Smoking and diabetes mellitus

Smoking and diabetes mellitus

The Netherlands JOURNAL OF MEDICINE ELSEVIER Netherlands Journal of Medicine 48 (1996) 150-162 Review Smoking and diabetes mellitus R . I . J . D ...

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The Netherlands

JOURNAL OF MEDICINE ELSEVIER

Netherlands Journal of Medicine 48 (1996) 150-162

Review

Smoking and diabetes mellitus R . I . J . D i e r k x a,*, W . v a n d e H o e k

b, J . B . L . H o e k s t r a

c, D . W . E r k e l e n s

d

a Sint Joseph Hospital, De Run 4600, P.O. Box 7777, 5500 MB Veldhocen, Netherlands b Eemland Hospital, P.O. Box 1502, 3800 B M Amersfoort, Netherlands c Diakonessenhuis, Bosboomstraat I, 3582 KE Utrecht, Netherlands d Department o f Internal Medicine, Unicersity Hospital Utrecht, Heidelberglaan 100, P.O. Box 85500, 3584 C X Utrecht, Netherlands

Received 6 June 1995;accepted 4 December 1995

Abstract

The goal of this review is to determine the effects of smoking on diabetes mellitus, whether it aggravates diabetic complications or influences insulin metabolism and action. Also available anti-smoking programmes applicable for diabetic patients have been studied. The prevalence of smoking among diabetic patients has been investigated by conducting a meta-analysis. Compared with normal subjects, the prevalence of smoking among diabetic patients is significantly higher (27 vs. 33%, p < 0.0001), IDDM patients largely accounting for this difference. However, care must be used in interpreting these data. Smoking presents an extra risk for development of macro- and microvascular complications in these patients, contributing to increased cardiovascular morbidity and mortality. Smoking also increases the risk of diabetes itself. Neither acute nor habitual smoking causes substantial changes in insulin sensitivity in IDDM patients, whereas it does so in NIDDM. Studies in diabetic patients concerning anti-smoking strategies are scarce and only yield disappointing results. Making these patients abstain from smoking turns out to be extremely difficult, probably due to the considerable psychosocial stress experienced. Keywords: Anti-smoking programmes; Diabetic complications; Diabetes mellitus; Insulin action and metabolism;

Smoking; Smoking prevalence

1. Introduction

Patients with diabetes have a high incidence of both macro- and microvascular complications. Smoking cigarettes is an important separate risk factor in the development of vascular pathology. In addition, smoking induces haemodynamic and metabolic changes mediated through tissue by-

* Corresponding author: September 1944 Straat 67, 6418 AW Heerlen, Netherlands.

poxia, adrenergic, cholinergic, and other hormonal mechanisms. Thus, the question arises whether smoking aggravates diabetic complications or influences insulin metabolism. Diabetic patients probably smoke as heavily as non-diabetic subjects. As they are prone to develop vascular disease by the synergistic action of multiple risk factors, the incentives for diabetic patients to stop smoking should be very strong. The prevalence of smoking among diabetic patients has been studied by conducting a metaanalysis. The effects of smoking on insulin-depen-

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dent and non-insulin-dependent diabetes mellitus (IDDM and NIDDM) are presented, with particular attention to the acute effects of smoking on insulin metabolism and action. The association between smoking and the subsequent risk of diabetes is also examined. Furthermore, the macroand microvascular complications of smoking in diabetes are discussed. Attention to the psychosocial aspects of diabetes mellitus is necessary in developing effective anti-smoking programmes. Several efforts to effect a change in smoking behaviour of diabetic patients have already been made and their results are presented.

2. Prevalence of smoking in diabetic patients

There are few medium- or large-scale investigations comparing the frequency of smoking cigarettes in diabetic and non-diabetic subjects [1-8]. We have studied the prevalence of smoking among diabetic patients by conducting a metaanalysis. We combined data from 14 studies going back to 1976, found by computer search by combining the key words "diabetes mellitus" and "smoking" and by crosschecking references by reviewing the reference lists of articles found [1-14]. Publications up to January 1995 have been included. One study, only dealing with smoking history and not with current smoking status, was excluded from the analysis [15]. The publications reviewed provide information on the prevalence of smoking among diabetic patients and present 14 different surveys. In several of them, this prevalence is only a byproduct of examining other issues. Six studies provide information on the prevalence of smoking in the general population and in non-diabetic controls [2,3,5,6,8,10]. Definitions of smoking vary between the included articles and in some, only dealing with smoking habits, a definition is not given at all. In one study, the number of smokers includes not only cigarette but also pipe/cigar smokers [4]. In all studies ex-smokers are counted as non-smokers and one observer has reviewed and assessed all of them. We consider the 14 studies sufficiently similar in terms of study population to permit combination of data. Subgroups for age and sex

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have been created in view of their well-known effects on smoking behaviour. We have not made a qualitative assessment of available data, but combined and re-analysed all studies as if the data had come from one single, large study. Significances of differences were evaluated with Student's t-test, without weighing or correction for any matter. The prevalence of smoking among diabetic patients as a whole (insulin-dependent and non-insulin-dependent) is significantly higher than that in the general population (33 vs. 27%, p < 0.0001), although its clinical relevance must be put into perspective. Compared with non-diabetic subjects, the prevalence of smoking among IDDM contrary to N1DDM patients is also significantly higher (41 vs. 27%, p < 0.0001). Unfortunately, smoking is also prevalent among young diabetic patients, who have most to gain by discontinuing. Details are summarized in Tables 1 and 2. However, in regarding the results of the presented meta-analysis, one has to consider its limitations. For example, possible changes over time in smoking behaviour have not been taken into account and bias could also arise from geographic and demographic differences, such as age and sex, between the included studies. Repeated sampiing is probable in the studies described in References [8,10], concerning 181 diabetic patients at most. Since the analysis is partly based on studies in which determination of smoking prevalence is not the primary objective or studies including only small numbers of subjects, bias could operate, potentially distorting our findings. From this point of view, in 4 of 8 larger studies the prevalence of smoking in diabetic patients does not appear to be much different from the general population, except for the lower prevalence in older diabetic patients [1-4]. Even a lower smoking prevalence among diabetic patients has been demonstrated in three larger studies [5-7]. Therefore, the significantly higher smoking prevalence in diabetic patients, resulting from our meta-analysis, must be interpreted with some caution. Our findings may partly arise from inclusion of a relatively large number of studies, only dealing with diabetic patients and demonstrating a higher smoking prevalence than among normal

