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1 [Human Vaccines 5:3, 1-5; March 2009]; 2009 Landes Bioscience This manuscript has been published online, prior to printing.once the issue is complete and page numbers have been assigned, the citation will change accordingly. Research Paper Monitoring the rate of hospitalization before rotavirus immunization in Italy utilizing ICD9-CM regional databases Federico Marchetti, 1 Barouk Assael, 2 Giovanni Gabutti, 3 Alfredo Guarino, 4 Pier Luigi Lopalco, 5 Alessia Marocco, 1 Franco Ruggeri, 6 Lucina Titone, 7 Alberto Tozzi, 8 Giovanni Vitali Rosati, 9 Carla Zotti 10 and Elisabetta Franco 11 1 Medical Department; GlaxoSmithKline S.p.A; Verona, Italy; 2 Cystic Fibrosis Regional Hospital; Verona, Italy; 3 Department of Clinical and Experimental Medicine; University of Ferrara; Ferrara, Italy; 4 Department of Pediatrics; University of Naples; Naples, Italy; 5 Department of Public Health; University of Bari; Bari, Italy; 6 Virology Unit; Istituto Superiore di Sanità; Rome, Italy; 7 Department of Pediatrics; University of Palermo; Palermo, Italy; 8 Epidemiology Unit; Bambin Gesù Hospital; Rome, Italy; 9 Family Pediatrician; Florence, Italy; 10 Department of Public Health; University of Turin; Turin, Italy; 11 Department of Public Health; University of Rome Tor Vergata; Rome, Italy Abbreviations: ESPID, european society of paediatric infectious diseases; ESPGHAN, european society of gastroenterology, hepatology and nutrition; NHS, national healthcare system; RV, rotavirus; ICD, international classification of diseases; PD, primary diagnosis; RVE, rotavirus enteritis; VE, viral enteritis; SD, secondary diagnosis; s.d, standard deviation; HDD, hospital discharge databases; SSN, national heath care system Key words: rotavirus, enteritis, vaccine, hospitalization ICD9-CM, database Background: Recently, two Rotavirus (RV) vaccines were licensed in Italy, rendering RV illness a vaccine preventable disease. To assess the RV hospitalization rate in Italy, a study focused on the Regional hospital discharge forms (HDD) databases was carried out. Results: Regional HDD databases from Piemonte, Veneto, Friuli-Venezia-Giulia and Marche were analyzed. A total of 434,335 hospitalizations were counted in the study timeframe and 13,234 VE diagnoses (3% of hospitalizations) were collected. A total of 8546 RVE cases (2% of hospitalizations, 64% of all VE) were observed, of which 1.2% were primary diagnoses (PD) and 0.8% secondary diagnosis (SD). The RVE hospitalization peak (4.9 %) was observed at the age of 1 year (4.5% in 7 12 months of age) with a median hospital stay of 4.4 days (s.d ± 4.2). Two deaths (out of 8546 RVE cases) were identified. Patients and methods: Regional HDD databases with the diagnosis of viral enteritis (VE) and RV enteritis (RVE) (ICD9-CM code and 008.8) in any position of the first 20 discharge diagnoses in children aged less or equal to 5 years between 2001 and 2005 were requested. Conclusion: Despite some limitations due to the HDD synthetic contents and low potential for clinical interpretation, the Regional HDD databases, including PD and SD, may be a useful tool for monitoring the clinical impact of RV vaccination introduction in Italy. Introduction Rotavirus (RV) infects virtually all children during the first few years of life and constitutes a common cause of physician consultation, hospital admission and death throughout the world. 1 Two RV vaccines, developed with different biological strategies, 2 have been licensed in Europe, rendering RV illness a vaccine preventable disease. In 2007, the European Society of Paediatric Infectious Diseases (ESPID) and the European Society of Gastroenterology, Hepatology and Nutrition (ESPGHAN) announced the release of a European Recommendation on RV immunization in Europe. 3 The recommendation states that all healthy children should be vaccinated against RV; that both currently available RV vaccines are effective and safe; RV vaccination can be incorporated into all European vaccination schedules; and that RV immunization can reduce the burden of RV disease in Europe. 3 In Italy there are no specific surveillance systems for RV disease in place. A recent study carried out at European level by using a mathematical model, estimated nearly 10,000 hospitalizations, 80,000 physician visits, 320,000 episodes and 11 deaths were due to RV each year in Italy. 