Final Report for Investigation E-253-14

Outbreak of Enterococcus faecalis endocarditis associated with an oral surgery practice

July 20, 2016
Description
This Final Report replaces the New Jersey Department of Health (NJDOH) Interim Report dated
March 1, 2016 and supplements the Preliminary Report dated December 1, 2014 and the
NJDOH Updated Preliminary Report dated January 26, 2015.
This Final Report describes the investigation and findings of the outbreak of Enterococcus
faecalis (E. faecalis) endocarditis associated with breaches of infection prevention practices at
an oral surgery practice in Morris County, New Jersey (NJ). At the time of this report, NJDOH
has identified 15 cases of E. faecalis endocarditis including one death associated with this
outbreak among patients receiving intravenous sedation for invasive oral surgical procedures
from December 2012 through August 2014.
Summary
On October 20, 2014, a healthcare provider reported two cases of bacterial endocarditis caused
by E. faecalis. Both cases, 17 and 23 years of age (Table 1 Patient #10 and #12, respectively)
at the time of the report, had no known underlying risk factors for developing endocarditis but
both cases had undergone oral surgery at the same oral surgery practice in Morris County, NJ.
On November 6, 2014, NJDOH learned from the New Jersey Board of Dentistry (NJBOD) of an
additional case of endocarditis; the third case had also undergone prior oral surgery at the same
practice. A public health investigation conducted by NJDOH revealed that the third case, a 69year-old male who had a procedure at the oral surgery practice in December 2012, also had E.
faecalis isolated from blood cultures at the time of the endocarditis diagnosis.
Enterococci are gram-positive organisms that typically inhabit the gastrointestinal and
genitourinary systems of humans. The genus enterococcus includes more than 17 species, E.
faecalis and E. faecium are the most prevalent species cultured from humans, accounting for
more than 90 percent of clinical isolates. Other enterococal species known to cause human
infection include E. avium, E. gallinarum, E. casseliflavus, E. durans, E. raffinosis, and E.
mundtii (1). While there are reports of E. faecalis being implicated in endodontic infections, the
organism is not a usual component of oral flora (2).
Studies suggest that more than 700 species of bacteria may be identified in the human mouth
including aerobic and anaerobic gram-positive and gram-negative microorganisms.
Approximately 30 percent of the flora of the gingival crevices is streptococci, predominantly of
the viridans group. Of the more than 100 oral bacterial species recovered from blood cultures
after dental procedures, the most prevalent of these are viridans group streptococci and
anaerobes. The most common microbiologic causes of community-acquired native valve
infective endocarditis are Staphylococcus spp. and viridans group streptococci (3).
Approximately, only 5-10 percent of cases of endocarditis are caused by Enterococcus spp.
(4,5). Cases of enterococcal endocarditis are usually associated with gastrointestinal or
genitourinary disease or procedures involving the gastrointestinal or genitourinary systems;
often patients have underlying medical conditions (6,7).
1

