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Evaluation of the German surveillance system for hepatitis B regarding timeliness, data quality, and simplicity, from 2005 to 2014
Public Health 180 (2020) 141e148
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Original Research
Evaluation of the German surveillance system for hepatitis B regarding timeliness, data quality, and simplicity, from 2005 to 2014 L. Boes a, 1, C. Houareau a, b, 1, D. Altmann a, M. An der Heiden a, V. Bremer a, M. Diercke c, S. Dudareva a, A. Neumeyer-Gromen a, R. Zimmermann a, * a
Robert Koch Institute, Department for Infectious Disease Epidemiology, Unit for HIV/AIDS, STI and Blood-borne Infections, Robert Koch Institute, Berlin, Germany Charit e University Medicine, Berlin, Germany c Robert Koch Institute, Department for Infectious Disease Epidemiology, Surveillance Unit, Robert Koch Institute, Berlin, Germany b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 15 May 2019 Received in revised form 4 October 2019 Accepted 12 November 2019
Objectives: Germany has a mandatory surveillance system for acute hepatitis B (AHB) with the Protection against Infection Act as the legal basis in place since 2001. An amendment was introduced in 2013. We aimed at evaluating the surveillance systems' performance regarding timeliness, data quality, and simplicity from 2005 to 2014 and at assessing the effect of the amendment on timeliness of AHB surveillance. Study design: This study is a trend analysis of surveillance data. Methods: Aspects of simplicity versus complexity of the surveillance system were assessed by describing data flow, levels of reporting, and data management procedures. Data quality, in terms of data completeness, was evaluated by quantitative indicators, and timeliness was measured in days between different levels of the surveillance system, notification delay, and reporting delay. Trends over time in data quality were analyzed by logistic regression, while negative binomial regression was used to test for trend over time regarding mean notification and reporting delay. Results: Between January 2005 and December 2014, a total of 22,549 AHB infections were reported at the national level. The data flow of the German AHB surveillance system showed structural characteristics of a complex system. Over the 10-year period, completeness of reporting sex, age, probable route of transmission, and hepatitis B virus (HBV) vaccination were 99%, 100%, 25%, and 73%, respectively. However, data quality decreased over the evaluation period. Although notification delay improved over time (incident rate ratio [IRR] ¼ 0.95, 95% confidence interval [CI] ¼ 0.95e0.96; P < 0.05), reporting delay improved only since the amendment (IRR ¼ 0.76, 95% CI ¼ 0.70e0.82; P < 0.05). In total, mean notification and reporting delay were 3.0 days and 14.3 days, respectively. Conclusions: The German AHB surveillance system is operating in a timely manner. Although timeliness improved over the evaluation period and the amendment to the Protection against Infection Act succeeded in reducing reporting time, data quality in terms of completeness of information decreased considerably. As improved data completeness is required to adequately design prevention activities, reasons for this decrease should further be explored. © 2019 The Royal Society for Public Health. Published by Elsevier Ltd. All rights reserved.
Keywords: Acute hepatitis B HBV Surveillance Evaluation Timeliness Data quality
Introduction The global prevalence of chronic hepatitis B virus (HBV) infection was estimated to be 3.5% in 2015, with 257 million people living with chronic infection.1 Results of the German Health * Corresponding author. Robert Koch Institute Department for Infectious Disease Epidemiology Seestr. 10 13353 Berlin Germany. Tel.: þ49 30-18754-3801; fax: þ49 30-18754-3533 E-mail address: [email protected] (R. Zimmermann). 1 These authors share first authorship.
Examination Survey from 2008 to 2010 indicated a low prevalence of acute or chronic HBV infection of 0.3% in the general population, while 5.1% of the population had had previous exposure to HBV.2
Description of the German surveillance system The legal basis for the control of infectious diseases in Germany, the Protection against Infection Act (Infektionsschutzgesetz [IfSG]), came into effect in 2001.3 An electronic reporting system and
https://doi.org/10.1016/j.puhe.2019.11.012 0033-3506/© 2019 The Royal Society for Public Health. Published by Elsevier Ltd. All rights reserved.
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database for surveillance of notifiable infectious diseases (SurvNet@RKI) was created.4 Since then, cases of infectious diseases are electronically reported from local public health authorities (LPHAs) to state health authorities (SHAs) to national public health authorities. The Robert Koch Institute (RKI), the national public health institute, publishes case definitions (CDs) for notifiable diseases to be applied by the LPHAs. Furthermore, specific reference case definitions (RCDs) are applied by the RKI before publication of the notified data. According to the IfSG, acute hepatitis B (AHB) is a notifiable disease. Objectives of the national infectious disease surveillance system for AHB are as follows: (1) to detect trends in the incidence of AHB; and (2) to provide reliable information for implementation and modification of evidence-based prevention strategies to prevent further disease transmission.5 IfSG amendment The 2011 verotoxic Escherichia coli O104:H4 outbreak in Germany emphasized the necessity of a rapid surveillance system.6 An amendment to the IfSG introduced on March 29, 2013, aimed at decreasing reporting time within the German surveillance system.7 Since then, LPHAs and SHAs are requested to report all notifiable infections within one working day to the next level. A recent analysis showed that the amendment decreased overall reporting time without relevant loss of data quality.8 Objectives of the evaluation Thus far, neither the HBV surveillance system nor the impact of the amendment to the IfSG in 2013 on HBV surveillance has been assessed. Owing to relevant changes in the CDs for AHB in 2015, we evaluated the surveillance system over the ten-year period preceding these changes with regard to aspects of simplicity of the system, data quality (in terms of completeness), and timeliness.9 Methods Case definitions CD for AHB The CD of AHB included laboratory and clinical criteria. The laboratory criteria for confirmation of AHB were either a positive polymerase chain reaction for hepatitis B nucleic acid (HBV-DNA) or the detection of IgM hepatitis B core antibodies (anti-HBc IgM) or hepatitis B surface antigen (HBsAg) with a confirmatory test. The clinical criteria were defined as the presence of at least one of the following criteria: jaundice, elevated levels of serum transaminases, or upper abdominal pain. All cases with laboratory confirmation with, without or with unknown clinical criteria, were reported to the RKI. HBV cases classified as chronic do not fulfill the CD.
from the national surveillance database at the RKI, as of March 1, 2015. Simplicity To assess aspects of simplicity or complexity of the surveillance system, the flow of data including reporting structure, levels of reporting, and data management in the German HBV surveillance system was described by integrating information gathered from system documents and publications (Fig. 1).4,9,10 We followed the Centers for Disease Control and Prevention (CDC) guidelines for evaluating public health surveillance systems9 to determine simplicity/complexity of the system by assessing the chain of reporting (single versus dual chain of reporting) and methods of data entry and management (electronic versus manual data entry and electronic transfer versus telefax). A system is considered simple in design if it has a single reporting structure within a complete electronic notification system and few levels of reporting.9 Data quality We assessed data quality in terms of completeness of surveillance data. As indicators for completeness, we defined the following key variables: sex, age, probable routes of transmission, and vaccination status of all reported AHB infections. The variables sex and age were considered as complete if the respective sex or age of the person was specified. Information on probable routes of transmission was considered as complete if at least one route of transmission was specified. Completeness of information on HBV vaccination status was achieved if it was specified as information available: ‘yes’ or ‘no.’ Timeliness of HBV notifications We defined two time periods to evaluate timeliness: 1. The time period from the date of diagnosis by a physician or a laboratory until the date of notification to the responsible LPHA (defined as: notification delay) 2. The time period from the date of notification to the LPHA until the date of reporting to the RKI (defined as: reporting delay) For both time periods, a minimum delay of zero days was accepted for analysis. A maximum notification delay of 21 days and a maximum reporting delay of 91 days were considered as plausible and accepted for analysis. Cases were only included in the evaluation of timeliness if valid notification and reporting dates to the LPHAs and to the RKI were available. Median and mean of both time periods are reported including interquartile range (IQR) and standard deviation (SD).