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Table 1 Prevalence of smoking in the various groups of diabetic patients [1-14] Group

Reference

Number of patients (n)

Number of smokers (n)

Prevalence of smoking (%)

IDDM and NIDDM patients < 30 years > / 3 0 years Men Men < 30 years Men > / 3 0 years Women Women < 30 years Women > / 3 0 years

[1-14] [2,12] [2] [1,2,4-6,9,14] [2] [2] [1,2,4-6,9,14] [2] [2]

13 940 183 808 4 140 63 356 4 482 43 452

4542 51 260 1 897 20 142 1 106 24 118

33 28 32 46 32 40 25 56 26

IDDM patients Men Women

[ 1,4,6,8-13] [ 1,4,8,9] [1,4,8,9]

4 264 1 578 1 414

1 769 789 524

41 50 37

subjects in the other included studies, dealing with both diabetic and non-diabetic subjects and demonstrating comparable smoking prevalences in both groups. As a consequence these studies demonstrate a lower smoking prevalence in diabetic patients compared with our study. The same accounts for the high smoking prevalence in the IDDM group. Another explanation may be the inclusion of studies dealing with both diabetic and normal subjects and showing comparable, relatively high smoking prevalences, from which only the diabetic group has been included, because concerning the normal group only percentages and no absolute figures were available. Also the inclusion of studies in which a high smoking prevalence exists in both groups, but only including a relative small number of normal subjects, may distort our findings. Despite these limitations the prevalence of smoking is comparable for subjects with and without diabetes mellitus and may even be higher in the former.

Only few studies demonstrated a lower smoking prevalence among patients with diabetes mellitus. One of them, a Polish study, demonstrated a lower prevalence of current smokei's (29 vs. 35%, p < 0.01) and a greater frequency of exsmokers (20 vs. 16%, p < 0.01) in diabetic patients compared with a representative sample of the general population [5]. In a Scottish study, diabetic patients who did smoke, did so less frequently (67 vs. 51% smoked < 20 cigarettes) and gave up smoking more often (13 vs. 7%) than non-diabetic subjects [2]. Many IDDM patients are diagnosed at the age at which they are most likely to initiate smoking and education against it could be an explanation for its lower prevalence among young diabetic patients in some studies. Several factors concerning the prevalence of smoking among diabetic patients have been studied. Older diabetic and non-diabetic populations have lower prevalence rates of smoking than younger age groups in some studies [1,2,16,17].

Table 2 Prevalence of smoking in the general population [2,3,5,6,8,10] Group

Reference

Number of persons (n)

Number of smokers (n)

Prevalence of smoking (%)

Both men and women Men Women

[2,3,5,6,8,10] [2,5,8] [2,5,8]

64 550 2 651 3 115

17 594 1 308 833

27 49 27

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Explanations include excess mortality among smokers, leaving a higher prevalence of nonsmokers among the survivors, and intervention in smoking behaviour. However, a recent study demonstrated a low prevalence of smoking among diabetic teenagers as compared with young diabetic adults, after leaving the paediatric clinic (9 vs. 48%) [12]. In another study, the relationship between outpatient clinic attendance and smoking has been investigated [1]. Insulin-treated patients who did not attend any outpatient clinic were more frequently smokers. This difference was only significant for men (56 vs. 43%, p < 0.05), who were also less likely to have stopped smoking (20 vs. 26%, p < 0.025) or decreased consumption. Both men and women non-attenders were more likely to have started smoking after the onset of diabetes. The possible influence of therapy on smoking behaviour has been investigated [1,2]. Only a modest or no difference at all in smoking prevalence has been found between insulin-treated and non-insulin-treated patients. However, the Polish study demonstrated the highest number of smokers and the lowest number of ex- and non-smokers in the insulin-treated group (respectively 47, 13, and 40%) [5]. Regarding the influence of gender on smoking behaviour, significantly more diabetic men than women smoked more than 20 cigarettes per day (22 vs. 14%, p < 0.05) and significantly more female subjects were never smokers (32 vs. 20%, p < 0.01) [1,4,18]. Comparable results are found in the general population (Table 2) [2,5,8]. The already mentioned possible operating bias may be an explanation for the lack of a significant difference in smoking when studying men and women with and without diabetes mellitus separately.

3. Deleterious effects of smoking in normal and diabetic subjects Cigarette smoking produces a variety of pathophysiological changes, independent of diabetes meUitus, in organs such as the heart, the arteries,

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the kidneys, the liver, and the eyes. Major toxic constituents of cigarette smoke include carbon monoxide, nicotine, and various carcinogenic polycyclic hydrocarbons. The pathophysiological mechanisms underlying the adverse health effects are complex. Smoking increases carboxyhaemoglobin concentration, which results in tissue hypoxia, inducing functional and structural changes and possibly contributing to the development of atherosclerosis [19,20]. Smoking enhances platelet aggregability and increases packed cell volume and fibrinogen levels in the blood, factors which promote thrombus formation. Sympathoadrenal and cholinergic mechanisms are also stimulated, the former inducing acute haemodynamic and metabolic changes. Also the vasoconstrictory effect of nicotine induces a transient rise of pulse rate and blood pressure [21]. Hormonal changes are also induced by smoking [22]. Metabolic control is worse in smoking compared with non-smoking diabetic patients, as reflected by hyperglycaemia and increased levels of glycosylated haemoglobin in the former [4,13,23]. This worse metabolic control leads to the development of diabetic complications. In normal subjects smokers have also, however slightly, higher levels of glycosylated haemoglobin. Smoking is also associated with higher serum concentrations of cholesterol, triglycerides, very- low-density lipoprotein (VLDL) cholesterol, and low-density lipoprotein (LDL) cholesterol, and lower serum concentrations of high-density lipoprotein (HDL) cholesterol and apolipoprotein A1 compared with non-smokers. Plasma levels of apolipoprotein B are also influenced [20,24]. In a recent study, smokers with IDDM reported hospitalizations, bed days, and poor health significantly more frequently than non-smokers with or without IDDM [6]. For each morbidity measure the magnitude of smoking by diabetes interaction was greater than multiplicative and 50-75% of excess morbidity over the combined effects of smoking and IDDM was due to this interaction. However, the possible confounding effect of overweight on the reported morbidity by smokers with diabetes mellitus must be considered.

