Export of Antimicrobial Drugs by West African Travelers Iruka N. Okeke and Adebayo Lamikanra eled with medicines for the management of chronic conditions, such as hypertension, asthma, and diabetes. In contrast, 232 (54.7%) of all respondents traveled with at least 1 antimicrobial drug. Of these, 218 (94%) traveled with at least 1 antimalarial and 129 (55.6%) with at least 1 antibacterial drug (Table 1). Twenty-three (5.4%) of the respondents traveled with 2 antimalarials (the most common combination being chloroquine and sulfadoxine-pyrimethamine [12 respondents]). Twenty-one (5%) respondents traveled with 2 or more antibacterial medicines and 6 of these with 3 or more. Fifty-one (35.9%) of respondents that did not travel with medicines and 188 (66.7%) of those that did reported that they had suffered fever or malaria away from their countries. The commonest response to a perceived malaria attack was to take medicines brought along on the trip (Table 2). Only 31.7% of respondents who did not travel with medicines and 13.8% of those that did said that they would visit a doctor or hospital. The majority of the travelers visited Europe and North America. We observed that the minority that traveled to South America, Asia, and Australia were more likely to travel with antibiotics Antimicrobial use has been correlated with the prevalence of resistance among microorganisms. Resistant strains are particularly likely to be selected when antibiotics are used inappropriately. This is a common feature in many developing countries, where antimalarials and antibiotics are available from multiple sources without prescription and professional health care is expensive or unavailable.1,2 Increasing numbers of African residents make short-term visits to countries where antibiotics are only available by prescription. We sought to determine how commonly these individuals traveled with antimicrobials purchased in their own countries; how often they considered themselves infected abroad; and what was their primary response to presumed infection. Questionnaires were administered to 424 West Africans normally resident in Nigeria, who had traveled by air to another country (other than their country of origin), in the previous 3 years. Of the respondents, 328 (77.4%) of these individuals were Nigerians, 53 (12.5%) were Ghanaians, and 43 (10.1%) were citizens of other countries, including Senegal (10), Niger (9), Cameroon (3) and Togo (3). More than half of the respondents, 224 (52.8%), traveled to Europe, and 86 (20.3%) visited the Americas. The destination of 61 (14.4%) was another African country; 20 (4.7%), Asia/Oceania; and 15 (3.5%), the Middle East. Two hundred and three (47.9%) travelers were 41 or more years old and 221 (52.1%) were aged between 18 and 40 years. A total of 282 (66.5%) respondents admitted that they traveled with medicines. Only 18 (4.2%) traveled with herbal or other traditional medicines, and 71 (16.7%) trav- Table 1 Antimalarials and Antibiotics Exported by West African Travelers Antimicrobial Drugs Exported No. (%) of Respondents (n = 424) All antimalarials Sulfadoxine-pyrimethamine (Fansidar) Chloroquine Halofantrine Mefloquine Pyrimethamine (Daraprim) Proguanil hydrochloride (Paludrine) Metakelfin Amodiaquine Proguanil-atovaquone (Malarone) Artemisinin Iruka N. Okeke, PhD: Department of Biology, Haverford College, Haverford, Pennsylvania; Adebayo Lamikanra, PhD: Faculty of Pharmacy, Obafemi Awolowo University, Ile-Ife, Nigeria. 222 (52.4) 112 (26.4) 88 (20.8) 10 (2.4) 9 (2.1) 7 (1.7) 7 (1.7) 4 (0.9) 3 (0.7) 2 (0.5) 1 (0.2) All antibacterials 129 (30.4) Tetracycline 54 (12.7) Ampicillin 29 (6.8) Ampicillin-cloxacillin 17 (4.0) Amoxicillin 2 (0.5) Amoxicillin-clavulanic acid (Augmentin) 1 (0.2) Metronidazole 27 (6.4) Trimethoprim-sulfamethoxazole 24 (5.7) Chloramphenicol 4 (0.9) Erythromycin 1 (0.2) This work was funded by grant NIG01 from the International Program in the Chemical Sciences, Sweden. The authors had no financial or other conflicts of interest to disclose. Reprint requests: Adebayo Lamikanra, BPharm, PhD, Department of Pharmaceutics, Faculty of Pharmacy, Obafemi Awolowo University, Nigeria. J Travel Med 2003; 10:133–135. 