The Role of Poverty in Antimicrobial Resistance

Poverty and Resistance in Developing Countries

In developing countries with high mortality, infectious diseases remain the main cause of death.⁴ In 1990, an estimated 78% of the world's population lived in developing countries. In those countries, 23% of deaths were attributable to infectious and parasitic disease.⁵

Resistant bacteria have emerged in these developing countries. In 1996, in Bangladesh, over 95% of Shigella dysenteriae isolates were resistant to ampicillin, co-trimoxazole, and nalidixic acid, and up to 40% were resistant to mecillinam.⁶ In Quetta, Pakistan, 69% of Salmonella typhi isolated from blood were multidrug resistant.⁷ In tropical countries, there has been an emergence of Streptococcus pneumoniae that is resistant to penicillin, cefotaxime, and chloramphenicol.⁸ Neisseria gonorrhoeae has developed strains resistant to penicillin, sulfonamides, tetracyclines, and fluoroquinolones.⁹

This problem of multidrug-resistant organisms in developing countries can also directly affect and threaten more developed countries (such as the United States) because international travel, driven by globalized trade, allows for easier dissemination of these strains. For example, penicillin-resistant and multidrug-resistant pneumococci, like the serotype 23F clone, have been found not only in Mexico, South Africa, South Korea, and Croatia, but also in Portugal, France, and the United States.¹⁰

Reasons for multidrug-resistant organisms in developing countries are numerous, but the inadequate access to effective drugs, the unregulated manufacture and dispensation of antimicrobials, and the lack of money available to pay for appropriate, high-quality medications are some of the major poverty-driven factors contributing to antimicrobial resistance.^1–3

In some developing countries, regulation of the manufacture of antibiotics may not exist to any extent that would assure the quality and potency of the medications. A 500-mg capsule of ciprofloxacin that was acquired locally in Vietnam was analyzed and found to contain the equivalent of only 20 mg of ciprofloxacin.² Studies conducted in several other developing countries have also demonstrated counterfeit drugs with few or no active ingredients.³

Many developing countries allow the dispensation of antibiotics without a prescription; this can lead to self-medication and dispensation of drugs by untrained people. In one survey from the Rajbari district of Bangladesh, 100,000 doses of antibiotics had been dispensed without a prescription in 1 month.¹¹ In another study from Bangladesh, 92% of medications dispensed by pharmacies were dispensed without a prescription.¹² In Manila, Philippines, a survey of drugstores showed that 66% of antibiotic purchases were made without a prescription.¹³ The ease of obtaining an antibiotic without a prescription was directly experienced by this author, who was able to purchase antimicrobials without a prescription from local pharmacies in both Lahore, Pakistan and Iquitos, Peru.

Poverty-stricken patients may forgo the cost of a physician consultation and self-medicate.³ They may be more likely to purchase the least expensive (and possibly least potent drug) under the assumption that they were all bioequivalent. Furthermore, these people may only complete a truncated course of therapy because of their inability to pay for the full course of medications.^1,3,13 Such inappropriate use of antibiotics for inadequate periods of time can exert strong selective pressures on bacterial populations and can contribute to resistance.

Poverty-Driven Practices in the Unites States

Although it is one of the wealthiest nations in the world, the United States is home to 37 million people living below the poverty line; 46.6 million are without health insurance.¹⁴ There are also 35.9 million seniors (aged 65 and over), 10% of whom live in poverty, with many others having limited income and prescription coverage.¹⁵ For these people, the cost of pharmaceuticals can be prohibitive.

Through limited research and anecdotal experience, it is known that some seniors and low-income patients obtain antimicrobials from other countries and may engage in the sharing of medications.^16–18 Some save antibiotics from regimens that they did not complete (so-called “leftover” antibiotics) and will take them at the onset of upper respiratory infection symptoms.¹⁹

Such self-medication can lead to antimicrobial resistance because of the inappropriate use of antibiotics for viral illness, the inappropriate choice of medication for the specific organism, and the inappropriate dose or duration of therapy. Unfortunately, such practices are probably more widespread than realized. McKee et al¹⁸ surveyed an ethnically diverse population in an urban setting regarding antibiotic use in the setting of an upper respiratory infection. They found that 26% obtained antibiotics from a source other than a physician's prescription. Larson et al¹⁷ reported that, in a largely Hispanic neighborhood in Manhattan, antibiotics were readily available over the counter at local bodegas (small stores). They also reported the sharing of antibiotics among family members or between friends. In one survey of emergency room patients, 17% reported taking “leftover” antibiotics for upper respiratory infection symptoms.¹⁹

As health care and prescription costs soar, more and more people with limited incomes may turn to foreign countries for more affordable medications. A survey of adults in Los Angeles County showed that 14% had crossed the border into Mexico for health care. Nearly 80% of those were uninsured. Of the 28% who purchased medications in Mexico, 90% were uninsured. Many of these purchases were of antibiotics that were readily available without a prescription.¹⁶