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4. Macrovascular complications of smoking in diabetes 1DDM and N I D D M are associated with considerable excess morbidity and mortality at all ages [6,23,25,26]. Diabetic patients have a 2- to 3-fold excess risk of atherosclerotic complications, also occurring at an earlier age, compared with non-diabetic subjects [20,23,27]. Coronary heart disease appears to be an increasingly important cause of death among IDDM subjects with increasing age [25,28]. Diabetes is also a particularly strong risk factor for coronary heart disease mortality in young adults [29]. Diabetic women younger than 55 years have a 16-fold higher risk and diabetic men less than 45 years old have an 8-fold higher risk of dying from this disease. As already mentioned above, cigarette smoking is also an important risk factor for chronic disease and mortality by causing atherosclerotic c o m p l i c a t i o n s [8,16,30-32]. S o m e of the smoking-related pathophysiological changes associated with atherosclerosis are also found in (non-smoking) diabetic subjects [20,24,33-35]. It is reasonable to suspect, therefore, that smoking may predispose these patients to the development of vascular complications. It has been demonstrated that up to 65% of cardiovascular deaths in smoking diabetic patients could be attributed to the interaction of smoking and diabetes [29,36,37]. The adverse vascular effects of smoking are related to its duration and the number of cigarettes smoked. The excess morbidity and mortality is greater than that expected from the combined effects of smoking and diabetes mellitus. This rather multiplicative than additive relation suggests a synergistic effect of both in the development of atherosclerosis. A common deficiency in most studies is that I D D M and N I D D M are not examined separately. Diabetes appears to have a more significant adverse effect on cardiovascular disease in women than in men. An American study in I D D M patients demonstrated smoking to be a significant independent predictor of all-cause mortality in female, but not male diabetic patients (relative

risk 2.57 vs. 1.21, p = 0.04) [8]. The excess mortality in women was explained by a marked excess risk of coronary heart disease mortality in smokers. As regards causes of mortality, it turned out that in male IDDM patients the rates of coronary disease and diabetic nephropathy deaths were approximately equal, whereas in women the mortality due to coronary disease was twice that of renal disease. Other studies also support the higher risk of cardiovascular complications in female diabetic patients and that, as a consequence, cardiovascular mortality in them equals that of men [34,38,39]. The smoking-induced increase in 2-hydroxylation of estradiol, resulting in a clinically important anti-oestrogenic effect, may play a role in this [22]. Diabetic dyslipidaemia, which potentiates atherosclerosis, appears to have a more deleterious effect in women than in men, especially concerning levels of HDL- and VLDL-cholesterol [33,34,40]. This may also explain the greater increased risk of coronary heart disease mortality among diabetic women. Besides dyslipidaemia, obesity and hypertension have been observed to cluster in diabetic women [38]. Atherosclerosis is much more prevalent in younger, non-diabetic men than women [8]. In young IDDM women the interaction of smoking and diabetes could be important in increasing the risk of coronary heart disease mortality, whereas in men the progressive vascular disease due to diabetes alone may substantially enhance the risk of heart disease with only an unexpectedly small additional effect due to smoking. Obviously, further research is needed to determine in which way a sex interaction is present. Users of oral contraceptives have higher relative risks of coronary heart disease associated with smoking than other women [41]. No comparable data are available on the risk of smoking among diabetic women taking oral contraceptives. However, it appears justified to assume that such females are at an extra increased risk of cardiovascular complications. This fact may also have contributed to the increased risk of smoking in women observed in the American study mentioned above.

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5. Microvascular complications of smoking in diabetes

Smoking has been associated with the development of microvascular complications in diabetes. Both diabetic nephropathy [4,7,23,42-51] and diabetic retinopathy [7,9,23,42,52-55] have been associated with smoking. Other studies, however, failed to confirm an association between smoking and diabetic retinopathy and controversy about this complication persists [4,17,36,43,56-61]. Increasing cigarette consumption has been associated with a higher frequency of diabetic nephropathy and poor metabolic control, altered blood rheology, and vascular hyperreactivity could be implicated in its pathogenesis [62-64]. The pathophysiological link between smoking and diabetic nepbropathy, however, remains to be elucidated. Recent studies also suggest smoking as a risk indicator for extra-articular connective tissue changes, leading to limited joint mobility, in both diabetic and non-diabetic subjects [65], and as a risk indicator for neuropathy in IDDM patients [7,66,67]. Disturbances of sexual function in diabetic patients such as impotence may also be aggravated by smoking [68,69]. Moreover, smoking and diabetes mellitus are risk indicators for periodontal disease [70-72] and pancreatic carcinoma [73]. Studies describing associations between smoking and microangiopathy often include small numbers of selected patients and unmeasured confounding variables cannot be excluded. Furthermore, failure to find an association in several larger studies may also result from selective mortality [58,59,65]. Since subjects cannot be randomly assigned to smoking or even to stop smoking, definite evidence considering this association will be difficult to obtain.

6. Effects of smoking on insulin metabolism and action

It is conceivable that smoking may further reduce insulin-mediated glucose disposal in dia-

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betic patients via two mechanisms. First, peripheral vasoconstriction during smoking could reduce the capillary surface area, thus decreasing glucose transport from the intravascular to the extravascular space [74,75]. Second, smoking increases the secretion of counterregulatory hormones, which could impair insulin secretion and reduce insulin-mediated glucose uptake by influencing a- and/3-adrenoceptors [21,36,76-79]. Studies comparing insulin requirements in smoking and non-smoking diabetic subjects indicated similar [17,42,80-82] or increased [4,56] daily insulin doses in smokers. One confounding factor in this comparison was the finding of a delayed absorption of insulin from the injection site by smoking [83]. A more recent study did not find such a delayed absorption, which had been based on a suggested smoking-induced hampered subcutaneous blood flow [84]. Moreover, the insulin dose only provides a rough estimate of insulin sensitivity [85]. A recent study among NIDDM patients has shown smoking to impair insulin action, not its endogenous secretion [79]. By impairing insulin action on the liver, adipose tissue, and muscle, nicotine may contribute to hyperglycaemia, thus exaggerating insulin resistance, the typical feature of NIDDM. Another recent study in non-diabetic subjects also shows smoking to impair insulin action, mainly due to a lower peripheral glucose uptake [86]. Smoking-induced mechanisms contributing to hyperglycaemia are increased hepatic glucose production, diminished anti-lipolytic action of insulin, and reduced peripheral glucose uptake, primarily by muscle. A counterargument for the latter may be that smoking leads to vascular changes, thus reducing blood flow to muscles, and thereby causing a decrease in insulin-mediated glucose uptake. The smoking-induced hyperglycaemia and hyperinsulinaemia, the marker of insulin resistance, contribute to the increased cardiovascular risk in diabetes. Smoking has been shown to increase the secretion of catecholamines (noradrenaline and adrenaline), growth hormone, cortisol, glucagon, and aldosterone and could thus lead to an increased insulin requirement in diabetic patients [21,82,86,87]. However, smoking-induced devia-

