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Recent diabetes-related mortality trends in Romania

Article  in  Acta Diabetologica · May 2018


DOI: 10.1007/s00592-018-1156-5

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Acta Diabetologica
https://doi.org/10.1007/s00592-018-1156-5

1
ORIGINAL ARTICLE

2 Recent diabetes-related mortality trends in Romania


3 Sorin Ioacara1,2   · Elisabeta Sava2 · Olivia Georgescu2 · Anca Sirbu1,2 · Simona Fica1,2

4 Received: 11 April 2018 / Accepted: 3 May 2018


5 © Springer-Verlag Italia S.r.l., part of Springer Nature 2018

6 Abstract
7 Aims  As there are no published articles on country-level diabetes-related mortality in Romania, we aimed to investigate
8 this aspect for the 1998–2015 period.

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9 Methods  Anonymized demographic and diabetes-related mortality data (underlying or first secondary cause of death)

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10 were retrospectively obtained from the National Institute of Statistics/Eurostat microdata. Age-standardized mortality rates
11 (ASMR) and their annual percentage change (APC) were analysed.
12 Results  During 1998–2015, 4,567,899 persons died in Romania, among whom, diabetes was responsible for 168,854 cases.

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13 The ASMR for diabetes was 39.34 per 100,000 person-years (p-y) (95% CI 39.32–39.35). There was an increase in ASMR
14 from 27.10 per 100,000 p-y (95% CI 27.01–27.19) in women and 30.88 per 100,000 p-y (95% CI 30.77–30.99) in men in

PR
1998 to 35.42 per 100,000 p-y (95% CI 35.34–35.51) in women and 48.41 per 100,000 p-y (95% CI 48.29–48.52) in men,
15
16 in 2015. The mean APC in women was 3.8% per year (95% CI 3.5–4.0, p < 0.001) during 1998–2010 and − 1.9% per year
17 (95% CI − 2.7 to − 1.1, p < 0.001) during 2010–2015. The mean APC in men was 5.3% per year (95% CI 5.0–5.5, p < 0.001)
18 during 1998–2010 and − 1.5% per year (95% CI − 2.2 to − 0.8, p < 0.001) during 2010–2015. Diabetes-related mortality
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19 rates increased with age, with men experiencing higher mortality rates than women for most age groups and calendar years.
20 Conclusions  Diabetes-related mortality rates increased significantly in Romania during 1998–2010, followed by a steady
21 decline during 2010–2015.
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22 Keywords  Mortality · Life expectancy


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23 Introduction both scientific and public debates, recent trends in diabetes- 32


related mortality received significantly less worldwide cov- 33
24 Diabetes mellitus affected 425  million adults aged erage [5, 6]. 34
25 20–79 years worldwide in 2017 (8.8% prevalence), and this A national survey conducted among primary care clin-
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35
26 number is expected to rise to approximate 629 million (9.9 ics during 2012–2014 estimated a diabetes prevalence in 36
27 prevalence) by the year 2045 [1]. Although some heteroge- Romania of 11.6% (including 2.4% previously unknown 37
28 neity does exist, mortality rates in people with diabetes are cases), significantly higher in men as compared with women 38
29 generally significantly higher as compared with the general [7]. The oral glucose tolerance test performed in this trial 39
30 population [2–4]. While cardiovascular and cancer mortal- showed an additional 16.5% prevalence for prediabetes 40
31 ity trends over the last decade received wide coverage in [7]. Life expectancy in people with diabetes significantly 41
increased during the last decades, making diabetes a major 42
burden on the public health system [8, 9]. Increasing life 43
A1 Managed by Massimo Porta. expectancy suggests that diabetes mortality rates might be 44
declining in Romania. However, no country-level study has 45
A2 * Elisabeta Sava
drelisabetasava@yahoo.com been yet conducted on this topic. Thus, the aim of this study 46
A3
was to investigate recent trends in diabetes-related mortality 47
A4 Sorin Ioacara
drsorin@yahoo.com in Romania, during 1998–2015. 48
A5

1
A6 “Carol Davila” University of Medicine and Pharmacy,
A7 Bucharest, Romania
2
A8 “Elias” University Emergency Hospital, Bucharest, Romania

