Professional Documents
Culture Documents
CHAPTER 5
Outbreaks Reported in
Ambulatory Care Settings
Kathleen Meehan Arias
Infection control staff must develop programs that address the special
needs of the ambulatory care setting, because this is where most medical
care will be given in the 21st century.1(p42)
INTRODUCTION
Despite the general belief that the risk of transmission of infectious dis-
eases and other illnesses in the ambulatory healthcare setting is low, numer-
ous outbreaks caused by a variety of bacterial, fungal, viral, and chemical
agents have been reported in outpatient settings.1,2 Many therapeutic, diag-
nostic, and surgical procedures formerly performed in the inpatient hospital
setting are now routinely done in freestanding or hospital-sponsored outpa-
tient facilities such as same-day or ambulatory surgery centers. As more
healthcare services move from inpatient to outpatient facilities, the potential
for healthcare-associated infections (HAIs) and other adverse events in the
ambulatory care setting increases.
This chapter reviews outbreaks that have been reported in ambulatory care
settings. One can use the findings of these outbreak investigations to identify
risk factors that may be contributing to a similar outbreak and to identify pre-
vention and control measures. For the purposes of this chapter, the ambula-
tory care setting is defined as one in which a patient does not remain
overnight for healthcare services. Examples include physicians’ offices, ambu-
latory surgery centers, dental offices, hemodialysis and peritoneal dialysis cen-
ters, chemotherapy facilities, outpatient clinics, and procedure suites (e.g.,
gastrointestinal endoscopy and bronchoscopy).
Little is known about the incidence of HAIs in the ambulatory care setting
because infection surveillance is not performed as often in outpatient settings
as it is in the acute care setting, and the populations at risk (i.e., the denomi-
nator numbers needed to calculate rates) are frequently difficult to define.
Unlike the routine surveillance methods used to detect HAIs in hospitalized
patients, no standardized surveillance methodology has yet been developed for
the ambulatory care setting. Therefore, it is likely that many HAIs and other
adverse events in these settings go undetected unless they affect large num-
bers of patients or cause significant morbidity. The risk of disease transmis-
sion in the outpatient setting varies according to the services provided and the
populations served. For instance, the risk of transmission of infectious agents
in an internal medicine practice that does not perform invasive procedures is
163
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lower than the risk of infection in a hemodialysis center, where the transmis-
sion of blood-borne pathogens has been well defined. Table 5–1 contains exam-
ples of outbreaks that have been reported in a variety of ambulatory care
settings.3–23
Year
Reported/
Outbreak Setting Associated With Reference
Burkholderia cepacia Hematology Probable contamination of multi- 2007 3
bloodstream infections oncology clinic dose medication vials due to lack
of aseptic technique, including
use of common needle and
syringe to access multiple
multidose vials
Pseudomonas Urology clinic Transrectal ultrasound (TRUS)- 2005 4
aeruginosa infections guided prostate biopsy with TRUS
following prostate equipment that had not been
biopsies adequately cleaned or properly
sterilized; biopsy needle guide was
soaked in high-level disinfectant
and should have been sterilized;
tap water rinse was used after
disinfection
Skin reactions Outpatient Unsafe injection practices by 2005 5
following mesotherapy treatment in unlicensed practitioner; non-FDA-
injections private home approved products
M. tuberculosis infection Renal dialysis Healthcare worker (HCW) with 20046
in personnel and center tuberculosis (TB); HCW had
patients in renal previous positive tuberculin skin
dialysis center test but never received treatment
for TB infection.
