key: cord-0276673-4m8s84f0
authors: Henriot, P.; Castry, M.; Luong Nguyen, L. B.; Shimakawa, Y.; Jean, K.; Temime, L.
title: Risk of HCV infection associated with hospital-based invasive procedures: a systematic review and meta-analysis
date: 2021-11-05
journal: nan
DOI: 10.1101/2021.11.04.21265936
sha: f5f939840d188f9072d89ff5038f69986334cd1f
doc_id: 276673
cord_uid: 4m8s84f0

Background: Healthcare settings, where invasive procedures are frequently performed, may play an important role in the transmission dynamics of blood-borne pathogens when compliance with infection control precautions remains suboptimal. This study aims at better understanding and quantifying the role of hospital-based invasive procedures on hepatitis C virus (HCV) transmission. Methods: We conducted a systematic review and meta-analysis to identify recent studies reporting association measures of HCV infection risk that are linked to iatrogenic procedures performed in hospital settings. Based on expert opinion, invasive procedures were categorized into 10 groups for which pooled measures were calculated. Finally, the relationship between pooled measures and the country-level HCV prevalence or the Healthcare Access and Quality (HAQ) index was assessed in meta-regressions. Findings: A total of 71 studies were included in the analysis. The most evaluated procedures were blood transfusion and surgery (60 and 37 studies, respectively). The pooled odds ratio (OR) of HCV infection varied widely, ranging from 1.46 (95%CI: 1.14-1.88) for dental procedures to 5.86 (1.26-27.24) for haemodialysis. The OR for blood transfusion was higher for transfusions performed before 1998 (3.77, 2.42-5.88) than for those without a specified date (2.26, 1.81-2.81). Finally, the country-level overall risk for all procedures was significantly associated with HCV prevalence, but not with the HAQ index. In procedure-specific analyses, the HCV infection risk was significantly negatively associated with the HAQ for endoscopy and positively associated with HCV prevalence for endoscopy and surgery. Interpretation: Various invasive procedures were documented to be significantly associated with HCV infection. Our results provide a ranking of procedures in terms of HCV risk that may be used for prioritization of infection control measures, especially in high HCV prevalence settings. Funding: INSERM-ANRS (France Recherche Nord and Sud Sida-HIV Hepatites)

hospital settings. Based on expert opinion, invasive procedures were categorized into 10 groups for 20 which pooled measures were calculated. Finally, the relationship between pooled measures and the 21 country-level HCV prevalence or the Healthcare Access and Quality (HAQ) index was assessed in meta-22

regressions. 23

Findings: A total of 71 studies were included in the analysis. The most evaluated procedures were 24 blood transfusion and surgery (60 and 37 studies, respectively). The pooled odds ratio (OR) of HCV 25 infection varied widely, ranging from 1·46 (95%CI: 1·14-1·88) for dental procedures to 5·86 (1·26-26 27·24) for haemodialysis. The OR for blood transfusion was higher for transfusions performed before 27 1998 (3·77, 2·42-5·88) than for those without a specified date (2·26, 1·81-2·81). Finally, the country-28 level overall risk for all procedures was significantly associated with HCV prevalence, but not with the 29 HAQ index. In procedure-specific analyses, the HCV infection risk was significantly negatively 30 associated with the HAQ for endoscopy and positively associated with HCV prevalence for endoscopy 31 and surgery. 32

Interpretation: Various invasive procedures were documented to be significantly associated with HCV 33 infection. Our results provide a ranking of procedures in terms of HCV risk that may be used for 34

prioritization of infection control measures, especially in high HCV prevalence settings. 35

Introduction 74

Hepatitis C virus (HCV) is mainly a blood-borne virus associated with an estimated global sero-75 prevalence of 2·5%. 1 However, wide between-country discrepancies are observed, with Egypt and 76

Pakistan having high anti-HCV prevalence in the general population. 1 we conduct a systematic review and meta-analysis of the current evidence regarding the strength of 98 association between HCV infection and a wide array of hospital-based invasive procedures, in order to 99

propose a prioritization of iatrogenic procedures and better understand their role in HCV transmission. 100

Methods 102

Search strategy and selection criteria 103

We searched three online databases (PubMed, Web of Science, Scopus) for studies published between 104

January 2000 and December 2020 using the keywords "hepatitis", "risk factor", "hospital", and 105

"procedure" as main lexical fields (Suppl Table S1 ). This study was registered in PROSPERO in February 106 2021 (ID: CRD42021224886), and is reported according to PRISMA guidelines. 107

Studies were eligible if: (i) Exposure group was composed of hospitalized adults in-or out-patients; (ii) 108 they reported measures of association (odds ratios, ORs; risk ratios, RRs; or prevalence ratios, PRs) 109 between one or more health-care procedures and the risk of HCV infection (defined by detection of 110 either HCV RNA or HCV antibodies). This later criterion implies that studies had to include a comparison 111 group unexposed to these procedures. All study designs were allowed during study selection. 112

