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Types of infectious outbreaks and their impact in elderly care facilities
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© The Author 2010. Published by Oxford University Press on behalf of the British Geriatrics Society.
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Types of infectious outbreaks and their impact in
elderly care facilities: a review of the literature
MOMOE UTSUMI1, KIYOKO MAKIMOTO1, NAHID QUROSHI1, NOBUYUKI ASHIDA2
1
Graduate School of Medicine, Division of Health Science, Osaka University, 1-7 Yamadaoka, Suita City, Osaka 565-0871, Japan
Division of Contemporary Business Administration, Koshien University, 10-1 Momijigaoka Takarazuka City, Hyogo 665-0006, Japan
2
Address correspondence to: K. Makimoto. Tel: (+81) 6 6879 2541; Fax: (+81) 6 6879 2541. Email: [email protected]
Abstract
Background: infectious outbreaks in long-term care facilities (LTCFs) tend to have a significant impact on infection rates
and mortality rates of the residents.
299
M. Utsumi et al.
Objectives: this review aimed to update the information on pathogens identified in such outbreaks and to try to explore
indicators that reflect the impact of outbreaks among residents and health care workers (HCWs).
Methods: MEDLINE (1966–2008) was used to identify outbreaks using the following thesaurus terms: ‘Cross-Infection’,
‘Disease Outbreaks’, ‘Urinary-Tract Infections’ and ‘Blood-Borne Pathogens’. Elderly care facilities were identified with the
following thesaurus terms: ‘Long-Term Care’, ‘Assisted-Living Facilities’, ‘Homes for the Aged’ and ‘Nursing Homes’. Age
category was limited using ‘Aged’.
Results: thirty-seven pathogens were associated with 206 outbreaks. The largest number of reported outbreaks by a
single pathogen involved the influenza virus, followed by noroviruses. Among residents, the highest median attack rate
for respiratory infection outbreaks was caused by Chlamydia pneumoniae (46%), followed by respiratory syncytial virus
(40%). In gastrointestinal tract infection outbreaks, high median attack rates were caused by Clostridium perfringens
(48%) and noroviruses (45%). Outbreaks with high median case fatality rates were caused by Group A Streptococci
(50%) and Streptococcus pneumoniae (44%). High median attack rates for HCWs were caused by C. pneumoniae (41%), noroviruses (42%) and scabies (36%).
Conclusion: a variety of infectious agents were identified as the cause of outbreaks in the elderly and HCWs in
LTCFs. Attack rates and case fatality rates are useful indicators for setting priorities for education and prevention
of the outbreaks.
Keywords: outbreak, elderly, long-term care facility
Background
Infectious outbreaks in long-term care facilities (LTCFs) or
nursing homes are likely to have a significant impact on infection rates and mortality rates of the residents. It is
estimated that several thousand outbreaks occur at LTCFs
in the USA each year [1]. Respiratory and gastrointestinal
(GI) tract infections are the most common causes of outbreaks in LTCFs [2–5].
The definition of LTCF and nursing home may vary in
different countries. In the USA, LTCFs are defined as institutions that provide health care to people who are unable to
manage independently in the community [1]. Nursing homes
accommodate persons who require nursing care and related
medical and psychosocial services, and the majority of nursing homes are LTCFs [6]. Elderly persons account for the
overwhelming majority of LTCF residents, the mean age
being 80 years old [1].
The acuity of illness in nursing home residents has increased in the past two decades as a result of the shortened
length of hospital stays [1]. Thus, LTCF residents are more
vulnerable to infections than previously thought [1]. Major
risk factors for infections among LTCF residents are decreased immunity, functional impairment (e.g. incontinence,
cough reflex), decreased cognitive function and the use of
invasive devices (e.g. urinary catheters and enteral feeding
tubes) [1]. In addition, the facility design and operational
methods such as multiple resident rooms and group activities
promote pathogen transmission [7].
A review of the literature on infectious outbreaks at
LTCFs has not been conducted in the last two decades. This
review aimed to update the information on pathogens identified in such outbreaks and to try to explore indicators that
reflect the impact of outbreaks among residents and health
care workers (HCWs). Outbreak indicators would be useful
300
for generating a comprehensive prevention plan and for setting priorities for infection prevention programmes at elderly
LTCFs.
