Endoscopy is not a risk factor for Helicobacter pylori infection—but medical practice is

Endoscopy is not a risk factor for Helicobacter pylori infection--but medical practice is Barbara Braden, MD, Li-Ping Duan, MD, Wolfgang F. Caspary, MD, Bernhard Lembcke, MD Frankfurt~Main, Germany

Background: Previous studies have suggested an increased risk for Heficobacterpylori infection in physicians who perform UGI endoscopy because of exposure to potentially infectious gastric secretions. Therefore, the H. pylori infection status of the endoscopy staff was compared with the H. pylori prevalence of medical staff without endoscopy experience and control subjects who had no contact with patients. Methods: The noninvasive 13C-urea breath test was performed in 2108 volunteers: 1460 physicians (mean age 44 + 12 years), 235 nurses (33 - 10 years), and 413 control subjects (43 +- 12 years) who were not working in clinical medicine. All subjects completed a questionnaire concerning the weekly frequency of gastroscopies and the duration of endoscopic experience. Results: Overall, 37.4% of the physicians and 35.3% of the nurses, but only 27.1% of the control subjects were infected. H. pylori infection was not significantly different between endoscopy-performing (37.8%; n = 1091) and general medical staff (35.9%; n -- 604). Neither the frequency of gastroscopies nor the duration of endoscopy practice correlated with H. pylori status. With respect to the age distribution; however, a statistically significant higher prevalence of H. pylori was observed in physicians and nurses compared with the 413 control subjects without patient contact (p < 0.01). Conclusion: UGI endoscopy is not a risk factor for H. pylori infection, but medical practice slightly raises H. pylori acquisition. (Gastrointest Endosc 1997;46:305-10).

Helicobacter pylori has been established as the cause of chronic gastritis and as an important etiologic factor for duodenal and gastric ulcer disease. Moreover, retrospective studies have linked H. pylori infection with an increased risk for gastric Received November 25, 1996. For revision February 3, 1997. Accepted June 11, 1997. From the Department of Internal Medicine II, Center of Internal Medicine, University of Frankfurt~Main, Germany. Results of the HARMONY Study (Helicobacter pylori Acquisition Risk in Medicine Or NurserY) Supported by the Else Kr6ner-Fresenius-Foundation (Oberursel, Germany) and by a substrate donation by ASTRA Chemicals GmbH (Wesel, Germany) and BykGulden (Konstanz, Germany). Parts of this study have been published in abstract form (Gastroenterology 1994;105:A). Reprint requests: Barbara Braden, MD, Internal Medicine II, University Hospital, Theodor Stern-Kai 7, D-60590 Frankfurt/ Main, Germany. Copyright © 1997 by the American Society for Gastrointestinal Endoscopy 0016-5107/97/$5.00 + 0 37/1/83922 VOLUME 46, NO. 4, 1997

carcinoma. 1-3 The epidemiology ofH. pylori infection reveals a close relationship of H. pylori prevalence with age, socioeconomic status, degree of education, and overcrowded living conditions. 4-~ The mode of transmission for H. pylori infection remains largely unknown. Person-to person transmission is likely, inasmuch as a higher prevalence of H. pylori infection is found in closed communities, v, s Based mainly on the detection of H. pylori antibodies, an increased risk of H. pylori infection has been suggested for endoscopists, but not for endoscopy nurses. 9'1° Because endoscopists and endoscopy nurses are likely to be exposed on a daily basis to contaminated gastric secretions from H. pyloriinfected patients, we conducted a prospective study of the prevalence of H. pylori infection in endoscopy personnel with reference to working conditions but adjusted for age and professional status. For epidemiologic studies of H. pylori, the noninvasive 13C-urea breath test 11 is a useful and appropriate diagnostic method t h a t is both practical and GASTROINTESTINAL ENDOSCOPY

