Compulsory and recommended vaccination in Italy: evaluation of coverage and non-compliance between 1998-2002 in Northern Italy

Background Since vaccinations are an effective prevention tool for maintaining the health of society, the monitoring of immunization coverage allows us to identify areas where disease outbreaks are likely to occur, and possibly assist us in predicting future outbreaks. The aim of this study is the investigation of the coverage achieved for compulsory (diphtheria, tetanus, polio, hepatitis B,) and recommended (pertussis, Haemophilus influenzae, measles-mumps-rubella) vaccinations between 1998 and 2002 in the municipality of Bologna and the identification of the subjects not complying with compulsory and recommended vaccinations. Methods The statistics regarding vaccinal coverage were elaborated from the data supplied by the Bologna vaccinal registration system (1998–2000) and the IPV4 program (2001–2002). To calculate the coverage for compulsory vaccinations and cases of non-compliance reference was made to the protocol drawn up by the Emilia Romagna Regional Administration. The reasons for non-compliance were divided into various categories Results In Bologna the levels of immunization for the four compulsory vaccinations are satisfactory: over 95% children completed the vaccinal cycle, receiving the booster for anti-polio foreseen in their 3rd year and for anti-dyphteria, tetanus, pertussis at 6 years. The frequency of subjects with total non-compliance (i.e. those who have not begun any compulsory vaccinations by the age of one year) is generally higher in Bologna than in the region, with a slight increase in 2002 (2.52% and 1.06% in the city and the region respectively). The frequency of the anti-measles vaccination is higher than that of mumps and rubella, which means that the single vaccine, as opposed to the combined MMR (measles-mumps-rubella) was still being used in the period in question. The most common reason for non compliance is objection of parents and is probably due to reduction of certain diseases or anxiety about the possible risks. Conclusion In Bologna the frequency of children aged 12 and 24 months who have achieved compulsory vaccination varied, in 2002, between 95% and 98%. As regards recommended vaccinations the percentage of coverage against Haemophilus influenzae is 93.3%, while the levels for measles, mumps and pertussis range from 84% to approx. 92%. Although these percentages are higher if compared to those obtained by other Italian regions, every effort should be made to strengthen the aspects that lead to a successful vaccinal strategy.


Background
Vaccinations are an effective prevention tool for maintaining the health of the individual and society as a whole. In Italy, however, certain diseases that are preventable with vaccines whose efficiency and safety have been fully tested and proven, still present a public health issue.
Monitoring immunization coverage allows us to identify areas where disease outbreaks are likely to occur, and possibly assist us in predicting future outbreaks. Also, monitoring can help keep immunization coverage high. One of the main aims of public health services throughout the world is therefore to obtain reliable data about the level of immunization with a view to supporting the implementation and monitoring of vaccination programs [1].
Vaccinal coverage is normally referred to in terms of the percentage of subjects vaccinated out of the total target population. In pediatric age the target population is made up of the cohorts of children who were under one year old as of 31 December in a given locality, while the vaccinal state is defined as the number of doses required to bring about immunity. To determine vaccinal coverage, the WHO (World Health Organization), on a yearly basis, considers the percentage of children who have received three doses of vaccines against diphtheria, tetanus, polio, hepatitis B, pertussis and Haemophilus influenzae (Hib), and one dose of anti-measles, mumps and rubella (MMR) by the age of 24 months.
In Italy the vaccination coverage of newborns (i.e. the relationship between the number of doses of vaccine administered at a certain age in a given geographical area and the resident population of the same age) is estimated every year by the regional authorities. The data are then sent to the Ministry of Health. In order to have a more detailed picture of the national situation (to identify areas lacking coverage, to confirm coverage where present and to obtain further details, for example, about reasons for delay in application), a cluster survey, called ICONA, was made in 1998 by means of interviews carried out at the subjects' home. The results showed a considerable difference between the coverage achieved for compulsory (diphtheria, tetanus, polio, hepatitis B) and for recommended (pertussis, Hib, measles, mumps ands rubella) vaccines [2].
After five years the national survey was repeated (ICONA 2003) [3], with the particular aim of checking the data supplied by regional authorities to the Ministry and investigating the reasons for non-compliance. The study revealed that while the situation had improved, there were still differences between one region and another.
In the wake of the approval of the National Health Plan (NHP) to eliminate measles and congenital Rubella (13 November 2003) and considering the current attempt to overcome the existing division between compulsory and recommended vaccinations, we decided to undertake a study with the following objectives: 1. To investigate the coverage achieved for compulsory and recommended vaccinations between 1998 (the year when the NHP set the objective of 95% coverage) [4] and 2002 in the municipality of Bologna (capital of Emilia-Romagna region), which coincides with the East and West Districts of the city's health service; 2. To identify the categories of subjects not complying with compulsory and recommended vaccinations

