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Causes, Burden, and Prevention of Clostridium difficile Infection

Gould, Carolyn V. MD, MSCR*; File, Thomas M. Jr MD, MSc†‡; McDonald, L. Clifford MD*

Infectious Diseases in Clinical Practice: November 2015 - Volume 23 - Issue 6 - p 281–288
doi: 10.1097/IPC.0000000000000331
NFID Clinical Updates
Free
CME

Clostridium difficile infection (CDI) is a potentially deadly cause of diarrhea that is virtually always connected to health care system exposures, both inpatient and outpatient. Once a disease mainly of hospitals, 75% of CDI cases are now diagnosed outside of hospitals. However, the diagnosis location may not reflect where C. difficile spores were acquired or antibiotic exposure occurred. Changing epidemiology and increasing awareness about the role of every segment of the health care system in mediating this disease make it clear that reducing its burden will also require active participation from all US health care professionals.

From the *Division of Healthcare Quality Promotion, Centers for Disease Control and Prevention, Atlanta, GA; †Division of Infectious Disease, Summa Health System, Akron, OH; and ‡Infectious Disease Section, Northeast Ohio Medical University, Rootstown, OH.

Correspondence to: Thomas M. File, Jr, MD, MSc, Chair of Infectious Disease Division, Summa Health System, 75 Arch St, Suite 506, Akron, OH 44304. E-mail: FileT@summahealth.org.

This publication is based on presentations by Dr Gould and Dr McDonald during an NFID webinar held in June 2015 (www.nfid.org//archived-webinars). The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention.

This activity is supported by an unrestricted educational grant from Merck & Co, Inc.

TARGET AUDIENCE

Physicians and other health care professionals interested in the causes and prevention of Clostridium difficile infection.

EDUCATIONAL OBJECTIVES

After the educational activity, participants will be able to describe the epidemiology and burden of Clostridium difficile infection (CDI); identify patient populations at risk for CDI; discuss the role of health care professionals and the health care system in the prevention of CDI; and list core actions all health care professionals should implement to prevent CDI.

PARTICIPATION IN THE LEARNING PROCESS

Credit is based on the approximate time it should take to read this publication and complete the assessment and evaluation. A minimum assessment score of 80% is required. Publication date is November 1, 2015. Requests for credit or contact hours must be postmarked no later than May 1, 2016, after which this material is no longer certified for credit.

CONTINUING MEDICAL EDUCATION

The National Foundation for Infectious Diseases (NFID) is accredited by the Accreditation Council for Continuing Medical Education to provide continuing medical education for physicians. The NFID designates this enduring material for a maximum of 0.75 AMA PRA Category 1 Credits. Physicians should claim only the credit commensurate with the extent of their participation in the activity.

DISCLOSURE

The NFID must ensure balance, independence, objectivity, and scientific rigor in its educational activities. All individuals with control over content are required to disclose any relevant financial interest or other relationships with manufacturer(s) of any product or service discussed in an educational presentation and/or with the commercial supporters of this activity. Disclosure information is reviewed in advance to manage and resolve any conflict of interest, real or apparent, that may affect the balance and scientific integrity of an educational activity. Marla Dalton, CAE (NFID staff, content reviewer), owns stock, stock options, or bonds from Merck & Co, Inc. Thomas M. File, Jr, MD (author), served as an advisor or consultant for Astellas, Cubist, Durata, GlaxoSmithKline, Nabriva, Pfizer Inc, and Tetraphase and received grant or research support from Cempra and Pfizer Inc. William Schaffner, MD (NFID Medical Director, content reviewer), served as an advisor or consultant for Merck & Co, Inc, Pfizer Inc, and Novavax. All other authors, planners, and content reviewers have no funding or conflicts of interest to disclose.

CME INSTRUCTIONS

To receive credit after reading the publication, complete and return the self-assessment examination, evaluation, and your contact information via e-mail to cme@nfid.org, fax to 301-907-0878, or by mail to NFID CME Office, 7201 Wisconsin Ave, Suite 750, Bethesda, MD 20814. No fee is required. Please allow two weeks for processing. Inquiries may be directed to 301-656-0003 or cme@nfid.org.