Methods
The term LTCFs for the elderly included the following: longterm care facility, nursing home care, low-level elderly care
facility, residential home for the elderly, long-term care home,
aged-care facility, skilled nursing facility for the elderly and
geriatric hospital.
Search strategy
MEDLINE (1966–2008) was used to identify outbreaks
using the following thesaurus terms: ‘Cross-Infection’, ‘Disease Outbreaks’, ‘Urinary-Tract Infections’ and ‘BloodBorne Pathogens’. Elderly care facilities were identified with
the following thesaurus terms: ‘Long-Term Care’, ‘AssistedLiving Facilities’, ‘Homes for the Aged’ and ‘Nursing
Homes’. Age category was limited using ‘Age’. Review articles of major pathogens were used to find additional articles
that met the selection criteria.
Inclusion criteria
An outbreak was generally defined as a disease incidence exceeding the expected rate. In this paper, any article or report
published in English reporting outbreaks involving elderly
care facilities was included.
Exclusion criteria
Hospital outbreaks, community outbreaks, surveillance reports, and randomised controlled trials for influenza
Types of infectious outbreaks and their impact in elderly care facilities
Table 1. Aetiologic agents of outbreaks reported in longterm care facilities (LTCFs)
Aetiologic agents
No. of reports
Influenza viruses
Noroviruses
Salmonella sp.
Group A Streptococcus
Sarcoptes scabei
Clostridium difficile
Escherichia coli
Streptococcus pneumoniae
Respiratory syncytial virus (RSV)
Legionella spp.
Parainfluenza viruses
Mycobacterium tuberculosis
Adenoviruses (epidemic keratoconjunctivitis)
Hepatitis B virus
Clostridium perfringens
Rhinoviruses
Chlamydia pneumoniae
Shigella sp.
Methicillin-resistant Staphylococcus aureus (MRSA)
Coronaviruses
Rotaviruses
Campylobacter sp.
Trichophyton
Others
Total
49
25
16
16
11
8
8
8
7
6
4
4
4
4
4
3
3
3
2
2
2
2
2
13
206
............................................................
Note: The list excluded fatal outbreaks and an outbreak caused by niacin overconsumption. If more than one pathogen was reported in one outbreak, each
was counted.
vaccine were excluded. Outbreaks reporting only culturepositive cases were also excluded.
Indicators reflecting the impact of infectious disease outbreaks were extracted. If there were more than two reports
per pathogen, median, minimum and maximum values were
tabulated.
Results
The search identified 601 articles or reports. Of these, 390 did
not include outbreak investigations or reports and 29 met the
exclusion criteria. Twenty-five articles were found by searching reference lists. In total, 207 articles were analysed.
The number of articles published per decade was two in
the 1970s, 64 in the 1980s and 77 in the 1990s. Between
2000 and 2008, 64 articles were published.
Outbreaks by country
Outbreaks in 19 countries were reported in English. The largest number were reported in the USA (109), followed by
Canada (30), UK (26), Australia (14), Japan (6), Germany
(4) and France (3). Spain, Norway and Belgium reported
two outbreaks each, and Czechoslovakia, Hong Kong, Israel, Italy, Singapore, Slovenia, Switzerland, Sweden and
Taiwan reported one each.
Infectious disease outbreaks
Aetiologic agents identified as the source of the outbreaks
are displayed in Table 1, and included bacteria (21 types),
viruses (12 types) and four types of other agents. Ninetyone were caused by bacteria, 102 by viruses and 14 by other
agents.
The largest number of reported outbreaks by a single
pathogen was influenza viruses (49) [8–56], followed by
noroviruses (25) [42, 57–80], Group A Streptococci (GAS)
(16) [81–96] and Salmonella sp. (15) [97–112].
There were four reports of concurrent outbreaks caused
by two types of pathogens [55, 56, 112, 113]. These were GI
tract infections and respiratory infections. There was a report of two outbreaks caused by different pathogens
occurring within 1 month of each other [41].
