NDT Advance Access originally published online on May 15, 2006
Nephrology Dialysis Transplantation 2006 21(8):2159-2165; doi:10.1093/ndt/gfl217
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© The Author [2006]. Published by Oxford University Press on behalf of ERA-EDTA. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org
Original Articles: Clinical Nephrology
Low birth weight does not increase the risk of nephropathy in Finnish type 1 diabetic patients
1 Folkhälsan Institute of Genetics, Folkhälsan Research Center, 2 Department of Clinical Chemistry, 3 The Finnish Genome Center, University of Helsinki and 4 Department of Medicine, Division of Nephrology, Helsinki University Central Hospital, Helsinki, Finland
Correspondence and offprint requests to: Per-Henrik Groop, MD, DMSc, Folkhälsan Research Center, Biomedicum Helsinki (C318b), PO Box 63, FIN-00014, University of Helsinki, Finland. Email: per-henrik.groop{at}helsinki.fi
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Abstract |
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Background. Low birth weight (LBW) has been linked to renal disease both in animal models and human studies. However, the role of birth weight in the development of diabetic nephropathy is unclear. We, therefore, studied the impact of birth weight on the development of diabetic nephropathy and other related traits, such as diabetic retinopathy and macrovascular disease, in Caucasian type 1 diabetic patients.
Methods. Data on size at birth were obtained from original birth certificates in 1543 Finnish patients with type 1 diabetes. The patients were divided into those with low (LBW; below the 10th percentile), normal (NBW; 11–90th percentile) and high birth weight (HBW; above the 90th percentile).
Results. Diabetic nephropathy was equally common in the groups with various birth weight (LBW vs NBW vs HBW: 21 vs 20 vs 17%, P = NS). End-stage renal disease (3 vs 5 vs 4%, P = NS), laser-treated retinopathy (31 vs 31 vs 31%, P = NS) and macrovascular disease (5 vs 5 vs 8%, P = NS) were equally prevalent in the various birth weight groups. The time from the onset of diabetes to the onset of diabetic nephropathy was similar irrespective of birth weight (log-rank test; P = NS).
Conclusions. Based on our cross-sectional data, LBW does not have an impact on the development of diabetic nephropathy, laser-treated retinopathy or macrovascular disease later in life in Caucasians with type 1 diabetes.
Keywords: albuminuria; diabetic nephropathy; intrauterine growth retardation; type 1 diabetes mellitus
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Introduction |
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Small size at birth has been linked to an increased morbidity later in life. For instance, individuals with low birth weight seem to be at increased risk of cardiovascular disease, type 2 diabetes, elevated blood pressure and renal disease [1–3]. The mechanisms causing intrauterine growth retardation and impaired health in adulthood remain to be elucidated, but environmental as well as genetic factors are suggested to play a role [1,4].
Birth weight correlates with the number of nephrons at birth [5]. It was therefore suggested that subjects with a low birth weight, and thereby with a congenitally reduced number of nephrons, are at an increased risk of glomerular and systemic hypertension later in life [3]. Indeed, an inverse correlation between birth weight and adult systolic blood pressure has consistently been reported [2], and individuals with essential hypertension have a markedly reduced nephron number [6]. We have recently extended the finding of an impact of birth weight on blood pressure to also include individuals with type 1 diabetes [7]. A 1 kg decrease in birth weight was associated with 
2 mmHg higher systolic blood pressure, a relationship that seemed stronger in females.
Individuals with low birth weight may therefore be at increased risk of diabetic kidney disease. Indeed, in a study in type 1 diabetic patients, Rossing et al. [8] found an increased risk of diabetic nephropathy among patients with low birth weight (below 2700 g) when compared with patients with high birth weight (over 4000 g). The observation was, however, limited to females. Subsequently, Pima Indian type 2 diabetic patients with a birth weight below 2500 g, but also those with a birth weight over 4500 g, were found to be at an increased risk of proteinuria [9]. No sex-specific effect was observed in this latter study. The diverging findings of the two studies could of course indicate differences between type 1 and type 2 diabetes. However, before further conclusions can be drawn, the role of size at birth in the development of diabetic kidney disease needs to be clearly defined.