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tions in counterregulatory hormones are minor and short-lived. Previous studies demonstrating an inhibitory effect of adrenaline on glucose disposal have employed external infusion raising plasma adrenaline up to 30-fold [76,88,89]. A decline in glucose disposal was not noted until adrenaline levels increased at least 5-fold above the baseline [89]. In a more recent study, plasma adrenaline only rose 2-fold during smoking, thus below the threshold required for the inhibitory effect on glucose disposal [82]. Contrary to other studies [21,87] plasma noradrenaline levels remained unchanged during smoking. In recent studies, no differences in plasma noradrenaline between smoking and non-smoking or between diabetic and non-diabetic subjects have been found either [64,86]. Smoking-associated haemodynamic (increments in pulse rate and blood pressure) and metabolic (increased blood glycerol levels) changes are adrenergic-mediated [21,87]. This sympathetic discharge can only in part be attributed to nicotine, since increased urinary adrenaline excretion during smoking of nicotinefree cigarettes has been reported [21,90]. Regarding the influence of growth hormone on glucose disposal, a 7- to 10-fold elevation for 2 hours failed to reduce glucose uptake [77]. Only after 12 hours of maintenance of these high concentrations did the inhibitory effect become significant. In a more recent study, growth hormone rose 6-fold during smoking [25]. However, by the end of 2 hours of smoking growth hormone levels were similar in the smoking and control study. In another study a 3-fold higher growth hormone level was observed during smoking [86]. A 4-fold rise in serum cortisol for 12 hours has been shown to reduce glucose disposal [78]. In more recent studies, serum cortisol and plasma glucagon did not show a significant increase during smoking [82,86]. In addition to sympathetic stimulation, smoking a cigarette is followed by transient increases of plasma cortisol and aldosterone levels in hypertensive subjects [87]. Cortisol and aldosterone showed an increase only after a rise in plasma ACTH had occurred. Plasma renin activity did not change significantly after

smoking. These results suggest activation of a pituitary-adrenal mechanism. During smoking an adrenergic- and not an angiotensin-mediated rise of blood pressure is present. The stimulation of aldosterone by smoking is not likely to lead to persistent hyperaldosteronism, because habitual smokers do not exhibit elevated levels of plasma aldosterone before smoking a cigarette. Moreover, during long-term ACTH administration aldosterone secretion progressively diminishes [91]. In conclusion, neither acute nor habitual smoking causes substantial changes in insulin sensitivity in IDDM patients, whereas it does so in NIDDM. The different origins of insulin resistance in both types of diabetes may be an explanation. The clinical relevance of a possible effect of smoking on insulin requirement in IDDM appears to be negligible, if it exists at all. In the individual patient who starts smoking or gives up smoking, such an influence will hardly be identifiable among the other more relevant factors which determine daily insulin requirement. However, regarding these findings, it should be stressed that the studies discussed almost all deal with acute effects, and that little is known about the chronic effects.

7. Smoking and development of diabetes mellitus In several studies a positive association between smoking and development of diabetes mellitus, mostly NIDDM, has been observed (relative risk varying from 1.42 to 3.3) [74,86,92,93]. A significant dose-response trend for higher risk among heavier smokers has been demonstrated. Alterations in relative weight, fat distribution, and insulin resistance and toxic effects on pancreatic tissue are implicated. Smoking is associated with a greater waist-to-hip ratio, a measure of fat distribution related to insulin resistance and overt diabetes. Smoking also increases glycosylated haemoglobin in both diabetic and normal subjects, which is explained by a smoking-induced hypoxic state [13,94]. Its formation is regarded as a model for glycosylation of body proteins, which is considered to underlie diabetic complications.

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8. Influence of diabetes on smoking behaviour

The greater cardiovascular risks for diabetic patients and the frequent contact they have with health care providers have only a minor effect on smoking behaviour. The knowledge itself of having diabetes also has a slight influence. In several studies, the numbers giving up smoking after diagnosis increased with time, but even after 5 years these were still fairly low [1,4]. While only 14% of the smokers had given up 5 years later, 8% of the non-smokers started smoking after diagnosis. Because of the likely excess mortality in smokers, the observed trends in the survivor populations available for study may overestimate the proportion giving up smoking and underestimate those starting smoking after diagnosis of diabetes. In ex-smokers the major attributable factor for ceasing smoking was a general concern for health, while the fear or the actual development of diabetic complications had not prompted anyone to stop smoking [95]. For the majority of smokers, diabetes and its complications did not appear to be regarded as health issues which were sufficiently serious to warrant cessation. This contrasts with other high-risk groups (e.g., cardiac patients), presumably because they perceive themselves to be far more vulnerable and are more likely to quit smoking [96]. Several studies revealing a high prevalence of smokers in insulin-treated patients suggest that cigarette smoking may be a method of suppression of anxiety and tension connected with the awareness of serious disease and the need for insulin injections [5,14,56].

9. Anti-smoking programmes among diabetic patients

In order to minimize the risk of cardiovascular disease, dissuading diabetic patients from smoking along with reducing hyperglycaemia, increased serum cholesterol concentration, and elevated blood pressure is necessary. A knowledge of the psychosocial aspects of diabetic patients and of their awareness of the effects of smoking