Studies were excluded if: (i) They were focused on paediatric patients, drug users, or blood donors 113 only, to avoid bias linked to either age-constraint or repetitive at-risk habits; (ii) patient inclusion 114 started before 2000; (iii) they were not written in French or English; (iv) they did not present original 115 results. 116

Based on the inclusion and exclusion criteria, articles titles and abstracts were screened by two 117 independent investigators (MC and PH) using the Covidence review tool. 14 Full-text articles were then 118 retrieved and assessed for eligibility by the same two authors. Any conflict in articles screening or full-119 text assessment were resolved by a third senior researcher (KJ or LT). 120

For each study, the following data were extracted by PH: (i) Total number of patients; (ii) patients type; 121

(iii) study design; (iv) measures of association and sample size of the control/exposed groups 122

After studies selection, the procedures reported were aggregated into 10 groups based on medical 124 expert opinion ( Table 1 ). Risk of blood borne infection was supposed to be homogeneous within these 125 groups. When two or more procedures classified in the same group were assessed within the same 126 study, a pooled group-level measure was computed using a fixed-effect model since these estimates 127

were calculated based on the same population. Measures associated with the same procedure but 128

reported across different populations (e.g., by gender) were considered independently. 129 Tooth extraction, dental anaesthesia, dental procedure, dental care, tooth filling 131

We performed a meta-analysis to compute pooled OR estimates of the risk of HCV infection associated 132

with each procedure using the R "meta" package. Measures that were not ORs (RRs and PRs) were 133 considered to be equivalent to ORs and included in the same analyses. When both adjusted ORs (AORs) 134

and crude ORs (CORs) were available in the same study, the AORs were preferred. If risk estimates 135

were available for dated and undated (without specified date) blood transfusion, estimates associated 136

with undated blood transfusion were preferred. 137

In a second step, pooled ORs for low HCV prevalence (< 5%) and high HCV prevalence (> %5) countries 138

were compared through subgroups analysis for each procedure group. Prevalence data for each 139 country were collected from the MapCrowd online global data on hepatitis C (Suppl Table S7 ). 15 Pooled 140

ORs were stratified by country for the 2 most represented procedure groups. 141 is the author/funder, who has granted medRxiv a license to display the preprint in (which was not certified by peer review) preprint

The copyright holder for this this version posted November 5, 2021. ;

Thirdly, the pooled OR for blood transfusion based on transfusions performed with either recent dated 142 an unspecified date of realization was compared to the one based on transfusions performed before 143 1998, which is the latest cut-off date used within selected articles. We assumed cut-off dates found in 144 the studies selected to reflect local implementation of mandatory HCV screening in blood donors. 145

In the last step of our analysis, meta-regressions were performed to investigate the potential effect 146 modifier of: (i) the HCV prevalence level, and (ii) the Healthcare access and quality (HAQ) index, a 0 to 147 100 score estimating the strength of healthcare quality and access based on amenable mortality data 148

in each country (Suppl Table S7 ). 16 149 Pooled estimates were computed using random effect models considering our aim to generalize results 150 beyond the selected studies. Each of these estimates was calculated together with the heterogeneity 151 level (I 2 statistics). 152

A bias analysis was conducted (by PH) on the articles included. Nine bias assessment criteria were 153 adapted from Lam et al. (2016c) 17 , and publication bias was assessed by testing for asymmetry in the 154 overall and procedure-specific funnel plots. 18 In addition, subgroups analyses were performed to 155 compare estimates between cohort and non-cohort studies. 156

The funder of the study had no role in study design, data collection, data analysis, data interpretation 158 or writing of the report. 159 is the author/funder, who has granted medRxiv a license to display the preprint in (which was not certified by peer review) preprint

The copyright holder for this this version posted November 5, 2021. ; https://doi.org/10.1101/2021.11.04.21265936 doi: medRxiv preprint Among the 1,961 initially identified studies, 71 were included in the review 18-89 , as described in the 165 flow diagram (Fig 1) . The total number of participants across all selected studies was 120,734. Pakistan (fourteen studies) and Egypt (nine studies) represented one third of all included studies 173 (Fig2.c). Over a fifth of studies were focused on haemodialysis patients (21·9%) (Fig 2.b) . Most studies 174

were cross-sectional (55%) or case-control (22·5%) studies (Fig 2d) . 175

Forty-five different procedures were assessed ( Table 1 ). The number of observations per each of the 176 ten procedure groups ranged from five to sixty, with surgery and transfusion as the largest groups 177

(respectively 37 and 60) (Fig. 3 is the author/funder, who has granted medRxiv a license to display the preprint in (which was not certified by peer review) preprint Overall, average estimates were always higher in high prevalence countries (Fig 6) , but a significant 209 difference was observed for endoscopy (Q=9·40, p-value=0·0022), surgery (Q=4·54, p-value=0·0331) 210 and injection (Q=5·40, p =0·0201) only. These results were supported by procedure-specific meta-211 regressions (Suppl Table S3 ) showing prevalence to have a significant positive effect on the OR level of 212 the endoscopy (p=0·004) and surgery (p=0·011) groups. Prevalence was also found to have a significant 213 . CC-BY-NC-ND 4.0 International license It is made available under a perpetuity.