4,5 Useful updated epidemiological data on the burden of RV disease in Europe (including Italy) coming from two direct prospective observations (REVEAL and SHRIK study) can be retrieved from the literature. 6,7 However, as it is not feasible to maintain large, specific observational studies to continually survey the burden of RV disease, a simpler surveillance method is needed. Hospital discharge databases (HDD) are one mean by which disease trends among hospitalizations after vaccine introduction may be observed. Hospital discharge databases have been reviewed in the USA since 1997 in order to obtain hospitalization rates for RV. 8,9 A specific active surveillance was subsequently implemented to validate the International Classification of Diseases (ICD) codes to estimate the proportion of children hospitalized for RV. 10 Recently, the largest USA HDD database available (HCUP) was used to study national rates, trends and risk factors of diarrhea, RV-associated hospitalizations and deaths among children <5 years of age to establish a baseline against which vaccine implementation could be measured. 11 *Correspondence to: Federico Marchetti; Pediatric Vaccines-Medical Department; GlaxoSmithKline S.p.A; Via A. Fleming, 2; Verona Italy; Tel.: ; Fax: ; fem75838@gsk.com Submitted: 05/13/08; Revised: 08/04/08; Accepted: 08/10/08 Previously published online as a Human Vaccines E-publication: 1 Human Vaccines 2009; Vol. 5 Issue 3
2 To assess the RV hospitalization rates in Italy, a preliminary study on the national ICD9-CM HDD database was conducted. 12 Briefly, the Italian HDD database, freely available from the web site of the national Ministry of Health, was searched to investigate the epidemiology of RV enteritis (RVE). The mean number of hospitalizations for RV in children aged <5 years was 4758 in , representing 84% of hospitalizations for viral enteritis (VE). RV was identified as agent in 17% of all intestinal infectious diseases in this age group. Despite confirming the predominant role of RV infections in children, the observed fraction was much lower than expected from the literature (0.52 hospitalizations due to RV per 100 children/year). 6 The main reasons for underestimation in the study were attributed to: (i) a high number of unidentified source of infections (no laboratory diagnosis), (ii) low sensitivity of ICD9-CM, (iii) the study was limited to the principal diagnosis in the HDD. 12 As only the latter issue could be improved, a study focused on the Regional HDD databases that allowed a review of all diagnostic levels in hospitalized patients was conducted. The primary objective of the study was to estimate the frequency of hospitalization for VE and RVE in children aged less than or equal to 5 years between 2001 and The secondary objectives were to describe the rates of primary (PD) and secondary (SD) diagnosis both for VE and RVE, main diagnostic/therapeutic procedures, outcomes and RV Diagnosis Related Group (DRG) codes. Results The reference population, those aged 5 years who were hospitalized between years in Piemonte, Veneto, Friuli Venezia Giulia and Marche, Italy, consisted of 434,335 hospitalizations (range 30,629 in Friuli Venezia Giulia to 171,997 in Veneto, Table 1). Admissions were approximately equally distributed over the studied years. A total of 13,234 VE diagnoses (range among regions ) were collected, representing 3% (13,234/434,335) of all hospitalizations in children aged 5 years. Of these 1.8% represented the PD, and 1.2% a SD. The peak in VE hospitalizations was observed in the first year of life. In this age group VE was responsible for 7.3% of all hospital admissions (4102/55,902), with the highest proportion (6.5% of all admissions, 2337/35,734) in the 7 12 months timeframe. The average hospital stay for VE was 4.1 days (s.d ± 3.9) and the median 3.0 days. A total of 8546 RVE cases (range between regions ), corresponding to 2% of all hospitalizations and 64.6% of all admissions for VE were observed. Of these, 1.2% were given as the PD, and 0.8% as a SD (Table 1). A peak in RVE hospitalizations was observed at the age of 1 year (Fig. 1). RVE was responsible for 4.9% of all admissions in children aged 1 year. As for VE, RVE accounted for