Outbreaks of serious pneumococcal disease in closed settings in the post-antibiotic era: A systematic review

doi:10.1016/j.jinf.2010.03.032

Journal of Infection

Volume 61, Issue 1, July 2010, Pages 21-27

https://doi.org/10.1016/j.jinf.2010.03.032 Get rights and content

Summary

Objectives

Since the introduction of antibiotics, pneumococcal disease is predominantly sporadic, with occasional outbreaks. Our objective was to review the epidemiology of reported outbreaks of serious pneumococcal disease in closed settings to inform the development of guidelines to manage such outbreaks.

Methods

We systematically reviewed the literature for reported outbreaks of serious pneumococcal disease in closed settings to inform the development of guidelines in managing such outbreaks.

Results

We identified 42 outbreaks reported in 39 papers – 14 in hospitals, 12 in long term care facilities, five outbreaks in households, four in military settings, three in child care settings and two each in homeless shelters and jails. The serotype/group most frequently associated with outbreaks was 14 (seven outbreaks) followed by 4 (five outbreaks) then serotypes/groups 1, 9 and 9 V each causing four outbreaks. The median outbreak size was four cases (2 - 46). The median duration was eight days, with 84% of cases occurring within 14 days of the first case.

Conclusion

Outbreaks of serious pneumococcal disease are likely to continue happening requiring early recognition and implementation of public health measures in order to interrupt transmission. This study facilitated the development of the first UK interim guidelines for managing such outbreaks.

Introduction

In 1903, Sinigar described one of the first documented outbreaks of pneumococcal disease in a closed setting among patients and staff of an asylum.¹ In 1918, a one-month epidemic of S. pneumoniae in a military camp in the USA resulted in 2349 hospital admissions and a 50% death rate.² Several other large outbreaks of pneumococcal pneumonia have been reported in the pre-antibiotic era occurring in families,³ mental institutions,⁴ hospitals,⁵ barracks ⁶ and schools.⁷ Although pneumococcal outbreaks are rarely reported now, when they occur, they still can cause significant morbidity and mortality, depending upon the population affected. Since the introduction of antibiotics, pneumococcal disease has occurred predominantly sporadically, with occasional outbreaks reported in various settings. The epidemiology of these outbreaks has varied widely in terms of size, duration, serotype, and setting. No systematic review of these outbreaks has been undertaken.

Our objective was to review the epidemiology of reported outbreaks of serious pneumococcal disease including in various closed settings such as residential and nursing homes, nurseries/day care, schools, prisons and hospitals to inform the development of evidence-based guidelines for their public health management. This review informed the “Interim UK Guidelines for the public health management of outbreaks of serious pneumococcal disease in closed settings” published in 2008.⁵⁸

Section snippets

Methods

A search of electronic databases was undertaken in May 2006 using Medline (1966 onwards), with subsequent reviews until February 2009. Serious pneumococcal disease was defined as pneumococcal pneumonia, meningitis or bacteraemia. We excluded from this study outbreaks of all non-invasive presentations other than pneumonia such as conjunctivitis and acute otitis media. Our search strategy included three primary MeSH terms; “Streptococcus pneumoniae”, “Pneumonia, Pneumococcal”, and “Meningitis,

Results

We found a total of 42 outbreaks in 39 papers reported from 1980 to 2006.8, 9, 10, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38, 39, 40, 41, 42, 43, 44, 45 In the post-antibiotic era, a median of one outbreak was reported per year in the literature. Between 1991 and 2000 the frequency of reported outbreaks was three times more than in the proceeding 10 years, with six outbreaks reported in 1999 alone. This trend appears to have

Discussion

We identified 42 outbreaks of serious pneumococcal disease in closed settings occurring most frequently in LTCF and hospitals and households. Given the frequency of pneumococcal pneumonia, particularly in the elderly, it was surprising how few outbreaks were reported. There are several possible explanations for the low reporting of outbreaks. Outbreaks may not be identified, may not be recorded or reported or reported outbreaks not published. Another reason might be that S. pneumoniae is a

Acknowledgements

We will like to acknowledge the contributions of the HPA group set up to develope guidelines for the management of serious pneumococcal disease in the United Kingdom. These include Dr Richard Pebody, Dr Deborah Wilson, Dr Isabel Oliver, Marion Bond, Dr Chikwe Ihekweazu, Dr Robert George, Dr Mary Slack, Dr Martin Donaghy, Dr David Dance, Dr Bharet Patel, Dr Alex Doroshenko, Dr Marina Basarab and Sarah Brill.