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49 Materials and methods problem. Diabetes-related death was defined based on the 96


presence of diabetes as the underlying or first secondary 97
50 Study population cause of death on the death certificate. 98

51 The Romanian National Institute of Statistics started to Statistical analysis 99


52 acquire country-level deaths-related data in 1994, based on
53 mandatory digital reporting of the death certificate. How- Diabetes-related crude mortality rates (CMR) and age-stand- 100
54 ever, data collection was not as reliable during the first ardized mortality rates (ASMR) were calculated using the 101
55 4 years as in the most recent period, mostly due to some WHO world standard population 2000–2025 [10]. We con- 102
56 changes in the methodology occurring in 1998 (i.e. regis- sidered 5 years age groups starting at age 20 years, with the 103
57 tration of a secondary cause of death). Consequently, data last group including all deaths at age 85 years and beyond 104
58 regarding 1994–1997 were omitted, and all consecutive (i.e. 20–24, 25–29, …, ≥ 85 years). All deaths under 20 years 105
59 subjects who lived and died in Romania during 1998–2015 were excluded from the study. The annual percentage change 106
60 were included in the study. An anonymized database was (APC) of the ASMR was analysed using the Poisson regres- 107
obtained from the National Institute of Statistics, based on sion. The APC and ASMR data were reported separately for

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61 108
62 the Eurostat microdata. 1998–2010 and 2010–2015 due to a significant change in 109

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trends around year 2010. Year 2010 was used in both periods 110
to avoid a gap in trend reporting. All calculations were done 111
Outcomes and confounders in Stata version 13 (http://www.stata​.com).

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63 112
The study was approved by the local ethics committee. 113
Death-related data were collected retrospectively using Informed consent was not obtained because this is a retro-

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64 114
65 the information available on the death certificate. Gender, spective, anonymized database-driven study. Written con- 115
66 date of birth, age at death, year of death, cause of death sent for data usage was obtained from the Eurostat/National 116
67 (underlying and first secondary cause of death) and place Institute of Statistics. 117
68 of death (at home, in hospital or elsewhere) were avail-
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69 able for analysis. Age- and sex-specific data on the alive
70 population were obtained from the National Institute of Results 118
71 Statistics (Tempo database), on a yearly basis. The data
72 used by the National Institute of Statistics to determine the During 1998–2015, 4,567,899 persons died in Romania, 119
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73 exposed population come from various administrative and among whom, diabetes as the underlying or first secondary 120
74 statistical sources, i.e. Directorate for Personal Records cause of death was responsible for 168,854 cases, 90,171 121
and Database Administration and Passports General Direc- (53.4%) women and 78,683 (46.6%) men. The corresponding 122
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75
76 torate provided data on internal and international migra- general population showed a linear increase from 16.6 mil- 123
77 tion, and about acquiring and withdrawing of Romanian lion in 1998 to 17.8 million in 2010, followed by a plateau 124
78 citizenship (biannual data). Exposed population was made until 2015 (17.8 million). This translated into a mean diabe- 125
available as mean estimates at July 1st, each year. Indi- tes-related CMR of 53.93 per 100,000 person-years (p-y),
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79 126
80 vidual level data were available only for deaths. Causes 55.60 per 100,000 p-y in women and 52.13 per 100,000 p-y 127
81 of death were encoded using a local code system during in men. The unadjusted and age- and sex-adjusted diabetes- 128
82 1998–1999, and the International Statistical Classifica- related mortality data (CMR/ASMR) are summarized in 129
83 tion of Diseases and Related Health Problems (ICD) tenth Table 1. Diabetes-related CMRs increased with age, and 130
84 revision during 2000–2015 (E10–E14). Underlying cause calendar year until 2010, followed by a decrease during 131
85 was defined as the first cause of death mentioned on the 2010–2015 in most age groups, in both women (Table 2) 132
86 death certificate, while first secondary cause was defined and men (Table 3). 133
87 as the secondary cause of death mentioned on the death During 1998–2015, the mean diabetes-related ASMR 134
88 certificate. Diabetes as the underlying cause of death could was 39.34 per 100,000 p-y (95% CI 39.32–39.35), signifi- 135
89 not be analysed because in the current study diabetes was cantly lower in women (35.24 per 100,000 p-y, 95% CI 136
90 almost 20 times more likely to be mentioned as the first 35.22–35.26) as compared with men (44.08 per 100,000 137
91 secondary cause of death as compared with the underly- p-y, 95% CI 44.05–44.11, p < 0.001). There was an 138
92 ing cause of death. Consequently, data were considered increase in diabetes-related ASMR in women from 27.10 139
93 unacceptable for a sensitivity analysis restricting observa- per 100,000 p-y (95% CI 27.01–27.19) in 1998 to 39.09 140
94 tions only to the underlying cause of death, which would per 100,000 p-y (95% CI 39.0–39.18) in 2010, followed by 141
95 severely underestimate the magnitude of the investigated a decrease to 35.42 per 100,000 p-y (95% CI 35.34–35.51) 142
in 2015; see Table 1. A similar rise was found in men from 143

