Mortality and educational level among diabetic and non-diabetic population in the Turin Longitudinal Study: a 9-year follow-up

Roberto Gnavi1, Alessio Petrelli1, Moreno Demaria2, Teresa Spadea1, Quirico Carta3 and Giuseppe Costa4

1 Epidemiology Unit, Local Health Authority 5 of Piedmont Region
2 Environmental Epidemiological Unit, Regional Environmental Protection Agency
3 Diabetes Regional Commission of Piedmont Region
4 University of Turin—Department of Public Health

Correspondence: Roberto Gnavi, ASL 5, Servizio di Epidemiologia, Via Sabaudia 164, 10095 Grugliasco (TO), Italy. E-mail: roberto.gnavi{at}epi.piemonte.it


    Abstract
 Top
 Abstract
 Methods
 Results
 Discussion
 References
 
Background People in a lower social position have a higher prevalence of unhealthy behaviour, more difficult access to healthcare, and lower compliance with drug treatment; as a consequence, social differences in mortality are likely to be higher in people with diabetes compared with the non-diabetic population. We compared diabetics with non-diabetics in terms of mortality and social differences in mortality.

Methods In all, 31 264 residents in Turin (northern Italy), who were ≥20 years old, registered in the local diabetes register between 1991 and 1999. They were followed up from recruitment to December 1999, and their cause-specific mortality by educational level was analysed. This was compared with that of the local non-diabetic population. Diabetes was classified as type 1 (≤35 years at diagnosis) or type 2 (>35 years).

Results For type 1 diabetes, the all-cause standardized mortality ratio (SMR) was 197.6 (95% CI:155.7, 247.4) in men and 336.0 (95% CI:259.3, 428.2) in women; for type 2 diabetes, the all-cause SMR was 142.8 (95% CI:138, 147.6) in men and 143.4 (95% CI:138.5, 148.5) in women. Whereas social differences in mortality were evident among non-diabetic men and women for all causes of death considered, no significant differences were found among diabetic women. Mortality was slightly increased among less educated diabetic men, particularly for neoplasms, although this gradient was less steep than that among non-diabetics.

Conclusions These results suggest that the regular clinical follow-up and health education provided by the local network of diabetic centres might play an important role in confronting the adverse effects of diabetes and in reducing social differences in health.


Keywords Diabetes mellitus, social class, mortality, Italy

Accepted 2 December 2003

For various causes of death, especially cardiovascular disease, mortality among those with diabetes is higher than that among people without this disease.1–3 To increase the sur- vival of diabetic patients, changes in lifestyle, appropriate drug treatment, regular glycaemic control, and the continuous surveillance of health status are necessary.4 In most countries, including Italy, social position has been shown to be inversely related to certain types of unhealthy behaviour,5,6 and to access to high quality care;7–9 thus social inequalities in mortality can be expected to be greater among people with diabetes, compared with those without diabetes. Nonetheless, very few studies have compared social differences in mortality between these two populations, and the available results are contradictory. Specifically, in the UK, there is a clear socioeconomic gradient in mortality both in diabetic and in non-diabetic populations,10,11 whereas in Finland, although social class differences have always been present among non-diabetic people, only in the 1990s did they emerge among people with diabetes.12,13 However, the differences in the results of these studies may have been due both to problems in data collection and differences in the health systems of the two countries.14,15

To compare diabetics with non-diabetics in terms of mortality and social differences in mortality, we conducted a study among people with diabetes living in the city of Turin, Italy, and compared them with Turin residents without diabetes.


    Methods
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 Abstract
 Methods
 Results
 Discussion
 References
 
The study population was selected from those registered in the Piemonte Diabetes Register (PDR), which since 1980 has collected data on diabetic patients residing in the Region of Piemonte (North-West Italy; capital city, Turin, approximately 900 000 inhabitants), mainly for administrative purposes. When a general practitioner suspects diabetes, he/she sends the patient to one of the 80 public local diabetes centres for a confirmation of the diagnosis. When diagnosis is confirmed, the diabetes centre asks the patient to register with the PDR. Since registered patients are provided with benefits such as free-of-charge drug prescriptions and laboratory testing, most patients agree to register. According to the PDR, the prevalence of diabetes increased from the early 1980s until 1990, which can be considered as an enrolment phase; since 1990 the prevalence has stabilized and is consistent with that observed in other areas of Piemonte.16 The present analysis was restricted to residents of Turin who registered with the PDR between 1 January 1991 and 31 December 1999 and who were ≥20 years of age in 1991 (so as to allow all participants the chance to achieve the highest level of education).