Methods
In Bologna the vaccination of subjects under 18 years of age is carried out almost exclusively by the Community Pediatric Service (which combines the former pediatric surgeries and the Nursery and Infant School Medical Service). In the current make-up of Bologna Health Services, this operative Unit is situated within the Department of Primary Care, and is divided into two districts: Bologna East and Bologna West.
Until 2000 the registration of vaccinations was carried out by the Public Health Department by means of a computerized system run by the Municipality of Bologna. The office had access to registration records (they could check the issuing of vaccination certificates), but not to the more detailed data processing system (search for cases of noncompliance, new residents etc).
Details of births or new residents under the age of 6 years were passed on to the subject's local pediatric consultation centre by the municipal Registry Office, with the issuing of a vaccination booklet. At the end of the year the Office printed a list of non-compliances and sent it to the respective Pediatric Centres for a further check. Finally, full details were sent yearly to the Regional offices by the Community Pediatric Service. During the year health workers could check the extent of vaccinal coverage only by means of the paper documents (files) sent at the same time as the vaccination booklets. The only way that the employees who registered the vaccinations on the files could find out about subjects who had moved or died was by going directly to the municipal registry office. Alongside the installation of the vaccinal registration program, a project was launched to set up an on-line link between the various centres administrating the vaccines at pediatric age. This allows the immediate registration of vaccinal data at the moment of vaccination and the possibility to consult in real time the vaccinal situation of each subject, including details of any migration and access to the so-called "notes" (possible contra-indications, previous adverse reactions, refusals etc).
The great advantage of the revised system is that it is now possible to monitor vaccinal coverage at any time, obtain information pertaining to moves or deaths, and contact residents who have not been vaccinated.
The statistics regarding vaccinal coverage were elaborated from the data supplied by the vaccinal registration system of the Municipality of Bologna (1998)(1999)(2000) and the IPV4 program (2001)(2002).
To calculate the coverage for compulsory vaccinations and cases of non-compliance reference was made to the protocol drawn up by the Emilia Romagna Regional Administration: compulsory vaccinations at 12 months residents who reached one year during the year of reference and received at least 2 doses of each compulsory vaccine by the age of 12 months; compulsory vaccinations at 24 months residents who reached two years during the year of reference and received at least 3 doses of each compulsory vaccine by the age of 24 months. subjects totally or partially non-complying subjects who did not receive any compulsory vaccination by the age of one year or received only one dose of the compulsory vaccinations.
The reasons for non-compliance are categorized matching those used in the collection of regional data for coverage: -living abroad: children resident in Bologna but living abroad for a long period -refusals or objectors: children whose parents were explicitly against at least one compulsory vaccination -immigrants: children from other regions of Italy or from other countries -delays: children who received at least one vaccination after the pre-established dates For all recommended vaccinations (anti pertussis, anti Hib, anti measles-mumps-rubella) the extent of coverage was calculated at 24 months and also at 13 years for antimeasles and anti-rubella.

Results
The levels of immunization for the four compulsory vaccinations (taken as a whole) achieved during the five-year period in question are shown in table 1. In the municipality of Bologna these levels are satisfactory (>95%), but are lower than the overall levels reached in Emilia Romagna, although from the year 2000 the percentage of children vaccinated in the region also shows a slight decrease. Interestingly, the statistics differ from one district of the city to another: in Bologna East non-compliance tends to be higher. The frequency of subjects with total non-compliance (i.e. those who have not begun any compulsory vaccinations by the age of one year) is generally higher in Bologna (especially in the East District) than in the region, with a    The underlying trend for such coverage tends to vary over the five-year period. The level of protection against pertussis remains more or less constant, even though it falls a little below the regional average. However, a steady rise can be seen for the other recommended vaccinations, especially evident in the case of anti-Hib (41.8% and 50.6% of children resident in Bologna and Emilia Romagna respectively in 1998, against 93.3% and 95.2% in 2002). The notable increase in anti-Hib vaccination can probably be attributed to the availability of a combined vaccine.
At 12 months a similar consistent increase in the number of subjects receiving the anti-Hib vaccination can again be seen in Bologna (from 26.7% to 91.6%) and throughout the whole of the region (from 40.9% to 96.0%). In Bologna the target percentage of 95% coverage for the recommended vaccinations has yet to be reached. Table 6 also shows how the frequency of the anti-measles vaccination is higher than that of mumps and rubella, which means that the single vaccine, as opposed to the combined MMR, was still being used in the period in question. From the year 2000, the levels of coverage reached in Bologna for anti-measles and anti-rubella at 13 years of age would seem to indicate a greater attention to these vaccinations in Bologna than in other parts of the region. Unlike the findings for the compulsory and recommended vaccinations, no difference was found between the two Districts of the city.