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on healthy is necessary in order to develop an effective anti-smoking programme. Furthermore, strategies already applied in diabetic and in other patient groups have to be studied. Up to now, only few guidelines are available on how antismoking programmes are best implemented in diabetic patients. The acceptance of a chronic disease requiring changes in lifestyle is difficult. This is particularly true in the case of diabetes, since these patients generally are aware of their vulnerability to late complications and shortened life expectancy. Understandably, the considerable psychosocial problems and dietary restrictions experienced in coping with diabetic treatment regimens often hamper these and appear to militate against antismoking advice being successful in other disease groups [3,7,14,36,97,98]. Not surprisingly, one of these studies in diabetic patients demonstrated smoking to be associated with depressive symptomatology [14]. Depression is more prevalent among diabetic patients and among those who smoke and may explain the lower smoking cessation rates in diabetic patients. The mood-altering effects of nicotine may encourage smoking in these patients, dealing with increased stress associated with diabetes management. Studies examining the impact of diabetes on patients' psychosocial adjustment and relationship of this adaptation to management and treatment outcomes have demonstrated a link between coping with diabetes and metabolic control [14,99,100]. According to motivation theory, by applying avoiding coping strategies, smokers are less concerned with the long-term consequences of poor metabolic control and focus more on the immediate positive outcomes of certain (noncompliant) behaviours [13]. Younger diabetic patients have particular difficulty in stopping smoking, despite regular anti-smoking advice. Nicotine addiction reduces appetite, particularly for sweet tasting foods, and its withdrawal is associated with an increased desire for such foods [14,36]. Evidence suggesting an important role for neuropsychologic aberrations in the development and clinical expression of atherosclerosis has been obtained [15,101-104]. In a detailed screening of

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personality patterns in patients with long-standing diabetes important differences were found between those with and without vascular complications. It is suggested that risk factors have a much more ominous significance in individuals with type A rather than type B personality. Biochemical correlates of the former are exemplified by enhanced catecholamine responses to various stimuli. These findings suggest that clinically useful psychological predictors may become available for use in identifying patients at greater risk for diabetic complications. Considering knowledge of the adverse effects of smoking on health, most patients recognized that smoking is harmful. However, their specific knowledge of how health could be affected was poor, especially concerning their awareness of the interaction between smoking and diabetic complications [95]. While 89% of diabetic patients knew that smoking is detrimental to general health, only 10 to 23% were able to state that smoking could worsen diabetic complications. Inadequate patient education has been suggested as an explanation. Generally, health care providers can play an important role in helping people to stop smoking. Minimal physical counselling has been shown to be effective in leading to a 5% success rate at 1 year [105]. Structured group session programmes have yielded success rates up to 45% at 1 year [106]. The best short-term results in stopping smoking have been seen after dramatic lifethreatening, smoking-related illnesses (e.g., myocardial infarction), when 60% of patients were able to stop [107]. In contrast, diabetic subjects are clinically stable in most cases and have an illness which is not directly caused by smoking. Several studies on anti-smoking programmes in diabetic patients showed very disappointing results [95,97,108]. It turned out to be even more difficult to convince a diabetic patient to stop smoking than a non-diabetic person. An Australian study determining the optimal time and content of anti-smoking intervention demonstrated a high drop-out rate, irrespective of the programme's content [95]. Better patient responses were demonstrated several months after diagnosis.

The results of routine and intensive anti-smoking advice for young (aged < 40 years) diabetic smokers have been compared in a British study [97]. Being unconvinced of the health hazards of cigarettes or already too restricted by a diabetic treatment regimen were reasons for making no serious attempt to give up smoking in half of these patients. The other half only stopped smoking for a few days. A recent study in IDDM patients also demonstrated an extensive behaviour therapy intervention to be no more successful than unstructured physician's advice [108]. Moreover, few smoking patients with diabetes are willing to participate in a smoking cessation programme. If they do not themselves initiate efforts to stop, almost all attempts motivated by external forces are unsuccessful. In conclusion, regarding experience with antismoking programmes, approaches which concentrate on providing information or behaviour therapy alone are extremely time-consuming with only little result. Alternative strategies are warranted such as behaviour modification combined with pharmacological aids like nicotine chewing gum or transdermal nicotine patches for patients highly dependent on nicotine. Antidepressant agents, as a means of treating depressive moods associated with nicotine withdrawal, allow time to better incorporate behavioural strategies which are critical in learning how to deal with problems of stress or anxiety which interfere with smoking cessation.

10. Conclusion

The prevalence of smoking among diabetic patients is significantly higher than that in the general population, largely accounted for by IDDM patients. However, these findings must be interpreted with some caution. Regarding the late effects of smoking, evidence is accumulating that smoking presents an extra risk for the development of macro- and microvascular complications in diabetic patients. The adverse vascular effects demonstrated by smoking and diabetes appear to be caused by a synergistic effect of both

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o n the c o m p o n e n t s of the vascular wall a n d are m o r e p r o m i n e n t in w o m e n t h a n in men. Considering the i n t e r r e l a t i o n s h i p s b e t w e e n smoking a n d the d e v e l o p m e n t of diabetes, f u r t h e r research is needed. It has b e e n shown that n e i t h e r acute n o r habitual smoking causes substantial c h a n g e s in insulin sensitivity in I D D M patients. T h e smoking-ind u c e d c h a n g e s in insulin c o u n t e r r e g u l a t o r y horm o n e s a n d in o t h e r factors significant in glucose u p t a k e are so m i n o r that the effects are negligible. Studies in diabetic subjects c o n c e r n i n g antismoking strategies are scarce a n d only yield disa p p o i n t i n g results. M a k i n g diabetic p a t i e n t s abstain from smoking t u r n s out to be extremely difficult. T h e c o n s i d e r a b l e psychosocial p r o b l e m s e x p e r i e n c e d by these p a t i e n t s a p p e a r to militate against a n t i - s m o k i n g advice, which is successful in o t h e r disease groups. A p p r o a c h e s which c o n c e n trate o n providing i n f o r m a t i o n alone are almost without success. D i a b e t i c p a t i e n t s have their own specific p r o b l e m s that have to be addressed to help t h e m stop smoking. Obviously, t h e r e is a n e e d to develop alternative strategies. Possibly, i n t e r v e n t i o n s applying psychological strategies, like b e h a v i o u r m o d i f i c a t i o n a n d g r o u p sessions, a n d p h a r m a c o l o g i c a l aids such as n i c o t i n e chewing g u m a n d a n t i d e p r e s s a n t agents will be m o r e successful.

References [1] Jones RB, Hedley AJ. Prevalence of smoking in a diabetic population: The need for action. Diabet Med 1987;4:233-236. [2] Kesson CM. Smoking in diabetics (Letter). Lancet 1979;1:504-505. [3] Ford ES, Newman J. Smoking and diabetes mellitus. Findings from 1988 behavioral risk factor surveillance system. Diabetes Care 1991;14(10):871-874. [4] Telmer S, Sandahl Christiansen J, Andersen AR, Nerup J, Deckert T. Smoking habits and prevalence of clinical diabetic microangiopathy in insulin-dependent diabetics. Acta Med Scand 1984;215:63-68. [5] Czyzyk A, Krolewski AS. Is cigarette smoking more frequent among insulin-treated diabetics? Diabetes 1976;25:717-718.