To obtain data on educational level and to perform mortality follow-up, people registered in the PDR were linked to the database of the Turin Longitudinal Study (TLS),17,18 a dynamic, population-based, database whose core is represented by the Turin Population Register (TPR), which collects data on all residents of Turin. As part of the TLS, the TPR data are linked every 10 years to the database of the national census to assign individual socioeconomic variables; the TPR data are also linked to the Turin Mortality Register (TMR). Linkage is performed using a 10-step procedure based on the fiscal code. The validity of the record linkage was tested: values of sensitivity and specificity were, respectively, 98% and 99%. As a non-diabetic control group, we considered all other residents of Turin who were registered with the TPR and were ≥20 years of age in 1991.

Based on age at diagnosis, diabetes was classified as either type 1 (≤35 years of age) or type 2 (>35 years). Educational level was assigned using the data from the 1991 census, or, for people who moved to Turin after this census, using the self-reported information collected by the TPR. Educational level was classified into three groups: high (university or high school), medium (middle school), and low (primary school or no formal education).

Information on cause of death was limited to the underlying (primary) cause (secondary diagnoses are not recorded in the TMR), classified according to the International Classification of Diseases, Ninth Revision (ICD-9): neoplasms (140–239), lung cancer (162), diabetes (250), circulatory diseases (390–459), coronary heart disease (410–414), cerebrovascular disease (430–438), respiratory diseases (460–519), accidents and violence (E800–E999), and suicide (E950–E959).

Standardized mortality ratios (SMR) were calculated using cause-specific mortality rates among the non-diabetic population as the standard. A survival analysis was conducted to determine social differentials in mortality using Cox proportional hazards models. We considered as lost to follow-up people who moved out of Turin during the study period (7% with diabetes and 15% without diabetes), and, when assessing cause-specific mortality, those who died for causes other than those under study. All models were stratified by gender and type of diabetes and were adjusted for age and area of birth (northern, central, southern Italy, and abroad). The latter is a major confounder in Turin, given that most of the underprivileged are immigrants from southern Italy, an area with low mortality for some major causes of death.19 Reduction in normalized prediction function was used as a convergence criterion. Ties were handled using the approximate likelihood of Breslow. Goodness-of-fit of the models was also evaluated using the likelihood ratio method. Interactions were tested using the likelihood test. Tests for trend were performed using the slope parameter of the linear regression fitted on the estimated HR. The models were fitted using PROC PHREG by SAS System, version 8.02.20


    Results
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 Abstract
 Methods
 Results
 Discussion
 References
 
Between 1991 and 1999, 31 264 residents in Turin who were ≥20 years of age in 1991 registered with the PDR (1608 with type 1 diabetes and 29 656 with type 2 diabetes). They were followed for mortality for 195 855 person-years. The non-diabetic population consisted of 874 801 people who, in the same period, were registered with the TPR (followed for 6747329 person-years).

Table 1 shows the cause-specific mortality by gender among the two populations. During the study period, 6814 deaths were recorded among diabetics (141 deaths among type 1 diabetes and 6673 deaths among type 2 diabetes) and 79 927 deaths among non-diabetics. Compared with the non-diabetic population, the risk of death for those with type 1 diabetes was doubled in men and more than tripled in women. Excluding diabetes itself, circulatory disease showed the highest SMR (196.9 in men and 370.1 in women). No statistically significant differences were found between diabetics and non-diabetics for the other main causes of death, with the exception of respiratory disease among women. Among people with type 2 diabetes, the risk of death was approximately 40% higher than that among people without diabetes for both men and women. An increased risk was observed for almost all of the causes considered, with the exception of cerebrovascular disease and respiratory disease in both genders, lung cancer and accidents in women, and suicide in men. With specific regard to mortality for circulatory disease, overall, the risk among people with type 2 diabetes was slightly increased; most of this increase is attributable to coronary heart disease.


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Table 1 Number of deaths and standardized mortality ratios (SMRa) among diabetic compared to non-diabetic population, by type of diabetes, gender, and cause of death; Turin, Italy; 1991–1999

 
Interactions between social class and diabetes (separately for the two types), social class and age class, type of diabetes and age class were statistically significant (P-value < 0.01). Table 2 shows the mortality by age group and educational level among diabetics and non-diabetics. Among men, educational level was inversely related to mortality for all age groups and for people both with and without diabetes, although these inequalities were more evident for type 1 diabetes and in the youngest age group and less evident for type 2 diabetes and in the oldest age group. Among women, no statistically significant educational inequalities in mortality were observed at any age for type 2 diabetes, whereas there were significant disadvantages among the youngest and less educated women with type 1 diabetes and among non-diabetic women in every age group.