305

B Braden, L Duan, W Caspary, et al. highly sensitive. Therefore, we used the 13C-urea breath test t h a t (in contrast to serology) reflects the current status of tested individuals with regard to the presence or absence of H. pylori infection. METHODS Subjects Volunteers (n = 2108) were investigated for H. pylori infection after having given informed consent. The noninvasive 13C-urea breath test was offered on a self-test basis to 2108 volunteers between September 1993 and April 1995. Participants were categorized as follows: 1460 physicians (mean age 44 ± 12 years), 235 nurses (33 + 10 years), and 413 subjects not working in clinical medicine (43 + 12 years) who served as controls. The latter group was comparable to the collective of physicians with regard to age, socioeconomic background, and level of education (i.e., engineers, physicists, biologists, pharmacologists, journalists, and attorneys). All participants completed a questionnaire concerning age, sex, contact with patients, the frequency of gastroscopies performed per week, duration of endoscopic experience in years, field of work, smoking habits, personal and family history of ulcers and dyspepsia, and the use of antibiotics during the last year. In a subgroup of 576 participants, we explicitly asked about the use of gloves during endoscopy. The 13C-urea breath test was performed as described previously (sensitivity of 98%; specificity of 88%). 12 Breath samples were collected before and 30 minutes after drinking a solution of 75 mg 13C-urea in 200 ml 0.1 n citric acid. The 13CO2/12CO2 abundance ratio in breath samples was analyzed by continuous flow isotope ratio mass spectrometry (Tracermass, Europa Scientific, U.K.). Results were expressed as delta per rail (%°).A delta over baseline is the difference between the ratio (13CO2/12CO) in the test specimen and the corresponding ratio in the baseline sample. A delta value greater than 5%° over baseline indicated H. pylori infection.13 Tests of significance in 2 × 2 tables were performed by the chi square test. Chi square contingency table analysis was used to examine the relationships between H. pylori status and endoscopy activity. Probability levels greater than 0.05 were considered to indicate no statistical difference (not significant). Odds ratios were calculated to describe the power of the potential risk factor. Logistic regression was used to evaluate the association of each independent variable of the study on the frequency of H. pylori infection with adjustment for age. RESULTS Among the 2108 volunteers enrolled (mean age 43 _+ 12 years; range 19 to 87 years), 741 (35.2%) were infected by H. pylori. Two h u n d r e d four (31.3%) of the 651 participating women (38 _+ 12 years) and 537 (37.0%) of the 1450 men (45 ± 12 years) had positive H. pylori 13C-urea breath tests (p > 0.05). Thus, the data are presented with gender merged.

306 GASTROINTESTINAL ENDOSCOPY

Endoscopy not a risk factor for H. pylori infection, medicalpractice is A strong correlation between H. pylori infection with age (p < 0.0001) was found, which also held true for all subgroups (p < 0.003 for physicians, p < 0.05 for nursing personnel, and p < 0.05 for controls). Age related prevalence was similar for men and women. The H. pylori prevalences in all subgroups are shown in Table 1. One thousand ninety-one individuals (age 43 _+ 11 years) were working in endoscopy units either as endoscopists (n = 922) or as endoscopy nurses (n = 169). Although H. pylori prevalence among endoscopy s t a f f w a s 37.8% (412 of 1091; age 43 _+ 11 years), 35.9% of medical personnel (physicians and nurses) who had contact with patients but were not working in endoscopy units had H. pylori infection (217 of 604; age 42 _+ 14 years). This difference is not significant, even when age is not considered (p = 0.49). The prevalence of H. pylori among endoscopist physicians was significantly higher t h a n in control subjects of similar age distribution. However, physicians who did not perform endoscopy also had higher H. pylori infection rates t h a n the controls. The respective odds ratios are given in Table 1. Figure i presents the H. pylori prevalence in endoscopists and physicians without endoscopy experience by age decades. A statistically significant difference between endoscopist and nonendoscopist physicians was detectable in none of the age strata. Similarly, endoscopy nurses did not differ in their H. pylori prevalence from general nurses of the s a m e age (Fig. 2). Similarly, an apparent increase of H. pylori infection rate with increasing frequency of endoscopies performed per week was not significant and disappeared after adjusting for age (p = 0.21; Table 2). The duration of endoscopy experience is closely related to age; therefore, personnel with more t h a n 20 years of endoscopy experience had a high prevalence of H. pylori infection (53.2%; 56 -+ 7 years of age) while in less experienced (< 5 years, and accordingly also younger) staff members, H. pylori infection was less frequent (23.3%; 32 _+ 6 years of age) (Table 3). Adjusting for age eliminates this difference (p = 0.13). Among the 576 participants asked about the use of gloves during endoscopy 87.6% answered t h a t they routinely wear gloves. Of the nursing personnel, 97.4% always wore gloves d u r i n g endoscopy and during cleaning of endoscopes. Of the physiclans, 87.6% r o u t i n e l y used gloves d u r i n g endoscopic practice. No association between the use of gloves and the prevalence of H. pylori infection was observed.

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Endoscopy not a risk factor for H. pylori infection, medical practice is

B Braden, L Duan, W Caspary, et al.

