Editorials

Antibiotic Resistance Threats in the United States: Stepping Back from the Brink

 


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Am Fam Physician. 2014 Jun 15;89(12):938-941.

In a recently issued report, the Centers for Disease Control and Prevention (CDC) estimated the national burden of illnesses and deaths caused by the most common and most worrisome antibiotic-resistant pathogens.1 The report focused on 16 antimicrobial-resistant bacterial pathogens, as well as Candida infections, which together account for more than 2 million illnesses and at least 23,000 deaths every year in the United States.1 The report also included information on Clostridium difficile infections, which, like antibiotic resistance, are driven by antibiotic use. C. difficile causes more than 250,000 clinical infections annually and is associated with more than 14,000 deaths every year in the United States.1

In this report, the CDC categorized 18 pathogens (eTable A) into three groups (urgent, serious, and concerning) based on seven criteria: clinical impact, economic impact, incidence, 10-year projection of incidence, transmissibility, availability of effective antibiotics, and barriers to prevention.1 Three types of bacteria were included in the urgent category: carbapenem-resistant Enterobacteriaceae, drug-resistant Neisseria gonorrhoeae, and C. difficile. In the past, drug-resistant strains of Enterobacteriaceae and N. gonorrhoeae have shown a propensity to spread rapidly in the United States and around the world. Some strains of carbapenem-resistant Enterobacteriaceae are currently untreatable with available antibiotics, and the cephalosporin agents to which some gonococci are now showing emerging resistance are the last available drugs to effectively treat this infection. Thus, further spread of these strains constitutes a public health crisis. C. difficile infections already cause significant morbidity and mortality, and a recently emerging epidemic strain, BI/NAP1/027, appears to be more virulent.

View/Print Table

eTable A

Antibiotic-Resistant Microorganism Threats

MicroorganismNotable information

Urgent

Clostridium difficile A1,A2

Deaths related to C. difficile increased 400% between 2000 and 2007, in part because of a stronger strain

Most infections are connected to receiving medical care

Hand sanitizer does not kill C. difficile, and hand washing may not be sufficient

Carbapenem-resistant Enterobacteriaceae A3

Difficult to treat and, in some cases, untreatable

Kills up to one-half of patients who get bloodstream infections

Easily spreads antibiotic resistance to other bacteria

Drug-resistant Neisseria gonorrhoeae A4

Cases in the United States are more prevalent in the West and among men who have sex with men

All patients treated for gonorrhea should routinely be offered condoms, referred for risk-reduction counseling, and retested for gonorrhea three months later

Serious

Multidrug-resistant Acinetobacter A5

Increasingly common in U.S. health care facilities; hard to treat

Noted in U.S. service members wounded in Iraq and Afghanistan

Drug-resistant Campylobacter A6

Most cases are sporadic and not part of outbreaks

Ciprofloxacin (Cipro) resistance to Campylobacter increased from 12% in 1997 to 24% in 2011

Fluconazole- (Diflucan-) resistant Candida (fungus)A7A9

Antifungal resistance in mucosal candidiasis varies by species

Extended spectrum β-lactamase–producing Enterobacteriaceae A10,A11

Infections have become more common in recent years

Once confined largely to hospitals, these bacteria, especially Escherichia coli, are increasingly common in community-acquired infections, particularly urinary tract infections

Vancomycin-resistant Enterococcus A12A14

Enterococci are the fifth most common cause of health care–associated infections

Most likely to be found in urine and in wounds; may pose a risk for spreading in the outpatient setting

Multidrug-resistant Pseudomonas aeruginosa A15,A16

About 8% of all health care–associated infections are caused by P. aeruginosa; about 13% of severe P. aeruginosa health care–associated infections are multidrug resistant

P. aeruginosa may be isolated from outpatients with otitis, skin rash, and urinary tract infections

Drug-resistant non-typhoidal Salmonella A17,A18

Estimated 1.2 million cases occur each year in the United States; most go unreported

About 100,000 cases (8%) are caused by drug-resistant Salmonella

Outbreaks occur each year; some involve multiple states and/or national distribution

Drug-resistant Salmonella serotype Typhi A19

Estimated 5,700 cases annually in the United States

Most (up to 75%) are acquired during international travel

Increasing resistance to antibiotics, especially fluoroquinolones

Drug-resistant Shigella A20

High-risk groups include children in day care centers (younger than five years) and their caregivers, men who have sex with men, international travelers, and persons in custodial institutions

Increasing resistance to ciprofloxacin and azithromycin (Zithromax) is of particular concern

Methicillin-resistant Staphylococcus aureus A21A23

Although overall cases of invasive methicillin-resistant S. aureus are declining, the proportion of community-associated infections has increased

Should be considered in the differential diagnosis of skin and soft tissue infections