The aim of the present study was, therefore, to assess the impact of birth weight on the development of diabetic nephropathy. In addition, we aimed to study the association between birth weight and other diabetic late complications, such as diabetic retinopathy and macrovascular disease, in a large sample of Finnish type 1 diabetic patients.
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Subjects and methods |
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The Finnish Diabetic Nephropathy (FinnDiane) study is a nationwide, prospective, multicentre study that was initiated in November 1997. The primary aim is to identify genetic and environmental risk factors for diabetic nephropathy in type 1 diabetes. The patients are recruited from 20 university and central hospitals, from 23 local hospitals and from 16 primary healthcare centres. The study protocol is in accordance with the Declaration of Helsinki and it has been approved by the local ethics committee of each participating study centre.
The present study presents cross-sectional data from the baseline visit. All patients with a diagnosis of type 1 diabetes (E10 in ICD-10) attending the diabetic and renal out-patient clinics and dialysis units were asked to participate in the study in a consecutive manner when they visited the hospitals and the healthcare centres as part of their routine follow-up. Of the invited patients, 78% gave their informed consent. Based on medical records, the attending local physician completed a study form assessing diabetic micro- and macrovascular late complications. Furthermore, data on the mode of insulin therapy, daily insulin dose and other regular medication were obtained. The patients were asked to complete a questionnaire concerning place of birth, smoking habits, alcohol intake, educational level and social class.
For the present study, we selected all patients with an age at onset of diabetes <36 years, with insulin therapy initiated within 1 year after diagnosis, and with their data entered into the FinnDiane database by 31 October 2002. Of the 3115 patients fulfilling these criteria, 2313 reported birth at a hospital. Of these, we were able to obtain a copy of the original birth certificate for 1966 patients. After exclusion of twin pregnancies (n = 23), the final data set consisted of 1543 patients with data on birth weight available. Of these, 1419 had complete data on birth weight, height and gestational age (calculated from the last menstruation before pregnancy).
Definitions of long-term complications
While the classification of other diabetic late complications was based on the study form completed by the attending physician, the degree of renal involvement was classified centrally. All available data on urinary albumin excretion rate (UAER) was extracted from local medical records. A patient was classified as having microalbuminuria or diabetic nephropathy if the criteria mentioned subsequently were fulfilled at any time point after the diagnosis of diabetes. Diabetic nephropathy was defined as a UAER exceeding 200 µg/min (overnight collections) or 300 mg/24 h (24 h urine collections), or as a urinary albumin/creatinine ratio in a spot sample exceeding 25 mg/mmol (male) or 35 mg/mmol (female), in two out of three consecutive measurements. The corresponding cut-off values for microalbuminuria were 20–200 µg/min or 30–300 mg/24 h for UAER, and 2.5–25 mg/mmol (male) or 3.5–35 mg/mmol (female) for the urinary albumin/creatinine ratio. Two UAER measurements within the normal range were required to classify a patient as normoalbuminuric. The renal status was considered unclassifiable if there was insufficient data on UAER, or if UAER was elevated due to reasons other than diabetes (pregnancy, non-diabetic kidney disease, duration of diabetes <3 years). End-stage renal disease (ESRD), defined as renal replacement therapy due to diabetic nephropathy, was present in 74 patients.
Retinopathy was defined as a history of laser photocoagulation treatment. Manifestations of macrovascular disease (history of myocardial infarction, coronary revascularization procedure, stroke, amputation of a limb or peripheral arterial revascularization procedure) were combined to a single macrovascular end-point.
Other definitions
Current smoking was defined as regular cigarette smoking during the year prior to participation in the study. A patient was considered an ex-smoker if more than 1 year had elapsed since the cessation of smoking. Social class was defined as follows: I. upper white-collar workers, II. lower white-collar workers, III. skilled blue-collar workers, IV. unskilled blue-collar workers, V. farmers and VI. others.
