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Occupational Medicine Advance Access originally published online on January 3, 2006
Occupational Medicine 2006 56(2):122-128; doi:10.1093/occmed/kqj013
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© The Author 2006. Published by Oxford University Press on behalf of the Society of Occupational Medicine. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

Are endoscopy nurses at risk of infection with Helicobacter pylori from their work?

P. A. Noone1, E. R. Waclawski2 and A. D. Watt3

1 Occupational Health Department, Health Service Executive, Kells Road, Ardee, County Louth, Ireland
2 Argyll & Clyde Occupational Health Service, Dykebar Hospital, Grahamstown Road, Paisely PA2 7DE, UK
3 Greater Glasgow Primary Care Trust, Occupational Health Service, William Street Clinic, Glasgow G3 8HS, UK

Correspondence to: P. A. Noone, Occupational Health Department, Health Service Executive, Kells Road, Ardee, County Louth, Ireland; e-mail: noone.p{at}maile.HSE.ie


    Abstract
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Supplementary data
 Conflicts of interest
 References
 
Background In response to studies suggesting risk of occupational transmission of Helicobacter pylori (HP) to endoscopy staff, this cross-sectional study of seroprevalence to HP in gastroscopy nurses working in West of Scotland hospitals (an area of high endemicity of HP infection) was performed to determine if they were at excess risk relative to peers working in surgical specialities but without gastroscopy exposure. The study aimed to fulfil employer's duties to carry out a suitable risk assessment required by health and safety legislation.

Method This cross-sectional study compares the seroprevalence of HP in gastroscopy nurses and comparators drawn from orthopaedic and trauma units in 10 hospitals during 1998. A directly administered questionnaire collated exposure information on occupational and non-occupational risk factors for infection. Venepuncture was performed for latex agglutination test for IgG to HP. Confounding by socio-economic factors was controlled for by multivariate analysis.

Results Of the 222 participants, 74 were endoscopy staff (84% response) and 148 (59%) were comparators. Of these, 32.4% of gastroscopy and 33% of comparators were seropositive for HP (OR 0.97, P > 0.9, 95% CI 0.5–1.8). No association was found between gastroscopy exposure variables (frequency, years) or exposure to all endoscopy procedures and HP. Significant associations were found for age, childhood deprivation and greater number of siblings.

Conclusion No excess HP infection was found in gastroscopy nurses. Duties imposed by the health and safety legislation appear discharged by normal infection control procedures. Socio-economic factors are key determinants of HP status.

Keywords      Gastrointestinal endoscopy staff; HP; occupational infection


    Introduction
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Supplementary data
 Conflicts of interest
 References
 
Marshall first highlighted the role of Helicobacter pylori (HP) in peptic ulcer disease in 1983 [1] and HP was first classified by the International Agency for Research on Cancer as a Group 1 carcinogen in 1994, a definite cause of gastric adenocarcinoma in humans. Gastric cancer develops in ~1% of infected persons. Twenty per cent of those infected develop duodenal ulcers. Hansson et al. [2] argue that separate paths lead to these diseases and HP infection can lead to one or the other but seldom both. Other co-factors such as genetics of the host, genetics of the micro-organism itself or more importantly the time in life when the infection is acquired influence outcome of the infection. The mode of transmission of the organism is unclear and both oral–oral (or hand oral) and faeco-oral routes have been described. From the early 90s literature emerged the possibility of occupational acquisition of HP. A preliminary review of the literature revealed studies using polymerase chain reaction [3] techniques on isolates taken from patients and staff exposed to gastroscopy procedures. These studies identified common DNA sequences between patient and staff specimens, supporting the possibility of occupationally acquired transmission and spread of infection. Previous studies had reported an increase of HP infection in submarine crews and abattoir workers [4,5] with the possibility of person-to-person or zoonotic transmission but no such transmission in anaesthesiologists or dentists [6,7].

The high prevalence of infection with HP in the West of Scotland (60% for men and women over the age of 35 years) [7,8] was postulated to increase the risk of occupational exposure to gastroscopy staff.