Clostridium difficile infection (CDI) is a potentially serious life-threatening cause of diarrhea.1 Although CDI is often associated with hospital stays, community-onset infections are now more common than hospital-onset infections.2 Although nearly half of community-onset infections are termed community associated, data indicate that most of these patients (82%) had an outpatient health care visit within 12 weeks of testing positive for C. difficile.2,32,3

These findings indicate that health care professionals across all health care settings play a critical role in diagnosing and preventing the spread of C. difficile in their daily interaction with patients. Limiting the impact of CDI requires 2 specific actions by health care professionals: enacting protocols that reduce patient exposure to C. difficile spores and practicing effective antibiotic stewardship,1 that is, using appropriate antibiotics only when necessary and indicated.

Antibiotics cause vulnerability to CDI by disrupting the normal colonic microbiota and providing an environment where C. difficile spores can germinate in the small intestine and then pass through the large intestine where they multiply and produce diarrhea-causing toxins. Clostridium difficile spores, which are transmitted via the fecal-oral route, can persist on any surface, device, or material that becomes contaminated.1 These reservoirs of infection set the stage for transfer of the spores to patients, literally, at the hands of health care professionals.

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HOST DEFENSE AND RISK FACTORS FOR CDI

There are several important host defenses for CDI. First is intact (undisturbed) lower intestinal microbiota. There has been some suggestion that the appendix may be important to maintaining microbiota balance.4 Infants seem to have a natural defense against CDI. They often become colonized with C. difficile bacteria but do not develop infection; animal data suggest that a relative lack of toxin receptors during microbiota establishment in the first year of life may be protective.5 Many adults have antibodies to C. difficile toxins that are boosted after colonization or natural infection.6 Demonstration that administering monoclonal antibodies protects against CDI recurrence in humans is strong evidence for an important role of humoral immunity in host defense.7 The association of proton pump inhibitors (PPIs) with CDI could suggest a host defense role for stomach acid8; however, C. difficile spores are relatively acid resistant,9 and thus, this association may instead reflect the impact of PPIs on the intestinal microbiota.10,1110,11

Prior antibiotic treatment is the single most important risk factor for CDI.1 Other factors include older age, immunosuppressant therapy, inflammatory bowel disease, and enteral tube feeding. Tube feeds may increase the risk of CDI because these patients require more “hands-on” time from health care professionals, increasing the chance of spore transmission and ingestion. Alternatively or additionally, there may be important alterations of the intestinal microbiota affected by tube feeding. Proximity to infected patients increases risk of infection, which is why hospitals and nursing homes have historically been viewed as the most important vectors in CDI epidemiology. This view is expanding as we learn more about the role of other settings in C. difficile transmission.

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EPIDEMIOLOGIC CLASSIFICATION OF CDI CASES

Clostridium difficile infection is no longer associated only (or even predominantly) with inpatient hospital stays. Recognition of the role of nonhospital settings in C. difficile transmission has led to changes in epidemiologic classification categories used for disease surveillance. Per Centers for Disease Control and Prevention (CDC) surveillance definitions, classification depends on the patient's health care exposure in the 12 weeks before symptom onset and/or diagnosis and is divided broadly into community-associated or health care–associated disease. Cases are further classified by place of onset (Fig. 1).2,12,132,12,132,12,13

FIGURE 1

FIGURE 1

Surveillance data from the CDC National Healthcare Safety Network looked at the percentage of laboratory-identified CDIs by hospitalization status (present on admission or hospital onset).1 Approximately one half (52%) of the cases diagnosed in hospitals in 2010 were present on admission (ie, diagnosed within the first 3 days), although still largely health care related. Although many other patients may have recent inpatient exposures, only about 16% of these cases were among patients recently discharged from the same hospital. These data illustrate the interdependence of hospitals and the community in minimizing CDI while identifying the role of previous hospitalization as an important risk factor for CDI.