Patient fatalities from Hemodialysis Phytoplankton from the dialysis 20017
Cyanobacteria toxins clinic clinic’s water source
Pseudo-outbreak of Outpatient Reuse of single-use plastic 2000 8
Aureobasidium sp. bronchoscopy stopcocks between patients
lower respiratory tract suite undergoing bronchoalveolar lavage
infections
Sterile peritonitis Dialysis center Peritoneal dialysis solution from a 1998 9
among patients at a university single manufacturer; solution
undergoing continuous hospital potentially contained an endotoxin;
cycling peritoneal implicated lots were recalled
dialysis
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Introduction 165
Year
Reported/
Outbreak Setting Associated With Reference
Epidemic Eye care clinic Lack of handwashing by person- 1998 10
keratoconjunctivitis nel; inadequate decontamination
(EKC) of diagnostic lenses
Acremonium kiliense Ambulatory Air contaminated by A. kiliense in 1996 11
endophthalmitis surgery center ventilation system humidifier water
Pseudomonas putida Pulmonary clinic Bronchoscope contaminated by 1996 12
pseudo-pneumonia improper maintenance of
automated bronchoscope washer
Pseudomonas Urodynamic Improper reuse and disinfection 1996 13
aeruginosa urinary suite of single-use urodynamic testing
tract infections equipment
Pseudomonas Oncology clinic Contaminated 500 ml bag of 5% 1993 14
(currently Burkholderia) dextrose solution used to prepare
cepacia bacteremia heparin flush solution over a
2-week period
Patient-to-patient Private surgeon’s Unknown 1993 15
transmission of HIV office
Adenovirus type 8 EKC Outpatient eye Inadequate handwashing by 1993 16
clinic personnel; inadequate disinfection
of instruments
Legionella pneumophila Outpatient clinic Contaminated air conditioning unit 1990 17
pneumonia
MDR-TB in healthcare Outpatient HIV Human immunodeficiency virus 1989 18
workers and HIV clinic and (HIV)-infected patients with
infected patients hospital MDR-TB
Septic arthritis caused Physician’s Injection site and multidose vials 1987 19
by Serratia marcescens office cleansed with cotton balls soaked
in contaminated benzalkonium
chloride antiseptic
Hepatitis B Weight reduction Jet injector gun—nozzle tip 1986 20
clinic contaminated with blood was
difficult to disinfect
Hepatitis B Dentist’s office Dentist was asymptomatic carrier 1986 21
of hepatitis B
Group A beta Pediatrician’s Contamination of multidose vial 1985 22
hemolytic streptococcus office of diphtheria-tetanus-pertussis
abscesses vaccine
Measles Pediatrician’s 12-year-old boy with cough and 1985 23
office rash was in office for 1 hour
Contaminated Devices
Contaminated medical devices that have been associated with outbreaks in
outpatient care settings include jet gun injectors,20,34 bronchoscopes,12 and uro-
dynamic testing equipment.13 There are several reports of outbreaks associated
with the use of jet gun injectors. Thirty-one cases of hepatitis B occurred over a
23-month period in a weight reduction clinic where attendees received par-
enteral human chorionic gonadotrophin given by jet injection.20 One factor that
contributed to this outbreak was the design of the jet gun nozzle tip, which
made it difficult to clean and disinfect once it became contaminated with blood.
Another outbreak associated with a jet gun injector occurred in a podiatry
practice where eight patients developed Mycobacterium chelonae foot infections
after injection with lidocaine.34 The source of the organism was a distilled
water/quaternary ammonium disinfectant solution in which the jet injector
was soaked between procedures. These two outbreaks emphasize the need to
clean jet gun injectors carefully and to disinfect them appropriately with a
high-level disinfectant and according to the manufacturer’s instructions.
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Exhibit 5–1 Infection Control and Safe Injection Practices to Prevent Patient-to-Patient
Transmission of Blood-Borne Pathogens
Injection safety
• Use a sterile, single-use, disposable needle and syringe for each injection and discard
intact in an appropriate sharps container after use.
• Use single-dose medication vials, prefilled syringes, and ampules when possible. Do
not administer medications from single-dose vials to multiple patients or combine
leftover contents for later use.
• If multiple-dose vials are used, restrict them to a centralized medication area or for
single patient use. Never reenter a vial with a needle or syringe used on one patient if
that vial will be used to withdraw medication for another patient. Store vials in
accordance with manufacturer’s recommendations and discard if sterility is
compromised.
• Do not use bags or bottles of intravenous solution as a common source of supply for
multiple patients.
• Use aseptic technique to avoid contamination of sterile injection equipment and
medications.
Patient-care equipment
• Handle patient-care equipment that might be contaminated with blood in a way that
prevents skin and mucous membrane exposures, contamination of clothing, and
transfer of microorganisms to other patients and surfaces.
• Evaluate equipment and devices for potential cross-contamination of blood. Establish
procedures for safe handling during and after use, including cleaning and disinfection
or sterilization as indicated.
Work environment
• Dispose of used syringes and needles at the point of use in a sharps container that is
puncture-resistant and leak-proof and that can be sealed before completely full.
• Maintain physical separation between clean and contaminated equipment and
supplies.
• Prepare medications in areas physically separated from those with potential blood
contamination.
• Use barriers to protect surfaces from blood contamination during blood sampling.
• Clean and disinfect blood-contaminated equipment and surfaces in accordance with
recommended guidelines.
Hand hygiene and gloves
• Perform hand hygiene (i.e., hand washing with soap and water or use of an alcohol-
based hand rub) before preparing and administering an injection, before and after
donning gloves for performing blood sampling, after inadvertent blood contamination,
and between patients.