A comprehensive literature search revealed contradictory evidence of risk, with increased transmission rates to gastroscopy nursing staff in some studies [914], but not in others [1317]. The literature suggested that risk was well established in gastroenterologists [1012,1822], although some studies found no evidence of occupational acquisition [16,17,2328]. Variation in study design including study power, selection or response of comparator group or failure to match for, stratify or correct by logistical regression for potential confounders or baseline occupational risk factors could account for some of the observed differences. Evidence suggests that gastroenterologists probably have a different baseline risk of infection relative to their nursing colleagues due to differences in the nature of their clinical exposure or socio-economic backgrounds [9,11,27].

Faced with inconclusive evidence as to the presence of a risk or not, we designed a cross-sectional study to estimate the seroprevalence of HP in gastroscopy nurses relative to nursing colleagues without gastroscopy exposure. Because HP is a common and ubiquitous organism, comparison between groups becomes meaningless unless possible confounding factors, notably age, socio-economic, baseline occupational risk and ethnicity, can be controlled. We aimed to collate data to control for major known or potential confounding factors including age, gender, socio-economic status, smoking and alcohol consumption. The study aimed to assess whether there was an excess risk of HP infection among gastroscopy nurses. A secondary aim was to fulfil the employer's duties for ‘a suitable and sufficient assessment of the risk arising out of or in direct connection with the work’ required under the health and safety legislation [29]. These UK regulations oblige the employer to evaluate the risk and control exposures of employees to hazardous substances in the course of their work.


    Methods
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Supplementary data
 Conflicts of interest
 References
 
A cross-sectional design was employed to compare seropositivity rates for IgG to HP in nursing staff working in 10 gastroscopy units in the West of Scotland to nursing colleagues working in surgical specialities in the same hospitals. Retrospective data on proxy exposure variables for HP were recorded (e.g. number of gastroscopy procedures assisted at per week, years of gastroscopy exposure, reported glove use, mask use, hand washing between cases).

The study population was all comparable nursing staff employed in gastroscopy units in the West of Scotland at the time of the study (1 January 1998 to 30 June 1998) (n = 88) identified from respective NHS Trust payroll/personnel record systems. Two comparators for each endoscopy nurse were recruited contemporaneously from volunteers in nursing staff working in orthopaedic wards, theatre, out-patients, trauma units or orthopaedic rehabilitation units within the same hospitals. The comparator group was identified from personnel system records. These nursing volunteers accounted for 59% (n = 295) of the target population of nurses working in these clinical areas. Those with previous gastroscopy exposure but not presently working in gastroscopy units were excluded from the comparator group (n = 6).

Study participants were invited to complete a questionnaire detailing socio-demographic characteristics, occupational and personal history or family history of gastrointestinal symptoms such as heartburn, ‘water brash’, indigestion, dyspepsia or previous history of HP. All participants provided a blood sample for serology to HP. The ethical committees of the Acute NHS Trusts in Greater Glasgow and Argyll and Clyde Health Boards granted ethical approval conditional on appropriate clinical follow-up for symptomatic seropositive subjects. The main outcome measures were the crude odds ratio (OR) which estimated the relative risk of HP seropositivity of subjects to the exposed or comparator group categories, proxy occupational exposure variables and other potential confounding factors from univariate statistical analysis. Adjusted ORs were derived using multiple logistic regression identifying variables independently associated with HP positivity. This allowed us to control for socio-economic exposure factors in childhood in the regression model.

A power calculation using Fleiss' method [30], assuming seropositivity in 45.5% of exposed and 25% of the comparator group, determined that 56 exposed and 112 unexposed individuals were needed to detect a difference of 15% in seroprevalence with 80% power with a target OR of 2.5 with 90% confidence, P = 0.05.

The questionnaire using mainly closed questions, apart from items requesting simple factual information, was based on questionnaires used in previous occupational studies and compiled from demographic factors such as age, gender, job category and personal habits (smoking, alcohol consumption) [928]. It was piloted among 10 nurses working in the occupational health units in Glasgow confirming the questions were well understood. Some minor changes were made resulting from the comments received to the categorization of ethnicity, the question on sharing a bed as a child and those detailing history of dyspepsia or HP in family members. Copies of the questionnaire were distributed with a consent form to individual participants in the study with a consent form for the provision of a blood sample for serological testing. A unique code number was allocated to each participant to ensure confidentiality and anonymity of returned questionnaire information. The primary investigator visited each clinical department to take a blood sample and administer the questionnaire to each participant. The investigator provided assistance or clarification to completing the questionnaire as necessary. The investigator was not blind to each participant's occupational status or exposure.