133 134 Table 2 J o u r n a l o f Tr a v e l M e d i c i n e , Vo l u m e 1 0 , N u m b e r 2 Preferred Sources of Treatment (%) of West African Travelers Following Fever or Malaria Symptoms Response to Fever or Malaria Symptoms Abroad See doctor or hospital Take medicines brought Purchase over-the-counter medicines in the country visited Obtain medicine from friends or other sources Not seek treatment No response Travelers without Antimicrobials (n = 142) Travelers with Antimicrobials (n = 282) All Travelers (n = 424) 45 (31.7) 0 (0) 39 (13.8) 172 (61.0) 84 (19.8) 172 (40.6) 15 (10.6) 11 (3.9) 26 (6.1) 10 (7.0) 6 (4.2) 66 (46.5) 12 (4.3) 2 (0.7) 46 (16.3) 22 (51.9) 8 (1.9) 112 (26.4) and were less likely to choose to visit a doctor or hospital when they were ill (Fig. 1). Almost all the visitors to Asia and Australia traveled with antimalarials. Visitors to foreign African countries were equally likely to export antimicrobials as those to Europe and North America. These data suggest a tendency to export medicines during travel to tropical countries significantly distant from home. However, the number of respondents visiting these destinations was relatively small. The World Health Organization recommends that all patients with fever in malaria-endemic areas, particularly pediatric ones, be treated with antimalarials.3 Diagnosis and treatment of presumptive malaria is therefore rapid in West African countries, whether performed by a health professional, layman, or the patient. Physicians in temperate countries, even those who practice in areas that commonly receive travelers from malaria-endemic areas, tend to be of the opinion that malaria outside the Tropics is rare,4,5 and, therefore, the diagnosis and treatment of malaria cases outside of endemic areas is often fraught with delays and protocols that patients are unfamiliar with and perceive as incompetence.5 Travelers to endemic areas at which medical systems are unfamiliar or language difficulties may exist may also choose to export antimicrobials and avoid orthodox medical care. In addition, travelers try to avoid incurring medical costs when abroad. In the absence of prophylactic therapy, travelers from malaria-endemic areas are at risk of clinical malaria for several months after they leave the endemic area. There is therefore excellent rational for prophylactic therapy for West Africans visiting nonendemic areas and perhaps for empiric treatment of fever in recent arrivals from endemic areas. The results of this survey, however, suggest that a major reason for the export of antimalarials is to treat self-diagnosed malaria, should it occur, in order to avoid visiting a medical center during a trip abroad. Patients from West Africa are quick to diagnose malaria in themselves or their dependents and equally quick to self prescribe chemotherapy.6 A study conducted in Northern Cameroon observed that the majority of patients who claimed they had fever, in fact, did not and that self-diagnosis was therefore unreliable.7 This suggests that many travelers may be inadvertently misusing the antimalarials they carry. In addition, antimalarials and antibiotics sold within African countries are often of substandard quality.8–11 This increases the chance that treatment will be unsuccess- Multiple (n = 18) Europe (n = 224) North America (n = 82) South America (n = 4) Africa (n = 61) Australia (n = 3) and Asia (n = 17) Middle East (n = 15) Figure 1 Travelers visiting Asia, Australia, and South America were more likely to travel with antibiotics and to avoid professional medical care than those visiting Europe, North America, and other African countries. The majority of visitors to Asia and Australia traveled with antimalarials. O k e k e a n d L a m i k a n r a , E x p o r t o f A n t i m i c r o b i a l s b y Tr a v e l e r s Broad spectrum penicillins (p < .0001) Tetracycline (p = .06) 135 infection or