Non-bacterial or non-viral agents as a source of outbreaks were scabies (11) [114–124], Cryptosporidium parvum
(1) [125], giardiasis (1) [126] and Pulex irritans (1) [127]. Unusual outbreaks reported included one caused by niacin
overconsumption resulting from inadequate mixing of food
[128] and two fatal outbreaks [129, 130], where 21 and 15
deaths were reported in two clusters. Respiratory infections
were suspected [129, 130] but no specific pathogens were
identified.
Pseudo-outbreaks
Two pseudo-outbreaks were reported. These were cherry
haemangioma or senile haemangioma [131, 132]. In both
outbreaks, it was difficult to convince staff that these were
not infectious.
Affected sites
The respiratory tract accounted for 45% of the outbreaks
(n = 93), the GI tract for 36% (n = 74), the skin for 7% (n = 15)
and eyes for 2% (n = 4). Two pathogens were known to
cause infections in various sites, namely GAS [80–95]
and ceftazidime-resistant Klebsiella pneumoniae [133]. GAS
was involved in infections of the blood, respiratory tract
and skin. K. pneumoniae infected the lungs, urinary tract
and surgical sites [133].
Indicators reflecting the impact of outbreaks in
elderly care facilities
Outbreaks impacted both residents and HCWs. Indicators
reflecting the impact of outbreaks were attack rates for
the elderly and HCWs, the proportion of infected patients
admitted to hospital, the case fatality rate and the duration
of the outbreak.
An unusual impact of senile haemangioma pseudo-outbreaks was fear of exposure to an unknown pathogen.
The estimated cost for pseudo-outbreak control including
consultation and laboratory testing for differential diagnosis
was $10,000 [131].
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M. Utsumi et al.
Table 2. Attack rate, case fatality rate and duration of outbreaks in respiratory infection outbreaks in LTCFs
Agent
Attack rate
Fatality rate
Resident
Staff
Median duration of
outbreak in daysa
Resident
Median attack No. of reports Median attack No. of reports Median case fatality No. of reports
rate (%)a
rate (%)a
rate (%)a
.............................................................................................................................
Chlamydia pneumoniae
46 (34–68)
Respiratory syncytial virus (RSV) 40 (29–75)
Rhinoviruses
35 (5–62)
Influenza viruses
33 (4–94)
Parainfluenza viruses
41 (14–51)
Streptococcus pneumoniae
13 (7–15)
Legionella spp.
(5–13)
a
3
5
3
40
4
5
2
(22–60)
2
23 (3–58)
19
2 (0–3)
20 (2–20)
9.5 (3–21)
6.5 (0–55)
18 (16–20)
27 (20–71)
32 (5–50)
3
4
4
29
3
5
5
60
21
40
23
23
18
(22–82)
(19–42)
(19–60)
(4–180)
(10–32)
(9–60)
Median (lowest–highest). If the number of reports is 2, only the range is displayed.
Median attack rates for residents
Median attack rates for HCWs
The attack rate refers to the proportion of persons who developed infection among those exposed. The highest median
attack rate for respiratory infection outbreaks were caused
by Chlamydia pneumoniae (46%) [134–136], followed by respiratory syncytial virus (RSV; 40%) [137–141] (Table 2).
As for GI tract infection outbreaks, high median attack rates
were caused by Clostridium perfringens (48%) [142–144] and
noroviruses (45%) [57–80, 42] (Table 3). High attack rates
were also observed in other infection sites. The highest median attack rate was 70% (range: 15–93%) for scabies [114,
115, 118, 119, 122], followed by 42% (range: 31–49%) for
adenovirus [145, 148] (Table 4). One hundred percent attack
rates were reported in the two norovirus outbreaks [77, 79],
which occurred in small institutions in the 1980s.
Only one report was found for each of the following outbreaks, and reported attack rates were as follows: Bordetella
pertussis (36%) [149], human metapneumovirus (18%)
[150], Haemophilus influenzae (11%) [151] and Neisseria meningitidis (3%) [152]. Attack rates for GI tract outbreaks with a
small number of reports were Bacillus cereus (31%) [155], giardiasis (30%) [156], Cryptosporidium parvum (25%) [157],
Aeromonas hydrophila (17%) [158], Astrovirus (14%) [159]
and Vibrio cholerae (14%) [160]. The attack rate for Varicella-zoster virus was 4% [161].
