Antibiotic resistance 2

During 1997, an event doctors had been fearing finally occurred. In three geographically separate patients, an often deadly bacterium, Staphylococcus aureus, responded poorly to a once reliable antidote--the antibiotic vancomycin. Fortunately, in those patients, the bacteria remained susceptible to other drugs and was eradicated. But the appearance of S. aureus not readily cleared by vancomycin foreshadows trouble.

Worldwide, many strains of S. aureus are already resistant to all antibiotics except vancomycin. Emergence of forms lacking sensitivity to vancomycin signifies that variants untreatable by every known antibiotic are on their way. S. aureus, a major cause of hospital-acquired infections, has thus moved one step closer to becoming an unstoppable killer.

The looming threat of incurable S. aureus is just the latest twist in an international public health nightmare: increasing bacterial resistance to many antibiotics that once cured bacterial diseases readily. Ever since antibiotics became widely available in the 1940s, they have been hailed as miracle drugs -- magic bullets able to eliminate bacteria without doing much harm to the cells of treated individuals. Yet with each passing decade, bacteria that defy not only single but multiple antibiotics -- and therefore are extremely difficult to control -- have become increasingly common.

What is more, strains of at least three bacterial species capable of causing life-threatening illnesses (Enterococcus faecalis, Mycobacterium tuberculosis and Pseudomonas aeruginosa) already evade every antibiotic in the clinician's stockpile of more than 100 drugs. In part because of the rise in resistance to antibiotics, the death rates for some communicable diseases (such as tuberculosis) have started to rise again, after having declined in the industrial nations.

How did we end up in this worrisome, and worsening, situation? Several interacting processes are at fault. Analyses of them point to a number of actions that could help reverse the trend, if individuals, businesses and governments around the world can find the will to implement them.

One component of the solution is recognizing that bacteria are a natural, and needed, part of life. Bacteria, which are microscopic, single-cell entities, abound on inanimate surfaces and on parts of the body that make contact with the outer world, including the skin, the mucous membranes and the lining of the intestinal tract. Most live blamelessly. In fact, they often protect us from disease, because they compete with, and thus limit the proliferation of, pathogenic bacteria -- the minority of species that can multiply aggressively (into the millions) and damage tissues or otherwise cause illness. The benign competitors can be important allies in the fight against antibiotic-resistant pathogens.

People should also realize that although antibiotics are needed to control bacterial infections, they can have broad, undesirable effects on microbial ecology. That is, they can produce long-lasting change in the kinds and proportions of bacteria--and the mix of antibiotic-resistant and antibiotic-susceptible types--not only in the treated individual but also in the environment and society at large. The compounds should thus be used only when they are truly needed, and they should not be administered for viral infections, over which they have no power.

Although many factors can influence whether bacteria in a person or in a community will become insensitive to an antibiotic, the two main forces are the prevalence of resistance genes (which give rise to proteins that shield bacteria from an antibiotic's effects) and the extent of antibiotic use. If the collective bacterial flora in a community have no genes conferring resistance to a given antibiotic, the antibiotic will successfully eliminate infection caused by any of the bacterial species in the collection. On the other hand, if the flora possess resistance genes and the community uses the drug persistently, bacteria able to defy eradication by the compound will emerge and multiply.

Antibiotic-resistant pathogens are not more virulent than susceptible ones: the same numbers of resistant and susceptible bacterial cells are required to produce disease. But the resistant forms are harder to destroy. Those that are slightly insensitive to an antibiotic can often be eliminated by using more of the drug; those that are highly resistant require other therapies.

To understand how resistance genes enable bacteria to survive an attack by an antibiotic, it helps to know exactly what antibiotics are and how they harm bacteria. Strictly speaking, the compounds are defined as natural substances (made by living organisms) that inhibit the growth, or proliferation, of bacteria or kill them directly. In practice, though, most commercial antibiotics have been chemically altered in the laboratory to improve their potency or to increase the range of species they affect. Here I will also use the term to encompass completely synthetic medicines, such as quinolones and sulfonamides, which technically fit under the broader rubric of antimicrobials.

Whatever their monikers, antibiotics, by inhibiting bacterial growth, give a host's immune defenses a chance to outflank the bugs that remain. The drugs typically retard bacterial proliferation by entering the microbes and interfering with the production of components needed to form new bacterial cells. For instance, the antibiotic tetracycline binds to ribosomes (internal structures that make new proteins) and, in so doing, impairs protein manufacture; penicillin and vancomycin impede proper synthesis of the bacterial cell wall.

Certain resistance genes ward off destruction by giving rise to enzymes that degrade antibiotics or that chemically modify, and so inactivate, the drugs. Alternatively, some resistance genes cause bacteria to alter or replace molecules that are normally bound by an antibiotic--changes that essentially eliminate the drug's targets in bacterial cells. Bacteria might also eliminate entry ports for the drugs or, more effectively, may manufacture pumps that export antibiotics before the medicines have a chance to find their intracellular targets.