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Table 2 Mortality by type of diabetes, gender, age group at death, and educational level; hazard ratios (HRa) and 95% CI; Turin, Italy; 1991–1999

 
Table 3 shows the mortality by specific cause of death and educational level among diabetics (type 1 and type 2 combined) and non-diabetics. Among people without diabetes, an inverse association was present for all main causes of death for both men and women, whereas among diabetic men, only neoplasms, lung cancer, and respiratory disease showed higher mortality among the least educated, with social gradients that were similar to or less steep than those among non-diabetic men. Among diabetic women, the nearly absent social gradient for all-cause mortality was largely influenced by the absence of differences in mortality from neoplasms and from diabetes. All other causes of death roughly showed the same social pattern in the two populations.


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Table 3 Mortality among diabetic and non-diabetic population by specific cause of death and educational level; hazard ratios (HRa) and 95% CI; Turin, Italy; 1991–1999

 
Table 4 shows the cause-specific mortality among diabetics compared with non-diabetics by educational level. The risk of death was 68% higher among diabetic men with the highest educational level, yet only 38% higher among those with the lowest educational level. This disadvantage for the highest social group with diabetes was present for almost all causes of death, with the exception of neoplasms; the highest HR were found for diabetes, coronary heart disease, and accidents. A similar pattern was observed among women: the risk of death overall was 83% higher among diabetic women with the highest educational level and 45% higher among those with the lowest educational level. Diabetes, neoplasms, and accidents and violence showed the highest mortality among well-educated diabetic women, whereas for circulatory disease the intermediate group showed the highest excess.


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Table 4 Hazard ratios (HRa) and 95% CI of cause-specific death among diabetic population, as compared with non-diabetic population, by educational level; Turin, Italy; 1991–1999

 

    Discussion
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 Abstract
 Methods
 Results
 Discussion
 References
 
The availability of data from a regional diabetes register and from the Turin Longitudinal Study allows a unique opportunity, in Italy, to compare a diabetic population with a non-diabetic population in terms of mortality and social inequalities in mortality. With regard to differences in mortality, we confirmed that people with diabetes have an increased risk of death, specifically, a 42% increase, both in men and in women, for type 2 diabetes, and a 98% increase in men and a 236% increase in women for type 1 diabetes. These results are similar to those reported in another area of northern Italy.3 Diabetes itself and circulatory disease (mainly coronary heart disease) had the highest excesses.

With regard to social inequalities, among the non-diabetic population, people with a higher educational level had a lower mortality, yet surprisingly, among those with diabetes there were no significant social differences among women with type 2 diabetes in any of the age groups and only slight inequalities among men with type 2 diabetes, which were more evident for the youngest age group. On the other hand, men and women with type 1 diabetes had the steepest social gradient compared with both people with type 2 diabetes and non-diabetics. When considering type 1 and type 2 diabetes as a single group, for almost all main causes of death the social gradient in mortality was milder or even absent among people with diabetes, whereas it was quite evident among those without diabetes; among diabetics the risk of death was higher in those with a higher educational level.

In attempting to explain our results, potential biases should be considered. Specifically, the PDR could be incomplete, which would reduce the social gradient if people with a lower social position with less severe diabetes or people with a higher social position with more severe diabetes were preferentially included. For type 2 diabetes, it is likely that both of these conditions were present. People with a higher social position with mild diabetes could be less interested than the more disadvantaged in the economic advantages of registering with the PDR, making them less likely to register, which would lead to an overestimation of mortality among diabetics with a high social position. For type 1 diabetes, this source of bias is probably less relevant, given the higher severity of the disease, which involves more frequent clinical or biochemical evaluation. On the other hand, only 936 (1.2%) of deaths in the non-diabetic population were due to diabetes, which can be reasonably attributed, at least in part, to previously undiagnosed diabetes being discovered at the moment of death. Moreover, if the selection bias were strong, there would be no evident social gradient in mortality due to diabetes in the non-diabetic population, yet in our study (Table 3) a social gradient was present and it showed the same direction as that in the diabetic population. Secondly, we used a rather crude definition for type 1 and type 2 diabetes (i.e. based on age of diagnosis).16 However, since type 1 diabetes is rare in comparison with type 2 diabetes, most type 2 cases are probably correctly defined, whereas the type 1 group is likely to include a proportion of cases of type 2 diabetes. Thus, the mortality rates among type 2 diabetes were probably not seriously affected, whereas those among type 1 are likely to have been underestimated. Consequently, the SMR in Table 1 can be considered as underestimates for type 1 diabetes and as accurate for type 2. As a sensitivity analysis we re-analysed our data using the age of 25 at diagnosis as a cut-off between type 1 and type 2 diabetes. While social differences in people with type 2 diabetes remained almost unchanged, differences in subjects with type 1 diabetes increased, remaining statistically significant only in the lowest educational group. An additional consideration concerns the distribution of people who emigrated during the follow-up period: among people with diabetes 15% were in the highest educational group, while they were 39% in the group without diabetes. This difference is largely explained by the sex and age distributions of the two populations. Moreover, when mortality rates both 20% higher and 20% lower than those recorded were considered in people who emigrated, hazard ratios showed very slight variations.