Occupational exposure variables explored included job category, number of endoscopy procedures per week, years of gastroscopy exposure, ‘ever versus never’ exposure to any endoscopy procedures, use of protective gloves, masks and aprons or reported hand washing practice between cases.

The socio-economic origins of both study groups were compared using the categorical variable ‘DEPCAT’ [31] based on the ‘Carstairs score’ for postcode for childhood and current residence. This variable provides a relative measure of deprivation which ranges from Categories 1 (most affluent) to 7 (most deprived). The score for each postcode is a summary of weighting of four variables: (i) overcrowding, (ii) male unemployment, (iii) low social class (head of household is in Social class 4 or 5) and (iv) proportion living in households without a car. Data on other factors known to increase the risk of infection in childhood, including increased numbers of siblings and sharing a bedroom or bed, were collated [3235].

Details on past or present symptoms of dyspepsia or peptic ulcer disease in self or family member were collated by the questionnaire to ensure those with a positive test and present or previous history of dyspepsia were referred for appropriate investigation and treatment if appropriate.

A latex agglutination test ‘Pyloriset Dry Test’ was used to detect HP IgG antibodies in the study population. The test performance indicators (MDA/96/89, Her Majesty's Stationery Office) are: sensitivity 64%, specificity 90% and positive predictive value 78% as compared to the rapid urease Campylobacter like organism (CLO) test and histology and culture for HP, which have a sensitivity of 95% and specificity of 96%. It has been shown that specificity has a greater effect than sensitivity on the overestimation of most population-based estimates of HP prevalence. Specific antibody to HP remains constant over time and reflects cumulative lifetime exposure, not necessarily current infection. The test compares favourably with other non-invasive tests [36].

Non-parametric tests and {chi}2 contingency table analysis were used to examine the relationship between HP status and proxy exposure nominal categorical variables.

The data were coded and entered into a Microsoft Excel spreadsheet. The HP IgG antibody test result was recorded (positive = 1, negative = 2) and linked to the participants' exposure details. The data were exported to SPSS version 7, and Epi-info v 6.01 statistical packages for univariate analysis. Logistic regression using JMP Statistical Discovery Software, version 4 (SAS Institute), was used to identify the independent risk factors associated with seropositivity in the study population. With HP status as the dependent variable, we identified factors independently predictive of HP status. Age, gender, occupational exposure, childhood DEPCAT score, current DEPCAT score, sharing bed in childhood, number of siblings, and family member with peptic ulcer disease or HP were included in the initial model. Factors significant at the 0.05 level were retained. Adjusted ORs and 95% confidence intervals (CIs) were calculated.


    Results
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Supplementary data
 Conflicts of interest
 References
 
A total of 74/88 (84%) gastroscopy nurses were recruited. Three exposed subjects who had been previously investigated and successfully treated were excluded from the study. Five staff were on holiday and three were on maternity leave on the days the investigator visited their respective hospital sites. Three employees declined to provide a blood sample and were excluded from the study.

One hundred and forty-eight controls were recruited from nurses working in surgical departments in the same hospitals.

Five study subjects with a positive test result and a history of undiagnosed dyspepsia were referred to a gastroenterologist for investigation and treatment as appropriate [36]. Study subjects with a positive test but without symptoms were advised to consult their general practitioner if they subsequently developed symptoms. This advice was in accordance with current evidence-based guidelines on the management of dyspeptic disease [36].

The comparator group was younger but not significantly younger than the exposed group, as indicated by the overlapping CIs for median age of the exposed [39.5 years (95% CI 37.4–41.6)] and control groups [36 years (95% CI 35.4–38.4)]. The age range of participants was 21–58 years in the exposed and 21–60 years in the comparator group. Twenty-one (9.5%) were male and 201 (90.5%) were female. No significant difference in the gender composition of exposed or comparator groups was found ({chi}2 Fisher's exact, P > 0.6, OR 1.26, CI 0.5–3.2). The study group was overwhelmingly Caucasian in origin, 220 (99.1%) to 2 (0.9%) non-Caucasian. No significant difference was found between those reporting past or present dyspeptic symptoms in the exposed or unexposed groups (OR 1.3, 95% CI 0.7–2.3, P > 0.4). Similarly, no difference was found between exposed and comparator groups in those reporting having a family member with peptic ulcer disease (OR 1.3, 95% CI 0.75–2.5, P > 0.38) or in those reporting having an immediate family member diagnosed with HP infection (OR 2.2, 95% CI 0.85–5.4, P > 0.16).