ES~[]Endoscepying physicians Nonendoscopying physicians [ ~ Controls

70

70

60

[Z]

Controls

60

50 c ©

EZZ] Endoscopy nurses Nonendoscopying nurses

..................

40

b ":':":':::~

50

~i~iii~iiii_ co

P 30 &

i

~///~ i:i:ii:!:ii:i:

40

o_

35

I

20 i .........

i

2O

lO 0

30

30-39

: i iii:ii

40-49 50-59 Age [Years]

i?!ii->60 :,,iiiiii

Figure 1. H. pylori prevalence in endoscopists and general physicians by age strata.

10 0

<30

30-39

40-49

Age [Years]

50-59

i

>60

Figure 2. H. pylori prevalence in endoscopy nurses and general nurses by age strata.

DISCUSSION

The strong correlation between age and H. pylori prevalence may be caused by two different mechanisms: an age effect (a longer life increases the chance to acquire the infection) or a cohort effect (the risk for infection was higher in former times). 14 Our data, derived from a one-time investigation (September 1993 to April 1995), can neither distinguish between these effects nor estimate their contribution to the prevalences observed in our study population. If a cohort effect is excluded by hypothesis, we calculate an annual infection rate of about 0.8% for medical personnel and of about 0.4% for persons without patient contact. The increasing prevalence with age is a well known feature of the epidemiology of H. pylori infection.4,5, 14 However, only a relatively small amount of clinically relevant information is available about the sources or the routes of transmission between subjects. High prevalence rates in children from developing countries or in overcrowded populations suggest person-to-person transmission. 6 Gastroscopy units are unique settings in which there exists a high degree of contact with gastric secretions bearing a potential risk of infection. Dentists do not have an increased risk of H. pylori infection despite exposure to patients' saliva, i5 Serologic studies by Mitchell et al., 9 Lin et al., 1G and Chong et al. 17 and p r e l i m i n a r y d a t a from a Swiss group using the i3C-urea b r e a t h t e s t l° indicated t h a t endoscopists are at a n increased risk for H. pylori infection, w h e r e a s contradictory results are reported by Morris et a l } s and Pristautz. 19 We found an increased risk for physicians who perform endoscopy compared with control subjects not working in the field of medicine. Both groups

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were comparable with regard to age, education level, and socioeconomic status. This higher risk, however, was not related to endoscopy as the potential source of infection because the difference in H. pyloripositive breath tests was not significant compared with other physicians not performing endoscopy. Similarly, after adjusting for age, nurses showed an increased risk for H. pylori infection compared with controls of similar age. Our results concerning nurses in general are thus in agreement with the study ofWilhoite et al. 2° However, endoscopy nurses did not show higher H. pylori infection rates in comparison with nursing personnel outside of endoscopy units. The great majority of the endoscopy staff now use gloves during gastroscopy. Comparing the H. pylori status of these subjects to the infection rate in the small group of endoscopy personnel that does not wear gloves does not disclose significant differences. To our knowledge, our study evaluated the largest number of medical staff, endoscopists, and endoscopy nurses, physicians who do not practice endoscopy, and nonendoscopy nurses thus far tested for H. pylori infection. To demonstrate an increased risk for endoscopy personnel by virtue of occupational exposure during endoscopy, the prevalence of infection should be compared in this group to the infection rates in other medical colleagues and not just to nonmedical controls. This was done by Lin et al., 16 who compared the H. pylori prevalence in 37 practicing gastroenterologists (68%), 25 general physicians (40%), and control subjects (32%). Our results in larger cohorts (which are necessary to exclude the strong age effect) demonstrate an increased H. pylori prevalence in medical staff generally, but this is not related to endoscopy activity. Therefore, our

GASTROINTESTINAL ENDOSCOPY

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B Braden, L Duan, W Caspary, et al.