Serious

Drug-resistant Streptococcus pneumoniae A24

Increasing threat of antibiotic resistance makes vaccination according to the Advisory

Committee on Immunization Practices recommendations for children and adults more important

Drug-resistant tuberculosis A25,A26

Number of tuberculosis cases is declining in the United States 63% of tuberculosis cases in the United States occur among foreign-born persons

Proportion of primary multidrug-resistant tuberculosis cases occurring among foreign-born persons has been increasing

Concerning

Vancomycin-resistant S. aureus A27

Rare; 13 cases have been identified in the United States since 2002

Severity of the consequences of S. aureus resistance to vancomycin require continued vigilance for this pathogen

Erythromycin-resistant group A Streptococcus A28

Penicillin remains the drug of choice, but the resistance to other drugs needed for patients allergic to penicillin is worrisome

Of samples tested by the Centers for Disease Control and Prevention, 10% were erythromycin resistant and 3.4% were clindamycin resistant

Clindamycin-resistant group B Streptococcus A29

Neonates, pregnant women, and persons older than 65 years with underlying conditions are at highest risk

Penicillin remains the drug of choice, but the resistance to other drugs needed for patients allergic to penicillin is worrisome


note: Additional information on the microorganisms in this table can be found in the Centers for Disease Control and Prevention's antibiotic threats report at http://www.cdc.gov/drugresistance/threat-report-2013/index.html (accessed March 27, 2014).

eTable A

Antibiotic-Resistant Microorganism Threats

MicroorganismNotable information

Urgent

Clostridium difficile A1,A2

Deaths related to C. difficile increased 400% between 2000 and 2007, in part because of a stronger strain

Most infections are connected to receiving medical care

Hand sanitizer does not kill C. difficile, and hand washing may not be sufficient

Carbapenem-resistant Enterobacteriaceae A3

Difficult to treat and, in some cases, untreatable

Kills up to one-half of patients who get bloodstream infections

Easily spreads antibiotic resistance to other bacteria

Drug-resistant Neisseria gonorrhoeae A4

Cases in the United States are more prevalent in the West and among men who have sex with men

All patients treated for gonorrhea should routinely be offered condoms, referred for risk-reduction counseling, and retested for gonorrhea three months later

Serious

Multidrug-resistant Acinetobacter A5

Increasingly common in U.S. health care facilities; hard to treat

Noted in U.S. service members wounded in Iraq and Afghanistan

Drug-resistant Campylobacter A6

Most cases are sporadic and not part of outbreaks

Ciprofloxacin (Cipro) resistance to Campylobacter increased from 12% in 1997 to 24% in 2011

Fluconazole- (Diflucan-) resistant Candida (fungus)A7A9

Antifungal resistance in mucosal candidiasis varies by species

Extended spectrum β-lactamase–producing Enterobacteriaceae A10,A11

Infections have become more common in recent years

Once confined largely to hospitals, these bacteria, especially Escherichia coli, are increasingly common in community-acquired infections, particularly urinary tract infections

Vancomycin-resistant Enterococcus A12A14

Enterococci are the fifth most common cause of health care–associated infections

Most likely to be found in urine and in wounds; may pose a risk for spreading in the outpatient setting

Multidrug-resistant Pseudomonas aeruginosa A15,A16

About 8% of all health care–associated infections are caused by P. aeruginosa; about 13% of severe P. aeruginosa health care–associated infections are multidrug resistant

P. aeruginosa may be isolated from outpatients with otitis, skin rash, and urinary tract infections

Drug-resistant non-typhoidal Salmonella A17,A18

Estimated 1.2 million cases occur each year in the United States; most go unreported

About 100,000 cases (8%) are caused by drug-resistant Salmonella

Outbreaks occur each year; some involve multiple states and/or national distribution

Drug-resistant Salmonella serotype Typhi A19

Estimated 5,700 cases annually in the United States

Most (up to 75%) are acquired during international travel

Increasing resistance to antibiotics, especially fluoroquinolones

Drug-resistant Shigella A20

High-risk groups include children in day care centers (younger than five years) and their caregivers, men who have sex with men, international travelers, and persons in custodial institutions

Increasing resistance to ciprofloxacin and azithromycin (Zithromax) is of particular concern

Methicillin-resistant Staphylococcus aureus A21A23

Although overall cases of invasive methicillin-resistant S. aureus are declining, the proportion of community-associated infections has increased

Should be considered in the differential diagnosis of skin and soft tissue infections

Serious

Drug-resistant Streptococcus pneumoniae A24

Increasing threat of antibiotic resistance makes vaccination according to the Advisory

Committee on Immunization Practices recommendations for children and adults more important