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CDI BURDEN IN THE UNITED STATES

Based on active population- and laboratory-based surveillance across 10 geographic areas, there were an estimated 453,000 US CDI cases in 2011.2 Approximately two thirds of all cases (n = 293,300) were categorized as (inpatient) health care associated but only 24% (n = 107,600) as hospital onset. A similar percentage had nursing home onset (23%), and a somewhat smaller percentage had postdischarge onset (18%). The remaining approximately one third of cases (n = 159,700) were community associated and therefore without overnight inpatient health care exposures in the previous 12 weeks.2 By evaluating interviews in community-associated case patients from the same cohort January 1, 2009, through May 31, 2011, Chitnis et al3 noted that 82% reported outpatient health care exposures, such as visits to a doctor or dentist.

Lessa et al2 also reported 29,000 deaths within 30 days of CDI diagnosis and, based on other estimates from the literature, at least one half were likely attributable to C. difficile. The morbidity and financial impact of CDI are also considerable. There are a reported 83,000 annual recurrences within 8 weeks of the initial case. In their systematic review, Kwon et al14 looked at colectomy rates as a measure of the severity of CDI. The rate of colectomies began to increase dramatically in 2000 and has been reported as high as 6.2% in epidemic periods. They also reported that CDI extends inpatient hospital stays by 2.3 to 12 days and increases the financial burden by $2454 to $27,160 per case.

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EMERGING TOXIN GENE-VARIANT STRAIN OF C. DIFFICILE

Although US CDI rates have plateaued during the past 5 years, incidence increased dramatically from 2000 to 2010 such that CDI has become the most common cause of health care–associated infections in US hospitals.1,15–171,15–171,15–171,15–17 Much of this increase was likely caused by emergence of an epidemic toxin gene-variant strain, NAP1/ribotype 027.18–2118–2118–2118–21 Although previously uncommon, this strain is now epidemic in the United States.

The NAP1/027 strain is more resistant to fluoroquinolone antibiotics and more virulent than other strains.18 In a case-control study, the NAP1 strain was associated with greater odds of severe disease than other strains (adjusted odds ratio [AOR], 1.74; 95% confidence interval [95% CI], 1.36–2.22), severe outcome (AOR, 1.66; 95% CI, 1.09–2.54), and death within 14 days (AOR, 2.12; 95% CI, 1.22–3.68).22 NAP1/027, NAP4/014/020, and NAP11/106 comprise the 3 most common causes of infection in both community- and health care–associated CDI in the United States.2 NAP4/014/020 is the second most prevalent strain in the United States and is endemic in Europe.2,212,21 NAP11/106, which has been associated with outbreaks in Europe, is resistant to erythromycin and fluoroquinolones.

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KEY COMPONENTS OF CDI PREVENTION

In its 2012 Vital Signs report, the CDC highlighted CDI and reviewed 6 key components to prevention (Table 1).1 The report emphasized the importance of antibiotic stewardship along with infection control applied across different health care settings to achieve major reductions in CDI. Antibiotic stewardship is now on the forefront of CDI prevention efforts because of growing recognition that it is essential for a meaningful reduction in disease rates.23

TABLE 1

TABLE 1

The Vital Signs report emphasized measures to reduce transmission of C. difficile spores (ie, reducing patient exposure).1,241,24 This includes early and reliable diagnosis of CDI patients followed by immediate isolation and implementation of contact precautions, adequate cleaning of the patient care environment, augmented by use of an Environmental Protection Agency (EPA)–registered C. difficile sporicidal disinfectant (Table 2), and communication between facilities of prior, current, or suspected CDI on patient transfer. Interfacility communication is key to addressing regional prevention of CDI because patient exposures in 1 facility can impact infections in other settings. Modeling has demonstrated that a coordinated approach among public health authorities and interconnected health care facilities, using data to implement shared infection control actions, is more effective than traditional independent approaches.25

TABLE 2

TABLE 2

There is also growing concern about the possible association between use of gastric acid–suppression drugs, particularly PPIs, and development of CDI, although data are limited by heterogeneity of studies, low quality of evidence, and conflicting results among several studies.26,2726,27 The US Food and Drug Administration issued a 2012 warning about the possible association,8 but although some studies have shown that PPIs are independently associated with the risk of CDI,11,28,2911,28,2911,28,29 others have not.30,3130,31 The association may be confounded by the fact that PPIs themselves can cause diarrhea and predispose patients to increased testing, leading to more detection of asymptomatic carriage. In addition, potential bias in studies showing an association as a result of sicker patients being at greater risk for CDI and being more likely to receive PPIs has been suggested.31