the highest percentage of admissions in children 7 12 months of age (4.5%). The mean duration of hospitalization for RVE (PD or SD) was 4.4 days (s.d ± 4.2), median of 3.0 days. The expected seasonality of the RVE hospital admission was confirmed by a peak between January and May (Fig. 2). The overall RV hospitalization rate in the total regional population aged 0 5 years in the study timeframe for which population data were available ( ) was 279/100,000 residents (158/100,000 considering only cases of RV as PD). When introducing the SD into the database, the single Regional increment of RVE diagnosis ranged from 40% to 143% when compared to PD alone, (Table 1). The main (99.9%) DRG code for RVE as PD was 184 (esophagitis, gastroenteritis etc), while the main (51.4%) DRG code for RVE as SD was 298 (nutrition deviations, etc). The most frequent PD in RVE SD cases were dehydration (46.8%) and convulsions (4.3%). In RVE PD cases, more than 50% of HDD did not report any SD. The most frequent SD were dehydration (27.4%) and vomiting (2.7%). In 48.5% of RVE any medical procedure was recorded on the HDD; fluid infusion was reported in 32.3% of RVE cases. Two deaths (out of 8546 admissions for RVE) were identified, one in Piemonte and one in Veneto, both in males of 2 years of age. Overall, either for VE and RVE, the DRG costs were sustained by the NHS for nearly 99% of the cases. Discussion Our RVE hospitalization updated assessment confirms that RV disease remains a major cause of paediatric hospitalizations in Italy. RVE was implicated in 2.0% of all hospital admissions in children 5 years of age. The HDD analysis confirmed that RVE represents the greatest part of hospitalized VE, in agreement with previous results either in Italy, 12 other parts of Europe, 6,7 or the USA. 11 Direct comparisons with the previous study conducted in Italy using the national HDD database 12 can only be made with caution since the timeframe, the at-risk population and the geographical districts do not overlap. However, considering hospitalization rates with RVE as PD, the figures are comparable (158/100,000 versus 177/100,000). 12 Introducing the SD in the database led to a consistent increase (up to 143%) in RV diagnosis in Italy and to a hospitalization rate of 279/100,000. Such a result is likely to be a more sensitive estimate of the real disease burden, as it is closer to estimates, like the RVE hospitalization rates (between /100,000 in Europe) predicted by a mathematical model. 4,5 The study has some limitations related to the low number of Regions that participated in the study, poor sensitivity of the HDD, and the limited potential for clinical interpretation. In particular, we were unable to estimate what percentage of RVE SD was due to nosocomial infections. The results of the HDD analysis confirmed previous Italian data in terms of mean hospital stay for RV infection, 12 the early onset (in children <1 year of age) and the seasonality of RVE. The fluids infusion data and the RV-associated diagnosis (i.e., dehydration), may represent a surrogate for clinical severity at hospital entry. Data from the available studies document a higher clinical severity of RV positive acute gastroenteritis patients with respect to RV negative patients. 6,7,13 However, the lack of a severity score or at least surrogate clinical information can be seen as one of the major limitations of the HDD database analysis. The RV-related deaths identified in the study raised the issue of detection of RV mortality in Italy. Giambi et al., 4 reported 11 deaths caused by RV in Italy each year based on the modelling by Soriano et al. 5 To date, no deaths due to RV infection could be found out in the national Italian databases on infectious diseases. Thus, it can be assumed that in Italy, despite the lack of evidence, a number of deaths due to RV infection may take place each year. The DRG and mean hospital stay data documented in the study allows for rough calculation of hospital RV-associated costs for the National Healthcare System (NHS). However, as each Human Vaccines 2