Drug-resistant tuberculosis A25,A26

Number of tuberculosis cases is declining in the United States 63% of tuberculosis cases in the United States occur among foreign-born persons

Proportion of primary multidrug-resistant tuberculosis cases occurring among foreign-born persons has been increasing

Concerning

Vancomycin-resistant S. aureus A27

Rare; 13 cases have been identified in the United States since 2002

Severity of the consequences of S. aureus resistance to vancomycin require continued vigilance for this pathogen

Erythromycin-resistant group A Streptococcus A28

Penicillin remains the drug of choice, but the resistance to other drugs needed for patients allergic to penicillin is worrisome

Of samples tested by the Centers for Disease Control and Prevention, 10% were erythromycin resistant and 3.4% were clindamycin resistant

Clindamycin-resistant group B Streptococcus A29

Neonates, pregnant women, and persons older than 65 years with underlying conditions are at highest risk

Penicillin remains the drug of choice, but the resistance to other drugs needed for patients allergic to penicillin is worrisome


note: Additional information on the microorganisms in this table can be found in the Centers for Disease Control and Prevention's antibiotic threats report at http://www.cdc.gov/drugresistance/threat-report-2013/index.html (accessed March 27, 2014).

Prevention strategies can be effective, but the major goals of the CDC report are to (1) increase awareness of the magnitude and looming risk of untreatable infections, and (2) spur concerted action, both to prevent further spread of resistant pathogens and to preserve the effectiveness of existing antibiotics. Thinking of antibiotics as a precious and diminishing resource has engendered the concept of antimicrobial stewardship, a defined set of practices designed to improve the appropriate use of antimicrobial agents.2 Table 1 lists steps to help implement resistance prevention strategies. Family physicians have an important role in combating antibiotic resistance through carefully prescribing antibiotics, educating patients, and identifying and reporting unexpected treatment failures and suspected resistance.

View/Print Table

Table 1.

Steps to Combat Antimicrobial Resistance in Outpatient Settings

StepsSuggestions for implementation

Improve antibiotic prescribing

Use current clinical guidelines to support rational and appropriate antibiotic prescribing

Share unremarkable findings during the examination (e.g., “no inflammation” or “normal breathing”), while acknowledging the patient is sick

Determine the likelihood of a bacterial infection, especially for upper respiratory tract infections

Provide a specific diagnosis (e.g., “viral bronchitis” vs. “virus”)

Weigh benefits vs. harms of antibiotics

Implement judicious prescribing strategies

Communicate with patients about when and why antibiotics may not be necessary

Explain that unnecessary antibiotic use can be harmful (e.g., adverse effects associated with antibiotic use, potential resistance development)

Explain that treating viral infections with antibiotics does not work

Explicitly plan treatment of symptoms by describing the expected normal course of the illness, and instruct patients to call or come back if symptoms persist or worsen; consider providing care packages with nonantibiotic therapies

Educate patients if an antibiotic is needed

Encourage adherence

Discuss potential adverse effects

Create an office environment that promotes a reduction in antibiotic use

Start the process in the waiting room with videos, posters, and other materials

Hang posters in examination rooms to display a commitment to not prescribe antibiotics for viral infections

Involve office personnel in the reinforcement of the physician's messages

Prevent infections and the spread of resistant bacteria

Ensure that all patients get recommended vaccinations

Provide pneumococcal and influenza vaccines (to help avoid secondary bacterial infections), which are particularly important

Prevent cross-transmission

Counsel patients on how to avoid spreading or becoming infected with resistant pathogens in the community (e.g., methicillin-resistant Staphylococcus aureus)

Follow recommendations for infection control in outpatient settings (http://www.cdc.gov/hai/settings/outpatient/outpatient-care-guidelines.html)

Monitor antibiotic-resistant infections

Report notifiable diseases

When appropriate, report to the health department any diseases caused by bacteria on the Centers for Disease Control and Prevention's list of urgent and serious pathogens (reporting requirements differ by U.S. state and Canadian province); antibiotic-resistant strains of some bacteria (e.g., methicillin-resistant S. aureus) are reportable in some states

Be alert for treatment failures

Consider the possibility of antibiotic resistance in cases of treatment failure; obtain laboratory confirmation and notify local public health authorities in cases of unusual or unexpected treatment failure

Table 1.