Although the absolute risk for infective endocarditis from a dental procedure is impossible to
measure precisely, the best available estimates are as follows: if dental treatment causes one
percent of all cases of viridans group streptococcal infective endocarditis annually in the United
States, the overall risk in the general population is estimated to be as low as one case of
infective endocarditis per 14 million dental procedures. Even for people with underlying heart
disease, the risk of developing infective endocarditis is low. For people with underlying cardiac
conditions, the estimated absolute risk rate for infective endocarditis from a dental procedure is
one per 1.1 million procedures for patients with mitral valve prolapse, one per 475,000
procedures for patients with congenital heart disease, one per 142,000 procedures for patients
with rheumatic heart disease, one per 114,000 procedures for patients with a prosthetic cardiac
valve, and one per 95,000 procedures for patients with previous infective endocarditis (3).
Therefore, having three cases of endocarditis associated with dental extractions at a single oral
surgery office would be unusual. Having three cases of endocarditis with the same enterococcal
species, E. faecalis, would statistically be highly unlikely, particularly in persons without known
underlying disease. This extremely rare occurrence warranted a thorough assessment of the
infection prevention practices within the oral surgery practice to identify a common potential
source of exposure during the surgical procedure.
Given the facts obtained during the public health investigation, information from the literature
review, and the distribution of cases over time, it was determined that there was a potential
ongoing risk to public health and an unannounced, multiagency visit to the office was
scheduled.
On November 14, 2014, representatives of the Mount Olive Township Health Department,
Communicable Disease Service of the NJDOH, and the NJ Department of Consumer Affairs
Enforcement Bureau within the Department of Law and Public Safety visited the location where
all three oral surgeries were performed. During this visit, it was determined that the infection
prevention practices deviated from the guidelines promulgated by the Centers for Disease
Control and Prevention (CDC) and endorsed by the American Dental Association. The breaches
identified during the visit, particularly the injection safety breaches, have previously been linked
to disease transmission and were thought to constitute an ongoing risk to patients undergoing
procedures within the practice. Recommendations to improve infection prevention practices
were made to the oral surgeon and his staff in order to prevent possible ongoing disease
transmission. The findings and recommendations, which were summarized in the December 1,
2014 Preliminary Report, were also communicated to NJBOD.
On January 13, 2015, a follow-up site visit was performed by representatives from NJDOH, the
NJ Department of Consumer Affairs within the Department of Law and Public Safety, and
external consultants retained by NJBOD. The oral surgeon had made changes to his practice
based on the recommendations outlined in the December 1, 2014 Preliminary Report. However,
deficiencies were still noted and summarized in the January 26, 2015 Updated Preliminary
Report.
Single cases of endocarditis and enterococcal infections are not reportable conditions in NJ to
public health authorities. In accordance with N.J.A.C. 8:57, Reportable Communicable
Diseases, a healthcare provider is required to report all outbreaks or suspected outbreaks of
any condition to public health authorities. However, patients with a particular disease might seek
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care from different healthcare providers so that a single provider might not recognize the
increase in the number of cases of the disease.
In order to better evaluate the scope of infections associated with the implicated oral surgery
practice, NJDOH requested access to the oral surgeons appointment records for all of 2013
and 2014. NJDOH also requested access to data collected through the NJ Hospital Discharge
Data Collection System for the same time period. In 1976, NJDOH was among the first states to
collect utilization data on hospital inpatients. Utilization data includes information on admission
and discharge dates, hospital code, services rendered, charges, and type of insurer. Since
1981, inpatient data has been collected through Uniform Bill-Patient Summaries (UB). Starting
in 2004, NJDOH included outpatient data from hospital emergency departments, on UB forms.
Therefore, this data will capture all persons who visited an emergency department or were
hospitalized throughout NJ.
The appointment records obtained from the oral surgery practice and the UB-Patient Summary
data underwent a matching-algorithm using statistical software to determine if any of the oral
surgery practices patients were subsequently hospitalized or seen in emergency departments
within NJ. Inclusion criteria included undergoing an oral procedure at the implicated practice
within six months prior to hospitalization or emergency department visit. The search was further
narrowed to the following International Classification of Diseases, ninth revision (ICD-9)
diagnostic codes:
1.
2.
3.
4.
5.
6.

Endocarditis (421.)
Enterococcus (041.04)
Bacteremia (790.7)
Sepsis and Septicemia (995.9 and 038.)
Other endocardium (424.)
Oral abscess (528.3)

The medical records of all the potential cases were requested from the appropriate medical
facilities and reviewed. Through this process, 12 additional cases of E. faecalis endocarditis
associated with the oral surgery practice were identified, bringing the total number of cases to
15, including one death as of the date of this report. The death was due to complications of
endocarditis and resulting cardiac surgery.
All 15 cases or their representatives were interviewed by telephone using a standardized data
collection tool to understand their clinical presentation, determine the presence of any potential
underlying risk factors for endocarditis, and identify any other potential sources of enterococcal
infection. One of the 15 interviews was partially completed and considered lost to follow-up.
Characteristics of the cases
Based on available information, all 15 cases underwent invasive oral surgery procedures using
intravenous sedation at the implicated practice between December 2012 and August 2014. The
median age at the time of the procedure was 46 years (range, 16 77). The average age was
41.8 years. Eleven (73%) of the cases were male. Eleven (73%) of cases were less than 60
years of age in this patient population; nationally, less than half of patients with endocarditis
caused by any organism are less than 60 years. Twelve (80%) of the cases underwent cardiac
surgery as a consequence of their infection; of these 12 cases, eight had a valve replacement
3