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Hospital and Community-Wide Antibiotic Stewardship Efforts Needed

Antibiotic exposure has lasting impact on the microbiome and is the single most important risk factor for CDI. Chang et al32 observed that, of 84 patients diagnosed as having CDI after recent hospital discharge, 83 (99%) had received antibiotics within the previous 90 days in the inpatient setting, outpatient setting, or both. The odds of CDI increase during antibiotic therapy and in the 3 months after are highest while on antibiotic therapy and in the first month after completion (OR, 6.7–10.4).33 The lasting impact of antibiotics likely accounts for the high level of community-onset (postdischarge) CDI.33

Antibiotic stewardship is highlighted in a 2014 CDC MMWR Vital Signs that lays out 7 core elements critical to the success of hospital antibiotic stewardship programs.23 The Society for Healthcare Epidemiology of America and Infectious Diseases Society of America 2014 Practice Recommendation on preventing CDI in acute care hospitals34 emphasizes appropriate use of antibiotics as a basic practice for prevention of CDI for all hospitals, including avoiding patient exposure to unnecessary antibiotics and selecting antibiotics associated with a lower risk of CDI when possible. Antibiotics predisposing to CDI include fluoroquinolones, third- and fourth-generation cephalosporins, ampicillin, and clindamycin.34

Fluoroquinolones and cephalosporins in particular are commonly misused for presumed respiratory and urinary tract infections (eg, misdiagnosis of asymptomatic bacteriuria as a urinary tract infection).35 Both decreasing overuse and promoting appropriate use of these antibiotics are critical to reducing CDI incidence. Because use of these antibiotics extends into community practices, stewardship efforts should also extend into the community.

Chitnis et al3 report that 64% of patients with community-associated CDI were taking antibiotics within 12 weeks of having a positive stool test. The most common reasons for taking antibiotics were ear, sinus, or upper respiratory tract infection (34.7%); dental cleaning or oral surgery (15.1%); urinary tract infection (9.3%); skin infection (7.5%); and bronchitis or pneumonia (7.5%). Roughly the same proportion of patients received cephalosporins (23.6%), beta-lactam or beta-lactamase inhibitors (23%), penicillins (22.7%), and fluoroquinolones (22%), with a smaller percentage receiving clindamycin (18.9%).3

Also of note is that nearly 28% of all patients with CDI in this study reported recent PPI use and just more than 31% of the CDI patients with no prior antibiotic exposure received PPIs. The large proportion of patients with PPI exposure adds to the growing concern of a potential causal relationship between PPIs and CDI.3

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Antibiotic Stewardship: Role for Health Care Professional and Other Stakeholders

The CDC Vital Signs program recommends actions by a wide range of stakeholders to improve antibiotic stewardship and reduce CDI incidence (Table 3).36 The authors urge readers to examine Table 3 carefully to identify actions they can take.

TABLE 3

TABLE 3

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Small- and Large-Scale Antibiotic Stewardship Successes

A successful antibiotic stewardship program at a UK teaching hospital resulted in significant reductions in CDI incidence in elderly inpatients aged 80 years or older.37 The hospital's policy targeted replacement of broad-spectrum antibiotics, specifically cephalosporins and amoxicillin/clavulanate, with narrow-spectrum antibiotics such as benzyl penicillin, amoxicillin, and trimethoprim. There was a rapid and sustained move from broad- to narrow-spectrum antibiotics (all other antibiotic use remained unchanged) and a significant fall in CDI associated with the intervention but not in the control outcome, methicillin-resistant Staphylococcus aureus (CDI incidence rate ratios of 0.35 [0.17, 0.73, P = 0.009] compared with methicillin-resistant Staphylococcus aureus IRR of 0.79 [0.49, 1.29, P = 0.32]).37