159

[6] Gay E.C, Cai Y, Gale SM, et al. Smokers with IDDM experience excess morbidity. Diabetes Care 1992;15(8): 947-952. [7] Roberts M. Smoking and diabetes. Nurs Times 1992;88(8):59-60. [8] Moy CS, Laporte RE, Dorman JS, et al. Insulin-dependent diabetes mellitus mortality: the risk of cigarette smoking. Circulation 1990;82:37-43. [9] Nielsen MM, Hjollund E. Smoking and diabetic microangiopathy. Lancet 1978;2:533-534. [10] Songer TJ. What impact does insulin dependent diabetes mellitus (IDDM) have upon health behaviors? Diabetes 1988;37(suppl 1):124A(Abstract). [11] Masson EA, MacFarlane IA, Priestly CJ, Wallymahmed ME, Flavell HJ. Failure to prevent nicotine addiction in young people with diabetes. Arch Dis Child 1992;67:100-102. [12] Shaw NJ, McClure RJ, Kerr S, Lawton K, Smith CS. Smoking in diabetic teenagers. Diabet Med 1993;10(3): 275-277. [13] Bott U, Jorgens V, Grusser M, Bender R, Muhlhauser I, Berger M. Predictors of glycaemic control in type 1 diabetic patients after participation in an intensified treatment and teaching programme. Diabet Med 1994;11(4):362-371. [14] Haire-Joshu D, Heady S, Thomas L, Schechtman K, Fisher EB. Depressive symptomatology and smoking among persons with diabetes. Res Nurs Health 1994;17(4):273-282. [15] Dasvis WK, Hess GE, Hiss RG. Psychosocial correlates of survival in diabetes. Diabetes Care 1988;11(7):538545. [16] Fielding JE. Smoking: Health effects and control. N Engl J Med 1985;313:491-498. [17] Klein R, Klein BEK, Davis MD. Is cigarette smoking associated with diabetic retinopathy? Am J Epidemiol 1983;118:228-238. [18] Thorell B, Olsson L, Svardsudd K. Implementation of a structured care programme for diabetes mellitus in a defined population in mid-Sweden. Diabet Med 1994;11(5):458-464. [19] Dintenfass L. Elevation of blood viscosity, aggregation of red cells, haematocrit values and fibrinogen levels in cigarette smokers. Med J Aust 1975;1:617-620. [20] Ganda OMP. Pathogenesis of macrovascular disease in the human diabetic. Diabetes 1980;29:931-942. [21] Cryer PE, Haymond MW, Santiago JV, Shah SD. Norepinephrine and epinephrine release and adrenergic mediation of smoking-associated hemodynamic and metabolic events. N Engl J Med 1976;295:573-577. [22] Michnovicz JJ, Hershcopf RJ, Naganuma H, Bradlow HL, Fishman J. Increased 2-hydroxylation of estradiol as a possible mechanism for the anti-estrogenic effect of cigarette smoking. N Engl J Med 1986;315:1305-1309. [23] Muhlhauser I. Cigarette smoking and diabetes: an update. Diabet Med 1994;11:336-343.

160

R.LJ. Dierkx et al. / Netherlands Journal of Medicine 48 (1996) 150-162

[24] Craig WY, Palomaki GE, Haddow JE. Cigarette smoking and serum lipid and lipoprotein concentrations: an analysis of published data. Br Med J 1989;298:784-788. [25] Connell FA, Louden JM. Diabetes mortality in persons under 45 years of age. Am k Publ Health 1983;73:11741177. [26] Lestradet H, Papoz L, Hellouin de Menibus CL, et al. Long-term study of mortality and vascular complications in juvenile-onset (Type 1) diabetes. Diabetes 1981;30:175-179. [27] Kannel WB, McGee DL. Diabetes and cardiovascular disease. The Framingham Study. J Am Med Assoc 1979;241:2035-2038. [28] Krolewski AS, Kosinski E J, Warram JH, et al. Magnitude and determinants of coronary artery disease in juvenile-onset insulin-dependent diabetes mellitus. Am J Cardiol 1987;59:750-755. [29] DeStefano F, Ford ES, Newman J, et al. Risk factors for coronary heart disease mortality among persons with diabetes. Ann Epidemiol 1993;3(1):27-34. [30] Fowkes FG, Housley E, Riemersma RA, et al. Smoking, lipids, glucose intolerance, and blood pressure as risk factors for peripheral atherosclerosis compared with ischemic heart disease in the Edinburgh Artery Study. Am J Epidemiol 1992;135(4):331-340. [31] Kannel WB, McGee DL. Diabetes and cardiovascular risk factors: The Framingham Study. Circulation 1979;59:8-13. [32] Jarrett R J, Shipley MJ. Mortality and associated risk factors in diabetes. Acta Endocrinol 1985;l10(suppl 272):21-26. [33] Betteridge DJ. Diabetic dyslipidemia. Am J Med 1994;96(6A):25S-31S. [34] Goldschmid MG, Barrett-Connor E, Edelstein SL, Wingard DL, Cohn BA, Herman WH. Dyslipidemia and ischemic heart disease mortality among men and women with diabetes. Circulation 1994;89(3):991-997. [35] Stanton K. H.D.L. cholesterol in diabetes and heart disease. Lancet 1978;2:638, [36] Macfarlane IA. The smoker with diabetes: a difficult challenge. Postgrad Med J 1991;67(792):928-930. [37] Suarez L, Barrett-Connor E. Interaction between cigarette-smoking and diabetes mellitus in the prediction of death attributed to cardiovascular disease. Am J Epidemiol 1984;120:670-675. [38] Gordon T, Castelli WP, Hjortland MC, Kannel WB, Dawber TR. Diabetes, blood lipids, and the role of obesity in coronary heart disease risk for women. The Framingham study. Ann Intern Med 1977;87:393-397. [39] Garcia MJ, McNamara PM, Gordon T, Kannell WB. Morbidity and mortality in diabetics in the Framingham population: sixteen year follow-up study. Diabetes 1974;23:105 - 111. [40] Waldern WE, Knopp RH, Wahl PW, Beach KW, Strandness DE. Sex differences in the effect of diabetes mellitus on lipoprotein triglyceride and cholesterol concentrations. N Engl J Med 1984;311:953-959. [41] Croft P, Hannaford PC. Risk factors for acute myocar-

[42]

[43]

[44] [45] [46]

[47]

[48]

[49]

[50]