and four had valve debridement/repair procedures. One (7%) of cases died due to
complications of the infection and resulting cardiac surgery. The median number of days
between the procedure date and the first positive blood culture collection date is 82; average
number of days was 87 (range, 30 149). Eight cases (53%) reported a history of murmur.
Three cases (20%) had conditions that might place them at increased risk for endocarditis. Of
these three cases, one was known to have aortic stenosis, one had a previously undiagnosed
bicuspid aortic valve, and one had previously undiagnosed Partial Anomalous Pulmonary
Venous Return (PAPVR). While these three cases had conditions that might place them at
increased risk for endocarditis, none of the 15 cases had a high risk condition for which
antimicrobial prophylaxis is recommended prior to dental procedures. Antimicrobial prophylaxis
is recommended for patients at the highest risk for endocarditis including those with previous
infective endocarditis, prosthetic heart valves, certain types of congenital heart disease, or when
they develop cardiac valvulopathy after a cardiac transplant (3). In addition, none of the cases
had identified underlying illnesses placing them at increased risk for enterococcal infections
(e.g., indwelling catheters, cancer, chronic dialysis, gastrointestinal or genitourinary disease).
Among the intravenous medications routinely administered during invasive surgical procedures,
propofol and versed were common to all cases for whom complete oral surgery anesthesia
records were available. Table 1 illustrates the characteristics of the endocarditis cases. Figure 1
illustrates the number of known cases of endocarditis by date of oral surgery procedure. Table 2
details the doses of each intravenous medication administered to cases.
Table 1. Characteristics of endocarditis cases^
Intravenous
sedation

Number of days
between
procedure and
positive blood
culture

Cardiac
surgery

Yes

35

Yes

Valve replacement

20

Yes#

126

Yes

Valve debridement/repair

1/23/2013

54

Yes

118

Yes

History of murmur; valve

replacement; cases died due
to complications

4/4/2013

17

Yes

82

No

History of murmur

4/19/2013

46

Yes

48

No

6/3/2013

54

Yes

149

Yes

7/8/2013

18

Yes

59

Yes

8/27/2013

77

Yes

35

Yes

9/25/2013

65

Yes

30

No

History of murmur

10*

5/7/2014

16

Yes

147

Yes

Valve replacement

11

6/20/2014

29

Yes

75

Yes

Valve debridement/repair

Patient
identification
number(#)

Date of
procedure

Age at
time of
procedure

Sex

1+

12/20/2012

69

1/18/2013

Comments

History of murmur; valve

replacement; interview not
complete
Valve debridement/repair;
previously undiagnosed
bicuspid aortic valve
History of murmur; aortic
stenosis; valve replacement

12*

6/27/2014

23

Yes

110

Yes

13

7/18/2014

21

Yes

90

Yes

14

7/31/2014

69

Yes

128

Yes

15

8/21/2014

49

Yes

77

Yes

History of murmur; valve

debridement/repair; previously
undiagnosed PAPVR
History of murmur; valve
replacement
History of murmur; valve
replacement
Valve replacement

^Information from the dental records obtained from the practice, medical records, appointment book, and case interviews unless
otherwise noted.
+Patient reported to the NJ Board of Dentistry
#
Based on information from medical records, appointment book, and cases interviews; awaiting oral surgery anesthesia records.
*Patients reported to NJDOH in October 2014

Ketamine

Fentanyl

12/20/2012

10mg

8mg

1/18/2013

1/23/2013

10mg

8mg

4/4/2013

10mg

8mg

60mg

4/19/2013

10mg

8mg

6/3/2013

10mg

7/8/2013

Propofol

Dexamethasone

Glycopyrolate

Date of
procedure

Metoclopramide

Patient
#

Midazolam

Table 2. Intravenous medications administered to each patient during surgical procedure

4mg

0.2mg

100mg

0.2mg

100mg

4mg

0.2mg

200mg

4mg

0.2mg

150mg

8mg

0.2mg

70mg

10mg

8mg

60mg

4mg

0.2mg

50mg

8/27/2013

5mg

0.2mg

100mg

9/25/2013

5mg

8mg

0.2mg

70mg

10

5/7/2014

10mg

8mg

0.1mg

0.2mg

100mg

11

6/20/2014

12

6/27/2014

50mg

13

7/18/2014

14

7/31/2014

5mg

8mg

0.2mg

80mg

15

8/21/2014

5mg

4mg

0.2mg

100mg

Oral surgery anesthesia records not available

Oral surgery anesthesia records incomplete

5mg

8mg

Oral surgery anesthesia records incomplete

Figure 1. Number of known endocarditis cases associated with the oral surgery office
by date of oral procedure, 2012 - 2014