A national antibiotic stewardship program in the United Kingdom provides even more compelling evidence of its potential impact on reducing the burden of CDI. Faced with a CDI epidemic, the United Kingdom introduced a national antibiotic stewardship program to limit the use of second- and third-generation cephalosporins and fluoroquinolones. These antibiotic reductions were met with coincident decreases in hospital CDI rates.38 The target for CDI reduction was actually far exceeded, with a 61% reduction in CDI reports from 36,095 in 2008 to 2009 to 21,698 from 2010 to 2011.21

The C. difficile Ribotyping Network, established in the United Kingdom in 2007, also saw a gradual reduction in the prevalence of ribotype NAP1/027, which is resistant to fluoroquinolones, from 55% of all cases in 2007 to 36% in 2008 and 21% in 2009.21 In addition, the cases that occurred across time were decreasingly associated with both cephalosporins and fluoroquinolones.21

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Measures to Reduce Acquisition of C. difficile Spores

Reducing patient acquisition of C. difficile spores requires a multifaceted approach that includes prompt identification and isolation of infected patients, reducing spore contamination in patient care environments, adhering to Contact Precautions, and effective communication between health care facilities.

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Hand Hygiene, Gloves, and Contact Precautions

The core hand hygiene recommendations for care of patients with CDI follow CDC and World Health Organization guidelines and call for preferential use of soap and water in outbreak or hyperendemic settings.39 Special approaches to preventing CDI, which have already been adopted by many hospitals, call for hand washing with soap and water before exiting the room of any CDI patient.34 In all cases, measuring compliance is critical to success.

Glove use is most essential to reducing spore transmission.40Clostridium difficile spores are very difficult to remove from the hands even with proper washing. Therefore, strict adherence to glove use as part of Contact Precautions is essential to any effort to reduce spore transmission.

Patient hand washing should also be emphasized as part of CDI prevention efforts because patients may self-inoculate with the C. difficile spores if their hands come into contact with surfaces contaminated with the spores. Because hand washing is more effective than alcohol hand rub in removing spores,41 frequent patient hand washing should be encouraged, especially after using the bathroom and before eating.

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Extending Contact Precautions: Asymptomatic C. difficile Carriage

If CDI rates remain high despite adherence to core recommendations, the duration of Contact Precautions may need to extend beyond resolution of diarrhea symptoms. Patients frequently continue to shed C. difficile spores after resolution of diarrhea and beyond the end of treatment.42 The lowest point of shedding coincides with the end of treatment but then increases in the first 4 weeks after treatment before declining again.

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Environmental Cleaning and Use of Sporicidal Agents

There are limited data suggesting that disinfecting with a 1:10 bleach dilution prepared fresh daily reduces C. difficile transmission, particularly in units with high endemic rates such as bone marrow transplant units.43,4443,44 When considering a switch to a sporicidal agent, facilities may want to begin by focusing on units where C. difficile rates are high because some sporicidal agents may have adverse effects such as corrosion. A list of EPA-registered agents with sporicidal claims can be found in Table 2 and online at the EPA Web site where it is updated periodically.24

Another key to effective spore removal is measuring adequacy of cleaning procedures. Carling et al45 tested 1404 surface objects in 157 rooms in 3 hospitals and found that 47% of the objects had been cleaned. This cleaning audit, coupled with an educational intervention among cleaning staff, led to a sustained improvement in cleaning objects and a greater than 2-fold improvement in cleaning high-touch surfaces that had previously been cleaned less than 85% of the time.

As part of its toolkit on reducing hospital-associated infections, CDC provides a checklist for identifying high-touch surfaces (available at: cdc.gov/hai/pdfs/toolkits/environ-cleaning-eval-toolkit12-2-2010.pdf). The toolkit also reviews methods for assessing the adequacy of cleaning and pros and cons of different systems.

Rutala et al46 looked at spore count reduction on surfaces from several cleaning methods. Wiping alone with a nonsporicidal agent resulted in a 2.90 log reduction in spore count. The addition of a sporidical agent led to a greater reduction (3.70 log reduction). Spraying with a sporicidal disinfectant led to a 3.40 log reduction but is associated with prolonged drying time and lack of debris removal. The investigators concluded that wiping with a sporicidal agent is the best approach.