Reference case definition Among all cases fulfilling the CD for AHB, from 2005 to 2014, only cases fulfilling both laboratory and clinical criteria were analyzed at the national level and published in official statistics (RCD) according to the reference definition.
Influence of the amendment to the law in 2013
Data selection
Statistical analysis
We included all laboratory-confirmed cases of AHB reported to the RKI from January 2005 to December 2014. Data were extracted
Trends over time in data quality and the RCD were tested by logistic regression. The results of logistic regressions were reported
The influence of the amendment to the IfSG was assessed by comparing reporting delay for the period before the amendment and reporting delay since the amendment in 2013.
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Fig. 1. Flow chart and levels of reporting of the hepatitis B surveillance system.
in odds ratios (ORs) with 95% confidence intervals (CIs). The independent variable was the year of reporting to the RKI. However, for mean reporting and notification delay, negative binomial regression was used to test for trend over time. The independent variables were the year of notification to LPHAs or the year of reporting to the RKI, respectively. To analyze changes in mean reporting delay since the amendment, we also included the independent variable, year of notification since the amendment in 2013, as well as a constant for year of notification since the amendment, and a binary RCD variable. We also included an interaction of the RCD and the constant for the year of notification to analyze changes in mean reporting delay for the RCD since the amendment. The results were reported as incident rate ratios (IRRs) with 95% CI. The significant contributions to the model of all tests were reported in P-values. P-values <0.05 were considered statistically significant.
All analyses were performed using STATA® 15.1 (StataCorp LP, College Station, TX, USA). Results Simplicity Data flow in the surveillance system The surveillance system for HBV infection consists of multiple levels of reporting: all newly diagnosed AHB infections, regardless of the clinical picture, should be notified by name from the treating physician and the laboratory to the responsible LPHA (dual reporting), followed by anonymized reporting from the LPHA to the SHA, and from there finally to the RKI (multiple levels of reporting). Laboratories and physicians usually notify cases via telefax to the
Fig. 2. Number and percentage of hepatitis B cases by reference case definition (RCD; N ¼ 20,580), in Germany from 2005 to 2014.
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LPHAs, who enter these notifications into a software program and control for duplicate reports. The LPHAs are also responsible for investigation of cases, including telephone contacts by public health personnel to collect detailed information missed on the initial notification, and for initiating prevention measures. For management and reporting of cases, LPHAs use either a reporting software program developed by the RKI (SurvNet@RKI) or other commercially available software products. The software checks if the laboratory and clinical criteria of the CD are met, checks if the RCD is fulfilled, and labels cases accordingly. Cases are then pseudonymized and reported to the SHAs for data quality checks before reporting to the RKI (Fig. 1). Hepatitis B CDs A total of 22,549 HBV infections were reported to the RKI between January 2005 and December 2014. According to the CD, HBV infections classified as chronic (n ¼ 1963; 8.7%) and HBV infections without laboratory confirmation (n ¼ 6) were excluded from the analysis. All the remaining 20,580 HBV infections were included in the analysis (91.3%). Of those, 8708 (42.3%) infections fulfilled the RCD. Over time, the proportion of RCD cases over all notified cases significantly declined from 50.1% in 2005 to 32.7% in 2014 (OR ¼ 0.93, 95% CI ¼ 0.92e0.94; P < 0.001). The proportion of non-RCD cases with unknown symptoms increased considerably since 2013, leading to an increase in the proportion of RCD cases over all cases with information on symptoms (Fig. 2).
Data quality Over the 10-year evaluation period, completeness for the assessed variables differed (Table 1). Completeness of sex and age was very high, accounting for at least 99% each year. In contrast, both completeness of information on vaccination status and route of transmission were much lower and furthermore significantly decreased over the 10-year period (information on vaccination status: OR ¼ 0.92, 95% CI ¼ 0.91e0.93; P < 0.001; information on route of transmission: OR ¼ 0.94, 95% CI ¼ 0.93e0.95; P < 0.001). The drop in completeness of information on vaccination status was observed in particular since 2011 (Fig. 3). Furthermore, completeness of these two variables differed significantly between RCD and non-RCD cases (Table 1).
Timeliness of notification and reporting In 2847 (13.8%) of 20,580 cases, at least one of the required dates was missing, and 1886 (9.2%) cases exceeded the defined minimum or maximum delay. Therefore, 15,847 (77.0%) HBV infections were eligible for analysis. The mean notification delay was 3.0 days (SD ¼ 4.0; median ¼ 1 day, IQR ¼ 0e4 days). A significant trend over time in mean notification delay was found (IRR ¼ 0.95, 95% CI ¼ 0.95e0.96; P < 0.05; Fig. 4a), showing a decrease by 5% per year. Over the 10-year period, the mean reporting delay was 14.3 days (SD ¼ 14.8; median ¼ 9 days, IQR ¼ 5e18 days), showing no significant trend over time until 2013 (IRR ¼ 0.99, 95% CI ¼ 0.99e1.00; P > 0.05; Fig. 4b).
Table 1 Comparison of indicators for data quality regarding reference case definition (RCD; n ¼ 20,580), in Germany from 2005 to 2014. Completeness of information (in %) for the variables
All HBV infections (n ¼ 20,580)
RCD cases (n ¼ 8708)
Non-RCD cases (n ¼ 11,872)
P-value
Sex Age Probable routes of transmission Vaccinations against hepatitis B
99.4 100.0 25.3 72.9
99.5 99.9 32.1 81.6
99.4 100.0 20.4 66.5
ns ns <0.05 <0.05
ns, not statistically significant; HBV, hepatitis B virus.
Fig. 3. Completeness of information on HBV vaccination status and probable routes of transmission of acute hepatitis B cases reported to the RKI (n ¼ 20,580), in Germany from 2005 to 2014. HBV, hepatitis B virus; RKI, Robert Koch Institute.
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Fig. 4. Mean notification (a) and reporting delay in four-week periods (b) with the respective influence of the amendment to the law, in Germany from 2005 to 2014. RCD, reference case definition; RKI, Robert Koch Institute; LPHA, local public health authority.
Influence of the amendment in 2013 Before the amendment to the law, the mean reporting delay was 15.1 days (SD ¼ 14.5; median ¼ 10 days, IQR ¼ 6e18 days), showing no significant differences between RCD and non-RCD cases (IRR ¼ 1.01, 95% CI ¼ 0.98e1.04; P > 0.05; Fig. 4b). It significantly decreased by 27% after the amendment (IRR ¼ 0.73, 95% CI ¼ 0.67e0.79; P < 0.01), with a decline of 7% per year (IRR ¼ 0.93, 95% CI ¼ 0.87e0.99; P < 0.05). Since 2013, the mean reporting delay was 10.5 days (SD ¼ 15.1; median ¼ 5 days, IQR ¼ 2e12 days). In addition, since the amendment, mean reporting delay significantly increased by 12% for RCD compared with that for nonRCD cases (IRR ¼ 1.12, 95% CI ¼ 1.03e1.21; P < 0.01). The mean
reporting delay was then 11.3 days for RCD cases (SD ¼ 15.5; median ¼ 6 days, IQR ¼ 2e14 days) compared with 9.9 days (SD ¼ 15.1; median ¼ 4 days, IQR ¼ 2e11 days) for non-RCD cases (Fig. 4b).
Discussion This is the first comprehensive evaluation of the German national hepatitis B surveillance system since the implementation of the IfSG focusing on the description of the system and assessment of the surveillance attributes' simplicity, data quality in terms of completeness, and timeliness.