[51]

[52]

[53]

[54]

[55]

[56]

[57]

dial infarction in women: evidence from the Royal College of General Practitioners' oral contraception study. Br Med J 1989;298:165-168. Muhlhauser I, Sawicki P, Berger M. Cigarette-smoking as a risk factor for macroproteinuria and proliferative retinopathy in Type 1 (insulin-dependent) diabetes. Diabetologia 1986;500-502. Christiansen JS. Cigarette smoking and the prevalence of microangiopathy in juvenile-onset insulin-dependent diabetes mellitus. Diabetes Care 1978;1:146-149. Norden G, Nyberg G. Smoking and diabetic nephropathy. Acta Med Scand 1984;215:257-261. Saegmayr B, Lithner F. Tobacco and end stage diabetic nephropathy. Br Med J 1987;295:581-582. Borch-Johnson K, Nissen H, Henriksen E, et al. The natural history of insulin-dependent diabetes mellitus in Denmark. 1. Long-term survival with and without late diabetic complications. Diabetic Med 1987;4:201-210. Kumar S. American diabetes association annual scientific sessions, San Antonio, 20-23 June 1992. Diabet Med 1992;9(10):957-959. Sawicki PT, Didjurgeit U, Muhlhauser I, Bender R, Heinemann L, Berger M. Smoking is associated with progression of diabetic nephropathy. Diabetes Care 1994;17(2):126-131. Risk factors for development of microalbuminuria in insulin dependent diabetic patients: a cohort study. Microalbuminuria Collaborative Study Group, United Kingdom. Br Med J 1993;306(6887):1235-1239. Olivarius N de F, Andreasen AH, Keiding N, Mogensen CE. Epidemiology of renal involvement in newly-diagnosed middle-aged and elderly diabetic patients. Cross-sectional data from the population-based study "Diabetes Care in General Practice", Denmark. Diabetologia 1993;36(10):1007-1016. Klein R, Klein BE, Moss SE. Incidence of gross proteinuria in older-onset diabetes. A population-based perspective. Diabetes 1993;42(3):381-389. Paetkau ME, Boyd TAS, Winship B, Grace M. Cigarette smoking and diabetic retinopathy. Diabetes 1977;26:4649. Moss SE, Klein R, Klein BE. Ten-year incidence of visual loss in a diabetic population. Ophthalmology 1994; 101(6): 1061-1070. Marshall G, Garg SK, Jackson WE, Holmes DL, Chase HP. Factors influencing the onset and progression of diabetic retinopathy in subjects with insulin-dependent diabetes mellitus. Ophthalmology 1993;100(8):11331139. Sparrow JM, McLeod BK, Smith TD, Birch MK, Rosenthal AR. The prevalence of diabetic retinopathy and maculopathy and their risk factors in the non-insulin-treated diabetic patients of an English town. Eye 1993;7(Pt 1):158-163. Madsbad S, McNair P, Christensen MS. Influence of smoking on insulin requirement and metabolic status in diabetes mellitus. Diabetes Care 1980;3:41-43. The World Health Organisation multinational study of

R.LJ. Dierkx et al. / Netherlands Journal of Medicine 48 (1996) 150-162

[58]

[59]

[60]

[61]

[62]

[63]

[64]

[65]

[66]

[67]

[68] [69]

[70] [71]

[72]

[73]

vascular disease in diabetics. Prevalence of small vessel and large vessel disease in diabetic patients from 14 centres. Diabetologia 1985;28:615-640. West KM, Erdreich LS, Stober JA. Absence of a relationship between smoking and diabetic microangiopathy. Diabetes Care 1980;3:250-252. West KM, Ahuja MMS, Bennett PH, et al. Interrelationship of microangiopathy, plasma glucose and other risk factors in 3583 diabetic patients: a multinational study. Diabetologia 1982;22:412-420. Dornan T, Mann JI, Turner R. Factors protective against retinopathy in insulin-dependent diabetics free of retinopathy for 30 years. Br Med J 1982;285:1073-1077. Rand LI, Krolewski AS, Aiello LM, Warram JH, Baker RS, Maki T. Multiple factors in the prediction of risk of proliferative diabetic retinopathy. N Engl J Med 1985;313:1433-1438. Simpson LO. Intrinsic stiffening of red blood cells as the fundamental cause of diabetic nephropathy and microangiopathy: a new hypothesis. Nephron 1985;39: 344-351. Simpson LO, Shand BI, Olds RJ. A reappraisal of the influence of blood rheology on glomerular filtration and its role in the pathogenesis of diabetic nephropathy. J Diabet Complicat 1987;1:137-144. Bodmer CW, Valentine DT, Masson EA, Savage MW, Lake D, Williams G. Smoking attenuates the vasoconstrictor response to noradrenaline in type 1 diabetic patients and normal subjects: possible relevance to diabetic nephropathy. Eur J Clin Invest 1994;24(5):331-336. Eadington DW, Patrick AW, Collier A, Frier BM. Limited joint mobility, Dupuytren's contracture and retinopathy in Type 1 diabetes: association with cigarette smoking. Diabetic Med 1989;6:152-157. Mitchell BD, Hawthorne VM, Vinik AI. Increased prevalence of neuropathy associated with cigarette smoking in IDDM. Diabetes 1989;39(suppl 2)i16A (Abstract). Cruickshanks KJ, Gay E, Hamman RF. Smoking is related to symptoms of neuropathy in a cohort of young subjects with insulin-dependent diabetes mellitus (IDDM). Diabetes 1989;39(suppl 2):35A(Abstract). Muhlhauser I. Smoking and diabetes. Diabetic Med 1990;7:10-15. Wang CJ, Shen SY, Wu CC, Huang CH, Chiang CP. Penile blood flow study in diabetic impotence. Urol Int 1993;50(4):209-212. Genco RJ. Assessment of risk of periodontal disease. Compendium 1994;(suppl 18):S678-683:quiz $714-717. Haber J, Wattles J, Crowley M, Mandell R, Joshipura K, Kent RL. Evidence for cigarette smoking as a major risk factor for periodontitis. J Periodontol 1993;64(1): 16-23. Grossi SG, Zambon J J, Ho AW, et al. Assessment of risk for periodontal disease. 1. Risk indicators for attachment loss. J Periodontol 1994;65(3):260-267. Balkau B, Barrett-Connor E, Eschwege E, Richard JL,

[74]

[75] [76] [77]

[78]

[79]

[80]

[81]

[82]

[83]

[84]