3 Table 1 Hospitalization rates for rotavirus-associated disease as primary or secondary diagnosis among children 5 years of age in 4 Italian Regions, (total number of hospitalizations = 434,335), Regional HDD databases All regions Marche Friuli venezia giulia Piemonte Veneto Population 5 years 2001* (93624) (14285) (6460) (35930) (36949) (total hospitalizations) (89947) (13557) (6079) (34185) (36126) (86413) (13175) (6000) (32563) (34675) (82862) (12610) (6065) (31616) (32571) (81489) (12204) (6025) (31584) (31676) Total 2001* ,418,875 (434,335) (65831) (30629) (165878) (171997) Diagnosis of RVE N % N % N % N % N % Principal diagnosis (PD) Total RVE PD Secondary diagnosis (SD) Total RVE SD Total RVE PD or SD Rate All 279/100,000 PD 158/100,000 SD 121/100,000 N/% = number/percentage of all hospitalizations in the given year for the specified region. Rate = RVE hospitalizations per 100,000 population 5 years, * no population statistics available for DRG reimbursement class and the cost of 1-day of hospital stay may differ greatly from hospital to hospital and between Regions, no estimation of the RV-associated costs was calculated. Nevertheless, RV-generated direct medical costs for the NHS in Italy were recently estimated to be around 30 million euros/year in two independently carried out studies. 14,15 In conclusion, although the findings of the study suggest incomplete and underestimated detection of RVE, the substantial number of RV-associated hospitalizations and related costs underline the potential benefit of a universal RV immunization program in Italy. These data are in line with statements by ESPID/ESPGHAN in their European recommendations. 3 Despite incomplete coding of RV cases, the HDD data should provide consistent and timely information to monitor the impact of a RV immunization program. 10 To this purpose, the Regional HDD databases, including PD and SD, may be a useful tool for monitoring the clinical impact of RV vaccination introduction in Italy. Figure 1. Rotavirus-associated hospitalizations among children 5 years of age in 4 Italian Regions, , Number (A) and rate per 100,000 population (B) according to age. Regional HDD databases. 3 Human Vaccines 2009; Vol. 5 Issue 3
4 Figure 2. Seasonality of hospitalization for RV-associated disease among children 5 years of age in 4 Italian Regions, , Regional HDD databases. On the Y axis are reported the number of RVE hospitalizations for each month as the ratio RVE hospitalization/total hospitalization for each month could not be calculated in the study database (see Methods section). Methods This was a retrospective, observational study conducted using hospitalization data obtained from regional HDD in Piemonte, Veneto, Friuli-Venezia-Giulia and Marche in Italy. Together, these regions represent approximately 20% of the total Italian population and are geographically dispersed in central and northern Italy. 16 Source of data. The national HDD was established in 1994 and has been gradually expanded and improved. Currently the database contains nearly 13 million records relating to each individual year of operation and the degree of coverage of the flow of information is more than 95%. 17 The database requested from each Region included data from all the regional hospitals belonging to the NHS. The database included the following information: date of birth, start and end dates of hospitalizations, length of stay, PD and up to 19 SD, up to six diagnostic or therapeutic procedures, DRG and outcome. The data were acquired in electronic form, and were strictly anonymous. Study population. The study population included children aged 5 years who were hospitalized between the years 2001 and Hospitalizations were grouped by year and age. Visits without admission to hospital were excluded. Admissions with incomplete data and admissions coded as DRG 391 (healthy newborn) were also excluded from the study. Identification of enteric disease. Cases of VE were identified from diagnosis ICD9-CM codes Cases of RVE were identified using ICD9-CM code The following data were extracted: (i) the number of total hospitalisations, (ii) admissions coded with ICD9-CM code (VE) and (RVE) in any position within the first 20 discharge diagnoses (further to the usual 10 to increase sensitivity). No census or social condition analysis was performed as such data are not foreseen in the HDD. As the data collected in the study were retrospective and were retrieved from pre-existing databases released directly from the Regions, according to the national rules