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Table 1  Diabetes-related crude Death year Women Men


and age-standardized mortality
a b c
rates in Romania (1998–2015) N CMR ASMR 95% CI Na CMRb ASMRc 95% CI

1998 3322 38.61 27.10 27.01–27.19 2795 34.78 30.88 30.77–30.99


1999 3425 39.50 27.41 27.32–27.50 2799 34.58 30.56 30.45–30.67
2000 3551 40.63 28.19 28.10–28.28 2909 35.66 31.40 31.29–31.51
2001 3719 42.23 28.91 28.82–29.00 3079 37.48 32.78 32.67–32.89
2002 3895 43.99 29.84 29.75–29.93 3302 40.02 34.95 34.84–35.07
2003 4545 51.18 34.10 34.00–34.19 3911 47.30 40.82 40.70–40.94
2004 5042 56.59 37.15 37.05–37.25 4375 52.78 45.07 44.94–45.19
2005 5360 59.85 38.79 38.69–38.88 4625 55.52 47.17 47.05–47.30
2006 5540 61.57 39.34 39.24–39.44 4801 57.37 48.60 48.47–48.73
2007 5691 62.82 39.70 39.61–39.80 4853 57.58 48.76 48.64–48.89
2008 5500 60.32 37.84 37.74–37.93 4924 58.04 48.99 48.87–49.12
2009 6004 65.46 40.31 40.21–40.41 5325 62.42 52.03 51.91–52.16

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2010 5977 64.80 39.09 39.00–39.18 5439 63.43 52.63 52.51–52.76

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2011 5593 60.60 35.96 35.87–36.05 4995 58.25 47.61 47.49–47.73
2012 5748 62.21 36.51 36.42–36.60 5125 59.69 48.28 48.16–48.40
2013 5506 59.58 34.19 34.10–34.28 5004 58.26 46.46 46.35–46.58

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2014 5745 62.17 34.84 34.75–34.92 5079 59.12 46.78 46.67–46.90
2015 6008 65.08 35.42 35.34–35.51 5343 62.26 48.41 48.29–48.52
a

c
 Number of cases

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 Crude mortality rate per 100,000 person-years
 Age-standardized mortality rate per 100,000 person-years
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Table 2  Diabetes-related crude Year Women crude mortality rates per 100,000 person-years, by age
mortality rates in Romanian
women, by age (1998–2015) 20–29 years 30–39 years 40–49 years 50–59 years 60–69 years 70–79 years ≥ 80  years
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1998 1.12 1.75 6.45 22.51 88.22 166.38 151.01


1999 0.97 1.36 6.04 23.84 89.08 173.53 142.49
2000 0.60 1.70 6.00 25.70 88.08 174.74 160.91
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2001 0.43 1.23 6.14 26.26 90.84 185.18 157.61


2002 0.76 1.20 5.61 25.63 95.59 185.31 187.47
2003 0.99 1.82 6.47 27.21 108.37 217.11 223.81
2004 0.56 1.65 7.94 30.91 109.77 239.91 270.86
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2005 0.56 1.38 6.69 32.45 116.77 251.57 289.78


2006 0.46 1.17 6.31 33.14 112.10 261.36 309.53
2007 0.69 1.03 6.18 28.76 119.81 260.14 324.41
2008 0.41 1.13 5.83 27.98 109.51 241.51 332.52
2009 0.23 0.98 5.16 31.19 110.64 260.56 368.80
2010 0.24 0.66 4.18 29.85 102.63 262.50 363.06
2011 0.30 0.88 3.77 25.05 93.24 240.99 352.99
2012 0.56 0.77 3.61 26.97 93.25 242.54 363.14
2013 0.13 0.72 2.87 24.88 84.43 234.23 351.23
2014 0.26 0.62 3.19 23.78 84.16 244.45 370.42
2015 0.20 0.63 3.41 22.37 85.02 241.16 418.72