In total, 16 pathogens were reported to have affected
HCWs. High attack rates in HCWs were caused by C. pneumoniae (41%) [134, 136], noroviruses (42%) [57, 58, 60–65,
68–71, 74, 76–79] and scabies (36%) [118, 119]. Median attack rates could not be calculated for the following
outbreaks because of the small number: giardiasis (40%)
[126], rotavirus (29%) [153], B. cereus (24%) [155], C. parvum
(10%) [157] and Varicella-zoster virus (1%) [161]. There
were reports of secondary infections among families of
HCWs [26, 62, 65, 68, 71, 76, 78], which are mostly caused
by noroviruses [62, 65, 68, 71, 76, 78]. The number of reports was insufficient to examine the pattern.
Median hospital admission rate
Outbreaks with high median hospital admission rates were
caused by Legionella spp. (100%) [162–164] and GAS
(63%) [84, 85, 89–91]. The median admission rate was
14% for influenza [8, 9, 12–19, 22, 25, 26, 29, 31, 32, 34,
35, 37, 40, 42–45, 48, 53], 18% for Salmonellosis [100,
102, 104, 105, 108, 110, 111] and 6% for noroviruses [58–
60, 63–65, 68, 69, 72, 73, 78]. The hospital admission rates
could not be calculated because of the inadequate information provided.
Table 3. Attack rate, case fatality rate and duration of outbreaks in gastrointestinal (GI) infection outbreaks in LTCFs
Agent
Attack rate
Fatality rate
Resident
Staff
Median attack
rate (%)a
No. of reports
48 (31–49)
45 (13–100)
(36–68)
31 (9–53)
(17–40)
17 (6–29)
3
23
2
4
2
5
Median duration of
outbreak in daysa
Resident
Median attack
rate (%)a
No. of reports
Median case
fatality rate (%)a
No. of reports
42 (9–100)
12
0 (0–9)
17
1 (1–4)
18 (2–44)
31 (0–35)
3
(13–19)
2
21 (3–75)
(1–18)
2
(20–29)
2
21 (3–90)
.............................................................................................................................
Clostridium perfringens
Noroviruses
Rotaviruses
Escherichia coli
Shigella sp.
Salmonella sp.
a
Median (lowest–highest). If the number of reports is 2, only the range is displayed.
302
Types of infectious outbreaks and their impact in elderly care facilities
Table 4. Attack rate, case fatality rate and duration of outbreaks other than respiratory and GI tract infections in LTCFs
Agent
Attack rate
Fatality rate
Resident
Staff
Median duration of
outbreak in daysa
Resident
Median attack No. of reports Median attack No. of reports Median case fatality No. of reports
rate (%)a
rate (%)a
rate (%)a
.............................................................................................................................
Sarcoptes scabei
Adenovirus
(epidemic keratoconjunctivitis)
Hepatitis B virus
Group A Streptococcus
70 (15–93)
42 (31–49)
5
4
36 (17–83)
13 (8–44)
2
3
8 (4–10)
8 (3–30)
4
7
(2–7)
2
120 (57–365)
89 (84–120)
50 (8–100)
11
150 (150–240)
150 (150–240)
a
Median (lowest–highest). If the number of reports is 2, only the range is displayed.
Median case fatality rate
The case fatality rate refers to the proportion of deaths
among those infected. Outbreaks with high median case fatality rates were caused by GAS (50%) [81–85, 87, 89, 91,
92, 94, 95], S. pneumoniae (44%) [165–169], Escherichia coli
O157:H7 (31%) [169–171] and Legionella spp. (32%) [162,
164, 172, 173].
Case fatality rates not listed in the table because of the
limited number of reports were respiratory infections caused
by Neisseria meningitidis (33%) [152], methicillin-resistant
Staphylococcus aureus (MRSA)-related pneumonia (25%) [174]
and H. influenzae (20%) [151]. Lower case fatality rates were
found in GI tract infection outbreaks caused by rotavirus
(9%) [153, 154].