Endoscopy not a risk factor for H. pylori infection, medical practice is

Table 1. H. pylori (HP) infection rates, relative risk, and odds ratio in endoscopy personnel, general medical staff, and controls (*adjusted for age) Subjects

n

HPpositive

Prevalence (%)

Relative risk

95% CI

Odds ratio

95% CI

p

Physicians Controls Physicians Nurses* Medical Staff Controls Endoscopy physicians Nonendoscopy physicians Endoscopy physicians Controls Nonendoscopy physicians Controls Endoscopy nurses Nonendoscopy nurses Endoscopy nurses* Controls Nonendoscopy nurses* Controls Endoscopy staff Nonendoscopy medical staff Endoscopy staff Controls Nonendoscopy medical staff Controls

1460 413 1460 235 1695 413 922 538 922 413 538 413 169 66 169 413 66 413 1091 604

546 112 546 83 629 112 350 196 350 112 196 112 62 21 62 112 21 112 412 217

37.4 27.1 37.4 35.3 37.1 27.1 38.0 36.4 38.0 27.1 36.4 27.1 36.7 31.8 36.7 27.1 31.8 27.1 37.8 35.9

1.38

1.17-1.62

1.61

1.26-2.04

0.0001

0.98

0.82-1.16

0.96

0.73-1.28

0.24

1.337

1.16-1.61

1.59

1.25-2.01

0.0002

1.04

0.91-1.20

1.07

0.86-1.33

0.60

1.40

1.18-1.66

1.64

1.28-2.12

0.0002

1.34

1.11~1.63

1.54

1.17-2.04

0.0003

1.15

0.77-1.72

1.24

0.68-2.28

0.58

1.48

1.15-1.90

1.80

1.24-2.63

0.003

1.40

0.97-2.01

1.64

0.96-1.64

0.09

1.05

0.92-1.19

1.08

0.88-1.33

0.49

1091 413 604

412 112 217

37.8 27.1 35.9

1.39

1.17-1.65

1.63

1.27-2.09

0.0001

1.32

1.10-1.60

1.51

1.14-1.98

0.004

413

112

27.1

*Adjusted for age.

Table 2. H. pylori (HP) status in endoscopy personnel in relation to the frequency of gastroscopies performed per week UGI endoscopies

Physicians

per week (n)

HP-positive/n (%)

0 1-10 11-20 >20 Total

196/547 (35.8) 204/534 (38.2) 57/159 (35.9) 89/220 (40.5) 546/1460 (37.4)

Nurses Age (y) 44 46 45 47 44

± 14 _+ 10 _+ 10 ± 10 ± 12

Total medical personnel

HP-positive/n (%)

Age (y)

21/66 (32.3) 3/10 (30.0) 22/61 (33.3) 37/98 (37.8) 83/235 (35.3)

32 31 34 36 34

± ± ± ± ±

11 8 9 9 9

HP-positive/n (%) 217/613 (35.4) 207/544 (38.1) 79/220 (39.1) 126/318 (39.6) 629/1695 (37.1)

Age (y) 42 44 43 47 42

± 14 ± 12 -+ 10 ± 10 ± 12

Table 3. H. pylori (HP) status in endoscopy personnel in relation to the duration of gastroscopy practice Duration of work in endoscopy (y) <5 5-10 11-20 >20 Total

308

Endoscopy physicians HP-positive/n (%) 26/139 61/215 115/289 148/279 350/922

(18.7) (28.4) (39.8) (53.1) (37.9)

GASTROINTESTINAL ENDOSCOPY

Endoscopy nurses

Age (y) 32 37 44 56 45

± 6 ± 6 ± 5 ± 7 _+ 10

HP-positive/n (%) 33/114 (28.9) 14/28 (50.0) 12/22 (54.6) 3/5 (60.0) 62/169 (36.7)

Endoscopy personnel

Age (y) 31 37 43 48 35

± 7 _+ 7 ± 8 ± 7 ± 9

HP-positive/n (%) 59/253 (23.3) 75/243 (30.9) 127/311 (40.8) 151/284 (53.2) 412/1091 (37.8)

Age (y) 32 37 44 56 43

± 6 ± 7 ± 6 ± 7 -+ 11

VOLUME 46, NO. 4, 1997

Endoscopy not a risk factor for H. pylori infection, medical practice is r e s u l t s do not c o n t r a d i c t t h e objective r e s u l t s of f o r m e r studies t h a t g a s t r o e n t e r o l o g i s t s h a v e h i g h e r H. p y l o r i p r e v a l e n c e s t h a n control subjects w i t h o u t p a t i e n t contact. B u t on the basis of findings in t h e n o n e n d o s c o p y m e d i c a l staff, we i n t e r p r e t this h i g h e r infection r a t e in e n d o s c o p i s t s as not n e c e s s a r i l y c a u s e d by t h e i r endoscopic activity. P a r a l l e l s b e t w e e n t h e d i s t r i b u t i o n of H. p y l o r i p r e v a l e n c e s a n d of poliomyelitis a n d h e p a t i t i s A v i r u s infection w o r l d w i d e s u g g e s t a fecal-oral r o u t e of transmission. 21 I m p r o v e m e n t s in s a n i t a t i o n a n d