Number of endocarditis cases

3
Procedure date of
Patient #1 reported
to BOD

Procedure dates of
Patients #10 &12

NJDOH notified
of cases #10 and
#12

Date of oral procedure (month-year)

BOD New Jersey Board of Dentistry

NJDOH New Jersey Department of Health

Characteristics of the outbreak

The incidence of enterococcal endocarditis cases (number of newly diagnosed cases among
the total population at risk over a period of time) among patients receiving care at the oral
surgery practice for 2013 and 2014 is illustrated in Table 2. There were fourteen cases of
endocarditis with procedure dates during 2013 and 2014. (Note: Patient #1 with a procedure
date in 2012 was not included). The number of unique patients visiting the practice during 2013
and 2014 was used as the patient population; this number, obtained from the appointments
records provided by the oral surgeon, is estimated to be 3,756. A unique patient means that
each patient is counted once during the period specified even if the patient was seen multiple
times during that period of time.
Table 2. Incidence rates of endocarditis at oral surgery practice 2013, 2014 and 2013-2014

Total

Year

Number of
cases

2013
2014
2013-2014

8
6
14

Number of
unique
patients
2,143
1,954
3,756

Incidence per 100,000

patient population
373.3
307.0
372.7

National comparison
The incidence rate of all endocarditis cases in the United States is estimated to be 15 per
100,000 persons per year (8,9). It is estimated that 5-10 percent of cases of endocarditis are
caused by all Enterococcus spp. (e.g., E. faecalis, E. faecium, E.durans, etc.) (4,5). Therefore,
one would expect to see approximately 1.5 cases of enterococcal endocarditis per 100,000
persons per year. NOTE: The number of cases of enterococcal endocarditis caused specifically
to E. faecalis would be even less than this number.
The incidence rate of enterococcal endocarditis among patients at the practice for 2013
2014, 372.7 per 100,000, was more than 248 times greater than the national incidence.
Therefore, based upon these estimates, patients who received care during 2013 2014 at
the oral surgery practice under investigation were 248 times more likely to have
enterococcal endocarditis than people in the general population. Enterococcus spp. are
not part of the normal oral flora and are not commonly associated with bacteremias
following oral surgery procedures (2,10,11,12). This organism was most likely introduced
into the patients bloodstreams through breaches of infection prevention practices
during the administration of intravenous sedation at the practice - not through the oral
surgery procedure itself.
Multiple injection safety breaches that have been previously associated with cases and
outbreaks of infections were observed at the practice during the site visits. These breaches
included, but were not limited to, the use of single use vials of medication for multiple patients,
the use of multiple use vials of medication in the direct patient care area, the storage and use of
unwrapped syringes, the pre-drawing of medications in advance of the procedure, the use of
nonsterile products (e.g., multiple use alcohol dispensers), storage of medications in a locker in
the staff bathroom, and poor hand hygiene.
CDC is aware of more than 50 outbreaks since 2001 due to these types of unsafe injection
practices. More than half represented outbreaks of bacterial infections, most of which resulted in
severe bloodstream infections; almost all of the remaining outbreaks involved transmission of
hepatitis B or hepatitis C (13,14). In 2011, the NJDOH investigated an outbreak of 12 cases of
Klebsiella pneumoniae bacteremia associated with injection safety breaches at an oncology
practice. The oncology practice used a common bag of saline as a source of fluid for multiple
patients, stored unwrapped syringes, prefilled syringes, and had suboptimal hand hygiene
practices (15).
There are also numerous published reports of infections linked specifically to the administration
of intravenous anesthetics, particularly propofol. Propofol, a lipid-based product, supports
microbial growth. Unless strict aseptic technique is followed when handling propofol, the product
can become contaminated with bacteria (16,17,18,19,20,21,22). These bacteria can replicate
within the propofol, particularly when the contaminated product is prepared well in advance of
the procedure, and cause serious infections following injection.
Enterococci are common inhabitants of the gastrointestinal tract of humans. Enterococci are not
part of the normal oral flora and are not commonly associated with bacteremias following dental
procedures. However, enterococci are a frequent cause of healthcare-associated infections. In
hospitals in the United States, enterococci are the second most common organism recovered
from catheter-associated infections of the bloodstream and urinary tract, and from skin and soft7