Among HCWs, there was one death in an influenza virus
outbreak occurring in a 50-bed aged-care facility in 2002,
and the case fatality rate was 11% [14]. The attack rate
was 35% for residents and 21% for HCWs. In the pre-outbreak period, 90% of the residents received influenza
vaccine, while only 28% of the HCWs received the vaccine.
The vaccination status of the deceased employee was not
described [19].
Secular trends of attack rate and case fatality rates
for influenza outbreaks by decade
The secular trend of attack rates and case fatality rates for
influenza outbreaks were examined over three time periods
(1980–89, 1990–99 and 2000–08). The median attack rate
and ranges for residents for each time period were 28.0%
(0–94%), 28.0% (5–77%) and 48.8% (10–96%), respectively. The median case fatality rate and ranges for residents
were 7.0% (0–30%), 5.8% (0–55%) and 5.0% (0–15%), respectively. The median attack rate and ranges for HCWs
were 35.0% (3–58%), 20.0% (7.1–25%) and 31.4% (15–
50%), respectively. Vaccination rates were not consistently
reported. In summary, no decreasing trend was observed
for these indicators.
Median duration of the outbreak
The longest median duration of an outbreak was 150 days
involving the hepatitis virus [175–178]. Scabies also had a
long median outbreak duration of 120 days (range: 57–
365 days) [42, 58–65, 67–70, 72–76, 78, 79]. The shortest
median duration of outbreak was 1 day involving C. perfringens [142–144].
Outbreaks involving multiple facilities
Outbreaks spreading from one facility to another were
caused by noroviruses, Mycobacterium tuberculosis and Clostridium difficile. The cause of spread of the norovirus outbreak
was patient transfer [63] or the HCW's family working in
a different facility [73]. In a multi-facility tuberculosis outbreak, patient transfer and HCWs working in multiple
facilities were a likely cause of spread of the outbreak
[179]. Patient transfer also accounted for a multi-facility C.
difficile outbreak [180].
Occurrences of concurrent multi-facility outbreaks were
also common in influenza outbreaks. However, the mode of
spread to other facilities was not clear in many cases [18, 21,
26, 31, 36].
Discussion
In reviewing the literature, 37 aetiologic agents were identified as sources of outbreaks in LTCFs. Three outbreak
impact indicators were extracted and summarised. The attack rate is the most useful indicator to compare the
contagiousness of the pathogens and to evaluate an outbreak
containment programme. The case fatality rate reflects virulence and the degree of medical attention necessary as it
requires prompt identification of the pathogen and initiation
of appropriate treatment.
Previous research identified common pathogens in
LTCFs without specific indicators of contagiousness and
virulence. Attack and case fatality rates, surrogate measures
for contagiousness and virulence, can be used to categorise
aetiologic agents. These are (i) high attack rate and high case
fatality rate (e.g. RSV and E. coli 0157:H7), (ii) high attack
rate and low case fatality rate (e.g. C. pneumoniae and noroviruses), and (iii) low attack rate and high case fatality rate (e.
g. S. pneumoniae and GAS). This objective classification
scheme is useful for setting priorities for prevention plans,
resource allocation and education.
303
M. Utsumi et al.
Increased resources are being allocated for influenza vaccination of the elderly population in many countries [181].
Nevertheless, influenza outbreaks do occur in highly immunised LTCF residents because of increasing acuity [11].
Enhanced training of HCWs to conduct respiratory illness
surveillance in both residents and fellow HCWs has been
proposed [11].
This review found that HCWs were at an increased risk
of infection in an outbreak, which a previous review did not
examine in detail [2]. Thirteen different aetiologic agents
were identified in HCWs, and a majority had an attack rate
exceeding 20%. Three factors may be responsible for these
high attack rates. First, HCWs at LTCFs are working with
highly vulnerable elderly residents, and they tend to have
more exposure to the outbreak pathogens than HCWs in
acute care settings. Second, infection control programmes
at LTCFs are generally inadequate and infection control
personnel tend to be undereducated [1]. Third, HCWs providing direct care to the residents also tend to be undereducated
about infection prevention. Educating and reinforcing transmission-based precautions and hand hygiene would reduce
respiratory and GI tract infections among HCWs.