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The copyright holder for this this version posted November 5, 2021. ; positive effect on the risk of iatrogenic HCV infection as a whole (p=0·031, Suppl Table S5 ). On the 214 contrary, no overall association was found between HAQ level and risk of iatrogenic infection, while in 215 procedure-specific analyses a negative significant impact of the HAQ level was observed for endoscopy 216 only (p=0·016, Suppl Table S4) is the author/funder, who has granted medRxiv a license to display the preprint in (which was not certified by peer review) preprint

The copyright holder for this this version posted November 5, 2021. ; https://doi.org/10.1101/2021.11.04.21265936 doi: medRxiv preprint For blood transfusions performed before 1998, 17 studies were selected for the pooled OR calculation, 225

whereas there were 48 studies available for undated blood transfusions (Suppl Fig. S3 and S4) Across all studies, bias was low for most criteria, but some studies presented a potentially high risk of 244 bias for criteria related to exposure assessment and to potential confounding (Suppl Fig.S1 and Suppl 245 Table S2 ). No single study had high bias risk for all criteria. Nevertheless, the overall funnel plot showed 246 asymmetry and the associated Egger test was highly significant, suggesting potential publication bias 247 (Suppl Fig. S2 ). 248

Average ORs in non-cohort studies were found to be higher than in cohort studies (2·37 CI 95% [2·04-249 2·75] vs. 1·92 [1·48-2·50]) but this difference was not significant (Q = 1·85, p = 0·17). Per-procedure 250

comparisons between cohort and non-cohort studies only showed a significant difference for the 251 transplantation (Q = 6·32, p = 0·012) and the injection (Q = 4·62, p = 0·032) group, for which cohort 252 studies was found to be associated with lower estimates. 253 254 . CC-BY-NC-ND 4.0 International license It is made available under a perpetuity.

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In this systematic review and meta-analysis, we identified 71 studies assessing the association between 256

hospital-based invasive procedures and the risk of HCV infection, representing a total of 120,734 257 participants. The overall strength of evidence remained of limited confidence as the bias analysis found 258 a lack of high-quality studies. Nevertheless, we estimated pooled ORs of HCV infection that were 259 significantly associated with most invasive procedures performed in hospitals. Our results suggest a 260 prioritization of iatrogenic procedures: haemodialysis was associated with the highest risk of HCV 261 infection whereas dental procedures and endoscopy were associated with the lowest risk. We also 262 underlined a large between-procedure and between-country variability, and showed that the per-263 procedure risk tended to be higher in countries with high HCV prevalence, while the level of healthcare 264 quality and access in the country (as measured by the HAQ) only appeared to play a minor role. 265

The geographical coverage of selected studies was in line with global observed prevalence levels, with 266 a third of these studies coming from the two countries with the highest HCV prevalence worldwide 267 (Egypt and Pakistan). In addition, the most represented population was composed of haemodialysed 268 patients, for which the risk of HCV infection is historically high. 90 Regrettably, only few studies used 269 cohort data. 270

The estimated per-procedure risks seemed to be mostly in line with the available literature concerning 271

HCV. Generally, the risk was higher for procedures with frequent blood-contact. 272

First, although the associated confidence interval was wide, the highest OR estimate was found for 273 haemodialysis. HCV transmission commonly occurs within patients of the same dialysis unit, especially 274 when there is low compliance to recommended hygiene measures and recurrent contact with blood. 90 275

In addition, the risk of HCV infection during this procedure is highly related to the duration of 276 haemodialysis. 91 We found injection to be one of the lowest at-risk procedures. Iatrogenic injection was described in 288 the past as associated with a high risk of HCV infection, in particular because of the reuse of 289 contaminated syringes, 8 but this risk might have dropped over the last decade, in particular after the 290 publication of multiple WHO and CDC guidelines for safe injections. 93 291 Finally, dental procedures and endoscopy were found to be the lowest risk groups, in line with current 292 literature findings. Indeed, only a few cases of HCV contamination after endoscopy have been 293 described and dental practices are often at low risk of contamination. 90, 94 This result is also consistent 294

with previous estimations showing low risk associated with these two procedures. 13 295 Country-level prevalence was overall found to be related to a higher risk of HCV contamination, 296

although it was only significantly associated with endoscopy and surgery risks when looking at specific 297 . CC-BY-NC-ND 4.0 International license It is made available under a perpetuity.