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Simplicity The simplicity of a public health surveillance system refers to both its structure and ease of operation. According to the CDC guidelines, surveillance systems should be as simple as possible.9 The HBV surveillance system in Germany has an electronic database and shows structural characteristics of a more complex surveillance system, which is referenced to manual data entry, dual reporting structure, and multiple levels of reporting.9 This is also true for other disease surveillance systems in Germany, e.g., those for methicillin-resistant Staphylococcus aureus infection.11 At the LPHA level, data received via telefax are manually entered into the respective software program. This is a time-consuming process and may lead to errors in data entry, impacting on data validity. A decrease in complexity is considered by the planned German electronic system for infectious diseases (DEMIS). The future electronic notification system will allow physicians and laboratories to notify either via a Web-based electronic notification portal or through interfaces integrated in their respective software systems to reduce workload for LPHAs, to decrease reporting delay, and to increase data completeness and validity.12,13
Data quality (in terms of completeness) Basic demographic data (i.e., age and sex) of notified AHB cases were reported almost completely and showed no relevant decline over time, whereas information on vaccination and routes of transmission was less satisfactory. Basic demographic data are already included in the initial notification by the laboratory or physician, whereas more specific information, i.e., vaccination status and routes of transmission, needs to be collected actively by LPHAs because physicians rarely report such information.14 As shown in a qualitative study conducted in 2017 on difficulties and opportunities in the notification process of hepatitis B and C infection, LPHAs reported these inquiries about missing information to be time-consuming and often without success.14 However, to initiate prevention and control measures, it is crucial to collect specific risks and vaccination breakthrough infections of notified cases. The literature on data quality of AHB surveillance systems is rare.15 A European evaluation of HBV surveillance data in 30 countries reported incompleteness in many epidemiological variables, e.g., route of transmission and HBV vaccination status.16 In line with our findings, low completeness of epidemiological data is a challenge in most countries. Comparison of HBV infection surveillance systems of different countries is challenging. To improve comparability between countries, the European Centre for Disease Prevention and Control (ECDC) develops in collaboration with Member States EU surveillance system descriptors and disease surveillance standards,17 which may also include benchmarks for each descriptor.18 Within the disease network for viral hepatitis coordinated by the ECDC, different surveillance systems are compared and surveillance standards (e.g., case definitions) are harmonized.19 Completeness is not only a performance matter of the surveillance system because a relevant proportion of adults with AHB is asymptomatic and remains undetected.20,21 Without diagnosis and notification, no preventive measures can be initiated by LPHAs. Furthermore, our analysis was limited to the data available at public health authorities and did not include the prior step of notification to public health authorities so that assessing the level of underreporting within the system was not possible. Plass et al.22
assumed that only 25% of all AHB infections are detected by the surveillance system; they also showed that AHB is only responsible for a small proportion of the disease burden of HBV. Timeliness One main objective of hepatitis B surveillance is to prevent further transmission, which can be achieved by a fast surveillance system. While reporting delay showed no significant trend over time up to the amendment in 2013, we found a continuously decreasing time lag between diagnosis of hepatitis B infection and notification to LPHAs (notification delay). This fact might be the result of increasing acceptability of the notification system over the years by laboratories and physicians.9 Prevention of disease transmission leading to secondary cases can be achieved if notification occurs within one incubation period.23,24 Hepatitis B has a long incubation period of 75 days on average, varying from 30 to 180 days.25 Obtaining the necessary information on exposure and relevant for RCD classification can be time-consuming. Schumacher et al.8 showed that time from diagnosis to reporting to SHAs is much longer for hepatitis B than for most of the other infectious diseases, probably due to timeconsuming efforts of case investigation. However, in our evaluation, notification and reporting delay were well less than the minimum incubation period of hepatitis B. Combined with the necessary data on exposure, authorities would have enough time to implement measures to prevent further transmission. Influence of the amendment to the law in 2013 In 2013, the amendment to the IfSG aimed at decreasing reporting time of the infectious disease surveillance system. We showed that timeliness in reporting significantly improved since the amendment, meaning that the law achieved its aim to allow earlier initiation of control and prevention activities. In case of infections with longer incubation periods as those with HBV infection, the rapid identification of infection might not be as important as the rapid availability of exposure data to provide a basis for identifying exposures that may lead to further transmission.9 Considering this fact, completeness is as important in HBV cases as is the attribute timeliness. Contrary to Schumacher et al,8 we showed that the improvement in timeliness was accompanied by a continuous reduction in completeness, even if we did not observe relevant changes in data completeness since the amendment. However, we showed that since the amendment, timeliness significantly differed between RCD and non-RCD cases. Non-RCD cases were reported significantly faster to the RKI than RCD cases, which is consistent with the fact that LPHAs report HBV cases when CDs (laboratory criteria) are fulfilled and before all necessary information is gathered. Supporting this, since 2013, we found an increase in non-RCD cases without information on clinical symptoms. Up to 2015, HBV cases without information on clinical symptoms were not defined as RCD cases. Another reason to explain the increase of non-RCD cases without information on clinical symptoms might be a change in the epidemiology of HBV infection in Germany compared with the period before 2013. This could be related to the influx of asylum seekers originating from regions with higher prevalence of HBV infection to Germany starting from 2014.26e28 In some federal states of Germany, asylum seekers were systematically screened for HBV, leading to an increase of HBV notifications.29 Furthermore, HBV infections among asylum seekers might not have been
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systematically investigated owing to language barriers or to their transfers to other communities or federal states after the screening. Thus, information on clinical symptoms might not have been included, meaning that the RCD was not fulfilled. Unfortunately, we were not able to quantify this impact because information on asylum seeker status and the country of birth is collected routinely by the surveillance system only since September 2015, and data on nationality are only collected since July 2017, with another amendment of the infectious disease act.30 At the beginning of 2015, the RCD was modified, and clinical symptoms were no longer required in addition to a laboratory confirmation to fulfill the RCD.31 This adapted RCD now includes potentially infectious HBV infections with missing clinical information. Further evaluation is necessary to identify the influence of these recent amendments and the new RCD on the performance of the surveillance system.
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C.H. and L.B. prepared and submitted the manuscript for publication. All authors read and approved the final manuscript. Acknowledgements The authors thank all current and past staff of local public health authorities, state health authorities, laboratories, physicians, and the Robert Koch Institute for their contribution to the hepatitis B virus surveillance in Germany. Ethical approval For analysis, pseudonymized surveillance data were used. Because our data were part of mandatory acute hepatitis B virus surveillance, no ethical approval was considered necessary. Funding
Limitations There are limitations with regard to our evaluation. To gain a more comprehensive picture, further aspects of simplicity could have been evaluated by including counts and measures or by interviewing key stakeholders. This was not feasible in the framework of our study; however, we discussed our results with SHAs and selected LPHAs. Regarding data quality, we limited our analysis to completeness of data available at public health authorities. A full assessment of data quality including the amount of underreporting would have required a distinct study such as a review of sampled data or patient interviews as data quality might be influenced by the performance of diagnostic tests, the respective CD, the clarity of surveillance forms, the quality of training and supervision of involved staff, and the care exercised in data management.9 For the evaluation of timeliness, we had to exclude 23% of notified infections either because they exceeded the minimum or maximum plausible delay or because they lacked a plausible date for timeliness calculation. These 23% excluded cases are a justifiable data loss because we still evaluated a decade of timeliness of HBV surveillance based on 77% of all reported AHB cases. Conclusion In conclusion, the German HBV surveillance system is operating in a timely manner. It has a complete and electronic database at the national level. Over the evaluation period, HBV surveillance was modified to improve its performance. Especially, timeliness was improved to a level that allows control and prevention activities to be initiated early. Nonetheless, data completeness needs to be improved to allow adequately designed prevention activities. As completeness of information decreased considerably over the evaluation period, further research is needed to explore reasons for this decrease. Author statements Author contributions L.B. and R.Z. conceptualized the study. L.B. performed background research on the topic and developed the detailed concept and design of the study. C.H., L.B., and M.A.d.H. conducted the statistical analyses and interpreted the results. D.A. extracted study data from the surveillance database and provided the data set for statistical analyses. S.D. and R.Z. provided input during preparation of the manuscript. C.H. and L.B. drafted the manuscript, and M.D., D.A., A.N.-G., S.D., R.Z., and V.B. critically revised the manuscript.