• Wear gloves for procedures that might involve contact with blood and change gloves
between patients.
Source: Modified from Centers for Disease Control and Prevention. Transmission of hepatitis B and C
viruses in outpatient settings—New York, Oklahoma, and Nebraska, 2000–2002. MMWR. 2003;
52(38):904. http://www.cdc.gov/mmwr/preview/mmwrhtml/mm5238a1.htm. Accessed May 11, 2008.
57793_CH05_ARIAS.qxd 1/19/09 6:42 PM Page 172
2005, 66 confirmed cases of measles were reported to the Centers for Disease
Control and Prevention (CDC) and 34 of these were from a single outbreak in
Indiana associated with an unvaccinated 17 year old returning home to the
United States from Romania.65,66 Measles outbreaks can cause significant
morbidity and disruption in the healthcare, community, and public health set-
tings. In the Indiana outbreak, three persons were hospitalized, including a
healthcare worker who required treatment in the intensive care unit.
Strategies for preventing transmission of measles in physicians’ offices and
other ambulatory healthcare settings include:
• Prompt recognition of patients with measles (measles should be consid-
ered in any patient, whether an adult or a child, who has fever and a
rash)
• Separation of patients with known or suspected measles from other
patients (this may be difficult due to ease of airborne spread and lack of
adequate ventilation in many ambulatory care settings)
• Postexposure prophylaxis of potentially exposed contacts, such as
patients, persons accompanying patients, and medical personnel
• Postexposure immunization of patients and personnel according to
the recommendations of the Advisory Committee on Immunization
Practices.67,68
Transmission of measles can be prevented if recommendations for immu-
nization of children, adolescents, and adults are followed. Guidelines for pre-
venting transmission of measles have been published by the CDC69,70 and the
American Academy of Pediatrics.71 Measles outbreaks and prevention and con-
trol measures are discussed in detail in Chapter 3. Because the incidence of
measles in the United States is low,68 one case of measles should be considered
an outbreak and should promptly be reported by telephone to the local health
department so that measures to prevent further spread can be implemented
as soon as possible. Appendix C contains a protocol for controlling an outbreak
of measles in a healthcare facility, including a physician’s office (Appendix C is
available for download at this text’s Web site: http://www.jbpub.com/catalog/
9780763757793/).
Tuberculosis. Transmission of tuberculosis (TB) in the ambulatory care set-
ting is well recognized.18,35,72–74 Multiple outbreaks of TB infection and disease,
including multidrug-resistant tuberculosis, occurred in the United States in
the late 1980s and early 1990s. Several of these outbreaks involved patients
and personnel in outpatient settings.18,35,74 There are also reports of TB out-
breaks among emergency room personnel 73,75 and among patients and staff at
an outpatient methadone clinic72 following exposure to patients with pul-
monary TB.
The epidemiology and mode of transmission of Mycobacterium tuberculosis
and control measures used to prevent the spread of TB are discussed in Chap-
ter 7. Recommendations for preventing the spread of TB in the healthcare set-
ting have been published by the CDC and include the following76:
• Prompt recognition of persons (patients and personnel) that have signs
and symptoms suggestive of pulmonary TB
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DENTAL SETTINGS
patients were found to be identical using DNA sequencing. None of the dental
practice staff had HBV infection and no lapse in infection control technique
was found. Although the mode of transmission could not be determined, cross-
contamination via an environmental surface soiled with the blood of the HBV-
infected patient was suspected.
One of the most highly publicized events involving transmission of an infec-
tion from a healthcare provider to a patient was the 1990 report of HIV trans-
mitted to a patient by a dentist with acquired immune deficiency syndrome.90
Further investigation linked the Florida dentist to HIV infection in six of his
patients86,91,92; however, the mode of transmission of HIV was not able to be
determined.
Source: Centers for Disease Control and Prevention. Guidelines for Infection Control in Dental Health-
Care Settings, 2003. MMWR. 2003;52(RR-17):37. http://www.cdc.gov/oralhealth/infectioncontrol/
guidelines/index.htm. Accessed May 11, 2008.