The exposed and comparator nursing groups were broadly similar in both current and childhood socio-economic background. The median DEPCAT score based on childhood postcode area was the same for both groups (4, intermediate affluence) with a mode of 5 (moderate deprivation) for the gastroscopy group and of 6 (deprived) for the comparator group (P > 0.3). The median and mode DEPCAT score for current postcode was 3 (less affluent) for the exposed group with a median score of 4 (intermediate) and a mode of 3 (less affluent) for the comparator group (P > 0.9).

The numbers of siblings reported by both groups were similar with a median number of two siblings for both with range 0–9 for the exposed group and 0–10 for the comparator group (P > 0.7).

The difference between numbers of nurses reporting sharing a bed in childhood in each group was statistically insignificant [exposed group 14/74 (19%), comparator group 34/148 (23%)] (P > 0.6, Fisher's exact test, OR 0.8, 95% CI 0.4–1.6). Similarly, no difference was found in those reporting sharing a bedroom in childhood in the exposed group (59/74, 78%) relative to the comparator group (120/148, 81%) (P > 0.9, Fisher's exact test, OR 0.9, 95% CI 0.46–1.8).

There was an association between increasing age and being positive for HP ({chi}2 for trend, 6.9, df 1, P < 0.008). No association was found between gender and HP status (OR 0.45, 95% CI 0.15–1.4, P > 0.16), living in a developing country (OR 1.12, 95% CI 0.4–3.2, P > 0.8) or ethnicity (P > 0.3).

Table 1 displays the cross-tabulation of proxy measures of gastroscopy exposure with serological status for HP. No association was found between reported gastroscopy exposure and HP status. No association was found for ‘ever’ exposure to endoscopy procedures (including bronchoscopy, endoscopic retrograde cholangiopancreatography, naso-endoscopy, other).


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Table 1. Occupational exposure and serological status for HP

 
Table 2 summarizes analysis for socio-economic factors and HP serological status. Associations were found for childhood postcode DEPCAT score, and social class based on Registrar General's OPCS Standard Occupational Classification (vol. 3, HMSO, 1991) based on parental occupation and seropositivity to HP.


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Table 2. Univariate analysis for socio-economic indicators and HP status

 
Multiple logistic regression was performed to control for confounding of occupational risk of acquisition by differences in socio-economic factors between or within the two groups. The factors predictive for HP seropositivity from the model are shown in Table 3. We found no evidence of interaction between deprivation score based on childhood postcode and number of siblings. These factors do not appear associated from the data from this study population. The wide CI on the OR for DEPCAT score based on childhood postcode reflects the small sample size.


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Table 3. Determinants of HP seropositivity (logistic regression model)

 
From the model, those categorized as ‘most deprived’ in childhood were 15 times more likely to be HP positive compared to those in the most affluent category (adjusted OR 15.0, 95% CI 3.0–107.0).

Those with more than two siblings were twice as likely as those who had two or less siblings to be HP seropositive (adjusted OR 2.1, CI 1.1–4.0). Those aged between 41 and 60 years were twice as likely as those aged between 21 and 40 years to be seropositive for HP (adjusted OR 2.0, CI 1.0–4.0).


    Discussion
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Supplementary data
 Conflicts of interest
 References
 
This cross-sectional study fails to find evidence of excess risk of being seropositive to HP for those working in gastroscopy units in the West of Scotland. The seroprevalence of HP in both groups is lower than previous population studies in this area of Scotland [8,37]. This may reflect differences in the age composition of study populations, ‘healthy worker effect’, lower sensitivity of the latex agglutination antibody test or combinations of these factors. Socio-economic factors particularly those pertaining to childhood appear most predictive of serological status in keeping with findings in previous community studies [3235] and the so-called ‘birth cohort phenomenon’.