The Robert Koch Institute is the government’s central scientific institution in the field of infectious diseases. The German Federal Ministry of Health was not involved in the study design, analysis and interpretation of the data, or in the writing of the publication. Competing interests The authors declare no relevant competing interests. References 1. Global hepatitis report 2017. Geneva: World Health Organization; 2017 [01 October 2019]; Licence: CC BY-NC-SA 3.0 IGO]. Available from: http://apps. who.int/iris/bitstream/handle/10665/255016/9789241565455-eng.pdf;jsessionid¼3587194E109903E39C300D11AACA2E42?sequence¼1. 2. Poethko-Muller C, Zimmermann R, Hamouda O, Faber M, Stark K, Ross RS, et al. Epidemiology of hepatitis A, B, and C among adults in Germany: results of the German health interview and examination Survey for adults (DEGS1). Bundesgesundheitsblatt - Gesundheitsforsch - Gesundheitsschutz 2013;56:707e15. 3. Infektionsschutzgesetz vom 20. BGBl. I S. 104. Juli 2000. Available from: http:// www.gesetze-im-internet.de/ifsg/. 4. Faensen D, Claus H, Benzler J, Ammon A, Pfoch T, Breuer T, et al. SurvNet@RKI–a multistate electronic reporting system for communicable diseases. Euro Surveill : bulletin Europeen sur les maladies transmissibles ¼ European communicable disease bulletin 2006;11:100e3. 5. Bales S, Baumann HG, Schnitzler N, Kramer M. Infektionsschutzgesetz: Kommentar und Vorschriftensammlung. Kohlhammer; 2003. 6. Buchholz U, Bernard H, Werber D, Bohmer MM, Remschmidt C, Wilking H, et al. German outbreak of Escherichia coli O104:H4 associated with sprouts. N Engl J Med 2011;365:1763e70. 7. Gesetz zur Durchführung der Internationalen Gesundheitsvorschriften. (IGVDurchführungsgesetz e IGV-DG) vom 21.3.2013. BGBl. I S. 566. 2005. Available from: http://www.gesetze-im-internet.de/igv-dg/. 8. Schumacher J, Diercke M, Salmon M, Czogiel I, Schumacher D, Claus H, et al. Timeliness in the German surveillance system for infectious diseases: amendment of the infection protection act in 2013 decreased local reporting time to 1 day. PLoS One 2017;12:e0187037. 9. Centers for Disease Control and Prevention. Updated guidelines for evaluating public health surveillance systems: recommendations from the Guidelines Working Group. MMWR (Morb Mortal Wkly Rep) 2001;50:1e35. 10. Krause G, Altmann D, Faensen D, Porten K, Benzler J, Pfoch T, et al. SurvNet electronic surveillance system for infectious disease outbreaks, Germany. Emerg Infect Dis 2007;13:1548e55. €nfeld V, Diercke M, Gilsdorf A, Eckmanns T, Walter J. Evaluation of the 11. Scho statutory surveillance system for invasive MRSA infections in Germany, 2016e2017. BMC Public Health 2018;18:1063. 12. Diercke M. [German electronic notification system for infectious diseases (DEMIS)]. Epidemiol Bull 2017;30:291e3. 13. Diercke M. [Presentation of latest information on DEMIS]. Epidemiol Bull 2018;9:91e3. 14. Simeonova Y. [Procedure, difficulties, and potential for improvement in the mandatory notification of hepatitis-B- and C from the local public health authorities point of view]. Hamburg: Hamburg University of Applied Sciences; 2018. 15. Tosti MELS, de Waure C, Mele A, Franco E, Ricciardi W, Filia A. Assessment of timeliness, representativeness and quality of data reported to Italy's national integrated surveillance system for acute viral hepatitis (SEIEVA). Public Health 2015;129:561e8.
148
L. Boes et al. / Public Health 180 (2020) 141e148
16. Duffell EF, van de Laar MJ, Amato-Gauci AJ. Enhanced surveillance of hepatitis B in the EU, 2006-2012. J Viral Hepat 2015;22:581e9. 17. European Centre for Disease Prevention and Control. Long-term surveillance strategy 2014 e 2020. Stockholm: ECDC; 2013. 18. Reintjes R, Thelen M, Reiche R, Csohan A. Benchmarking national surveillance systems: a new tool for the comparison of communicable disease surveillance and control in Europe. Eur J Public Health 2007;17:375e80. 19. Duffell EF, van de Laar MJ. Survey of surveillance systems and select prevention activities for hepatitis B and C, European Union/European Economic Area, 2009. Euro Surveill 2015;20:17e24. 20. World Health Organization. Technical considerations and case definitions to improve surveillance for viral hepatitis: technical report. 2016 [21 December 2018]; Available from: http://apps.who.int/iris/bitstream/10665/204501/1/ 9789241549547_eng.pdf?ua¼1. 21. Gibbons CL, Mangen MJ, Plass D, Havelaar AH, Brooke RJ, Kramarz P, et al. Measuring underreporting and under-ascertainment in infectious disease datasets: a comparison of methods. BMC Public Health 2014;14:147. 22. Plass D, Mangen M-J, Kraemer A, Pinheiro P, Gilsdorf A, Krause G, et al. The disease burden of hepatitis B, influenza, measles and salmonellosis in Germany: first results of the burden of communicable diseases in Europe study. Epidemiol Infect 2014;142:2024e35. 23. Bonacic Marinovic A, Swaan C, van Steenbergen J, Kretzschmar M. Quantifying reporting timeliness to improve outbreak control. Emerg Infect Dis 2015;21: 209e16.
24. Reijn E, Swaan CM, Kretzschmar ME, van Steenbergen JE. Analysis of timeliness of infectious disease reporting in The Netherlands. BMC Public Health 2011;11: 409. 25. World Health Organization. Hepatitis B - fact sheet. 2019 [01 October 2019]; Available from: http://www.who.int/news-room/fact-sheets/detail/hepatitis-b. 26. German Federal Office for Migration and Refugees. Summery of the main results of the 2014 migration report. 2014 [01 October 2019]; Available from: http:// www.bamf.de/SharedDocs/Anlagen/EN/Publikationen/Migrationsberichte/ migrationsbericht-2014-zentrale-ergebnisse.html?nn¼1450238. 27. Bashour H, Muhjazi G. Hepatitis B and C in the Syrian Arab Republic: a review. Eastern Mediterranean health journal ¼ La revue de sante de la Mediterranee orientale ¼ al-Majallah al-sihhiyah li-sharq al-mutawassit, vol. 22; 2016. p. 267e73. 28. Khan S, Attaullah S. Share of Afghanistan populace in hepatitis B and hepatitis C infection's pool: is it worthwhile? Virol J 2011;8:216. €st S, Bozorgmehr K. [Health examination of asylum seekers: a 29. Wahedi K, No nationwide analysis of regulations in Germany]. Bundesgesundheitsblatt Gesundheitsforsch - Gesundheitsschutz 2017;60:108e17. 30. Infektionsschutzgesetz vom 20. Juli 2000 (BGBl. I S. 1045), das zuletzt durch Artikel €ndert worden ist. BGBl. I S. 1 des Gesetzes vom 17. Juli 2017 (BGBl. I S. 2615) gea 26152017; Available from: https://www.gesetze-im-internet.de/ifsg/IfSG.pdf. 31. Diercke M, Benzler J, Schoneberg I, Mucke I, Altmann D, Claus H, et al. [The 2015 edition of case definitions for the surveillance of notifiable infectious diseases in Germany]. Bundesgesundheitsblatt - Gesundheitsforsch - Gesundheitsschutz 2014;57:1107e10.