144 30.88 per 100,000 p-y (95% CI 30.77–30.99) in 1998 to per year (95% CI 3.5–4.0, p < 0.001) during 1998–2010 148
145 52.63 per 100,000 p-y (95% CI 52.51–52.76) in 2010, fol- and − 1.9% per year (95% CI − 2.7 to − 1.1, p < 0.001) 149
146 lowed by a decrease to 48.41 per 100,000 p-y (95% CI during 2010–2015. The mean APC in men was 5.3% per 150
147 48.29–48.52) in 2015. The mean APC in women was 3.8% year (95% CI 5.0–5.5, p < 0.001) during 1998–2010 and 151

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Table 3  Diabetes-related crude Year Men crude mortality rates per 100,000 person-years, by age
mortality rates in Romanian
men, by age (1998–2015) 20–29 years 30–39 years 40–49 years 50–59 years 60–69 years 70–79 years ≥ 80 years

1998 1.02 3.46 12.01 35.68 88.58 173.22 143.36


1999 0.67 2.26 10.10 33.89 98.14 161.69 150.21
2000 0.47 1.65 10.70 36.24 98.29 165.46 164.35
2001 0.78 3.10 9.96 37.51 102.12 176.43 162.32
2002 0.63 2.44 11.65 37.45 111.08 182.77 200.64
2003 0.53 2.50 13.57 42.09 125.66 228.84 236.42
2004 0.86 3.47 13.20 47.79 136.54 257.82 266.67
2005 0.70 3.08 13.46 51.02 143.30 265.87 298.10
2006 0.77 2.41 13.60 53.52 147.49 270.99 315.84
2007 0.33 2.64 13.38 55.01 145.69 268.27 322.36
2008 0.39 2.28 13.04 54.15 148.91 264.72 331.16
2009 0.56 2.20 12.41 58.42 147.99 287.51 381.40

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2010 0.28 2.74 11.78 57.49 150.85 293.83 376.27

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2011 0.18 1.84 9.77 52.44 132.22 266.41 376.39
2012 0.48 0.90 8.48 48.18 133.85 293.11 373.78
2013 0.24 1.23 10.01 45.42 130.71 281.98 356.39

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2014 0.37 1.19 9.53 45.17 136.80 273.91 367.34
2015 0.32 1.31 7.96 47.77 137.03 283.16 421.66