concerning the clinical research, notification of the study to Ethics Committees was not applicable, nor was informed consent of patients required. Patients privacy was secured by the Regions in accordance with legal requirements. Estimate of RV hospitalisation rates. The frequency of admissions with a PD or SD of VE or RVE was calculated as the ratio between patients with any VE or RVE diagnosis over the total aggregate observed in the database. Population statistics retrieved by the National Institute of Statistics (ISTAT) website 16 were used to estimate hospital admissions rates for RVE. Statistical analysis. Mean values and median with standard deviation (s.d) were calculated for numerical variables, percentages and absolute values were calculated for qualitative variables. The 95% confidence interval (CI) was derived from the binomial distribution. Acknowledgements This study was funded by GlaxoSmithKline S.p.A. References 1. Parashar U, Gibson C, Breese J, Glass R. Rotavirus and severe childhood diarrhea. Em Infect Dis 2006; 12: Glass R, Parashar U. The promise of new rotavirus vaccines. N Engl J Med 2006; 354: Vesikari T, Van Damme P, Giaquinto C, Gray G, Mrukowicz J, Dagan R, Guarino A, Szajewska H, Usonis V. European Society for Paediatric Infectious Diseases/European Society for Paediatric Gastroenterology, Hepatology and Nutrition evidence-based recommendations for rotavirus vaccination in Europe. JPGN 2008; 46: Giambi C, Tozzi A, Ciofi degli Atti M. Approfondimento sui rotavirus. EpiCentro 2007, Numero 15 Marzo. URL: 5. Soriano-Gabarrò M, Mzrukowic J, Vesikari T, Verstraeten T. Burden of rotavirus disease in European Union Countries. Ped Infect Dis J 2006; 25: Van Damme P, Giaquinto C, Huet F, Gothefors L, Maxwell M, Van der Wielen M. REVEAL Study Group. Multicenter prospective study of the burden of rotavirus acute gastroenteritis in Europe, : the REVEAL study. J Infect Dis 2007; 195: Human Vaccines 4
5 7. Forster J, Guarino A, Parez N, et al. Hospital-Based Surveillance to Estimate the Burden of Rotavirus Gastroenteritis among European Children Aged <5 Years. In: 25 th Annual Meeting of the European Society for Paediatric Infectious Diseases, Porto, Portugal Parashar UD, Holman RC, Clarke MJ, Bresee JS, Glass RI. Hospitalization associated with RV diarrhea in the United States 1993 through 1995: surveillance based on the new ICD9- CM RV-specific diagnostic code. J Infect Dis 1998; 177: Parashar UD, Chung M, Holman R, Ryder R, Hadler JH, Glass R. Use of hospital discharge data to assess the morbidity from rotavirus diarrhea and to monitor the impact of a rotavirus immunization program: a pilot study in Connecticut. Pediatrics 1999; 104: Hsu VP, Staat MA, Roberts N, Thieman C, Bernstein D, Breese J, Glass R, Parashar UD. Use of active surveillance to validate ICD code estimates of RV hospitalization in children. Pediatrics 2005; 115: Fisher KT, Viboud C, Parashar U, Malek M, Steiner C, Glass R, Simonsen L. Hospitalizations and deaths from diarrhea and rotavirus among children <5 years of age in the United States, J Infect Dis 2007; 195: Marocco A, Assael B, Gabutti G, Guarino A, Lopalco PL, Marchetti F, Ruggeri FM, Titone L, Tozzi AE, Vitali Rosati G, Zotti C, Franco E. Ricoveri per enterite da Rotavirus in Italia valutati mediante analisi delle Schede di Dimissione Ospedaliera negli anni Ig Sanita Pubbl 2006; 62: Albano F, Bruzzese E, Bella A, Cascio A, Titone L, Arista S, Izzi G, Virdis R, Pecco P, Principi N, Fontana M, Guarino A. Rotavirus and not age determines gastroenteritis severity in children: a hospital-based study. Eur J Pediatr 2007; 166: Standaert B, Marocco A, Assael B, et al. Analisi di costo-efficacia della vaccinazione universale in Italia con il vaccino Rix4414 contro i rotavirus. Pharmacoeconomics-Italian Research Articles 2008; 10: Giaquinto C, Callegaro S, Andreola B, et al. Costi della gastroenterite da rotavirus acquisita in comunità in età pediatrica a Padova in Italia. Pharmacoeconomics-Italian Research Articles 2007; 9: Istituto Italiano di Statistica (ISTAT). URL: Ministero della Salute. Ricoveri, diagnosi, interventi effettuati e durata delle degenze di tutti gli ospedali [accessed 2008]. Available at ric_informazioni/default.jsp 5 Human Vaccines 2009; Vol. 5 Issue 3
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