Laboratory assays
Serum creatinine concentration (normal reference values: male <115 µmol/l, female <100 µmol/l) was measured centrally with a kinetic Jaffe reaction on a Hitachi 917 automated analyser. Data on the latest HbA1c measurement were obtained from local medical records. All patients without ESRD (n = 1469) were asked to perform a 24 h urine collection for central measurement of UAER, and the data were obtained in 1312 patients (89%). Of patients with previously well-documented diabetic nephropathy, current UAER in this single measurement had regressed to micro- or normoalbuminuria in 32% of the patients. Correspondingly, 24% of the microalbuminuric patients had a current UAER in the normoalbuminuric range.
Other calculations
Creatinine clearance was estimated using the Cockcroft–Gault formula corrected for body surface area [10]. Whole-body insulin sensitivity was calculated using the estimated glucose disposal rate (eGDR) formula [11].
Statistics
In order to test whether low birth weight predisposes to diabetic complications, the patients were classified into those with low (below the 10th percentile; group I), intermediate (groups II and III) and high (over the 90th percentile; group IV) birth weight. As birth weight differed between males and females, the procedure was performed separately in each sex. The impact of low birth weight was assessed in the combined set of males and females, but, due to previous findings [7,8], predefined gender-stratified analyses were also carried out.
The analyses were performed using the SPSS 11.5 statistical package (SPSS Inc. Illinois, USA). The significance of differences in categorical variables was assessed with the chi-squared test, while continuous variables were analysed with ANOVA (normally distributed) or the Kruskal–Wallis test (non-normally distributed). Normally distributed variables are presented as mean ± SD, while variables with skewed distribution are presented as median and 25th and 75th percentiles. The significance of correlations between normally distributed variables was tested using Pearson's correlation coefficient. A P-value <0.05 was considered statistically significant. Despite the cross-sectional study design, the time from the onset of diabetes to the onset of diabetic nephropathy could be retrospectively assessed using Kaplan–Meier survival analysis. The statistical significance of differences between the groups was assessed with the log-rank test.
A power calculation was performed with the UnifyPow SAS module using the SAS 8.02 version (SAS Institute Inc., Cary, NC, USA).
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Results |
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As previously presented in detail [7], the patients included in the present study (n = 1543) were younger, had a shorter duration of diabetes and a lower prevalence of both micro- and macrovascular complications than the patients without available data on birth weight (n = 1572).
The patients were divided into four groups based on birth weight percentiles. Perinatal and current characteristics are presented in Tables 1 and 2, respectively. Patients with a low birth weight had shorter gestational age and were also thinner since their ponderal index was lower. There was a positive correlation between birth weight and adult weight (R = 0.176, P < 0.001) and height (R = 0.230, P < 0.001). The HbA1c was slightly higher in patients with a birth weight in the 50–90th percentiles (group III) when compared with the other birth weight groups (groups I, II and IV). Systolic blood pressure was higher and estimated creatinine clearance lower in patients with low compared with high birth weight.
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In an analysis restricted to patients without ESRD, there was a weak positive correlation between birth weight and estimated creatinine clearance in adulthood (R = 0.076, P = 0.004).
The prevalence of diabetic long-term complications is presented in Table 3. There was no difference in the prevalence of the assessed micro- or macrovascular complications between any of the groups with various birth weights irrespective of the mode of comparison (low birth weight vs high, low vs rest, high vs rest, low and high vs intermediate). The eGDR, a surrogate measure of insulin sensitivity, did not differ between the groups. As depicted in Figure 1, a sex-stratified analysis revealed no significant differences in the prevalence of diabetic nephropathy in the groups with different birth weight in either males or females.
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The impact of size at birth on the time of onset of diabetic nephropathy was further assessed using a Kaplan–Meier survival analysis (Figure 2). In this analysis, we found no evidence of an earlier onset of nephropathy in patients with low birth weight. A sex-stratified survival analysis revealed similar results in both males and females (data not shown).
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We also used alternative definitions of intrauterine growth retardation (birth weight below 2500 g, a ponderal index in the lowest 10th percentile), but these analyses yielded similar results to those now presented.
