Thamlikitkul  V. Antibiotic dispensing by drug store personnel in Bangkok, Thailand. J Antimicrob Chemother. 1988;21:12531. DOIPubMed
  42. Kigotho  AW. Ugandan doctors request antibiotic moratorium. Lancet. 1997;350:1014. DOIPubMed
  43. 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;38:71724. DOIPubMed
  44. Singh  J, Raje  N. The rise of Western medicine in India. Lancet. 1996;348:1598. DOIPubMed
  45. Haak  H. Pharmaceuticals in two Brazilian villages: lay practices and perceptions. Soc Sci Med. 1988;27:141527. DOIPubMed
  46. Kafle  KK, Gartoulla  RP, Pradhan  YM, Shrestha  AD, Karkee  SB, Quick  JD. Drug retailer training: experiences from Nepal. Soc Sci Med. 1992;35:101525. DOIPubMed
  47. Rahman  F, Andersson  R, Svanstrom  L. Medical help seeking behaviour of injury patients in a community in Bangladesh. Public Health. 1998;112:315. DOIPubMed
  48. 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;98:2416.PubMed
  49. Van der Geest  S. Marketplace conversations in Cameroon: how and why popular medical knowledge comes into being. Cult Med Psychiatry. 1991;15:6990. DOIPubMed
  50. Wolff  MJ. Use and misuse of antibiotics in Latin America. Clin Infect Dis. 1993;17(Suppl 2):S34651.PubMed
  51. Obaseiki-Ebor  EE, Akerele  JO, Ebea  PO. A survey of antibiotic outpatient prescribing and antibiotic self- medication. J Antimicrob Chemother. 1987;20:75963. DOIPubMed
  52. 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;43:617. DOIPubMed
  53. Okeke  I, Lamikanra  A. Quality and bioavailability of tetracycline capsules in a Nigerian semi-urban community. Int J Antimicrob Agents. 1995;5:24550. DOIPubMed
  54. Hossain  MM, Glass  RI, Khan  MR. Antibiotic use in a rural community in Bangladesh. Int J Epidemiol. 1982;11:4025. DOIPubMed
  55. Goel  P, Ross-Degnan  D, Berman  P, Soumerai  S. Retail pharmacies in developing countries: a behavior and intervention framework. Soc Sci Med. 1996;42:115561. DOIPubMed
  56. 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;50:14550.PubMed
  57. Abosede  OA. Self-medication: an important aspect of primary health care. Soc Sci Med. 1984;19:699703. DOIPubMed
  58. 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;152:11149.PubMed
  59. 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;12:9868.PubMed
  60. 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):S9981000.PubMed
  61. 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):S27085.PubMed
  62. Haak  H, Hardon  AP. Indigenised pharmaceuticals in developing countries: widely used, widely neglected. Lancet. 1988;2:6201. DOIPubMed
  63. 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;23:40712. DOIPubMed
  64. Strang  JK. Tracing patients in rural Africa. Lancet. 1996;348:10834. DOIPubMed
  65. Esezobo  E, Offiong  E. In vitro studies on some brands of oxytetracycline capsules available in Nigeria. Nigerian Journal of Pharmacology. 1986;17:248.
  66. Agom  JK, Akanni  AO, Dawodu  TO. Quality of ampicillin/cloxacillin preparations on the Nigerian market. Nigerian Journal of Pharmacology. 1990;21:368.
  67. Taylor  RB, Shakoor  O, Behrens  RH. Drug quality, a contributor to drug resistance? Lancet. 1995;346:122. DOIPubMed
  68. 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;57:316.PubMed
  69. Hogerzeil  HV, Battersby  A, Srdanovic  V, Stjernstrom  NE. Stability of essential drugs during shipment to the tropics. BMJ. 1992;304:2102. DOIPubMed
  70. Shakoor  O, Taylor  RB, Behrens  RH. Assessment of the incidence of substandard drugs in developing countries. Trop Med Int Health. 1997;2:83945. DOIPubMed
