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Guideline for the Prevention and Control of Norovirus Gastroenteritis Outbreaks in Healthcare Settings, 2011

Evidence Table Q3 - Recovery of norovirus

Author, Yr (Ref) Study Design Quality Study Objective Population and Setting N Results Comments Ref ID_Data extracted by

Dalling, J; 2004 153

Systematic review

1,2,3,7

To identify if environmental contamination contributes to prolonged or recurring outbreaks and to clarify appropriate terminal cleaning measures.

Search of Health Electronic Resources Online in Northern England (HEROINE). Databases included Books@Ovid, MyOvid@Hand, journals@OvidFullText, Cochrane Database of Systematic Reviews, American College of Physicians Journal Club, DARE and CCTR, Allied and Complementary Medicine (AMED), Cumulative Index Nursing and Allied Health, EMBASE, PREMEDLINE and MEDLINE (1996 to present), British Nursing Index, and the National Research Register. Websites included the Department of Health, Public Health Laboratory Service, CDC, Infection Control Nurses Association, and the World Health Organization.

Search terms included (“Norwalk” OR “norovirus” OR “Winter Vomiting” OR “Viral gastroenteritis” OR  “SRSV” OR “Calicivirus”) AND (“Outbreak” OR “Management” OR “Environment” OR “Disinfect” OR “Decontaminate” OR “Decontamination” OR “Clean” OR “Contaminate” OR “Contamination” OR “Precautions” OR “Control”).

Limited to English language. Articles excluded if unrelated to viral gastroenteritis or environmental contamination; or focused on the source of infection (i.e., food borne gastroenteritis) or laboratory diagnosis techniques. References of articles reviewed to identify additional relevant articles. Articles critiqued using a tool adapted from Cormack.

11 articles.
5 articles included data from environmental sampling.

Transmission due to environmental contamination
Identified that environmental contamination occurred during outbreaks – 5/11 (55%)
Environmental contamination considered cause of transmission – 9/11 (82%)
Identified environmental contamination as cause of prolonged or recurring outbreaks – 0/11 (0%)

Environmental sampling
Identified environmental contamination – 3/5 studies
76/210 (36%) swabs positive from curtains, cushions, carpets, lockers, commodes, toilet rims, seats and handles, taps, basins, telephones, door handles, physiotherapy instrument handle, and horizontal surfaces above and below 1.5 meters including light fittings and mantelpieces.

Laboratory testing methods
Studies using RT-PCR – 100%
Two studies recognized that RT-PCR positive for norovirus does not necessarily represent viable virus.

Sampling methods
Methods of specimen collection
3/5 studies used saline or transport medium moistened swabs for sampling; 0%, 31%, and 42% samples were positive.
1/5 studies used dry swabs; 0% samples were positive.
1/5 studies used wet and dry swabs; 13% samples were positive.
There appeared to be more positive swabs in studies that used moistened swabs.
Timing of collection
Unclear in 3/5 studies whether swabs samples were collected before or after environmental cleaning.
Selection of sampling sites
4/5 studies did not explain why certain sites were swabbed and did not identify total swabs taken from each site.

Virus survival
1 study reported 21-28 day survival in a dried state at room temperature.
2 studies reported virus survival for at least 12 days; 1 paper repeated sampling and did not find virus in a previously contaminated environment after 5 months. 1 study suggested that carpets may have viable virus for at least 12 days that is not removed by routine vacuum cleaning.

Changing curtains
2 studies recommend changing curtains, but there is no evidence examining impact of curtain changes on duration or recurrence of outbreaks.

Carpet decontamination
3 studies advised steam cleaning of carpets but there is no evidence examining impact of steam cleaning on norovirus survival.
1 study recommended steam cleaning carpets and changing curtains as Category II “strongly recommended and viewed as effective by experts in the field and by the working group, based on strong rationale and suggestive evidence, even though definitive studies may not have been done.”
1 study identified carpets as a cleaning priority due to high levels of norovirus by RT-PCR.

Cleaning and disinfection
4 studies recommended and/or performed terminal cleaning.
3 papers recommended a cleaning or disinfectant agent; all recommended hypochlorite 1000 ppm.

Chadwick et al. recommendations based on Doultree et al. which recommended glutaraldehyde 0.5% and iodine 0.8%, but not 75% ethanol, quarternary ammonia 1:10 and anionic detergent 1%. Doultree et al. gives no reference for the recommendation.