Patients with a low birth weight had a shorter gestational age. As a birth weight of, for instance, 2500 g indicates intrauterine growth retardation in the full-term child, it reflects normal intrauterine growth in the pre-termly born individual. Therefore, in a logistic regression analysis, we assessed the odds ratio of diabetic nephropathy in the different birth weight groups after adjustment for gestational age. However, the analysis had no effect on the results (Table 4).
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A power calculation was performed with patients with low birth weight (group I) vs those without (groups II–IV). Assuming that the prevalence of nephropathy in groups II–IV is 20% as observed, our sample size would have detected a prevalence of nephropathy of 30% in group I as statistically significantly higher (P < 0.05) with a power of 0.80.
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Discussion |
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This study found no impact of size at birth on the risk of diabetic nephropathy in patients with type 1 diabetes. Similarly, no association was observed between birth weight and laser-treated diabetic retinopathy or macrovascular disease.
Ots and colleagues [12] demonstrated that nephron mass (or number) is instrumental in the development of arterial hypertension and glomerular hyperfiltration by studying the effects of kidney transplantation in subtotally nephrectomized rats. In humans, a markedly reduced number of nephrons has been found in patients with primary hypertension [6]. Further evidence suggests an increased risk of progressive renal disease in diabetic subjects with only one kidney [13]. The link between a reduced number of nephrons, elevated blood pressure and progressive renal disease therefore seems irrefutable.
In a separate analysis of this cohort of type 1 diabetic patients, we recently reported an inverse relationship between birth weight and systolic blood pressure and pulse pressure [7]. In the present article, we found a weak positive correlation between weight at birth and adult glomerular filtration rate. It should be noted, however, that although the correlation was statistically highly significant, birth weight explained <1% of the variation in estimated adult creatinine clearance. Furthermore, as many of our patients had normal kidney function, the Cockcroft–Gault formula may be suboptimal in estimating kidney function. Nonetheless, elevated systemic blood pressure and impaired kidney function are well-recognized players in the vicious circle leading to progressive renal failure. The question arises: why was low birth weight not associated with an increased risk of overt diabetic nephropathy?
First, as already mentioned, although statistically significant, the effects of birth weight on both systemic blood pressure [7] and kidney function were not profound. In a process where the degree of chronic hyperglycaemia is fundamental [14], the derangements associated with size at birth may simply be too small to have any impact on the development of progressive renal damage.
Second, although intrauterine growth retardation is associated with a reduced number of nephrons at birth [5], birth weight must be viewed only as a surrogate marker for the nephron number.
Third, the underlying cause of small size at birth, whether genetic, environmental or a combination of these two, may be of crucial importance. Animal studies have shown that intrauterine growth retardation induced by environmental changes, such as protein or salt depletion during pregnancy, is associated with signs of renal impairment in the offspring [15,16]. In humans, retrospective studies have reported a link between low birth weight and later progressive renal damage or related traits, such as congenital renal failure [17], diabetic nephropathy [8,9], albuminuria [18] and ESRD of any cause [19]. These findings have been observational and the causes of the retarded growth in utero have not been possible to define.
Several of the positive associations have been found in populations with a high incidence of ESRD, such as type 2 diabetic Pima Indians [9], aborigines [18] and a population from the southeastern region of the USA [19]. Interestingly, the mean birth weight in these previous studies was lower (3.38 [9], 2.71 [18] and 3.25 kg [19], respectively) than in the present (3.51 kg). The genetic background of these populations is undoubtedly different from that of our Finnish type 1 diabetic population. However, the environment may also differ substantially. Of the patients in our study, 85% were born after 1960. After the decade following the Second World War, due to governmentally financed prenatal care readily available for all citizens, malnutrition during pregnancy has become extremely rare in Finland. This has led to an infant mortality rate that has been one of the lowest in the world during the last decades [20]. If fetal malnutrition is crucial in the aetiology of intrauterine growth retardation and subsequent renal failure, this environmental factor may simply not have been present to any significant degree in our population.