57793_CH05_ARIAS.qxd 1/19/09 6:42 PM Page 176
Year Reported/
Outbreak Comments/Associated With Reference
Tuberculosis Exposure to hemodialysis technician with 20046
pulmonary tuberculosis
Sterile (culture- Use of dialysate containing icodextrin; 2003126
negative) peritonitis such reactions could be due to a substance
following peritoneal contaminating the icodextrin or to
dialysis hypersensitivity to icodextrin
Vascular access site Malfunctioning catheters from a single 2002119
infections manufacturer; manufacturer later recalled
catheter
Acute illness and Cases occurred on a single day in the same 2002124
hospitalization shortly outpatient dialysis center; most likely due to
following hemodialysis parenteral exposure to volatile sulfur-containing
compounds from the water near the reverse
osmosis (RO) unit; improperly maintained RO
membrane allowed sulfur-reducing bacteria to
grow and produce toxic levels of disulfides; re-
sulted in 16 patients hospitalized and 2 deaths
Pyrogenic reactions Extrinsic (in-use) contamination of medication 2001115
and Serratia (epoetin alfa) due to repeated use of single-use
liquefaciens vials to obtain multiple doses and pooling of
bloodstream infections residual epoetin alpha from single-use vials
for later use
Acute liver failure Parenteral exposure to cyanotoxins from 1998127
causing morbidity phytoplankton in water source used by 20017
and mortality dialysis center
57793_CH05_ARIAS.qxd 1/19/09 6:42 PM Page 177
Year Reported/
Outbreak Comments/Associated With Reference
Hemolysis following Blood tubing sets produced by a single 1998123
hemodialysis manufacturer had a narrow aperture that
caused mechanical lysis of red blood cells
Bacterial bloodstream Contamination of the waste drain ports in the 1998113
infections—Canada, same model of hemodialysis machine 1999114
United States, Israel
Bloodstream Contamination of newly installed attachment 1998112
infections caused by used to drain spent priming saline in
multiple pathogens hemodialysis system
Hepatitis B virus Lack of separation of patients with chronic HBV 199699
(HBV) infection, Texas infection from HBV-negative patients; lack of
review of monthly HBsAg* results; lack of use of
standard precautions; poor compliance with
recommendations for HBV prevention
Human immuno- Reusable needle used on patient with HIV 1995108
deficiency virus (HIV) improperly processed with benzalkonium
infection chloride by soaking in a common pan with
needles used on other patients
Anaphylactoid Reuse of hollow-fiber hemodialyzers repro- 1992120
reactions cessed with automated reprocessing system
Bacteremia with Venous blood tubing cross-contaminated with 1992109
gram-negative ultrafiltrate waste
organisms and
Enterococcus
casseliflavus
Hepatitis C virus No common source or person-to-person mode 1992103
infection of transmission documented; probable cause
was lack of adequate infection prevention and
control precautions
Hypotension Ultrafilters preserved in sodium azide were not 1990122
rinsed prior to installation in dialysis center
water treatment system; dialysis water became
contaminated with sodium diazide
Hepatitis B virus Failure to isolate patient with chronic HBV; 1989100
infection shared equipment and staff
Hepatitis B virus Associated with shared multidose vial used by 1983101
infection patient with chronic HBV
• HBV may be present in high titers (≥109 virus particles per milliliter) in
the blood and body fluids of infected patients.99
• HBV can survive for a prolonged period in the environment.128
• Equipment and surfaces in dialysis settings can easily become contami-
nated with blood.128
Continued
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Source: Centers for Disease Control and Prevention. Recommendations for preventing transmission of
infections among chronic hemodialysis patients. MMWR. 2001;50(RR-05):20–21. http://www.cdc.gov/
mmwr/PDF/rr/rr5005.pdf or http://www.cdc.gov/mmwr/preview/mmwrhtml/rr5005a1.htm. Accessed
May 11, 2008.
* Results of HBV testing should be known before the patient begins dialysis.
† HBsAg=hepatitis B surface antigen; anti-HBc=antibody to hepatitis B core antigen;
anti-HBs=antibody to hepatitis B surface antigen; anti-HCV=antibody to hepatitis C virus;
ALT=alanine aminotransferase.
Source: Centers for Disease Control and Prevention. Recommendations for preventing transmission of
infections among chronic hemodialysis patients. MMWR. 2001;50(RR-05):18. http://www.cdc.gov/
mmwr/preview/mmwrhtml/rr5005a1.htm. Accessed April 11, 2008.
the first operative day of the week or soon after the operating room opened.
Cultures of perioperative medications and environmental samples were nega-
tive for A. kiliense except for water from a grossly contaminated humidifier
reservoir in the heating, ventilation, and air-conditioning (HVAC) system.
Further investigation revealed that the HVAC system was routinely turned
off after the last case on Thursday and switched back on when surgery
resumed the following Tuesday. The investigators concluded that the HVAC
system was contaminated by the humidifier water, and agitation of the system
probably dislodged fungal spores when the system was turned on. The spores
were then carried on air currents into the operating room. No further cases
occurred after the HVAC system was left running 7 days a week and the
humidifier was removed.