2/5 studies that studied environmental sampling reported decontamination methods; both used 500 ppm hypochlorite, which is no longer advised in current guidelines.
0/5 studies evaluated the effectiveness of currently used disinfectants.

Specific areas for decontamination
4 studies listed recommendations including decontamination of frequently handled objects, taps, door handles, toilets and bathrooms, bath rails, toys, carpets, and surfaces contaminated by stools or vomit.
The only area recommended by > 1 study was bathrooms, despite 2 papers identifying by swabs contamination of both toilets and door handles.

Sample size and power not reported.

3958_IL

Wu, H; 2005 154

Prospective controlled study

1,3,4

To identify the likely mode of transmission,  characterize risk factors for illness, and evaluate for environmental contamination in a norovirus outbreak.

Residents and employees of a long term care facility in Philadelphia. 97% residents were male, median age 77 yrs (range 40-103), 87% had a cardiovascular or chronic pulmonary condition, 28% had a gastrointestinal disorder, 24% had diabetes and 70% had organic brain disease, dementia or a psychiatric disorder.

246 residents and 246 employees

Cases (follow up 41 days)
127 residents and 84 employees met the case definition.

Transfer to acute care hospital (follow up 41 days)
All results RR(95% CI) with non-case residents used as control
All case residents – 2.2(1.1-4.3)
Case-residents during the early period – 1.7(0.8-3.5)
Case-residents during the late period – 3.8(1.8-8.0)

Mortality  (follow up 41 days)
All results RR(95% CI) with non-case residents used as control
All case residents – 1.2(0.5-2.9)
Case-residents during the early period – 1.0(0.4-2.5)
Case-residents during the late period – 2.1(0.8-5.9)

Positive stool or vomitus samples (follow up 41 days)
All 8 stool samples and 1 of 3 vomitus samples from cases tested positive for norovirus

Environmental contamination (follow up 41 days)
10 samples tested, 5 positive and match clinical sample genotype
Positive swabs – toilet seat, dining room table, elevator button, bed rail, toilet seat and hand rails
Negative swabs – table, elevator button, handrail, wheelchair, bedrail, bedside table

Cases were defined as:
three or more occurrences of loose stools in a 24 hr period OR
one or more episodes of unexplained vomiting OR
a physician diagnosis of acute gastroenteritis

Stool/virus samples and environmental swabs were tested with RT-PCR

181 employees (74%) returned the surveys.
“Early period” was defined as symptom onset before or during the peak of the outbreak, while “late period” was defined as after the early period

Power and sample size not reported

406_RA

Jones, E; 2007 155

Descriptive study

1,2,3,4

To describe the role of fomite contamination during a norovirus outbreak

Participants in three consecutive 5-night educational boating trips. 36/54 were females. Study was conducted in Arizona, USA

54

Positive fomites
Bathroom surfaces – 5/6 (83%)
Kitchen surface samples – 2/5 (40%)
Doorknob samples – 3/3 (100%)

Samples of onboard potable water supplies were all negative

Random samples from interior boat surfaces and toilet reservoirs were collected by swabbing surfaces. norovirus was confirmed using RT-PCR. Stool samples were not available.

95_RA

Clay, S; 2006 156

Descriptive Study

3

To assess the survival of FCV on fomites. FCV was used as a surrogate.

Fomites – keyboard keys, computer mouse, brass disks (as a representative for water faucets or door knobs), telephone buttons, telephone receiver and telephone wire.

N/A

Time to 90% reduction in viral titer (hrs) (follow up 144 hr)
Keyboard keys – 0 to 4
Computer mouse – 0 to 4
Brass – 0 to 4
Telephone buttons – 12 to 24
Telephone receiver – 4 to 8
Telephone wire – 0 to 4

Time to undetectable virus (hrs) (follow up 144 hr)
Keyboard keys – 8 to12
Computer mouse – 24 to 48
Brass – 8 to 12
Telephone buttons – 48 to 72
Telephone receiver – 48 to 72
Telephone wire – 24 to 48

 

361_RA

Gallimore, C; 2006 157

Descriptive Study

1,3

To determine if gastroenteric viruses were present on surfaces and equipment. Environmental sampling was done using swabs and subsequent nucleic acid extraction and RT-PCR assays.