tissue infections. These organisms are hardy and can survive for long periods on environmental
surfaces, including medical equipment, bed rails, and doorknobs (23).
Summary
Through retrospective analysis of data, NJDOH has recently identified additional patients who
developed E. faecalis endocarditis following an oral surgical procedure at one specific oral
surgery practice by one specific oral surgeon. Fifteen cases of endocarditis have been identified
to date including one death; NJDOH is continuing surveillance efforts to detect additional cases
associated with this outbreak. The magnitude of this prolonged outbreak is likely to be greater
than the number of cases detected since the method used to detect cases is insensitive.
The organism was likely introduced into the patients bloodstreams during the administration of
intravenous sedation.
Evidence for this claim is as follows:

Bacterial endocarditis following oral surgery is rare. The overall risk in the general
population is estimated to be as low as one case of infective endocarditis per 14 million
dental procedures. Even for people with underlying heart disease, the risk of developing
infective endocarditis remains low. For people with underlying cardiac conditions, the
estimated absolute risk rate for infective endocarditis from a dental procedure is one per
1.1 million procedures for patients with mitral valve prolapse, one per 475,000
procedures for patients with congenital heart disease, one per 142,000 procedures for
patients with rheumatic heart disease, one per 114,000 procedures for patients with a
prosthetic cardiac valve, and one per 95,000 procedures for patients with previous
infective endocarditis (3).

Viridans streptococci, a major component of normal oral flora, are associated with
endocarditis following dental procedures.

Enterococcus is not part of the normal oral flora and is not commonly associated with
bacteremias following dental procedures.

Enterococcus is a hardy organism that can survive in the environment and is a leading
cause of health-care associated infections.

Injection safety breaches that have been previously associated with cases and
outbreaks of disease were identified during the site visit to the oral surgery practice.

Based on available information, all of the cases who developed endocarditis received
intravenous sedation at the practice prior to the onset of the infection. NJDOH did not
identify any cases who developed endocarditis after undergoing invasive procedures at
the practice with only local anesthesia. NJDOH did not identify any cases who
developed endocarditis after visiting the practice for noninvasive procedures or
consultation.

Conclusions
1) Corrective action was instituted by the oral surgeon following the December 2014 and
January 2015 site visits.
2) NJDOHs ability to detect cases of enterococcal endocarditis is insensitive and
surveillance for new cases after the institution of corrective measures is difficult and not
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timely. Therefore, NJDOH cannot be certain that all cases were detected and
investigated and that transmission within the practice has stopped. Ongoing surveillance
efforts include:
-Continued matching
NJDOH obtained the 2015 appointment records and the 2015 UB data in order to detect
cases that might have occurred after the institution of corrective measures. Access to
the 2016 UB data will be requested since infections associated with procedures late in
2015 might not manifest until 2016.
-A call for cases
On March 2, 2016, NJDOH sent notification of this outbreak via email to healthcare
providers via the NJ Local Information Network and Communication System Health Alert
Network. Separate email communications targeting infectious disease specialists were
also sent on the same date. Additionally, NJDOH contacted several infectious disease
specialists via telephone. NJDOH requested that healthcare providers ask patients with
E. faecalis bacteremia or endocarditis if they have had an invasive oral surgery
procedure within six months prior to symptom onset and to report to NJDOH any patient
meeting the following criteria:
a. E. faecalis bacteremia or endocarditis and
b. Absence of an underlying condition placing him/her at higher risk for
enterococcal infections and
c. A history of an invasive oral surgery procedure within six months prior to
symptom onset and
d. Symptom onset after January 1, 2015.
3) An infection preventionist visited the practice on March 12, 2015; however, it does not
appear that the preventionist is providing ongoing services or oversight. To ensure
patient safety, NJDOH recommends that the practice retain the ongoing services of an
infection preventionist to optimize infection prevention practices, assess staff
competencies, and provide oversight.
4) NJDOH will work with the NJBOD to ensure that the implicated oral surgeon is informed
of these new findings and made aware of the magnitude of this outbreak.
5) NJDOH will continue to work through the NJBOD to obtain incomplete and missing oral
surgery anesthesia records from the implicated oral surgeon.
6) NJDOH will work with the NJBOD to schedule a repeat visit to the office to review the
current infection prevention practices at the oral surgery practice.

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