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Original Research
Evaluation of the German surveillance system for hepatitis B regarding timeliness, data quality, and simplicity, from 2005 to 2014 L. Boes a, 1, C. Houareau a, b, 1, D. Altmann a, M. An der Heiden a, V. Bremer a, M. Diercke c, S. Dudareva a, A. Neumeyer-Gromen a, R. Zimmermann a, * a
Robert Koch Institute, Department for Infectious Disease Epidemiology, Unit for HIV/AIDS, STI and Blood-borne Infections, Robert Koch Institute, Berlin, Germany Charit e University Medicine, Berlin, Germany c Robert Koch Institute, Department for Infectious Disease Epidemiology, Surveillance Unit, Robert Koch Institute, Berlin, Germany b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 15 May 2019 Received in revised form 4 October 2019 Accepted 12 November 2019
Objectives: Germany has a mandatory surveillance system for acute hepatitis B (AHB) with the Protection against Infection Act as the legal basis in place since 2001. An amendment was introduced in 2013. We aimed at evaluating the surveillance systems' performance regarding timeliness, data quality, and simplicity from 2005 to 2014 and at assessing the effect of the amendment on timeliness of AHB surveillance. Study design: This study is a trend analysis of surveillance data. Methods: Aspects of simplicity versus complexity of the surveillance system were assessed by describing data flow, levels of reporting, and data management procedures. Data quality, in terms of data completeness, was evaluated by quantitative indicators, and timeliness was measured in days between different levels of the surveillance system, notification delay, and reporting delay. Trends over time in data quality were analyzed by logistic regression, while negative binomial regression was used to test for trend over time regarding mean notification and reporting delay. Results: Between January 2005 and December 2014, a total of 22,549 AHB infections were reported at the national level. The data flow of the German AHB surveillance system showed structural characteristics of a complex system. Over the 10-year period, completeness of reporting sex, age, probable route of transmission, and hepatitis B virus (HBV) vaccination were 99%, 100%, 25%, and 73%, respectively. However, data quality decreased over the evaluation period. Although notification delay improved over time (incident rate ratio [IRR] ¼ 0.95, 95% confidence interval [CI] ¼ 0.95e0.96; P < 0.05), reporting delay improved only since the amendment (IRR ¼ 0.76, 95% CI ¼ 0.70e0.82; P < 0.05). In total, mean notification and reporting delay were 3.0 days and 14.3 days, respectively. Conclusions: The German AHB surveillance system is operating in a timely manner. Although timeliness improved over the evaluation period and the amendment to the Protection against Infection Act succeeded in reducing reporting time, data quality in terms of completeness of information decreased considerably. As improved data completeness is required to adequately design prevention activities, reasons for this decrease should further be explored. © 2019 The Royal Society for Public Health. Published by Elsevier Ltd. All rights reserved.
Keywords: Acute hepatitis B HBV Surveillance Evaluation Timeliness Data quality
Introduction The global prevalence of chronic hepatitis B virus (HBV) infection was estimated to be 3.5% in 2015, with 257 million people living with chronic infection.1 Results of the German Health * Corresponding author. Robert Koch Institute Department for Infectious Disease Epidemiology Seestr. 10 13353 Berlin Germany. Tel.: þ49 30-18754-3801; fax: þ49 30-18754-3533 E-mail address: [email protected] (R. Zimmermann). 1 These authors share first authorship.
Examination Survey from 2008 to 2010 indicated a low prevalence of acute or chronic HBV infection of 0.3% in the general population, while 5.1% of the population had had previous exposure to HBV.2
Description of the German surveillance system The legal basis for the control of infectious diseases in Germany, the Protection against Infection Act (Infektionsschutzgesetz [IfSG]), came into effect in 2001.3 An electronic reporting system and
https://doi.org/10.1016/j.puhe.2019.11.012 0033-3506/© 2019 The Royal Society for Public Health. Published by Elsevier Ltd. All rights reserved.
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database for surveillance of notifiable infectious diseases (SurvNet@RKI) was created.4 Since then, cases of infectious diseases are electronically reported from local public health authorities (LPHAs) to state health authorities (SHAs) to national public health authorities. The Robert Koch Institute (RKI), the national public health institute, publishes case definitions (CDs) for notifiable diseases to be applied by the LPHAs. Furthermore, specific reference case definitions (RCDs) are applied by the RKI before publication of the notified data. According to the IfSG, acute hepatitis B (AHB) is a notifiable disease. Objectives of the national infectious disease surveillance system for AHB are as follows: (1) to detect trends in the incidence of AHB; and (2) to provide reliable information for implementation and modification of evidence-based prevention strategies to prevent further disease transmission.5 IfSG amendment The 2011 verotoxic Escherichia coli O104:H4 outbreak in Germany emphasized the necessity of a rapid surveillance system.6 An amendment to the IfSG introduced on March 29, 2013, aimed at decreasing reporting time within the German surveillance system.7 Since then, LPHAs and SHAs are requested to report all notifiable infections within one working day to the next level. A recent analysis showed that the amendment decreased overall reporting time without relevant loss of data quality.8 Objectives of the evaluation Thus far, neither the HBV surveillance system nor the impact of the amendment to the IfSG in 2013 on HBV surveillance has been assessed. Owing to relevant changes in the CDs for AHB in 2015, we evaluated the surveillance system over the ten-year period preceding these changes with regard to aspects of simplicity of the system, data quality (in terms of completeness), and timeliness.9 Methods Case definitions CD for AHB The CD of AHB included laboratory and clinical criteria. The laboratory criteria for confirmation of AHB were either a positive polymerase chain reaction for hepatitis B nucleic acid (HBV-DNA) or the detection of IgM hepatitis B core antibodies (anti-HBc IgM) or hepatitis B surface antigen (HBsAg) with a confirmatory test. The clinical criteria were defined as the presence of at least one of the following criteria: jaundice, elevated levels of serum transaminases, or upper abdominal pain. All cases with laboratory confirmation with, without or with unknown clinical criteria, were reported to the RKI. HBV cases classified as chronic do not fulfill the CD.
from the national surveillance database at the RKI, as of March 1, 2015. Simplicity To assess aspects of simplicity or complexity of the surveillance system, the flow of data including reporting structure, levels of reporting, and data management in the German HBV surveillance system was described by integrating information gathered from system documents and publications (Fig. 1).4,9,10 We followed the Centers for Disease Control and Prevention (CDC) guidelines for evaluating public health surveillance systems9 to determine simplicity/complexity of the system by assessing the chain of reporting (single versus dual chain of reporting) and methods of data entry and management (electronic versus manual data entry and electronic transfer versus telefax). A system is considered simple in design if it has a single reporting structure within a complete electronic notification system and few levels of reporting.9 Data quality We assessed data quality in terms of completeness of surveillance data. As indicators for completeness, we defined the following key variables: sex, age, probable routes of transmission, and vaccination status of all reported AHB infections. The variables sex and age were considered as complete if the respective sex or age of the person was specified. Information on probable routes of transmission was considered as complete if at least one route of transmission was specified. Completeness of information on HBV vaccination status was achieved if it was specified as information available: ‘yes’ or ‘no.’ Timeliness of HBV notifications We defined two time periods to evaluate timeliness: 1. The time period from the date of diagnosis by a physician or a laboratory until the date of notification to the responsible LPHA (defined as: notification delay) 2. The time period from the date of notification to the LPHA until the date of reporting to the RKI (defined as: reporting delay) For both time periods, a minimum delay of zero days was accepted for analysis. A maximum notification delay of 21 days and a maximum reporting delay of 91 days were considered as plausible and accepted for analysis. Cases were only included in the evaluation of timeliness if valid notification and reporting dates to the LPHAs and to the RKI were available. Median and mean of both time periods are reported including interquartile range (IQR) and standard deviation (SD).