The design provided a way of estimating the prevalence of the problem within the exposed population within a relatively short time period. Despite limitations of the cross-sectional design, the results permitted us to provide some reassurance to gastroscopy nurses working in an area of high population prevalence [8,37] for HP. We believe this is one of the first occupational studies to control for the effects of confounding by socio-economic exposure differences between the occupationally exposed and unexposed groups and our results bear testament of the importance of these factors as determinants of HP acquisition. Information bias was minimized by using a directly administered previously piloted questionnaire. This ensured consistency and accuracy of the exposure data collated. We believe blinding of the investigator was neither possible nor necessary to prevent bias in this regard.

Given persuasive evidence of risk in gastroenterologists [1014,1822], a difference in exposure risk appears to exist in these two gastroscopy staff groups. We postulate that differences in use of gloves, masks, aprons or hand washing by gastroscopy staff during these procedures could be a reason for the observed differences in risk between different gastroscopy staff groups found in previous studies. We cannot conclude from this study that differences in observed measures of occupational risk of infection with HP in gastroscopy nurses and gastroenterologists relate to differences in reported use of protective equipment such as gloves, masks or aprons or reported hand washing between cases. Other possible explanations for our negative findings include selection bias, Type 2 (ß) error, measurement bias or healthy worker effect. The response rate was high in the exposed study population (74/88, 84%) agreed to participate. The matching of two comparators to each gastroscopy nurse precluded against sufficient numbers to allow for selection of a randomized comparator group. This could result in systematic sampling error in either a positive or a negative direction. However, no significant association was found between the comparator group and having a personal or family history of dyspepsia or HP, so significant bias is unlikely or if present would be in the direction of Type 2 error. As serology is indicative of ever exposure and not just current infection with HP, any healthy worker effect will be equally distributed between the groups and significant confounding effect from general nursing exposure is unlikely. Even including the three gastroscopy employees with past treated HP would mean that differences between the exposed and comparator groups would not be significant. Exposure misclassification or reporting bias would only be significant if comparators failed to report past endoscopy work. Any failure of the latex agglutination test to identify all those with a past or present infection with HP would result in non-differential misclassification equally distributed between the two groups. The limitations of study design and power require caution in interpreting findings beyond the study population itself, but do provide some reassurance. Based on our results, they appeared to be at no excess risk of being seropositive to HP relative to their colleagues not exposed to these procedures. This supports the findings of previous work on this topic [1217]. Our findings replicate those in community studies carried out in different countries and continents [27,3235] and this provides some validation of the design, sampling strategy, selected outcome measures and measurements made.

Despite the limitations imposed by sample size (indicated by wide confidence limits in Table 3), this study suggests that having two or more siblings correlates with increased risk of acquisition of HP independent of measures of housing density or deprivation. This is consistent with previous studies of children in both developing and developed countries [33,34] where having greater numbers of siblings between the ages of 2 and 9 years and being of later order of birth correlates with increased risk. Deprivation is a composite variable that appears to be independently determinative for infection with HP.

Previous studies show gastroenterologists [1014,1822] to be at risk of HP infection from occupational exposure. Testing of their stored blood given for hepatitis B serology for HP status could be the basis of further study to estimate risk of infection in relation to endoscopy exposure.


    Supplementary data
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Supplementary data
 Conflicts of interest
 References
 
Appendix 1 (Multivariate model of Helicobacter pylori seropositive status cross-tabulated with independent predictor variables) is available as supplementary data at Occupational Medicine Online.


    Conflicts of interest
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Supplementary data
 Conflicts of interest
 References
 
None declared.


    Acknowledgements
 
We thank I. S. Symington of Glasgow Occupational Health and E. B. Macdonald of University of Glasgow. Particular thanks to K. Rice, Department of Public Health, North Eastern Health Board, Ireland, for multivariate analysis, and also those nurses and staff of the gastroscopy units, orthopaedic, trauma and out-patient departments who kindly participated in this study. Funding was provided from the Glasgow Occupational Health departmental research budget.


    References
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 Abstract
 Introduction
 Methods
 Results
 Discussion
 Supplementary data
 Conflicts of interest
 References
 

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