Swab sites in a pediatric primary immunodeficiency unit that were chosen to represent areas commonly in contact with hands. Three patients were also studied (two were patients with immunodeficiency < 1 month of age; one was a 4 yr old patient with lactose intolerance)

11 swab sites and 3 patients

Environmental swabs positive for norovirus (every 2 weeks during a 6 month period)
All results number of positive swabs/number of swabs taken for each swab site
Staff toilet door handle – 1/14
Staff toilet taps – 4/14
Telephone outside rooms 3 and 4  which contained the patients– 1/14
Microwave oven – 3/14
Room 4 outside flow syringe pump – 3/14
Room 3 outside flow syringe pump – 3/14
Parents’ phone – 5/14
Parents’ room door handle – 2/14
Game console – 1/14
Parents’ toilet door handle – 1/14
Parents’ toilet taps – 4/14

Recommendation: consider chlorine-based disinfectant for hard surfaces

norovirus detected in stool of patients with PCR (during a 6 month period)
norovirus was detected in the stool of 1 of the 3 patients

 

360_RA

Kuusi, M; 2002 158

Descriptive study

1

To conduct an epidemiological, environmental and virological investigation of an outbreak.  

Guests and staff at a rehabilitation center. Environmental samples were collected from water supply system, swimming pools, surfaces of 2 accommodation rooms with symptomatic guests, 2 sauna rooms, 2 bathrooms, 2 gym rooms, ultrasound treatment room, main entrance and restaurant.

280

Positive environmental samples (during ~1 month)
Ultrasound physiotherapy instrument’s handle
A bathroom door handle in a room of a symptomatic guest
A toilet seat in a room of a symptomatic guest
A toilet seat in a public toilet for women

The environmental strain was identical to the strain detected from patient samples. Water samples and swimming pools were negative.

 

Detected using RT-PCR

 

914_RA

Cheesbrough, J; 2000 159

Descriptive study

1,2,3,4

To investigate the pattern of norovirus contamination during and after an outbreak

Guests at a hotel in England. Demographic characteristics not reported.

144 environmental swabs

Positive fomites during outbreak (61/144)
All results positive fomites/total fomites; %
Carpet (known recent vomit) – 5/8; 62
*Carpet had been cleaned with detergent, water and then vacuumed prior to testing
Carpet (no known recent vomit) – 9/12; 75
Toilet rims or seats – 8/11; 73
Toilet handles, taps, basins and surfaces – 13/33; 39
Horizontal surfaces (outside toilet) below 1.5 m, e.g. tables, ledges – 11/29; 37
Horizontal surfaces (outside toilet) above 1.5 m, e.g. mantle piece, light fittings – 6/12; 50
Frequently handled objects, phones, door handles – 7/29; 24
Soft furnishings, cushions, curtains, etc – 2/10; 20

Post-outbreak follow-up (5 months after outbreak)
0/144 positive samples

norovirus was confirmed by RT-PCR

1098_RA

Schvoerer, E; 1999 160

Descriptive study

3

To describe an outbreak of norovirus gastroenteritis

Patients at a re-education ward of a hospital in France.

6

Symptoms
Nausea – 6/6
Vomiting – 2/6
Abdominal pain – 6/6
Fever – 2/6

Positive water samples
3/7 samples tested were positive for norovirus

Positive stool samples
3/6 samples tested were positive for norovirus

norovirus was confirmed using RT-PCR on stool samples

Outbreak was associated with contaminated drinking water

1280_RA

Green, J; 1998 161

Descriptive study

1,3

To describe a norovirus outbreak occurring in a hospital for the mentally ill

Patients and staff at a hospital for the mentally ill in the UK. The environmental sampling sites were all within dormitory 4, a bay in which symptomatic patients were cohort nursed.

28 patients and staff; 36 environmental swabs

Positive environmental samples
11/36(27%) environmental swabs collected on the affected ward were positive for SRSV on day 3 of outbreak.  The sites shown to be contaminated included lockers, curtains and commodes, all in proximity to symptomatic patients

norovirus in environmental samples was characterized using RT-PCR

1317_RA

Mattison, K; 2007 112

Basic Science Study

N/A

To assess virus survival in foods and on sufaces. FCV was used as a surrogate for norovirus to investigate its survival.

Food (lettuce, strawberry, ham) and metal surfaces. Study was conducted in Canada.

N/A

Survival of virus
At 30 min
Lettuce – 20%
Strawberry – 1%
Ham – 43%
Metal disk – 11%
At 7 days
There was a signifiant reduction in viral titer after 7 days for all samples at both room temperature (RT) and 4°C (P<0.05).