The cross-sectional study design has well-known limitations. Selective excess mortality may have diluted a true association between low birth weight and diabetic renal disease. However, to our knowledge, no prospective studies dealing with the impact of birth weight on diabetic or non-diabetic kidney disease are so far available. The previous observations reporting an association between birth weight and diabetic renal disease were also cross-sectional, but of considerably smaller size [8,9]. In addition to size, our finding is strengthened by the fact that we have data on the time of (known) onset of diabetic nephropathy available. Notably, we found no evidence of an earlier onset of persistent proteinuria in patients with low birth weight.
In conclusion, our present findings do not support a role for low birth weight in the development of diabetic nephropathy or other diabetic late complications in Finnish type 1 diabetic patients. Although prospective follow-up studies are needed to fully define the role of size at birth in the pathogenesis of diabetic renal disease, it seems unlikely that low birth weight would be a clinically relevant risk factor for diabetic nephropathy in Caucasians with type 1 diabetes.
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Acknowledgments |
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Maija Rinne, Johan Groop, Maikki Parkkonen and Tarja Vesisenaho are acknowledged for their skillful assistance. This work has been financially supported by The Folkhälsan Research Foundation, Samfundet Folkhälsan, The Else och Wilhelm Stockmann Foundation, The Liv och Hälsa Foundation, The Finnish Medical Society, The Perklen Foundation, The K. Albin Johansson Foundation, The Finnish Association for Kidney Diseases and the European Commission (The Euragedic Study; Contract QLG2-CT-2001-01669).
This study would not have been possible without the assistance of the whole Finnish Diabetic Nephropathy Study Group: Anjalankoski Health Center: S. Koivula, T. Uggeldahl; Central Finland Central Hospital: T. Forslund, A. Halonen, A. Koistinen, P. Koskiaho, M. Laukkanen, J. Saltevo, M. Tiihonen; Central Hospital of Aland Islands: A.-C. Blomqvist, M. Forsen, H. Granlund, B. Nyroos; Central Hospital of Kanta-Hame: P. Kinnunen, A. Orvola, T. Salonen, A. Vähänen; Central Hospital of Kymenlaakso: R. Paldanius, M. Riihelä, L. Ryysy; Central Hospital of Lansi-Pohja: P. Nyländen, A. Sademies; Central Ostrobothnian Hospital District: S. Anderson, B. Asplund, U. Byskata, T. Virkkala; City of Espoo Health Center: (Espoonlahti): A. Nikkola, E. Ritola; (Leppävaara): L. Penttinen, H.-L. Siekkinen; City of Helsinki Health Center: (Suutarila): A. Kaprio, J. Kärkkäinen, B. Rantaeskola; City of Hyvinkää Health Center: S. Klemetti, T. Nyandoto, E. Rontu, S. Satuli-Autere; City of Vantaa Health Center: (Korso): R. Toivonen, H. Virtanen; (Martinlaakso): M. Laine, T. Pellonpää, R. Puranen; (Myyrmäki): A. Airas, J. Laakso, K. Rautavaara; (Rekola): M. Erola, E. Jatkola; (Tikkurila): R. Lönnblad, A. Malm, J. Mäkelä, E. Rautamo; Heinola Health Center: P. Hentunen, J. Lagerstam; Helsinki University Central Hospital (Department of Medicine, Division of Nephrology): H. Rosvall; Hospital of Lounais-Häme, Forssa: T. Kalliomäki, J. Koskelainen, R. Nikkanen, N. Savolainen, H. Sulonen, E. Valtonen; Iisalmi Hospital: E. Toivanen; Jokilaakso Hospital, Jämsä: A. Parta, I. Pirttiniemi; Jorvi Hospital, Espoo: S. Aranko, S. Ervasti, R. Kauppinen-Mäkelin, A. Kuusisto, T. Leppälä, K. Nikkilä, L. Pekkonen; Kainuu Central Hospital: S. Jokelainen, P. Kemppainen, A.