Reference case definition Among all cases fulfilling the CD for AHB, from 2005 to 2014, only cases fulfilling both laboratory and clinical criteria were analyzed at the national level and published in official statistics (RCD) according to the reference definition.
Influence of the amendment to the law in 2013
Data selection
Statistical analysis
We included all laboratory-confirmed cases of AHB reported to the RKI from January 2005 to December 2014. Data were extracted
Trends over time in data quality and the RCD were tested by logistic regression. The results of logistic regressions were reported
The influence of the amendment to the IfSG was assessed by comparing reporting delay for the period before the amendment and reporting delay since the amendment in 2013.
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Fig. 1. Flow chart and levels of reporting of the hepatitis B surveillance system.
in odds ratios (ORs) with 95% confidence intervals (CIs). The independent variable was the year of reporting to the RKI. However, for mean reporting and notification delay, negative binomial regression was used to test for trend over time. The independent variables were the year of notification to LPHAs or the year of reporting to the RKI, respectively. To analyze changes in mean reporting delay since the amendment, we also included the independent variable, year of notification since the amendment in 2013, as well as a constant for year of notification since the amendment, and a binary RCD variable. We also included an interaction of the RCD and the constant for the year of notification to analyze changes in mean reporting delay for the RCD since the amendment. The results were reported as incident rate ratios (IRRs) with 95% CI. The significant contributions to the model of all tests were reported in P-values. P-values <0.05 were considered statistically significant.
All analyses were performed using STATA® 15.1 (StataCorp LP, College Station, TX, USA). Results Simplicity Data flow in the surveillance system The surveillance system for HBV infection consists of multiple levels of reporting: all newly diagnosed AHB infections, regardless of the clinical picture, should be notified by name from the treating physician and the laboratory to the responsible LPHA (dual reporting), followed by anonymized reporting from the LPHA to the SHA, and from there finally to the RKI (multiple levels of reporting). Laboratories and physicians usually notify cases via telefax to the
Fig. 2. Number and percentage of hepatitis B cases by reference case definition (RCD; N ¼ 20,580), in Germany from 2005 to 2014.
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LPHAs, who enter these notifications into a software program and control for duplicate reports. The LPHAs are also responsible for investigation of cases, including telephone contacts by public health personnel to collect detailed information missed on the initial notification, and for initiating prevention measures. For management and reporting of cases, LPHAs use either a reporting software program developed by the RKI (SurvNet@RKI) or other commercially available software products. The software checks if the laboratory and clinical criteria of the CD are met, checks if the RCD is fulfilled, and labels cases accordingly. Cases are then pseudonymized and reported to the SHAs for data quality checks before reporting to the RKI (Fig. 1). Hepatitis B CDs A total of 22,549 HBV infections were reported to the RKI between January 2005 and December 2014. According to the CD, HBV infections classified as chronic (n ¼ 1963; 8.7%) and HBV infections without laboratory confirmation (n ¼ 6) were excluded from the analysis. All the remaining 20,580 HBV infections were included in the analysis (91.3%). Of those, 8708 (42.3%) infections fulfilled the RCD. Over time, the proportion of RCD cases over all notified cases significantly declined from 50.1% in 2005 to 32.7% in 2014 (OR ¼ 0.93, 95% CI ¼ 0.92e0.94; P < 0.001). The proportion of non-RCD cases with unknown symptoms increased considerably since 2013, leading to an increase in the proportion of RCD cases over all cases with information on symptoms (Fig. 2).
Data quality Over the 10-year evaluation period, completeness for the assessed variables differed (Table 1). Completeness of sex and age was very high, accounting for at least 99% each year. In contrast, both completeness of information on vaccination status and route of transmission were much lower and furthermore significantly decreased over the 10-year period (information on vaccination status: OR ¼ 0.92, 95% CI ¼ 0.91e0.93; P < 0.001; information on route of transmission: OR ¼ 0.94, 95% CI ¼ 0.93e0.95; P < 0.001). The drop in completeness of information on vaccination status was observed in particular since 2011 (Fig. 3). Furthermore, completeness of these two variables differed significantly between RCD and non-RCD cases (Table 1).
Timeliness of notification and reporting In 2847 (13.8%) of 20,580 cases, at least one of the required dates was missing, and 1886 (9.2%) cases exceeded the defined minimum or maximum delay. Therefore, 15,847 (77.0%) HBV infections were eligible for analysis. The mean notification delay was 3.0 days (SD ¼ 4.0; median ¼ 1 day, IQR ¼ 0e4 days). A significant trend over time in mean notification delay was found (IRR ¼ 0.95, 95% CI ¼ 0.95e0.96; P < 0.05; Fig. 4a), showing a decrease by 5% per year. Over the 10-year period, the mean reporting delay was 14.3 days (SD ¼ 14.8; median ¼ 9 days, IQR ¼ 5e18 days), showing no significant trend over time until 2013 (IRR ¼ 0.99, 95% CI ¼ 0.99e1.00; P > 0.05; Fig. 4b).
Table 1 Comparison of indicators for data quality regarding reference case definition (RCD; n ¼ 20,580), in Germany from 2005 to 2014. Completeness of information (in %) for the variables
All HBV infections (n ¼ 20,580)
RCD cases (n ¼ 8708)
Non-RCD cases (n ¼ 11,872)
P-value
Sex Age Probable routes of transmission Vaccinations against hepatitis B
99.4 100.0 25.3 72.9
99.5 99.9 32.1 81.6
99.4 100.0 20.4 66.5
ns ns <0.05 <0.05
ns, not statistically significant; HBV, hepatitis B virus.
Fig. 3. Completeness of information on HBV vaccination status and probable routes of transmission of acute hepatitis B cases reported to the RKI (n ¼ 20,580), in Germany from 2005 to 2014. HBV, hepatitis B virus; RKI, Robert Koch Institute.
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Fig. 4. Mean notification (a) and reporting delay in four-week periods (b) with the respective influence of the amendment to the law, in Germany from 2005 to 2014. RCD, reference case definition; RKI, Robert Koch Institute; LPHA, local public health authority.
Influence of the amendment in 2013 Before the amendment to the law, the mean reporting delay was 15.1 days (SD ¼ 14.5; median ¼ 10 days, IQR ¼ 6e18 days), showing no significant differences between RCD and non-RCD cases (IRR ¼ 1.01, 95% CI ¼ 0.98e1.04; P > 0.05; Fig. 4b). It significantly decreased by 27% after the amendment (IRR ¼ 0.73, 95% CI ¼ 0.67e0.79; P < 0.01), with a decline of 7% per year (IRR ¼ 0.93, 95% CI ¼ 0.87e0.99; P < 0.05). Since 2013, the mean reporting delay was 10.5 days (SD ¼ 15.1; median ¼ 5 days, IQR ¼ 2e12 days). In addition, since the amendment, mean reporting delay significantly increased by 12% for RCD compared with that for nonRCD cases (IRR ¼ 1.12, 95% CI ¼ 1.03e1.21; P < 0.01). The mean
reporting delay was then 11.3 days for RCD cases (SD ¼ 15.5; median ¼ 6 days, IQR ¼ 2e14 days) compared with 9.9 days (SD ¼ 15.1; median ¼ 4 days, IQR ¼ 2e11 days) for non-RCD cases (Fig. 4b).
Discussion This is the first comprehensive evaluation of the German national hepatitis B surveillance system since the implementation of the IfSG focusing on the description of the system and assessment of the surveillance attributes' simplicity, data quality in terms of completeness, and timeliness.