Some people with low income may purchase discounted drugs via the internet. This contributes to antimicrobial resistance through the use of suboptimal-quality drugs. Between 1992 and 1994, 51% of counterfeit drug cases uncovered by the World Health Organization carried no active ingredient, 17% contained the wrong ingredient, and 11% contained less than the recommended concentration of active ingredient. Furthermore, 70% of these counterfeiting cases were discovered in developing countries.¹ In the summer of 2003, the Food and Drug Administration examined 1153 shipments that arrived at Miami, New York, and 2 California mail facilities. Of these, 88% contained unapproved drugs from various countries; 16% were from Canada, 14% were from India, 14% came from Thailand, and 8% came from the Philippines.²⁰

Surveillance studies throughout the United States reveal the emergence of multidrug resistance in common infectious organisms. One study showed Streptococcus pneumoniae resistance to penicillin, ceftriaxone, erythromycin, clindamycin, tetracycline, and trimethoprim-sulfamethoxazole. Approximately 22% of those isolates were multidrug resistant. There was also a trend toward increased fluoroquinolone resistance.²¹ Neisseria gonorrhoeae has shown increasing resistance to penicillin and tetracycline and an emerging resistance to fluoroquinolones.²² In 2002, Salmonella that was resistant to amoxicillin/clavulanate, ampicillin, cefoxitin, ceftiofur, cephalothin, chloramphenicol, streptomycin, sulfamethoxazole, and tetracycline was detected in 5 states.²³

Appropriately, much of the blame for the emergence of resistance in the United States has been placed on inappropriate antibiotic prescribing practices by clinicians and on poor patient compliance. However, the poverty-driven practices of medication sharing, self-treatment, and use of poor-quality, foreign-made drugs are also likely contributors to multidrug-resistant organisms. Unfortunately, there is currently a dearth of research into how these practices directly affect resistance patterns within a community in the United States.

A causal relationship is suggested by the results of research conducted on the resistance of Escherichia coli in a community along the border of the United States and Mexico, where crossing the border to obtain medications is not unusual. In this community, resistance rates were higher than the national average.²⁴ A better understanding of the impact that these practices have on resistance can lead to an understanding of whether interventional efforts to reduce these practices can lead to a significant reduction of antimicrobial resistance in the community.

Discussion

Analysis of the information above indicates that poverty may play a role in antimicrobial resistance worldwide. It further suggests that effective intervention cannot be done in isolation. Because of international travel, multidrug-resistant organisms in one country can be more easily disseminated to another country. The ease of obtaining antibiotics without a prescription in some developing countries can lead to self-medication, not only in those developing countries, but in the United States as well. In addition, because of the internet, low-quality and counterfeit drugs affect not only the country of origin, but also populations in the United States. The United States cannot effectively combat antimicrobial resistance within its borders if it ignores the contributing factors from developing countries, and it cannot design effective intervention if it fails to study and recognize the poverty-driven socioeconomic and behavioral factors that may contribute to resistance.

Areas for Further Study Within the United States

The United States is lagging behind the international community in recognizing the role of poverty in antimicrobial resistance. To rectify the situation, studies analyzing socioeconomic and behavioral factors regarding antibiotic use need to be undertaken to recognize the impact of these factors on antimicrobial resistance and to identify areas for education and intervention.

Suggestions for further investigation include:

1. Determine antimicrobial practices in the low-income population. Determine the duration of compliance to therapy, reasons for noncompliance, sources of medications, prevalence of medication sharing, and prevalence of use of drugs not made in the United States. Specific studies of low-income seniors and various low-income ethnic groups should be undertaken because practices and beliefs may differ among these various populations.

2. Correlate resistance rates in communities that engage in self-medication (ie, medication sharing, purchasing of medications without a prescription, taking leftover antibiotics) with national resistance rates for various common organisms to determine how these practices impact resistance.

3. Examine perceptions regarding the role and benefit of antibiotics, including assessing the prevalence of common misperceptions regarding antibiotics. For example, within this author's primary care practice, patients have expressed the opinions that antibiotics provide symptom relief, they are necessary at the appearance of green sputum, and they can prevent progression of symptoms (ie, “nip it in the bud” mentality).

4. Continue to assess the efficacy of interventions involving community-wide education regarding appropriate antibiotic use and the problem of antimicrobial resistance.

Poverty has long been recognized in the international community as a driving force in antimicrobial resistance. But the role of poverty in antimicrobial resistance remains unrecognized in the United States, as evidenced by the dearth of related research. A problem that is not fully understood cannot be effectively solved. As the problem of antimicrobial resistance continues to escalate, it becomes more imperative that the effect of poverty on antimicrobial resistance be further studied, so that effective interventions can be implemented.