-M. Mankinen, M. Sankari; Kivelä Hospital, Helsinki: A. Aimolahti, E. Huovinen; Koskela Hospital, Helsinki: V. Ilkka, M. Lehtimäki; Kouvola Health Center: E. Koskinen, T. Siitonen; Kuopio University Hospital: E. Huttunen, R. Ikäheimo, P. Karhapää, P. Kekäläinen, M. Laakso, T. Lakka, E. Lampainen, L. Mykkänen, L. Niskanen, U. Tuovinen, I. Vauhkonen, E. Voutilainen; Kuusankoski Hospital: E. Kilkki, L. Riihelä; Laakso Hospital, Helsinki: T. Meriläinen, P. Poukka, R. Savolainen, N. Uhlenius; Lahti City Hospital: A. Mäkelä, M. Tanner; Lapland Central Hospital: L. Hyvärinen, S. Severinkangas, T. Tulokas; Lappeenranta Health Center: P. Linkola, I. Pulli; Lohja Hospital: T. Granlund, M. Saari, T. Salonen; Länsi-Uusimaa Hospital, Tammisaari: I.-M. Jousmaa, J. Rinne; Malmi Hospital, Helsinki: H. Lanki, S. Moilanen, M. Tilly-Kiesi; Mikkeli Central Hospital: A. Gynther, R. Manninen, P. Nironen, M. Salminen, T. Vänttinen; North Karelian Hospital: U.-M. Henttula, A. Rissanen, P. Kekäläinen, M. Voutilainen; Oulaskangas Hospital, Oulainen: E. Jokelainen, P.-L. Jylkkä, E. Kaarlela, J. Vuolaspuro; Oulu Health Center: L. Hiltunen, R. Häkkinen, S. Keinänen-Kiukaanniemi; Päijät-Häme Central Hospital: H. Haapamäki, A. Helanterä, H. Miettinen; Palokka Health Center: (Palokka): P. Sopanen, L. Welling; (Vaajakoski): K. Mäkinen, P. Sopanen; Pieksämäki Hospital: V. Javtsenko, M. Tamminen; Pietarsaari Hospital: M.-L. Holmbäck, B. Isomaa; Pori City Hospital: P. Ahonen, P. Merensalo, K. Sävelä; Porvoo Hospital: M. Kallio, B. Rask, S. Rämö; Raahe Hospital: A.Holma, M.Honkala, A.Tuomivaara, R.Vainionpää; Rauma Hospital: K. Laine, K. Saarinen, T. Salminen; Riihimäki Hospital: E. Immonen, L. Juurinen; Salo Hospital: A. Alanko, J. Lapinleimu, P. Rautio, M. Virtanen; Satakunta Central Hospital: M. Asola, M. Juhola, P. Kunelius, M.-L. Lahdenmäki, P. Pääkkönen, M. Rautavirta; Savonlinna Central Hospital: T. Pulli, P. Sallinen, E. Tolvanen, H. Valtonen, A. Vartia; Seinajoki Central Hospital: E. Korpi-Hyövälti, T. Latvala, E. Leijala; South Karelia Hospital District: T. Hotti, R. Härkönen, U. Nyholm, J. Toivanen; Tampere University Hospital: I. Ala-Houhala, T. Kuningas, P. Lampinen, M. Määttä, H. Oksala, T. Oksanen, K. Salonen, H. Tauriainen, S. Tulokas; Tiirismaa Health Center, Hollola: T. Kivelä, L. Petlin, L. Savolainen; Turku Health Center: I. Hämäläinen, H. Virtamo, M. Vähätalo; Turku University Central Hospital: K. Breitholz, R. Eskola, K. Metsärinne, U. Pietilä, P. Saarinen, R. Tuominen, S. Äyräpää; Vammala Hospital: I. Isomäki, R. Kroneld, M. Tapiolinna-Mäkelä; Vasa Central Hospital: S. Bergkulla, U. Hautamäki, V.-A. Myllyniemi, I. Rusk.
Conflict of interest statement. None declared.
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Accepted in revised form: 29. 3.06
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