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Simplicity The simplicity of a public health surveillance system refers to both its structure and ease of operation. According to the CDC guidelines, surveillance systems should be as simple as possible.9 The HBV surveillance system in Germany has an electronic database and shows structural characteristics of a more complex surveillance system, which is referenced to manual data entry, dual reporting structure, and multiple levels of reporting.9 This is also true for other disease surveillance systems in Germany, e.g., those for methicillin-resistant Staphylococcus aureus infection.11 At the LPHA level, data received via telefax are manually entered into the respective software program. This is a time-consuming process and may lead to errors in data entry, impacting on data validity. A decrease in complexity is considered by the planned German electronic system for infectious diseases (DEMIS). The future electronic notification system will allow physicians and laboratories to notify either via a Web-based electronic notification portal or through interfaces integrated in their respective software systems to reduce workload for LPHAs, to decrease reporting delay, and to increase data completeness and validity.12,13
Data quality (in terms of completeness) Basic demographic data (i.e., age and sex) of notified AHB cases were reported almost completely and showed no relevant decline over time, whereas information on vaccination and routes of transmission was less satisfactory. Basic demographic data are already included in the initial notification by the laboratory or physician, whereas more specific information, i.e., vaccination status and routes of transmission, needs to be collected actively by LPHAs because physicians rarely report such information.14 As shown in a qualitative study conducted in 2017 on difficulties and opportunities in the notification process of hepatitis B and C infection, LPHAs reported these inquiries about missing information to be time-consuming and often without success.14 However, to initiate prevention and control measures, it is crucial to collect specific risks and vaccination breakthrough infections of notified cases. The literature on data quality of AHB surveillance systems is rare.15 A European evaluation of HBV surveillance data in 30 countries reported incompleteness in many epidemiological variables, e.g., route of transmission and HBV vaccination status.16 In line with our findings, low completeness of epidemiological data is a challenge in most countries. Comparison of HBV infection surveillance systems of different countries is challenging. To improve comparability between countries, the European Centre for Disease Prevention and Control (ECDC) develops in collaboration with Member States EU surveillance system descriptors and disease surveillance standards,17 which may also include benchmarks for each descriptor.18 Within the disease network for viral hepatitis coordinated by the ECDC, different surveillance systems are compared and surveillance standards (e.g., case definitions) are harmonized.19 Completeness is not only a performance matter of the surveillance system because a relevant proportion of adults with AHB is asymptomatic and remains undetected.20,21 Without diagnosis and notification, no preventive measures can be initiated by LPHAs. Furthermore, our analysis was limited to the data available at public health authorities and did not include the prior step of notification to public health authorities so that assessing the level of underreporting within the system was not possible. Plass et al.22
assumed that only 25% of all AHB infections are detected by the surveillance system; they also showed that AHB is only responsible for a small proportion of the disease burden of HBV. Timeliness One main objective of hepatitis B surveillance is to prevent further transmission, which can be achieved by a fast surveillance system. While reporting delay showed no significant trend over time up to the amendment in 2013, we found a continuously decreasing time lag between diagnosis of hepatitis B infection and notification to LPHAs (notification delay). This fact might be the result of increasing acceptability of the notification system over the years by laboratories and physicians.9 Prevention of disease transmission leading to secondary cases can be achieved if notification occurs within one incubation period.23,24 Hepatitis B has a long incubation period of 75 days on average, varying from 30 to 180 days.25 Obtaining the necessary information on exposure and relevant for RCD classification can be time-consuming. Schumacher et al.8 showed that time from diagnosis to reporting to SHAs is much longer for hepatitis B than for most of the other infectious diseases, probably due to timeconsuming efforts of case investigation. However, in our evaluation, notification and reporting delay were well less than the minimum incubation period of hepatitis B. Combined with the necessary data on exposure, authorities would have enough time to implement measures to prevent further transmission. Influence of the amendment to the law in 2013 In 2013, the amendment to the IfSG aimed at decreasing reporting time of the infectious disease surveillance system. We showed that timeliness in reporting significantly improved since the amendment, meaning that the law achieved its aim to allow earlier initiation of control and prevention activities. In case of infections with longer incubation periods as those with HBV infection, the rapid identification of infection might not be as important as the rapid availability of exposure data to provide a basis for identifying exposures that may lead to further transmission.9 Considering this fact, completeness is as important in HBV cases as is the attribute timeliness. Contrary to Schumacher et al,8 we showed that the improvement in timeliness was accompanied by a continuous reduction in completeness, even if we did not observe relevant changes in data completeness since the amendment. However, we showed that since the amendment, timeliness significantly differed between RCD and non-RCD cases. Non-RCD cases were reported significantly faster to the RKI than RCD cases, which is consistent with the fact that LPHAs report HBV cases when CDs (laboratory criteria) are fulfilled and before all necessary information is gathered. Supporting this, since 2013, we found an increase in non-RCD cases without information on clinical symptoms. Up to 2015, HBV cases without information on clinical symptoms were not defined as RCD cases. Another reason to explain the increase of non-RCD cases without information on clinical symptoms might be a change in the epidemiology of HBV infection in Germany compared with the period before 2013. This could be related to the influx of asylum seekers originating from regions with higher prevalence of HBV infection to Germany starting from 2014.26e28 In some federal states of Germany, asylum seekers were systematically screened for HBV, leading to an increase of HBV notifications.29 Furthermore, HBV infections among asylum seekers might not have been
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systematically investigated owing to language barriers or to their transfers to other communities or federal states after the screening. Thus, information on clinical symptoms might not have been included, meaning that the RCD was not fulfilled. Unfortunately, we were not able to quantify this impact because information on asylum seeker status and the country of birth is collected routinely by the surveillance system only since September 2015, and data on nationality are only collected since July 2017, with another amendment of the infectious disease act.30 At the beginning of 2015, the RCD was modified, and clinical symptoms were no longer required in addition to a laboratory confirmation to fulfill the RCD.31 This adapted RCD now includes potentially infectious HBV infections with missing clinical information. Further evaluation is necessary to identify the influence of these recent amendments and the new RCD on the performance of the surveillance system.
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C.H. and L.B. prepared and submitted the manuscript for publication. All authors read and approved the final manuscript. Acknowledgements The authors thank all current and past staff of local public health authorities, state health authorities, laboratories, physicians, and the Robert Koch Institute for their contribution to the hepatitis B virus surveillance in Germany. Ethical approval For analysis, pseudonymized surveillance data were used. Because our data were part of mandatory acute hepatitis B virus surveillance, no ethical approval was considered necessary. Funding
Limitations There are limitations with regard to our evaluation. To gain a more comprehensive picture, further aspects of simplicity could have been evaluated by including counts and measures or by interviewing key stakeholders. This was not feasible in the framework of our study; however, we discussed our results with SHAs and selected LPHAs. Regarding data quality, we limited our analysis to completeness of data available at public health authorities. A full assessment of data quality including the amount of underreporting would have required a distinct study such as a review of sampled data or patient interviews as data quality might be influenced by the performance of diagnostic tests, the respective CD, the clarity of surveillance forms, the quality of training and supervision of involved staff, and the care exercised in data management.9 For the evaluation of timeliness, we had to exclude 23% of notified infections either because they exceeded the minimum or maximum plausible delay or because they lacked a plausible date for timeliness calculation. These 23% excluded cases are a justifiable data loss because we still evaluated a decade of timeliness of HBV surveillance based on 77% of all reported AHB cases. Conclusion In conclusion, the German HBV surveillance system is operating in a timely manner. It has a complete and electronic database at the national level. Over the evaluation period, HBV surveillance was modified to improve its performance. Especially, timeliness was improved to a level that allows control and prevention activities to be initiated early. Nonetheless, data completeness needs to be improved to allow adequately designed prevention activities. As completeness of information decreased considerably over the evaluation period, further research is needed to explore reasons for this decrease. Author statements Author contributions L.B. and R.Z. conceptualized the study. L.B. performed background research on the topic and developed the detailed concept and design of the study. C.H., L.B., and M.A.d.H. conducted the statistical analyses and interpreted the results. D.A. extracted study data from the surveillance database and provided the data set for statistical analyses. S.D. and R.Z. provided input during preparation of the manuscript. C.H. and L.B. drafted the manuscript, and M.D., D.A., A.N.-G., S.D., R.Z., and V.B. critically revised the manuscript.