Comparison of virus survival at RT and 4°C (on day 7)
Lettuce – undetectable at RT; 1% survival at 4°C; statistical differences were not reported
Strawberry – undetectable at both RT and 4°C; survived for 5 days at 4°C, compared with 1 day at RT; statistical differences were not reported
Ham – P>0.05
Metal disk – P>0.05

Comparison of virus survival among the different samples
The survival on ham was significantly greater when compared to all other surfaces at both temperatures (P<0.05)

 

154_RA

D’Souza, D; 2006 162

Basic science study

N/A

To investigate the stability of norovirus on various food preparation surfaces and to evaluate the degree of virus transfer from these surfaces to a model ready-to-eat food (lettuce). Artificial contamination was done with: 1) norovirus, 2)  norovirus RNA, or 3) FCV.

Stainless steel, formica and ceramic coupons sterilized by autoclaving were used as the environmental surfaces

N/A

Detection of virus
1. norovirus
Could be detected on all 3 surfaces for up to 7 days post inoculation

2. norovirus RNA
Not detected on stainless steel beyond 24 hrs. Data for the other surfaces not reported

3. FCV
Could be detected on all 3 surfaces for up to 7 days post inoculation, with 6-7 log10 drop in virus titer over the 7 day period. There were no significant differences in recovery between the three surfaces tested (P>0.05). Statistically significantly higher recovery at time point 0 (P<0.05), but virus recovery at 1, 2, 4, 8 and 24 hours not significantly different from each other (P>0.05). Virus recovery at 24 and 48 hrs not significantly different from each other (P>0.05). Virus recovery at 7 days significantly lower from prior time points (P<0.05).

Virus transfer between stainless steel surfaces
All results are number of lettuce samples testing positive for norovirus at 10, 30 and 60 min virus drying time
Dry lettuce – 9/9; 0/9; 0/9
Wet lettuce – 8/9; 6/9; 7/9

Pressure applied to the samples did not have a statistically significant effect on transfer. Significantly higher transfer to wet lettuce (P<0.01).
For dry lettuce, the transfer at time 0 was statistically significantly higher than at times 30 and 60 min (P<0.05).
For wet lettuce, the transfer at time 0 was statistically significantly higher than at times 10, 30 and 60 min (P<0.05).

Virus recovery was evaluated by RT-PCR (for norovirus and norovirus RNA) or by plaque assay (for FCV) using feline kidney cells

337_RA

Paulson, DS; 2005 163

Basic science

Current food code requires food handlers to wear gloves when handling ready-to-eat food. The study objective was to evaluate the amount of virus transferred from contaminated surfaces to gloved hands.

 

A simulation study was performed to determine the amount of virus transferred from contaminated stainless steel surfaces, spatulas, forks, cutting boards, door knobs, and lettuce to vinyl food handler gloves.

Objects were inoculated with CaCV strain F9 viral suspension, and air dried for 5 or 15 minutes. A gloved fingertip was pressed lightly into the contaminated area for 5-10 seconds. The baseline viral load on the test items and the viral load recovered from gloved hands post-transfer were assessed.

Virus transferred
All results – Baseline; post-transfer recovery in virus log10 values
5 minute dry time
Average baseline – 5.9; post-transfer recovery – 4.7-5.4
Spatula – 5.9 ± 0.23; 5.4 ± 0.03
Lettuce – 5.9 ± 0.23; 5.1 ± 0.20
Fork – 5.9 ± 0.23; 5.3 ± 0.15
Cutting board – 5.9 ± 0.23; 5.3 ± 0.13
Door knob – 5.9 ± 0.23; 4.7 ± 0.07
Stainless steel coupon – 5.9 ± 0.23; 5.2 ± 0.11

15 minute dry time – All results virus log10 values
Average  baseline – 5.8; post-transfer recovery – 4.9-5.3
Spatula – 5.8 ± 0.31; 5.3 ± 0.15
Lettuce – 5.8 ± 0.31; 5.3 ± 0.04
Fork – 5.8 ± 0.31; 5.2 ± 0.23
Cutting board – 5.8 ± 0.31; 5.2 ± 0.09
Door knob – 5.8 ± 0.31; 4.9 ± 0.18
Stainless steel coupon – 5.8 ± 0.31; 4.9 ± 0.13

As few as 10-100 viral particles may be sufficient to cause infection so there is definite risk for transmission by food handlers wearing gloves. 

Remaining questions: 1) How long can norovirus remain on inanimate surfaces and still be infectious and 2) how much virus is transferred from gloved hands to food?

4356_IL

 

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