In conclusion, we feel that we can be confident in our conclusions, in that a large number of people were studied, the follow-up was relatively long, people with diabetes were excluded from the reference population, and an individual social position indicator was used, although the conclusions involving the classification of diabetes as type 1 or type 2 have to be considered with caution. Even if the risk of death were overestimated among patients with a high educational level, the main result of this study remains unchanged: socially dis-advantaged diabetics do not seem to differ from more affluent ones in terms of the probability of survival. This is particularly surprising when considering that people in a lower social position have a higher prevalence of unhealthy behaviour, more difficult access to healthcare, and lower compliance with drug treatment, and that these factors make it difficult to obtain and maintain appropriate glycaemic control.4 The high social differences in type 1 diabetes can be explained by the higher severity of the disease in younger people, who are probably less likely to adopt the types of behaviour necessary for contrasting the most severe effects of diabetes.

Our finding of a less-marked increase in the risk of mortality among people with diabetes compared with the increases reported in previously published studies,1,2 together with the absence of a significant social gradient, needs to be explained. In Italy, although the National Health Service ensures that all citizens are provided with quality healthcare at nearly no cost, there do exist social differences in health.21 This means that a formally equitable health service is not sufficient for guarantee-ing that all citizens, irrespective of their social position, have the same health status, but the way in which healthcare is organized and provided may be of relevance. Regular clinical follow-up provided by general practitioners22 and attendance at diabetes centres have been shown to increase the probability of survival among diabetic patients.23 A plausible, although unproven, explanation is that in Turin a network of diabetes centres has existed since the end of the 1970s and patient education and working in close co-operation with general practitioners have always been a central part of their activities. Moreover, the diabetes centres offer courses aimed at modifying unhealthy behaviours and provide medical and laboratory examinations at no cost to all patients registered in the PDR. The advantages of being followed by a well-organized medical staff which adheres to well-defined clinical guidelines are reflected in the lack of a social gradient in mortality for those causes of death that benefit most from regular clinical examinations, such as diabetes itself, female cancers (through the early referral of symptoms), cerebrovascular disease (through hypertension control), and, to some extent, accidents and violence (through psychological support). On the other hand, the presence of social differences in mortality for causes of death that are attributable to unhealthy behaviour (as in the case of smoking and lung cancer and, to a lesser extent, coronary heart disease) suggest that improvements in education among patients could further strengthen the care provided. Moreover, young people with type 1 diabetes and poorer levels of education represent a group requiring special efforts to prevent premature deaths.

In conclusion, we believe that the local network of diabetic centres might play an important role in confronting the adverse effects of diabetes and in reducing social differences in health. Further investigation into the way in which diabetes care is conducted could provide information on how to confront social inequities in health in other fields of medical care.


KEY MESSAGES

  • Mortality, mainly from cardiovascular disease, is increased in people with diabetes, but there are wide variations between countries and, apparently, social groups.
  • In the period 1991–1999 people with diabetes resident in Turin (northern Italy) showed an increased risk of mortality, mainly from cardiovascular disease when compared with the local population without diabetes. This result is similar to those reported in other areas of Italy, but the risk is less marked compared with that reported in most previously published studies.
  • Whereas social differences in mortality were evident among men and women without diabetes, no significant differences were found among women with diabetes. Mortality was slightly increased among less-educated men with diabetes, although this gradient was less steep than that among men without diabetes.

 


    Acknowledgments
 
The study was supported by the 1998 Research Program of the Italian Ministry of Health—‘Programmi speciali’ ex art. 12 D. Lgs.502/92—entitled ‘Un sistema informativo, un libro bianco, un modello di monitoraggio per implementare gli obiettivi di equità nella salute e nell'assistenza in Italia’.


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