The Robert Koch Institute is the government’s central scientific institution in the field of infectious diseases. The German Federal Ministry of Health was not involved in the study design, analysis and interpretation of the data, or in the writing of the publication. Competing interests The authors declare no relevant competing interests. References 1. Global hepatitis report 2017. Geneva: World Health Organization; 2017 [01 October 2019]; Licence: CC BY-NC-SA 3.0 IGO]. Available from: http://apps. who.int/iris/bitstream/handle/10665/255016/9789241565455-eng.pdf;jsessionid¼3587194E109903E39C300D11AACA2E42?sequence¼1. 2. Poethko-Muller C, Zimmermann R, Hamouda O, Faber M, Stark K, Ross RS, et al. Epidemiology of hepatitis A, B, and C among adults in Germany: results of the German health interview and examination Survey for adults (DEGS1). Bundesgesundheitsblatt - Gesundheitsforsch - Gesundheitsschutz 2013;56:707e15. 3. Infektionsschutzgesetz vom 20. BGBl. I S. 104. Juli 2000. Available from: http:// www.gesetze-im-internet.de/ifsg/. 4. Faensen D, Claus H, Benzler J, Ammon A, Pfoch T, Breuer T, et al. SurvNet@RKI–a multistate electronic reporting system for communicable diseases. Euro Surveill : bulletin Europeen sur les maladies transmissibles ¼ European communicable disease bulletin 2006;11:100e3. 5. Bales S, Baumann HG, Schnitzler N, Kramer M. Infektionsschutzgesetz: Kommentar und Vorschriftensammlung. Kohlhammer; 2003. 6. Buchholz U, Bernard H, Werber D, Bohmer MM, Remschmidt C, Wilking H, et al. German outbreak of Escherichia coli O104:H4 associated with sprouts. N Engl J Med 2011;365:1763e70. 7. Gesetz zur Durchführung der Internationalen Gesundheitsvorschriften. (IGVDurchführungsgesetz e IGV-DG) vom 21.3.2013. BGBl. I S. 566. 2005. Available from: http://www.gesetze-im-internet.de/igv-dg/. 8. Schumacher J, Diercke M, Salmon M, Czogiel I, Schumacher D, Claus H, et al. Timeliness in the German surveillance system for infectious diseases: amendment of the infection protection act in 2013 decreased local reporting time to 1 day. PLoS One 2017;12:e0187037. 9. Centers for Disease Control and Prevention. Updated guidelines for evaluating public health surveillance systems: recommendations from the Guidelines Working Group. MMWR (Morb Mortal Wkly Rep) 2001;50:1e35. 10. Krause G, Altmann D, Faensen D, Porten K, Benzler J, Pfoch T, et al. SurvNet electronic surveillance system for infectious disease outbreaks, Germany. Emerg Infect Dis 2007;13:1548e55. €nfeld V, Diercke M, Gilsdorf A, Eckmanns T, Walter J. Evaluation of the 11. Scho statutory surveillance system for invasive MRSA infections in Germany, 2016e2017. BMC Public Health 2018;18:1063. 12. Diercke M. [German electronic notification system for infectious diseases (DEMIS)]. Epidemiol Bull 2017;30:291e3. 13. Diercke M. [Presentation of latest information on DEMIS]. Epidemiol Bull 2018;9:91e3. 14. Simeonova Y. [Procedure, difficulties, and potential for improvement in the mandatory notification of hepatitis-B- and C from the local public health authorities point of view]. Hamburg: Hamburg University of Applied Sciences; 2018. 15. Tosti MELS, de Waure C, Mele A, Franco E, Ricciardi W, Filia A. Assessment of timeliness, representativeness and quality of data reported to Italy's national integrated surveillance system for acute viral hepatitis (SEIEVA). Public Health 2015;129:561e8.
148
L. Boes et al. / Public Health 180 (2020) 141e148
16. Duffell EF, van de Laar MJ, Amato-Gauci AJ. Enhanced surveillance of hepatitis B in the EU, 2006-2012. J Viral Hepat 2015;22:581e9. 17. European Centre for Disease Prevention and Control. Long-term surveillance strategy 2014 e 2020. Stockholm: ECDC; 2013. 18. Reintjes R, Thelen M, Reiche R, Csohan A. Benchmarking national surveillance systems: a new tool for the comparison of communicable disease surveillance and control in Europe. Eur J Public Health 2007;17:375e80. 19. Duffell EF, van de Laar MJ. Survey of surveillance systems and select prevention activities for hepatitis B and C, European Union/European Economic Area, 2009. Euro Surveill 2015;20:17e24. 20. World Health Organization. Technical considerations and case definitions to improve surveillance for viral hepatitis: technical report. 2016 [21 December 2018]; Available from: http://apps.who.int/iris/bitstream/10665/204501/1/ 9789241549547_eng.pdf?ua¼1. 21. Gibbons CL, Mangen MJ, Plass D, Havelaar AH, Brooke RJ, Kramarz P, et al. Measuring underreporting and under-ascertainment in infectious disease datasets: a comparison of methods. BMC Public Health 2014;14:147. 22. Plass D, Mangen M-J, Kraemer A, Pinheiro P, Gilsdorf A, Krause G, et al. The disease burden of hepatitis B, influenza, measles and salmonellosis in Germany: first results of the burden of communicable diseases in Europe study. Epidemiol Infect 2014;142:2024e35. 23. Bonacic Marinovic A, Swaan C, van Steenbergen J, Kretzschmar M. Quantifying reporting timeliness to improve outbreak control. Emerg Infect Dis 2015;21: 209e16.
24. Reijn E, Swaan CM, Kretzschmar ME, van Steenbergen JE. Analysis of timeliness of infectious disease reporting in The Netherlands. BMC Public Health 2011;11: 409. 25. World Health Organization. Hepatitis B - fact sheet. 2019 [01 October 2019]; Available from: http://www.who.int/news-room/fact-sheets/detail/hepatitis-b. 26. German Federal Office for Migration and Refugees. Summery of the main results of the 2014 migration report. 2014 [01 October 2019]; Available from: http:// www.bamf.de/SharedDocs/Anlagen/EN/Publikationen/Migrationsberichte/ migrationsbericht-2014-zentrale-ergebnisse.html?nn¼1450238. 27. Bashour H, Muhjazi G. Hepatitis B and C in the Syrian Arab Republic: a review. Eastern Mediterranean health journal ¼ La revue de sante de la Mediterranee orientale ¼ al-Majallah al-sihhiyah li-sharq al-mutawassit, vol. 22; 2016. p. 267e73. 28. Khan S, Attaullah S. Share of Afghanistan populace in hepatitis B and hepatitis C infection's pool: is it worthwhile? Virol J 2011;8:216. €st S, Bozorgmehr K. [Health examination of asylum seekers: a 29. Wahedi K, No nationwide analysis of regulations in Germany]. Bundesgesundheitsblatt Gesundheitsforsch - Gesundheitsschutz 2017;60:108e17. 30. Infektionsschutzgesetz vom 20. Juli 2000 (BGBl. I S. 1045), das zuletzt durch Artikel €ndert worden ist. BGBl. I S. 1 des Gesetzes vom 17. Juli 2017 (BGBl. I S. 2615) gea 26152017; Available from: https://www.gesetze-im-internet.de/ifsg/IfSG.pdf. 31. Diercke M, Benzler J, Schoneberg I, Mucke I, Altmann D, Claus H, et al. [The 2015 edition of case definitions for the surveillance of notifiable infectious diseases in Germany]. Bundesgesundheitsblatt - Gesundheitsforsch - Gesundheitsschutz 2014;57:1107e10.