fever. Only small proportions of these people seek medical care abroad, preferring to self-medicate or obtain medicines from friends. Reported imported infections may represent only a proportion of cases from developing countries. The importation of a culture of self-medication for infection may have adverse effects on the prevalence of resistant organisms in countries visited. Acknowledgment Antibiotic resistance research in Nigeria by AL and INO is funded by the International Program in the Chemical Sciences, Uppsala University, Sweden. References Figure 2 Age-related antibiotic preferences. Respondents under 40 years of age were more likely to travel with broad spectrum penicillins whereas those aged 40 and above selected tetracycline. ful or that resistant pathogens will be selected during treatment even if the self-diagnosis was accurate9. The export of antibiotics is more disturbing than of antimalarials. Almost a third of the travelers carried antibiotics, most of which were broad-spectrum agents. There is no rationale for traveling with antibiotics as the likelihood of these travelers correctly self-diagnosing a bacterial infection, without medical consultation and laboratory diagnosis, is small. It is far more likely that travelers needlessly expose flora with which they interact with on their travels to antibiotics, increasing the risk of selecting resistant bacteria. The tendency to export antibiotics was not related to country of origin or age. We, however, noted that older travelers were more likely to carry tetracycline whereas those aged 40 and under preferred broad-spectrum penicillins, such as ampicillin and amoxicillin (Fig. 2). This could suggest that tetracycline is loosing popularity among younger generations, whereas the abuse of antibiotics is not. Resistance to both classes of drugs, particularly tetracycline (which appears to have been abused longer), is increasing in West African countries. In some studies, over 90% of isolates demonstrate tetracycline resistance and the trends seen with ampicillin misuse suggest that a similar situation may occur in years to come.1,2,12 A large proportion of West Africans travel with antimicrobial drugs, which they use to treat presumed 1. Kariuki S. Kenya: antibiotic resistance. Lancet 1997; 349: SIII9–SIII10. 2. Okeke IN, Lamikanra A, Edelman R. Socioeconomic and behavioral factors leading to acquired bacterial resistance to antibiotics in developing countries. Emerg Infect Dis 1999; 5:18–27. 3. Schapira A. A standard protocol for assessing the proportion of children presenting with febrile disease who suffer from malarial disease. Geneva: World Health Organization, 1994. 4. Weinstein R. Malaria, imported — USA (Virginia) from West Africa. Available at http://www.promedmail.org/pls/ askus. Accessed January 10, 2003. 5. Matteelli A, Volonterio A, Gulletta M, et al. Malaria in illegal Chinese immigrants, Italy. Emerg Infect Dis 2001; 7:1055–1088. 6 Hamel M, Odhacha A, Roberts J, Deming M. Malaria control in Bungoma District, Kenya: a survey of home treatment of children with fever, bednet use and attendance at antenatal clinics. Bull World Health Org 2001; 79:1014–1023. 7. Einterz EM, Bates ME. Fever in Africa: do patients know when they are hot? Lancet 1997; 350:781. 8. Okeke IN, Lamikanra A. Quality and bioavailability of tetracycline capsules in a Nigerian semi-urban community. Int J Antimicrob Ag 1995; 5:245–250. 9. Basco LK, Ringwald P, Manene AB, Chandenier J. False chloroquine resistance in Africa. Lancet 1997; 350:224. 10. Shakoor O, Taylor RB, Behrens RH. Assessment of the incidence of substandard drugs in developing countries. Trop Med Int Health 1997; 2:839–845. 11. Taylor RB, Shakoor O, Behrens RH, et al. Pharmacopoeial quality of drugs supplied by Nigerian pharmacies. Lancet 2001; 357:1933–1936. 12. Okeke I, Fayinka S, Lamikanra A. Antibiotic resistance trends in Escherichia coli from apparently healthy Nigerian students (1986-1998). Emerg Infect Dis 2000; 6:393–396.
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