Discussion
The principal infant vaccinations have now been included in the Essential Levels of Assistance that the Region must guarantee free of charge to all citizens. Despite this, however, the levels of coverage for compulsory and recommended vaccinations have not yet reached homogeneous levels. In the municipality of Bologna the frequency of children aged 12 and 24 months who have been vaccinated against DTP, tetanus, polio, hepatitis B and pertussis varied, in 2002, between 95% and 98%. As far as the recommended vaccinations are concerned, the percentage of coverage against Hib is 93.3%, while the levels for measles, mumps and pertussis range from 84% to approx. 92%. Although these percentages are generally lower than the regional levels, they can nevertheless be considered fairly good if compared to those obtained by certain other Italian regions [5] and Italy as a whole. -to reduce and maintain the incidence of Congenital Rubella Syndrome (CRS) at levels below 1 case in every 100.000 live-borns.
-to achieve and maintain the elimination of measles at a national level, interrupting its indigenous transmission.
It should be stressed that the inadequate vaccinal coverage achieved for anti-measles does not interrupt the circulation of the virus and may even bring about a greater probability of complications and outbreaks; it prolongs the interval between epidemics and delays the outbreaks until later in adult life, as presumably occurred in the Campania region [9]. It has also been shown that low coverage rates tend to enhance epidemics associated with imported viruses [10]. In 2002 there was quite a large outbreak of measles in Italy. The geographic distribution of cases strictly coincided with that of the vaccine coverage, which is lower in southern Italy [11].
As far as the data on non-compliance (compulsory vaccinations) is concerned, it is interesting to note that the frequency is higher in Bologna than the regional average and, in particular, Bologna East has a higher percentage than Bologna West both at 12 and 24 months. The percentage of total non-compliance is also greater in the East district than the West. Furthermore, the number of children in this category is steadily increasing: passing from 0.88% in 1998 (regional mean 0.40%) to 2.52% in 2002 (regional mean 1.06%).
The most common reason for non compliance is objection of parents. Objection to compulsory vaccinations, especially in Bologna (but not throughout the whole of Italy), is on the rise, even though vaccinal coverage remains above 95%. There is an increasing tendency not to comply with vaccinal obligations, probably because the disappearance (diphtheria, polio) or limited incidence (tetanus, hepatitis B) of certain diseases has led some people to believe that the relative vaccines are obsolete and there is less concern about the risk of contracting infectious diseases. However, recent reports [12] indicate that Italy could risk the importation of the wild polio virus on account of the continuous exchanges with North African countries which are currently in danger of an epidemic due to their negative behaviour towards the vaccination, thus allowing the virus to pass into otherwise polio-free areas.
A further reason for the refusal of vaccination is the anxiety about the possible risks associated with receiving the vaccines. In other words there is the pressure, especially in industrialised countries, from organised groups opposing the practice of vaccination and spreading alarmist and often inaccurate information [13,14]. For example, there is absolutely no scientific evidence that the presence of thiomerosal in vaccines can be linked to the increase in autism [15] or that there is any link between autism and the anti-measles vaccination [16,17]. If the tendency not to vaccinate children becomes more pronounced over the coming years, it could result in serious consequences for public and individual health. It should be remembered that many children still die from preventable infectious diseases and connected pathologies not only in the socalled "poor" countries, but also in other nations. In Europe, the political, social and economic changes that took place following the fall of the Berlin Wall have led to a decline in the levels of immunization in many regions of Eastern and Central Europe, resulting in thousands of new cases of diseases such as diphtheria [18]. For this reason the level of dissent needs to be constantly monitored.
The computerized system adopted in Bologna can, in fact, help improve the identification of non-vaccinated subjects and verify the phenomenon of immigration.

Conclusion
In Bologna the frequency of children aged 12 and 24 months who have achieved compulsory vaccination varied, in 2002, between 95% and 98%; As regards recommended vaccinations the percentage of coverage against Hib is 93.3%, while the levels for measles, mumps and pertussis range from 84% to approx. 92%. Although these percentages are higher if compared to those obtained by other Italian regions, it is necessary to take into account that in Italy, during the 1998-2002 period the mean number of cases of measles, rubella and mumps was 5456, 3685 and 24663 respectively [19]. Therefore, every effort should be made to strengthen the aspects that lead to a successful vaccinal strategy: the continuous improvement in the quality of services, the provision of accurate information to parents and, finally, the training of health workers -in accordance with the suggestions of the WHO -to monitor adverse reactions and maintain an open and constant dialogue with the media about the problems of vaccine safety [18,20].