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The copyright holder for this this version posted November 5, 2021. ; https://doi.org/10.1101/2021.11.04.21265936 doi: medRxiv preprint procedures. The lack of significance for other procedures may be explained in several ways. First, many 298 countries were represented by less than 3 studies, leading to a lack of power for some procedures and 299 countries and less accurate OR estimates. Second, these non-significant associations may also indicate 300 the presence of other sources of heterogeneity. In particular, there may be high differences in terms 301 of prevalence between hospital settings within the same country. Observed between-country 302 variations may also result from different infection control practices; we explored this assumption using 303 the HAQ index, which is internationally validated and available for all countries in our analysis. 304

However, we found no significant relationship between the risk of getting HCV contaminated and this 305 index, except for the risk linked to endoscopy. First, the HAQ index may not be the right indicator to 306 accurately reflect compliance with infection control measures within hospitals. Second, there could be 307 a high heterogeneity in this compliance between settings within the same country, that this index is 308 unable to capture. 309

Our study carries several methodological as well as more study-related limitations. 310

First, no grey literature or papers in languages other than French or English were included in this 311 review, resulting in a potential information loss. Some other methodological simplifications could have 312 influenced our final results. In fact, pooling adjusted and non-adjusted measures could have led to 313 overestimation of risks associated with some procedures. Our results also highly depend on the initial 314 procedures classification we proposed, as homogeneity in terms of HCV infection risk cannot be 315 assured. In particular, some procedures within the "other procedures" group might not imply a blood 316 contact but this was not specified within selected articles. 317

This study highlighted several caveats in the existing literature. Bias analysis showed a lack of high-318 quality studies. On the one hand, 90% of studies presented at least a probably high bias concerning 319 the assessment of exposure to hospital-based procedures, mostly using questionnaires to collect risk 320 factors for HCV infection. This is consistent with the distribution of studies design, since almost 80% of 321 studies were either cross-sectional or case-control studies. This over-representation of non-322 longitudinal designs may in particular have led to overestimated ORs of HCV infection associated with 323 invasive iatrogenic procedures, due to differential recall bias between cases and controls. On the other 324 hand, more than 50% of studies included a potential risk of bias due to incomplete or missing use of 325 adjustment variables when estimating measures of association between HCV infection and iatrogenic 326

procedures. Overall, heterogeneity in measures associated with iatrogenic procedures was shown and 327 may reveal potential publication bias. In particular, non-significant risk measures might have been 328 voluntarily neglected resulting, again, in an overestimation of the risk associated with these two groups 329 of procedures. 330

For some procedure groups, only few data were available, which led to important uncertainty in the 331 associated OR estimates. Half of procedure groups had less than ten risk measures, wound care being 332 the procedure for which this number was the lowest with only five studies. Also, some procedures like 333 surgery might have described operations during which multiple systematic procedures were 334 performed and not taken into account (pre-surgical anaesthesia, …). More generally, we rarely had 335 access to measures of risks associated with a unique realization of each procedure. Patients might have 336 undergone the same procedure multiple times but this information was not taken into account. In 337 particular, as mentioned previously, the risk of getting HCV infected during haemodialysis is highly 338 related to the duration of haemodialysis and the risk related to blood transfusion is somehow is the author/funder, who has granted medRxiv a license to display the preprint in (which was not certified by peer review) preprint

The copyright holder for this this version posted November 5, 2021. ;

In addition, the date of realization of a procedure was not always available, and some measures might 342

have been based on procedures performed a long time ago, thus leading again to an overestimation 343 of the risk. Indeed, we found the pooled OR of blood transfusions performed before 1998 to be higher 344 than that of undated blood transfusions, strongly suggesting that the risk was higher for older 345

procedures -all the more so that the undated procedures could also have included old procedures. 346

In conclusion, despite the uncertainty in our estimates and the probable decrease in the general risk 347

of HCV infection through hospital-based procedures over the last twenty years, this work shows that 348 healthcare settings remain an important gateway of HCV infection and underline the importance of 349

implementing efficient infection control. 350

Our results suggest a risk-based ranking for iatrogenic procedures, haemodialysis being the most at-351 risk procedure, and confirm the important role of blood screening in decreasing the risk of HCV 352

infection. We also show that HCV infection risk tend to be higher in high prevalence countries. is the author/funder, who has granted medRxiv a license to display the preprint in (which was not certified by peer review) preprint is the author/funder, who has granted medRxiv a license to display the preprint in (which was not certified by peer review) preprint is the author/funder, who has granted medRxiv a license to display the preprint in (which was not certified by peer review) preprint

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This study was funded by INSERM-ANRS (France Recherche Nord and Sud Sida-HIV Hépatites), grant 384 number 12320 B115. 385