Steps to Combat Antimicrobial Resistance in Outpatient Settings

StepsSuggestions for implementation

Improve antibiotic prescribing

Use current clinical guidelines to support rational and appropriate antibiotic prescribing

Share unremarkable findings during the examination (e.g., “no inflammation” or “normal breathing”), while acknowledging the patient is sick

Determine the likelihood of a bacterial infection, especially for upper respiratory tract infections

Provide a specific diagnosis (e.g., “viral bronchitis” vs. “virus”)

Weigh benefits vs. harms of antibiotics

Implement judicious prescribing strategies

Communicate with patients about when and why antibiotics may not be necessary

Explain that unnecessary antibiotic use can be harmful (e.g., adverse effects associated with antibiotic use, potential resistance development)

Explain that treating viral infections with antibiotics does not work

Explicitly plan treatment of symptoms by describing the expected normal course of the illness, and instruct patients to call or come back if symptoms persist or worsen; consider providing care packages with nonantibiotic therapies

Educate patients if an antibiotic is needed

Encourage adherence

Discuss potential adverse effects

Create an office environment that promotes a reduction in antibiotic use

Start the process in the waiting room with videos, posters, and other materials

Hang posters in examination rooms to display a commitment to not prescribe antibiotics for viral infections

Involve office personnel in the reinforcement of the physician's messages

Prevent infections and the spread of resistant bacteria

Ensure that all patients get recommended vaccinations

Provide pneumococcal and influenza vaccines (to help avoid secondary bacterial infections), which are particularly important

Prevent cross-transmission

Counsel patients on how to avoid spreading or becoming infected with resistant pathogens in the community (e.g., methicillin-resistant Staphylococcus aureus)

Follow recommendations for infection control in outpatient settings (http://www.cdc.gov/hai/settings/outpatient/outpatient-care-guidelines.html)

Monitor antibiotic-resistant infections

Report notifiable diseases

When appropriate, report to the health department any diseases caused by bacteria on the Centers for Disease Control and Prevention's list of urgent and serious pathogens (reporting requirements differ by U.S. state and Canadian province); antibiotic-resistant strains of some bacteria (e.g., methicillin-resistant S. aureus) are reportable in some states

Be alert for treatment failures

Consider the possibility of antibiotic resistance in cases of treatment failure; obtain laboratory confirmation and notify local public health authorities in cases of unusual or unexpected treatment failure

There are three main elements of preventing and controlling antibiotic resistance that are most applicable to outpatient practice. First, physicians must improve their antibiotic prescribing. Antibiotic use is the principal driver of antibacterial resistance. A considerable proportion of antibiotics in inpatient and outpatient settings are prescribed in cases when they are not needed or in which the choice of antibiotic, the dose, or the duration of therapy is inappropriate.3,4 Rates of outpatient antibiotic prescribing vary widely by region and state—a much greater variation than is likely explained by differences in patient populations or rates of bacterial diseases.5 It has been documented that inappropriate antibiotic prescribing, especially for viral upper respiratory tract infections, is common in ambulatory care.6 These illnesses are the most common reason for seeking medical attention in the United States and are associated with up to 75% of total antibiotic prescriptions each year.7 The causes of the overuse of antibiotics, which is a problem throughout the world, are complex and well described.8,9

The second main element is preventing infections and the spread of resistance. Preventing an infection eliminates the possibility that the infection could be drug resistant. Immunization and rigorous infection control, including hand washing, clearly reduce the likelihood of infection. On its website, the CDC provides information for patients on how to protect themselves from many types of infections, such as by ensuring safe food handling to prevent Salmonella and Campylobacter infections10 and by avoiding gonorrhea and other sexually transmitted infections.11 Counseling patients on how to avoid spreading or becoming infected with resistant pathogens in the community is an important role for physicians. For example, if an athlete is diagnosed with a methicillin-resistant Staphylococcus aureus infection, he or she should keep the wound properly covered, avoid whirlpools or therapy pools, shower after participation, clean uniforms and equipment after each use, and report infection to coaches and trainers.

The third main element is public health reporting. Gathering, analyzing, and disseminating information on resistant infections and the prevalence of resistant microorganisms is a critical strategy that informs clinical and public health decision making. A key component of detecting emerging and spreading resistance is identifying the cause of unexpected treatment failures. Patients who return with persistent or recurrent symptoms shortly after treatment should be retested by culture, and isolates should be submitted for antimicrobial susceptibility testing. Any case of unexplained treatment failure or a positive culture result after appropriate empiric treatment should be reported promptly to local or state health departments.12 Ultimately, public health surveillance is dependent on reporting by physicians and laboratories.

The nightmare scenario of the spread of pan-resistant bacteria is a real and frightening possibility. Cases of untreatable infections are already occurring. Preventing and controlling resistance requires the engagement of many different sectors of society. However, the physician's role in this effort is singularly important.12 As the threat becomes more urgent, the leadership of the medical community is the most critical factor to ensure a successful response.

The findings and conclusions of this report are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention. Mention of trade names or commercial products does not constitute endorsement or recommendation for use by the U.S. government.

Author disclosure: No relevant financial affiliations.

Address correspondence to Steven L. Solomon, MD, at ssolomon@cdc.gov. Reprints are not available from the authors.

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