152
153
− 1.5% per year (95% CI − 2.2 to − 0.8, p < 0.001) during
2010–2015.
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2015, p < 0.001), and men (66.8 ± 15.0 years in 1998, and
71.1 ± 14.2 years in 2015, p < 0.001).
182
183
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154 Most patients died at home (n = 102,489, 60.7%), fol-
155 lowed by in hospital (n = 59,597, 35.3%) and elsewhere
156 (n = 6768, 4.0%). As comparison, deaths not related to dia- Discussion 184
157 betes were more likely to happen at home (71.7%, p < 0.001)
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158 and elsewhere (7.5%, p < 0.001), and less likely in the hos- Age-standardized diabetes-related mortality rates increased 185
159 pital (20.8%, p < 0.001). There was a significant increase significantly during 1998–2015 in Romania, but most of this 186
160 in the proportion of diabetes-related deaths registered in increase was accounted for during 1998–2010, followed by 187
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161 the hospital, from 27.6% (95% CI 26.5–28.7) in 1998 to a significant mortality improvement during 2010–2015. The 188
162 41.3% in 2015 (95% CI 40.4–42.2, p < 0.001), with a cor- last 6 years showed a significant descending trend in both 189
163 responding significant decrease for deaths at home from genders, which is expected to continue in the next years. This 190
164 68.7% (95% CI 67.5–69.8) in 1998 to 45.4% in 2015 (95% is in line with findings from other studies showing negative 191
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165 CI 41.7–49.4, p < 0.001). Diabetes-related deaths registered diabetes-related mortality rates in the last decades [11–14]. 192
166 elsewhere were relatively stable (around 4%) throughout the Diabetes-related mortality rates increased with age, with 193
167 study period. Diabetes unrelated deaths registered a similar men experiencing higher mortality rates than women for 194
168 trend, with a significant decrease for dying at home (76.3% most age groups and calendar years (Tables 2, 3). Mean age 195
169 in 1998, down to 62.2% in 2015, p < 0.001), and a significant at death was higher in women as compared with men, and it 196
170 increase for dying in the hospital (16.6% in 1998, and 29.3% improved significantly over the study period in both genders. 197
171 in 2015, p < 0.001) and elsewhere (7.1% in 1998, and 8.5% Diabetes-related deaths were associated with a lower mean 198
172 in 2015, p < 0.001). age at death as compared with death unrelated to diabetes in 199
173 There was a significant 6.1 (95% CI 5.7–6.5) years women, but not in men. This discrepancy indirectly suggests 200
174 increase in the women’s mean age at (diabetes related) a higher diabetes burden in women as compared with men 201
175 death from 69.7 ± 10.1 years in 1998 to 75.8 ± 9.7 years in the studied population. 202
176 in 2015 (p < 0.001). Similarly, the mean age at (diabe- The general tendency towards underreporting of diabetes 203
177 tes related) death in men increased 5.0 (95% CI 4.5–5.5) as underlying cause as compared with other concomitant 204
178 years, from 66.3 ± 11.3 years in 1998 to 71.3 ± 10.8 years causes was confirmed in the current study, where diabetes 205
179 in 2015 (p < 0.001). This was paralleled by a significant was almost 20 times more likely to be mentioned as the first 206
180 increase in mean age at death unrelated to diabetes in both secondary cause of death as compared with the underlying 207
181 women (73.8 ± 13.5 years in 1998, and 78.1 ± 12.4 years in cause of death [15]. Based on this finding, we considered 208

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209 the available data as unreliable for a secondary analysis the Danish National Diabetes Registry and applied this to 262
210 restricted to the underlying cause of death. national mortality data in Germany, aiming to evaluate the 263
211 Obesity, aging population, lower education level and excess mortality attributable to diabetes [22]. However, their 264
212 westernized lifestyle are major players driving the surge in method cannot be applied here due to significant differences 265
213 diabetes incidence and prevalence, while increased treatment in mortality and other health care statistics between Den- 266
214 availability for cardiovascular risk factors and active screen- mark and Romania. 267
215 ing may counteract by providing benefits on diabetes-related In conclusion, diabetes-related mortality rates in Roma- 268
216 mortality [7, 16–19]. Romania is experiencing high rates of nia increased with age in both genders, and in time during 269
217 obesity (31.9%), overweight (34.7%), primary (9.8%) and 1998–2010, followed by a steady decline during 2010–2015. 270
218 secondary education dropout rates (12.4%), which pose a Further research must be performed for the clarification of 271
219 high toll on diabetes incidence and mortality [16, 20]. Pri- these patterns in diabetes-related mortality. 272
220 mary care access significantly improved over time, steadily
221 releasing the pressure non-serious patients were putting on Compliance with ethical standards  273
222 the hospitals. As hospitals begin to be less crowded with
low severity cases, there was a consequent increase in Conflict of interest  The authors declare that they have no competing 274

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223
interest. 275
224 hospital admissions for more severe cases, many of them
suffering from diabetes. This might explain the increasing

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225 Research involving human/animal participants  All procedures per- 276
226 percent of diabetes-related deaths registered in the hospital formed in studies involving human participants were in accordance 277
over the study period. Population growth linear ascending with the ethical standards of the institutional and/or national research 278

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227
committee and with the 1964 Helsinki declaration and its later amend- 279
228 trend stopped in 2010 most likely due to increased migration ments or comparable ethical standards. 280
towards western European countries following the country

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229
230 admission as a European Union member in 2007. The initial Informed consent  For this type of study formal consent is not required. 281
231 population growth might have dampened the rise in mortal-
232 ity rates (as denominator in the CMR formula), while the
233 latter steady state makes the descending diabetes-related
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Journal : Large 592 Article No : 1156 Pages : 6 MS Code : ACDI-D-18-00190 Dispatch : 15-5-2018

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