  71. Gustafsson  LL, Wide  K. Marketing of obsolete antibiotics in Central America. Lancet. 1981;1:313. DOIPubMed
  72. Ali  HM, Homeida  MM, Abdeen  MA. Drug dumping in donations to Sudan. Lancet. 1988;333:5389. DOI
  73. 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;337:18425. DOIPubMed
  74. Guidelines for drug donations. Geneva: World Health Organization; 1996. Report No.: WHO/DAP/96.2.
  75. Adjepon-Yamaoah  K. Drugs for the tropicstheir uses and abuses. Afr Health. 1980;:146.
  76. Land  T. Combating counterfeit drugs. Nature. 1992;355:192.PubMed
  77. McGregor  A. Counterfeit drugs flood developing world. Lancet. 1997;350:1690. DOI
  78. Alubo  SO. Death for sale: a study of drug poisoning and deaths in Nigeria. Soc Sci Med. 1994;38:97103. DOIPubMed
  79. Couper  MR. Strategies for the rational use of antimicrobials. Clin Infect Dis. 1997;24(Suppl 1):S1546.PubMed
  80. Huang  WF, Wen  KC, Hsiao  ML. Adulteration by synthetic therapeutic substances of traditional Chinese medicines in Taiwan. J Clin Pharmacol. 1997;37:34450.PubMed
  81. Michel  JM. Why do people like medicines? A perspective from Africa [letter]. Lancet. 1985;1:2101. DOIPubMed
  82. 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.
  83. Ogunbona  FA, Akanni  AO. Comparative bioavailability studies on some brands of ampicillin capsules. Pharmazie. 1985;40:479.PubMed
  84. Ali  HM. Reduced ampicillin bioavailability following oral coadministration with chloroquine. J Antimicrob Chemother. 1985;15:7814. DOIPubMed
  85. Ogunbona  FA, Oluwatudimu  OO. Effect of a non-European (Nigerian) diet on the bioavailability of nitrofurantoin in man. Int J Pharmaecutics. 1985;29:1913. DOI
  86. Attef  OA, Ali  AA, Ali  HM. Effect of Khat chewing on the bioavailability of ampicillin and amoxycillin. J Antimicrob Chemother. 1997;39:5235. DOIPubMed
  87. Johri  RK, Zutshi  U. An Ayurvedic formulation `Trikatu' and its constituents. J Ethnopharmacol. 1992;37:8591. DOIPubMed
  88. 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;50:2758. DOIPubMed
  89. 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;34:5158.PubMed
  90. 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;75:45362.PubMed
  91. 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;55:917.
  92. 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.
  93. Korte  R, Rehle  T, Merkle  A. Strategies to maintain health in the Third World. Trop Med Parasitol. 1991;42:42832.PubMed
  94. Horton  R. The infected metropolis. Lancet. 1996;347:1345. DOIPubMed
  95. 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;63:40935.PubMed
  96. Meers  PD. Infection control in developing countries. J Hosp Infect 1988;11 Suppl A:406-10.
  97. 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. DOI
  98. ARI Program for the control of acute respiratory infections. Geneva: World Health Organization; 1994.
  99. Shann  F. The management of pneumonia in children in developing countries. Clin Infect Dis. 1995;21(Suppl 3):S21825.PubMed
  100. Brown  RC. Antibiotic sensitivity testing for infections in developing countries: lacking the basics [letter]. JAMA. 1996;276:9523. DOIPubMed
  101. 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;82:8438.PubMed
  102. 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;337:1569. DOIPubMed
  103. Andrews  JM, Brown  D, Wise  R. A survey of antimicrobial susceptibility testing in the United Kingdom [letter]. J Antimicrob Chemother. 1996;37:1878. DOIPubMed
  104. 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;66:4417.PubMed
  105. Shah  VP. Trends in health, nutrition, and socio-economic status in Nigeria, India, and Brazil (1960-1990). J Trop Pediatr. 1993;39:11827.PubMed
  106. Summerfield  D. Health in the developing world. Health loses out to the arms trade. BMJ. 1993;307:387. DOIPubMed
  107. Murray  CJ, Lopez  AD. Global mortality, disability, and the contribution of risk factors: Global Burden of Disease Study. Lancet. 1997;349:143642. DOIPubMed
  108. Dodge  CP. Health implications of war in Uganda and Sudan. Soc Sci Med. 1990;31:6918. DOIPubMed
  109. Goma Epidemiology Group. Public health impact of Rwandan refugee crisis: what happened in Goma, Zaire, in July, 1994? Lancet. 1995;345:33944. DOIPubMed
  110. 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;272:37781. DOIPubMed
  111. Cornwall  J. Tuberculosis: a clinical problem of international importance. Lancet. 1997;350:6601. DOIPubMed

Main Article

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.
file_external