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Interfacility Transfers

The 2 key factors in CDI burden, antibiotic exposure and spore acquisition, can occur in different settings, making it difficult to attribute cases to a specific facility or segment of the health care system. Because patient transfers among a variety of settings (eg, acute care hospitals, long-term care, nursing homes, home health, etc) are common, facilities must focus on optimizing communication during these transfers to prevent C. difficile transmission to other facilities.

It is essential that discharging and receiving facilities communicate key information about patients during transfer. This includes whether the patient has or had C. difficile or any other drug-resistant organism. The CDC provides a sample Interfacility Infection Control Transfer Form as part of its online toolkit for reduction of health care–associated infections (http://www.cdc.gov/hai/pdfs/toolkits/InfectionControlTransferFormExample1.pdf).

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CONCLUSIONS

Virtually all CDI cases are health care related. The primary causes of CDI—antibiotic exposure and spore acquisition—occur in a variety of settings. Clostridium difficile infection onset and diagnosis can likewise happen in a variety of inpatient and outpatient settings. The current epidemiology of CDI necessitates active participation from all segments of the health care community in a comprehensive approach to reduce the burden of CDI through effective antibiotic stewardship and active measures to reduce spore transmission.

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REFERENCES

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42. Sethi AK, Al-Nassir WN, Nerandzic MM, et al. Persistence of skin contamination and environmental shedding of Clostridium difficile during and after treatment of C. difficile infection. Infect Control Hosp Epidemiol. 2010; 31(1): 21–27.
43. Mayfield JL, Leet T, Miller J, et al. Environmental control to reduce transmission of Clostridium difficile. Clin Infect Dis. 2000; 31(4): 995–1000.
44. Wilcox MH, Fawley WN, Wigglesworth N, et al. Comparison of the effect of detergent versus hypochlorite cleaning on environmental contamination and incidence of Clostridium difficile infection. J Hosp Infect. 2003; 54(2): 109–114.
45. Carling PC, Briggs JL, Perkins J, et al. Improved cleaning of patient rooms using a new target method. Clin Infect Dis. 2006; 42(3): 385–388.
46. Rutala WA, Gergen MF, Weber DJ. Efficacy of different cleaning and disinfection methods against Clostridium difficile spores: importance of physical removal versus sporicidal inactivation. Infect Control Hosp Epidemiol. 2012; 33(12): 1255–1258.
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Self Assessment Examination

A minimum assessment score of 80% is required.

  1. Development of CDI usually requires:
    1. diagnosis of irritable bowel syndrome.
    2. disruption of the fecal microbiota (typically via exposure to antibiotics).
    3. acquisition of the organism via the fecal-oral route.
    4. A and B
    5. B and C
  2. What precautions should all health care personnel use to help prevent the spread of CDI?
    1. Wear gloves and gowns when caring for CDI patients.
    2. Pay careful attention to environmental cleaning of high-touch surfaces.
    3. Notify receiving facilities or units of CDI status (including recently resolved infections) on transfer.
    4. A and C
    5. All of the above
  3. Which of the following is true?
    1. Once a patient becomes asymptomatic, shedding no longer poses a transmission risk.
    2. The lowest point of shedding usually coincides with the end of treatment.
    3. Shedding is higher in the first 4 weeks after treatment than it is at treatment completion.
    4. A and B
    5. B and C
  4. Which of the following most accurately approximates the annual US burden of CDI?
    1. 250,000 cases and 19,000 deaths within 30 days
    2. 350,000 cases and 19,000 deaths within 30 days
    3. 350,000 cases and 29,000 deaths within 30 days
    4. 450,000 cases and 19,000 deaths within 30 days
    5. 450,000 cases and 29,000 attributable deaths
  5. Which of the following antibiotics pose the highest risk for CDI?
    1. Erythromycin, clarithromycin, and azithromycin
    2. Cephalosporins, fluoroquinolones, and clindamycin
    3. Trimethoprim/sulfamethoxazole
    4. Tetracycline
    5. Amoxicillin, penicillin
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Keywords:

Clostridium difficile; CDI; antibiotic stewardship; health care–associated infection

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