An outbreak of Proteus mirabilis surgical site infections occurred in pa-
tients who underwent outpatient podiatric surgery.158 An investigation traced
the source to inadequately sterilized bone drills. The cluster of infections
was recognized in part because it was caused by an uncommon strain of
P. mirabilis.
An outbreak of Serratia marcescens infections occurred in 2001 in 11 patients
who had procedures in a hospital-affiliated ambulatory surgery center (five cases
with meningitis, one with septic arthritis, and five with epidural abscess).159 An
investigation revealed that all of the patients had received epidural or joint
injections with contaminated betamethasone that had been compounded at a
local pharmacy. This appears to be the first reported outbreak of infections asso-
ciated with improper pharmacy compounding.159
In 2007 the American Society of Cataract and Refractive Surgery and the
American Society of Ophthalmic Registered Nurses published recommended
practices for cleaning and sterilizing intraocular surgical instruments.160 To
prevent infections and other adverse events associated with improperly
processed intraocular surgical instruments, infection control professionals
(ICPs) should refer to these guidelines when developing infection prevention
programs for cataract surgery centers.
The CDC published guidelines for preventing surgical site infections in
ambulatory, same-day, and outpatient operating rooms as well as conventional
inpatient operating rooms,161 and these should be used when developing infec-
tion surveillance, prevention, and control programs for the ambulatory
surgery setting.
Because the incidence of SSIs associated with the types of procedures per-
formed in outpatient surgery centers is low, many ambulatory surgical centers
do not routinely conduct surveillance for SSIs. Therefore, it is likely that clus-
ters and outbreaks of infection in this setting are not detected unless they are
caused by an unusual organism or result in significant morbidity or mortality.
As more procedures are moved from the inpatient to the outpatient setting,
surveillance programs for HAIs and other adverse events in ambulatory
surgery settings should be implemented to detect adverse events in these set-
tings so that risk factors and preventive measures can be identified.161–163 The
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Conclusions 185
In the past few decades the majority of health care in the United States has
transitioned from the acute care hospital setting to outpatient and ambula-
tory care, long-term care, and home care settings.164 Many ICPs have
expanded their infection surveillance, prevention, and control programs to
include these settings. As discussed in this chapter, guidelines for developing
infection surveillance, prevention, and control programs in ambulatory care
settings have been published by individuals, professional organizations, and
government agencies, and there are many resources on professional and gov-
ernment agency Web sites.
Information on developing and implementing surveillance programs in a
variety of healthcare settings, including ambulatory care, can be found in
Chapter 2.
In a study conducted by the Association for Professionals in Infection Con-
trol and Epidemiology on the status of infection surveillance, prevention, and
control programs in the United States from 1992 through 1996, the number of
facilities performing surveillance for HAIs in outpatient settings increased by
44.0%, from 100 to 144.165 However, surveillance programs for ambulatory
care settings are not as well developed as those for acute care settings, and the
epidemiology of HAIs in the outpatient setting has not been well character-
ized. The CDC National Healthcare Safety Network will be expanding to
include data on HAIs associated with outpatient care.166 This should help to
characterize the epidemiology of HAIs in ambulatory care settings.
CONCLUSIONS
Many outbreaks in ambulatory care settings occur because (1) the responsi-
bility for implementing an infection surveillance, prevention, and control pro-
gram is often not assigned to a specific individual, and (2) personnel working
in outpatient care settings are frequently not familiar with basic infection con-
trol practices.
Based on the reports of the outbreaks discussed in this chapter, one can
identify the following risk factors as causing or contributing to infectious dis-
ease outbreaks in the ambulatory care setting:
• Inadequate cleaning, disinfection, sterilization, and storage of instru-
ments and equipment
• Inappropriate use of barrier precautions, such as gloves, by healthcare
personnel
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Suggested Readings
Garcia-Houchins S. Dialysis. In: APIC Text of Infection Control and Epidemiology. Washington,
DC: Association for Professionals in Infection Control and Epidemiology. 2005:49-1–49-17.
Goodman RA, Solomon SL. Transmission of infectious diseases in outpatient health care settings.
JAMA. 1991;265:2377–2381.
Herwaldt LA, Smith SD, Carter CD. Infection control in the outpatient setting. Infect Control
Hosp Epidemiol. 1998;19:41–74.
Resources
The following national agencies and organizations have guidelines, position papers, or stan-
dards that can be used for developing infection surveillance, prevention and control programs in
the ambulatory care setting.