[85]

[86]

[87]

[88]

[89]

161

Claude JR, Ducimetiere P. Diabetes and pancreatic carcinoma. Diabet Metab 1993;19(5):458-462. Facchini FS, Hollenbeck CB, Jeppesen J, Chen YDI, Reaven GM. Insulin resistance and cigarette smoking. Lancet 1992;339:1128-1130. Roth GM, Shick RM. Effect of smoking on the cardiovascular system of man. Circulation 1958;17:443-459. Dreibert DC, DeFronzo RA. Epinephrine-induced insulin resistance in man. J Clin Invest 1980;65:717-721. Bratusch-Marrain PR, Smith D, DeFronzo RA. The effect of growth hormone on glucose metabolism and insulin secretion in man. J Clin Endocrinol Metab 1982;55:973-983. Rizza RA, Mandarino LI, Gerich JE. Cortisol-induced insulin resistance in man: impaired suppression of glucose production and stimulation of glucose utilization due to a postreceptor defect of insulin action. J Clin Endocrinol Metab 1982;54:131-138. Epifano L, Di Vincenzo A, Fanelli C, et al. Effect of cigarette smoking and of a transdermal nicotine delivery system on glucoregulation in type 2 diabetes mellitus. Eur J Clin Pharmacol 1992;43:257-263. West KM. Association of smoking with insulin requirement and serum triglyceride level. Diabetes Care 1980;3:641. Mathiesen ER, Soegaard U, Christiansen JS. Smoking and glycernic control in male insulin dependent (Type 1) diabetics. Diabetes Res 1984;1:155-157. Helve E, Yki-Jarvinen H, Koivisto VA. Smoking and insulin sensitivity in Type 1 diabetic patients. Metabolism 1986;35:874-877. Klemp P, Staberg B, Madsbad S, Kolendorf K. Smoking reduces insulin absorption from subcutaneous tissue. Br Med J 1982;284:237. Muhlhauser I, Cuppers HJ, Berger M. Smoking and insulin absorption from subcutaneous tissue. Br Med J 1984; 288:1875 - 1876. Yki-Jarvinen H, Taskinen M-R, Kiviluoto T, et al. Site of insulin resistance in type 1 diabetes: insulin-mediated glucose disposal in vivo in relation to insulin binding and action in adipocytes in vitro. J Clin Endocrinol Metab 1984;59:1183-1192. Attvall S, Fowelin J, Lager I, Von Schenck H, Smith U. Smoking induces insulin resistance - a potential link with the insulin resistance syndrome. J Intern Med 1993;233:327-332. Baer L, Radichevich I. Cigarette smoking in hypertensive patients--blood pressure and endocrine responses. Am J Med 1985;78:564-568. Rizza RA, Cryer PE, Haymond MW, Gerich JE. Adrenergic mechanism for the effects of epinephrine on glucose production and clearance in man. J Clin Invest 1980;65:682-689. Clutter WE, Brier DM, Shah SD, Cryer PE. Epinephrine plasma metabolic clearance rates and physiologic thresholds for metabolic and hemodynamic actions in man. J Clin Invest 1980;66:94-101.

162

R.I.J. Dierkx et al. / Netherlands Journal of Medicine 48 (1996) 150-162

[90] Ague C. Urinary catecholamines, flow rate and tobacco smoking. Biol Psychol 1974;1:229-236. [91] Newton MA, Laragh JH. Effect of corticotropin on aldosterone excretion and plasma renin in normal subjects, in essential hypertension and in primary aldosteronism. J Clin Metab 1968;28:1006-1013, [92] Rimm EB, Manson JE, Stampfer MJ, et al. Cigarette smoking and the risk of diabetes in women. Am J Public Health 1993;83(2):211-214. [93] Feskens E J, Kromhout D. Cardiovascular risk factors and the 25-years incidence of diabetes mellitus in middle-aged men. Am J Epidemiol 1989;130:1101-1108. [94] Modan M, Meytes D, Rozeman P, et al. Significance of high HbA1 levels in normal glucose tolerance. Diabetes Care 1988;11(5):422-428. [95] Fowler PM, Hoskins PL, McGill M, Dutton SP, Yue DK, Turtle JR. Anti-smoking programme for diabetic patients: the agony and the ecstasy. Diabetic Med 1989;6:698-702. [96] Pederson L. Compliance with physician advice to quit smoking: a review of the literature. Prev Med 1982;11:71-84. [97] Ardron M, MacFarlane IA, Robinson C, Heyningen C, Calverley PMA. Antismoking advice for young diabetic smokers: is it a waste of breath? Diabetic Med 1988;5:667-670. [98] Spangler JG, Konen JC. Predicting exercise and smoking behaviors in diabetic and hypertensive patients. Age, race, sex, and psychological factors. Arch Fam Med 1993;2(2):149-155.

[99] Hess GE, Davis WK, Harrison RV. A diabetes psychosocial profile. Diabetes Educ 1986;12:135-140. [100] Davis WK, Hess GE, Harrison RV, Hiss RG. Psychosocial adjustment to and control of diabetes mellitus: differences by disease type and treatment. Health Psychol 1987;6:1-14. [101] Glass DC. Stress, behavior patterns, and coronary disease. Am Sci 1977;65:177-187. [102] Rosenman RH. Role of type A behavior pattern in the pathogenesis of ischemic heart disease, and modification for prevention. Adv Cardiol 1978;25:35-46. [103] Murawski BJ, Chazan BI, Balodimos MC, Ryan JR. Personality patterns in patients with diabetes mellitus of long duration. Diabetes 1970;19:259-263. [104] Friedman M, Byers SO, Diamant J, Rosenman R. Plasma catecholamine response of coronary-prone subjects (type A) to a specific challenge. Metabolism 1975;24:205-210. [105] Russel MAH, Wilson C, Taylor C, Baker CD. Effect of general practitioners' advice against smoking. Br Med J 1979;ii:231-235. [106] Tonnesen P, Fryd V, Hansen M, et al. Effect of nicotine chewing gum in combination with group counselling on the cessation of smoking. N Engl J Med 1988;318:15-18. [107] Burt A, Illingworth D, Shaw T, Thornley P, White P, Turner R. Stopping smoking after myocardial infarction. Lancet 1974;1:304-306. [108] Sawicki PT, Didjurgeit U, Muhlhauser I, Berger M. Behaviour therapy versus doctor's anti-smoking advice in diabetic patients. J Intern Med 1993;234(4):407-409.