A few articles reported the spread of outbreaks to other
facilities [63]. HCWs working in multiple facilities would increase the risk of spreading an outbreak to another facility.
HCWs' families are also at increased risk of secondary infection [26, 62, 65, 68, 71, 76, 78], mostly in norovirus outbreaks.
The infection control manual requires inclusion of prevention
strategies to minimise secondary infections, and education
programmes are necessary for HCWs on the risk of secondary
infections and specific prevention plans.
The duration of outbreaks varied for each pathogen. Exploring the reasons for prolonged outbreaks is beyond the
scope of this review. It may depend on the size of the facility, the proportion of private rooms, and the physical and
mental function of the residents.
Reports of pseudo-outbreaks were rare. Nevertheless,
pseudo-outbreaks of senile haemangioma illustrated the importance of educating staff about common skin conditions
[131, 132] as well as common infectious diseases in the elderly. Once staff were convinced of its infectivity, denying it
meant questioning their assessment [131]. Given the cost of
managing a pseudo-outbreak, staff education is a very
worthwhile investment.
This review has several limitations. First, we only
searched for papers written in English. Non-English-speaking countries with a high proportion of elderly may have
different outbreak patterns because the facility sizes and care
system differ among countries. Second, only Medline was
used for the literature search, while a search of reference lists
of relevant articles was used to find additional articles. Embase was not used because of limited access, which may
have resulted in fewer European outbreak reports.
Third, publication bias may exist, and the attack and case
fatality rates summarised here may be biased toward higher
rates. If the median attack rates were closer to the minimum,
then it is possible that the outbreaks with higher attack rates
304
were more likely to be reported than those with lower attack
rates. Overall, the results do not support this type of bias for
residents. Authors are encouraged to report essential information for the indicators. The variety of rare pathogens
reported indicates publication bias toward rare pathogens.
A relatively high frequency of GAS outbreaks suggests a
publication bias toward outbreaks with high case fatality. In
spite of these biases, the common pathogens in our results
were the same as the previous review with few exceptions
such as vancomycin-resistant Enterococci (VRE) [1]; the findings reflect common outbreak problems in LTCFs.
Culture-positive outbreaks were excluded in the review
as they require a separate review. Multi-drug resistance
pathogens (MDRPs) such as MRSA and VRE are endemic
in LTCFs [182, 183]. The high frequency of antibiotic usage
to treat infections in residents contributes to the emergence
of resistant organisms in LTCF residents and is also considered to be a major factor in increased incidence of C. difficileassociated disease [184]. Frequent transfer between acute
care and LTCFs provides ample opportunities to spread
MDRP in both settings [1], which suggests that an infection
control programme in one facility is not adequate to contain
the problem and appears to require a wider strategy for infection control.
In summary, this review identified 37 pathogens associated with 206 outbreaks at LTCFs. HCWs were infected
by 16 of the 37 pathogens. Indicators reflecting the impact
of an outbreak in the articles were attack rate, case fatality
rate and duration of the outbreak. Infectious outbreaks can
be classified into the following three categories: (i) high attack rate and high case fatality rate, (ii) high attack rate and
low case fatality rate, and (iii) low attack rate and high case
fatality rate. The objective classification scheme applied here
is useful for setting priorities for prevention plans, resource
allocation and education.
Key points
• Infectious outbreaks in long-term care facilities (LTCFs)
or nursing homes tend to have a significant impact on
infection rates and mortality rates of the residents.
• Attack and case fatality rates, surrogate measures for
contagiousness and virulence, can be used to categorise
aetiologic agents. These are (i) high attack rate and high
case fatality rate, (ii) high attack rate and low case fatality
rate, and (iii) low attack rate and high case fatality rate.
• This objective classification scheme is useful for setting
priorities for prevention plans, resource allocation and
education.
Acknowledgements
This work was supported by the Univers Foundation (grant
number 07.02.080).
Types of infectious outbreaks and their impact in elderly care facilities
We would like to thank the reference librarian Mr Toshiyuki
Swa at the Osaka University Life Science Library for
assisting us in conducting the literature search.
Supplementary data
Supplementary data are available at Age and Ageing online.
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Received 13 February 2009; accepted in revised form
20 January 2010
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