References (59)

H. Sinigar
The variability in virulence of pneumococcus
Lancet
(1903)
T.D. Cartmill et al.
Hospital outbreak of multiresistant Streptococcus pneumoniae
J Hosp Infect
(1992)
K.E. Collingham et al.
Pneumococcal meningitis in a husband and wife 1
J Infect
(1985)
N.F. Crum et al.
Halting a pneumococcal pneumonia outbreak among United States Marine Corps trainees
Am J Prev Med
(2003)
S. Dawson et al.
Outbreak of multiresistant pneumococci
J Hosp Infect
(1992)
A. Mercat et al.
An outbreak of pneumococcal pneumonia in two men's shelters
Chest
(1991)
M.R. Millar et al.
Outbreak of infection with penicillin-resistant Streptococcus pneumoniae in a hospital for the elderly
J Hosp Infect
(1994)
R.E. Quick et al.
Underutilization of pneumococcal vaccine in nursing home in Washington State: report of a serotype-specific outbreak and a survey
Am J Med
(1993)
D. Subramanian et al.
Rapid spread of penicillin-resistant Streptococcus pneumoniae among high-risk hospital inpatients and the role of molecular typing in outbreak confirmation
J Hosp Infect
(2003)
E.P. Moore et al.
Hospital transmission of multiply antibiotic-resistant Streptococcus pneumoniae
J Infect
(1988)

E.F. Hirsch et al.

An epidemic of pneumococcus bronchopneumonia

J Infect Dis

(1919)

R.C. Tilghman et al.

Pneumococcic infections in families

J Clin Invest

(1936)

W.G. Smillie et al.

A study of type 1 pneumococcus epidemic at the State Hospital in Worchester, Mass

Am J Public Health

(1938)

W.G. Smillie

A study of an outbreak of type II pneumococcus pneumonia in the Veterans Administration Hospital in Bedford, Massachusetts

Am J Hygiene

(1936)

J.L. Miller et al.

Epidemic of Streptococcus pneumonia and empyema at Camp Dodge, Iowa

JAMA

(1918)

E.G. Stillman

Further studies on the epidemiology of lobar pneumonia

J Exp Med

(1917)

Outbreak of invasive pneumococcal disease in a jail – Texas

MMWR Morb Mortal Wkly Rep

1989

(1989)

A nosocomial outbreak of Streptococcus pneumoniae infection

Commun Dis Rep CDR Wkly

(1992)

Outbreak of pneumococcal disease in a Kansas nursing home

Kans Med

(1993)

Outbreaks of pneumococcal pneumonia among unvaccinated residents of chronic-care facilities – Massachusetts, October 1995, Oklahoma, February, 1996, and Maryland, May–June 1996

MMWR Morb Mortal Wkly Rep

(1997)

M. Bain et al.

Pneumococcal cross-infection in hospitalized elderly patients

Br J Hosp Med

(1990)

S.L. Berk et al.

Type 8 pneumococcal pneumonia: an outbreak on an oncology ward

South Med J

(1985)

R.J. Carter et al.

Failure to control an outbreak of multidrug-resistant Streptococcus pneumoniae in a long-term-care facility: emergence and ongoing transmission of a fluoroquinolone-resistant strain

Infect Control Hosp Epidemiol

(2005)

T. Cherian et al.

A outbreak of invasive pneumococcal disease in young children in child care

JAMA

(1994)

A.S. Craig et al.

Carriage of multidrug-resistant Streptococcus pneumoniae and impact of chemoprophylaxis during an outbreak of meningitis at a day care center

Clin Infect Dis

(1999)

A.J. Davies et al.

Pneumococcal cross infection in hospital

Br Med J (Clin Res Ed)

(1984)

B.E. de Galan et al.

Hospital-related outbreak of infection with multidrug-resistant Streptococcus pneumoniae in the Netherlands

J Hosp Infect

(1999)

A. DeMaria et al.

An outbreak of type 1 pneumococcal pneumonia in a men's shelter

JAMA

(1980)

P.A. Fenton et al.

