Export of Antimicrobial Drugs by West African Travelers

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.