socioeconomic status resulted in a marked reduction of these infections. Our findings of higher H. pylori infection rates in personnel with contact to patients in general but not additionally in personnel with explicit exposure to gastric secretions during endoscopy indirectly supports the hypothesis of a fecaloral route of transmission, which has also been supported by the recent isolation of H. pylori from human feces. 22 Other arguments for a fecal-oral route of transmission include the long viability of H. pylori in water 23 and the results of a case-control study in Peru that point to water as a vehicle for H. pylori infection. 24 The possibility of an oral-oral route of transmission is supported by the fact that H. p y l o r i is d e t e c t e d in d e n t a l plaque. 25, 26 B o t h r o u t e s m a y possibly coexist. F u r t h e r i n v e s t i g a t i o n s to isolate 1t. p y l o r i f r o m h a n d s , feces, a n d environm e n t a l surfaces are r e q u i r e d to r e v e a l t h e mode of t r a n s m i s s i o n . B e c a u s e m o s t endoscopists performing g a s t r o s c o p y in G e r m a n y also p e r f o r m colonoscopy, our r e s u l t s c a n n o t differentiate b e t w e e n t r a n s m i s s i o n routes. O u r findings i n d i c a t e t h a t b o t h professional activities as a p h y s i c i a n or n u r s e in m e d i c a l practice a n d t h e c i r c u m s t a n c e of w o r k i n g in h o s p i t a l s c a r r y a small b u t d e m o n s t r a b l e a d d i t i o n a l "risk" to acquire H. p y l o r i infection. I n conclusion, t h e e x p o s u r e to g a s t r i c secretions a t e n d o s c o p y does n o t i n c r e a s e t h e risk for H. p y l o r i infection. B e c a u s e p h y s i c i a n s a n d n u r s e s show h i g h e r H. p y l o r i infection r a t e s t h a n control subjects, c o n t a c t w i t h p a t i e n t s d u r i n g clinical w o r k could be a risk factor.

ACKNOWLEDGMENTS The a u t h o r s w i s h to t h a n k Mrs. N. B u l g u r , A. Schmitt, M. D a d n i a , U. Bieniek, K. Severin, K. RuhSfer, a n d D. K r e u z for t e c h n i c a l a s s i s t a n c e a n d Prof. Dr. R. Hilgers ( D e p a r t m e n t of Medical Statistics, U n i v e r s i t y of G 6 t t i n g e n , FRG) for his help w i t h the statistical e v a l u a t i o n . We are f u r t h e r i n d e b t e d to all colleagues, n u r s e s , a n d o t h e r v o l u n t e e r s who e n a b l e d us to c o n d u c t this s t u d y b e c a u s e of t h e i r

VOLUME 46, NO. 4, 1997

B Braden, L Duan, W Caspary, et al. own scientific curiosity. L.P. D u a n is a r e s e a r c h fellow with the Alexander yon H u m b o l d t Foundation.

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Endoscopy not a risk factor for H. pylori infection, medical practice is

21. Szmuness W, Dienstag JL, Purcell RH, Stevens CE, Wong DC, Ikram H. The prevalence of antibody to hepatitis A antigen in various parts of the world: a pilot study. Am J Epidemiol 1977;106:392-8. 22. Kelly SM, Pitcher MCL, Farmery SM, Gibson GR. Isolation of Helicobacter pylori from feces of patients with dyspepsia in the United Kingdom. Gastroenterology 1994;107:1671-4. 23. Shahamat M, Mai U, Paszko-Kolva C, Kessel M, Colwell RR. Use of autoradiography to assess viability of Helicobacter pylori in water. Appl Environ Microbiol 1993;59:1232-5. 24. Klein PD, Graham DY, Gaillour A, Opekun AR, Smith EO.

Water source as risk factor for Helicobacterpylori infection in Peruvian children: Gastrointestinal Physiology Working Group. Lancet 1991;337:1503-6. 25. Nguyen AMH, Engstrand L, Genta RM, Graham DY, E1Zaatari FAK. Detection of Helicobacter pylori in dental plaque by reverse transcription-polymerase chain reaction. J Clin Microbiol 1993;31:783-7. 26. Banatvala N, Romero LC, Owen RJ. Use of the polymerase chain reaction to detect Helicobacter pylori in the dental plaque of healthy and symptomatic individuals. Microb Ecol Health Dis 1994;7.'1-8.

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