Pneumococcal bacteraemia in mother and son

Br Med J (Clin Res Ed)

(1983)

Cited by (24)

Outbreaks of severe pneumococcal disease in closed settings in the conjugate vaccines era, 2010–2018: A systematic review to inform national guidance in the UK
2019, Journal of Infection
Pneumococcal outbreaks are rare but they still occur, particularly in closed settings usually involving vulnerable groups. We undertook a systematic review to identify strategies for controlling pneumococcal outbreaks since the licensure of higher-valent pneumococcal conjugate vaccines (PCVs).
A systematic literature search was performed for pneumococcal outbreaks published since 2010. A cluster was defined as two or more cases of severe pneumococcal disease in a closed setting within 14 days.
Eleven reports were identified, including seven caused by serotypes in both the 13-valent PCV (PCV13) and the 23-valent polysaccharide vaccine (PPV23); two were due to a PCV13-only serotype (6A) and one each by a PCV13-related serotype (6C) and a non-vaccine serotype (15A). Eight reported infection control measures, including reinforcing hand washing, respiratory hygiene and patient cohorting. PPV23 was used in five outbreaks, while PCV13 and both vaccines were used in one outbreak each. Different antibiotics were used for chemoprophylaxis in eight outbreaks.
Most pneumococcal outbreaks are currently caused by vaccine-preventable serotypes, and PPV23 is the preferred vaccine in more than half the outbreaks. Early implementation of infection control measures is important, and antibiotic chemoprophylaxis should be considered for high-risk individuals.
Hospital-onset adult invasive pneumococcal disease in Israel: Sicker patients, different pathogens
2019, International Journal of Infectious Diseases
Citation Excerpt :
Nosocomial outbreaks of S. pneumoniae are rare and occur mainly in the institutional setting. A systematic review identified only 42 outbreaks between the years 1980 and 2006 (Ihekweazu et al., 2010). Our series encompassed sporadic cases from many centers over a 6-year period; therefore, the role of nosocomial transmission and outbreak in this study is probably negligible.
Invasive pneumococcal disease (IPD) usually has its onset in the community (CO-IPD), but it can commence following hospitalization (HO-IPD). This study compared HO-IPD and CO-IPD cases during the implementation of the pneumococcal conjugate vaccine (PCV) program for children in Israel.
This was a nationwide retrospective cohort study of adult (age >18 years) IPD patients covering the period from the implementation of the PCV7/13 program in 2009/2010 through 2015. HO-IPD and CO-IPD were defined as IPD with onset ≥4 and ≤2 days from admission, respectively. Patient characteristics, outcome measures, serotypes, and antimicrobial susceptibility were compared for the entire cohort, followed by a matched case–control analysis.
The study included 114 patients with HO-IPD and 2180 with CO-IPD. After matching HO-IPD to CO-IPD patients by age, sex, and comorbidities, the mortality rate and discharge to long-term care facility rate were significantly higher for HO-IPD patients than for CO-IPD patients (44.6% vs. 26.3% and 26.5% vs. 8.2%, respectively). HO-IPD isolates were less often covered by PCV13 (39.6% vs. 49.0%) and pneumococcal polysaccharide vaccine PPSV23 (56.6% vs. 71.3%) and more often resistant to penicillin (9.3% vs. 3.6%), ceftriaxone (3.8% vs. 0.75%), and levofloxacin (9.3% vs. 0.8%).
HO-IPD was associated with higher morbidity and mortality than CO-IPD and was more often caused by non-vaccine serotypes (primarily non-PCV13 types) and antibiotic-resistant strains.
Rapid increase in non-vaccine serotypes causing invasive pneumococcal disease in England and Wales, 2000–17: a prospective national observational cohort study
2018, The Lancet Infectious Diseases
Citation Excerpt :
The overall decline in PCV13-type disease was offset by an increase in non-PCV13 invasive pneumococcal disease, especially serotypes 8, 12F, and 9N, since 2013/14. These increases were observed throughout England and Wales, with no geographical or temporal clustering as has been reported elsewhere.14 Overall, we estimate that nearly 40 000 cases of invasive pneumococcal disease have been prevented since the introduction of PCV7, even after the additional cases due to serotype replacement disease were taken into account.
Pneumococcal conjugate vaccines (PCVs) have substantially reduced the incidence of invasive pneumococcal disease caused by vaccine serotypes; however, replacement disease with non-PCV serotypes remains a concern. We describe the population effect of the seven-valent and 13-valent PCVs (PCV7 and PCV13) on invasive pneumococcal disease in England and Wales.
Using national invasive pneumococcal disease surveillance data for 2016/17, we compared incidence rate ratios (IRRs) against pre-PCV13 (2008/09–2009/10) and pre-PCV7 (2000/01–2005/06) baselines. We also estimated the number of invasive pneumococcal disease cases prevented since the introduction of PCVs.
In 2016/17, overall invasive pneumococcal disease incidence (9·87 cases per 100 000; 5450 cases) across all age groups was 37% lower (IRR 0·63, 95% CI 0·60–0·65) than pre-PCV7 incidence (14·79 per 100 000; 8167 cases) and 7% lower (0·93; 0·89–0·97) than pre-PCV13 incidence (10·13 per 100 000; 5595 cases). By 2016/17, PCV7-type invasive pneumococcal disease incidence across all age groups had decreased by 97% (0·24 per 100 000; 0·03, 0·02–0·04) compared with the pre-PCV7 period, whereas additional PCV13-type invasive pneumococcal disease decreased by 64% (1·66 per 100 000; 0·36, 0·32–0·40) since the introduction of PCV13. Invasive pneumococcal disease incidence due to non-PCV13 serotypes doubled (7·97 per 100 000; 1·97, 1·86–2·09) since the introduction of PCV7, and accelerated since 2013/14—especially serotypes 8, 12F, and 9N, which were responsible for more than 40% of invasive pneumococcal disease cases by 2016/17. Invasive pneumococcal disease incidence in children younger than 5 years remained stable since 2013/14, with nearly all replacement disease occurring in adults. We estimated 38 366 invasive pneumococcal disease cases were prevented in the 11 years since the introduction of PCV7.