My Resistance Is Your Resistance

Bacteria can acquire resistance genes through a few routes. Many inherit the genes from their forerunners. Other times, genetic mutations, which occur readily in bacteria, will spontaneously produce a new resistance trait or will strengthen an existing one. And frequently, bacteria will gain a defense against an antibiotic by taking up resistance genes from other bacterial cells in the vicinity. Indeed, the exchange of genes is so pervasive that the entire bacterial world can be thought of as one huge multicellular organism in which the cells interchange their genes with ease.

Bacteria have evolved several ways to share their resistance traits with one another [see "Bacterial Gene Swapping in Nature," by Robert V. Miller; Scientific American, January]. Resistance genes commonly are carried on plasmids, tiny loops of DNA that can help bacteria survive various hazards in the environment. But the genes may also occur on the bacterial chromosome, the larger DNA molecule that stores the genes needed for the reproduction and routine maintenance of a bacterial cell.

Often one bacterium will pass resistance traits to others by giving them a useful plasmid. Resistance genes can also be transferred by viruses that occasionally extract a gene from one bacterial cell and inject it into a different one. In addition, after a bacterium dies and releases its contents into the environment, another will occasionally take up a liberated gene for itself.

In the last two situations, the gene will survive and provide protection from an antibiotic only if integrated stably into a plasmid or chromosome. Such integration occurs frequently, though, because resistance genes are often embedded in small units of DNA, called transposons, that readily hop into other DNA molecules. In a regrettable twist of fate for human beings, many bacteria play host to specialized transposons, termed integrons, that are like flypaper in their propensity for capturing new genes. These integrons can consist of several different resistance genes, which are passed to other bacteria as whole regiments of antibiotic-defying guerrillas.

Many bacteria possessed resistance genes even before commercial antibiotics came into use. Scientists do not know exactly why these genes evolved and were maintained. A logical argument holds that natural antibiotics were initially elaborated as the result of chance genetic mutations. Then the compounds, which turned out to eliminate competitors, enabled the manufacturers to survive and proliferate--if they were also lucky enough to possess genes that protected them from their own chemical weapons. Later, these protective genes found their way into other species, some of which were pathogenic.

Regardless of how bacteria acquire resistance genes today, commercial antibiotics can select for -- promote the survival and propagation of -- antibiotic-resistant strains. In other words, by encouraging the growth of resistant pathogens, an antibiotic can actually contribute to its own undoing.

How Antibiotics Promote Resistance

The selection process is fairly straightforward. When an antibiotic attacks a group of bacteria, cells that are highly susceptible to the medicine will die. But cells that have some resistance from the start, or that acquire it later (through mutation or gene exchange), may survive, especially if too little drug is given to overwhelm the cells that are present. Those cells, facing reduced competition from susceptible bacteria, will then go on to proliferate. When confronted with an antibiotic, the most resistant cells in a group will inevitably outcompete all others.

Promoting resistance in known pathogens is not the only self-defeating activity of antibiotics. When the medicines attack disease-causing bacteria, they also affect benign bacteria--innocent bystanders--in their path. They eliminate drug-susceptible bystanders that could otherwise limit the expansion of pathogens, and they simultaneously encourage the growth of resistant bystanders. Propagation of these resistant, nonpathogenic bacteria increases the reservoir of resistance traits in the bacterial population as a whole and raises the odds that such traits will spread to pathogens. In addition, sometimes the growing populations of bystanders themselves become agents of disease.

Widespread use of cephalosporin antibiotics, for example, has promoted the proliferation of the once benign intestinal bacterium E. faecalis, which is naturally resistant to those drugs. In most people, the immune system is able to check the growth of even multidrug-resistant E. faecalis, so that it does not produce illness. But in hospitalized patients with compromised immunity, the enterococcus can spread to the heart valves and other organs and establish deadly systemic disease.

Moreover, administration of vancomycin over the years has turned E. faecalis into a dangerous reservoir of vancomycin-resistance traits. Recall that some strains of the pathogen S. aureus are multidrug-resistant and are responsive only to vancomycin. Because vancomycin-resistant E. faecalis has become quite common, public health experts fear that it will soon deliver strong vancomycin resistance to those S. aureus strains, making them incurable.

The bystander effect has also enabled multidrug-resistant strains of Acinetobacter and Xanthomonas to emerge and become agents of potentially fatal blood-borne infections in hospitalized patients. These formerly innocuous microbes were virtually unheard of just five years ago.

As I noted earlier, antibiotics affect the mix of resistant and nonresistant bacteria both in the individual being treated and in the environment. When resistant bacteria arise in treated individuals, these microbes, like other bacteria, spread readily to the surrounds and to new hosts. Investigators have shown that when one member of a household chronically takes an antibiotic to treat acne, the concentration of antibiotic-resistant bacteria on the skin of family members rises. Similarly, heavy use of antibiotics in such settings as hospitals, day care centers and farms (where the drugs are often given to livestock for nonmedicinal purposes) increases the levels of resistant bacteria in people and other organisms who are not being treated--including in individuals who live near those epicenters of high consumption or who pass through the centers.

Given that antibiotics and other antimicrobials, such as fungicides, affect the kinds of bacteria in the environment and people around the individual being treated, I often refer to these substances as societal drugs--the only class of therapeutics that can be so designated. Anticancer drugs, in contrast, affect only the person taking the medicines.

On a larger scale, antibiotic resistance that emerges in one place can often spread far and wide. The ...

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