Both PCV7 and PCV13 have had a major effect in reducing the burden of invasive pneumococcal disease in England and Wales; however, rapid increases in some non-PCV13 serotypes are compromising the benefits of the programme.
Public Health England.
Serious pneumococcal disease outbreak in men exposed to metal fume – detection, response and future prevention through pneumococcal vaccination
2017, Vaccine
Citation Excerpt :
Although not collected systematically, it was noted that a significant proportion complained of current or recent respiratory symptoms; 109 (16%) reported respiratory symptoms within the last 2 months. This is the first outbreak of IPD in the context of an oil rig or shipyard that we are aware of; others have been described in settings such as nursing homes, hospitals, military camps and prisons [18]. We demonstrated a common strain of serotype 4 pneumococcus in two of the confirmed cases, but distinct pneumococcal strains (one serotype 3 and one serotype 4) in two further cases.
Welders and those exposed to metal fume are known to be at increased risk of pneumococcal pneumonia and invasive pneumococcal disease. Current UK guidance recommends that vaccination against pneumococcus be considered in those at risk of frequent or continuous occupational exposure to metal fume, taking into account the exposure control measures in place. We report an outbreak of serious pneumococcal disease that occurred between April and June 2015 among a multinational workforce exposed to metal fumes while working on the refurbishment of an oil rig in a Belfast shipyard. Four confirmed and five probable cases were identified, which occurred despite the use of environmental control measures and the availability of respiratory protective equipment. To provide direct protection to those at risk of pneumococcal disease and to eradicate carriage of pneumococcus and interrupt transmission, pneumococcal polysaccharide vaccine (PPV23) and antibiotic prophylaxis were offered to 680 individuals identified as potentially exposed to metal fume. Low levels of prior pneumococcal vaccination were reported among this target group (<1%). Genomic sequencing indicated a common strain of serotype 4 pneumococcus in two of the confirmed cases and a distinct serotype 4 in one case. The fourth confirmed case was identified as likely serotype 3 using a serotype-specific immunoassay on a urine specimen. Both serotypes 3 and 4 are vaccine-preventable strains covered by the conjugate and polysaccharide pneumococcal vaccines currently available. We propose that consideration should be given to strengthening implementation around pneumococcal vaccination for those exposed to metal fume through their work, even when other control measures are in place, to reduce the risk of future cases and outbreaks of serious pneumococcal disease.
Pneumococcal Polysaccharide Vaccines
2017, Plotkin's Vaccines
Effective management in clusters of pneumococcal disease: A systematic review
2011, The Lancet Infectious Diseases
Citation Excerpt :
In the 11 clusters where an intervention was implemented within 48 h of the last cluster case, termination of the cluster might be attributable to the measures taken. In two clusters, reported by Cherian and colleagues32 and Carter and colleagues,35 the intervention was implemented at least 2 weeks after the last cluster case was identified, by which time further cases might have been unlikely to occur.13 In 21 clusters, case finding or data on surveillance in the closed settings were not reported after the last cluster case was documented.
Outbreaks of serious pneumococcal disease can occur with high attack rates in certain settings. We systematically reviewed studies of interventions implemented in pneumococcal clusters and those reporting the effect of antibiotics on carriage reduction to assess the effectiveness of interventions. Evidence was graded according to the Scottish Intercollegiate Guidelines Network system. Of 28 identified cluster reports, one showed that administration of antibiotics to close contacts reduced risk of pneumococcal disease. In three of four clusters where rifampicin chemoprophylaxis was used and in four of five clusters where penicillin was used no further cases were seen after intervention. In clusters where pneumococcal polysaccharide vaccine was used, subsequent cases occurred, all within around 2 weeks of vaccination, which suggests delayed benefit with this approach (evidence grade D). Use of infection control measures alone was reported in eight clusters, with no further cases being reported in seven (grade D). From 21 selected carriage studies, large carriage reductions were observed consistently with use of penicillin and azithromycin, with median values being 90% and 73%, respectively (grade C). The findings were presented to a working group for pneumococcal cluster guidelines and used to develop key recommendations on the management of clusters that supported prompt use of amoxicillin or azithromycin chemoprophylaxis, pneumococcal vaccination for close contacts, and implementation of infection control measures.

View all citing articles on Scopus

View full text

ReviewOutbreaks of serious pneumococcal disease in closed settings in the post-antibiotic era: A systematic review

Summary

Objectives

Methods

Results

Conclusion

Introduction

Section snippets

Methods

Results

Discussion

Acknowledgements

Lancet

J Hosp Infect

J Infect

Am J Prev Med

J Hosp Infect

Chest

J Hosp Infect

Am J Med

J Hosp Infect

J Infect

An epidemic of pneumococcus bronchopneumonia

J Infect Dis

Pneumococcic infections in families

J Clin Invest

A study of type 1 pneumococcus epidemic at the State Hospital in Worchester, Mass

Am J Public Health

A study of an outbreak of type II pneumococcus pneumonia in the Veterans Administration Hospital in Bedford, Massachusetts

Am J Hygiene

Epidemic of Streptococcus pneumonia and empyema at Camp Dodge, Iowa

JAMA

Further studies on the epidemiology of lobar pneumonia

J Exp Med

MMWR Morb Mortal Wkly Rep

1989

A nosocomial outbreak of Streptococcus pneumoniae infection

Commun Dis Rep CDR Wkly

Outbreak of pneumococcal disease in a Kansas nursing home

Kans Med

Outbreaks of pneumococcal pneumonia among unvaccinated residents of chronic-care facilities – Massachusetts, October 1995, Oklahoma, February, 1996, and Maryland, May–June 1996

MMWR Morb Mortal Wkly Rep

Pneumococcal cross-infection in hospitalized elderly patients

Br J Hosp Med

Type 8 pneumococcal pneumonia: an outbreak on an oncology ward

South Med J

Failure to control an outbreak of multidrug-resistant Streptococcus pneumoniae in a long-term-care facility: emergence and ongoing transmission of a fluoroquinolone-resistant strain

Infect Control Hosp Epidemiol

A outbreak of invasive pneumococcal disease in young children in child care

JAMA

Carriage of multidrug-resistant Streptococcus pneumoniae and impact of chemoprophylaxis during an outbreak of meningitis at a day care center

Clin Infect Dis

Pneumococcal cross infection in hospital

Br Med J (Clin Res Ed)

Hospital-related outbreak of infection with multidrug-resistant Streptococcus pneumoniae in the Netherlands

J Hosp Infect

An outbreak of type 1 pneumococcal pneumonia in a men's shelter

JAMA

Pneumococcal bacteraemia in mother and son

Br Med J (Clin Res Ed)

Review
Outbreaks of serious pneumococcal disease in closed settings in the post-antibiotic era: A systematic review