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International Journal of Diabetes Mellitus 2 (2010) 47–50

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International Journal of Diabetes Mellitus


journal homepage: ees.elsevier.com/locate/ijdm

Review

Significance of spirometry in diabetic patients


Sultan Ayoub Meo *
Department of Physiology, College of Medicine, King Khalid University Hospital, King Saud University Riyadh, Saudi Arabia

a r t i c l e i n f o a b s t r a c t

Article history: Spirometry is a widely used pulmonary function test (PFT), ideally suited to describing the effects of
Received 7 November 2009 obstruction or restriction on lung function. It is a powerful diagnostic tool that plays a significant role
Accepted 6 December 2009 in the early diagnosis of lung damage and its associated structures. It is also used to monitor the thera-
peutic efficacy of various treatment regimes and the course of the disease. The spirometric parameters
have gained more popularity when it has been reported that impaired Forced Vital Capacity (FVC) and
Keywords: Forced Expiratory Volume in 1 s (FEV1) are emerging novel risk factors for type 2 diabetes mellitus. These
Diabetes mellitus
spirometric parameter derangements have been evident on spirometry long before the clinical diagnosis
Lungs
Spirometry
of diabetes mellitus or insulin resistance. In spite of this, spirometry is not used routinely as part of a
Pulmonary function test management system in diabetic patients. Its role is neither fully explored, nor fully utilized to achieve
quality of life when managing diabetes mellitus. The aim of the present review is to highlight the evi-
dence based significance of spirometry in the light of peer reviewed published literature. It may serve
as a brief reference for diabetes management teams to enable spirometry to be included in the algorithm
of the routine assessment of diabetic patients.
Ó 2009 International Journal of Diabetes Mellitus. Published by Elsevier Ltd.
Open access under CC BY-NC-ND license.

1. Diabetes mellitus these changes cause pulmonary dysfunction [7,8]. Diabetes melli-
tus can cause pulmonary complications due to collagen and elastin
Diabetes mellitus is a major, rapidly growing public health care changes, as well as micro-angiopathy [9]. Furthermore, pulmonary
problem. It is increasing in incidence, and brings with it long term function impairment and lung dysfunction in diabetic patients is
complications [1]. Chronic hyperglycemia of diabetes mellitus is secondary, due to immune function impairment [10].
associated with continuing damage, dysfunction, and failure of var-
ious organs, especially the eyes, kidneys, nerves, heart, lungs and
2. Spirometry and diabetes mellitus
blood vessels. Diabetes mellitus is an incurable life-long disease,
involving multiple systems, and with devastating complications
Cardio-respiratory clinical features in diabetic patients, such as
which end up in severe disability and death [2]. Diabetes mellitus
shortness of breath, dysponea, wheezing and easy fatigability make
is associated with the ongoing malfunction of various organs and
physicians more alert to coronary artery disease (CAD). No one can
its complications are mainly a consequence of macro-vascular
deny that diabetes mellitus is a major risk factor of coronary artery
and micro-vascular damage [3]. The mechanism by which im-
disease, but it must be borne in mind that the lung is also a target
paired glycemic control may lead to a reduction in lung function
organ in diabetic patients, and such clinical features might be due
is uncertain, though it has been suggested that the increased sys-
to pulmonary complications than CAD alone. A substantial number
temic inflammation associated with diabetes [3] may result in pul-
of patients who present with dysponea shows normal coronary
monary inflammation [4] as well, and hence, it can cause air way
arteries, and even normal cardiac perfusion and systolic function.
damage [5]. Moreover, secondary reduction in the antioxidant de-
Within this clinical scenario, patients’ complaints of shortness of
fense of lung and increased susceptibility to environmental oxida-
breath, dysponea and easy fatigability might need further investi-
tive insults results in the subsequent loss of lung function [6] and
gation. In this situation, the application of spirometry must be fully
ultimately, lung damage. It has been demonstrated that pulmonary
utilized to rule out pulmonary problems. The basic concepts of nor-
complications in diabetes mellitus are due to a thickening of the
mal pulmonary physiology that are involved in spirometry/pul-
walls of alveoli, alveolar capillaries and pulmonary arterioles, and
monary function testing include mechanics (airflows and lung
volumes), ventilation–perfusion interrelationship, diffusion and
gas exchange, as well as respiratory muscle strength [11] (see
* Address: Department of Physiology [29], College of Medicine, King, Khalid
University Hospital, King Saud University, P.O. Box 2925, Riyadh 11461, Saudi
Table 1).
Arabia. Tel.: +966 1 4671604; fax: +966 1 4672567. Spirometry is a powerful tool that can be used to detect, differ-
E-mail address: sultanmeo@hotmail.com entiate, follow and manage patients with pulmonary disorders.

1877-5934 Ó 2009 International Journal of Diabetes Mellitus. Published by Elsevier Ltd. Open access under CC BY-NC-ND license.
doi:10.1016/j.ijdm.2009.12.003
48 S.A. Meo / International Journal of Diabetes Mellitus 2 (2010) 47–50

Table 1 Table 3
Indications of spirometry in diabetic patients. Patho-physiological factors affecting the lung functions.

Diagnostic indications Physiological factors:


 Mandatory monitoring of lung functions in diabetic individuals every  Age, gender, height, weight, BMI, ethnicity, pregnancy, posture, exercise
two years  Customary activity, time of day, season, climate and geographical
 Diabetic patients with history of cigarette smoking, tobacco chewing, location
cough, phlegm production, chest pain, dyspnea or wheezing  Diet (malnutrition)
 Diabetic patients with abnormal laboratory tests such as blood gases
Environmental factors:
and chest radiograph
 Air pollution (occupational/environmental exposure)
 Evaluate the effect of diabetes mellitus on pulmonary function
 Smoking
 Screen all diabetic patients during their initial visits to ascertain the sta-
tus of lungs Pathological conditions:
 Screen all the diabetic patients with abnormal HBA1C and fasting blood  Chronic obstructive pulmonary disease (COPD), interstitial lung disease
glucose  Coronary artery disease
 Assessment of pre-operative risk in those diabetic who need to under-  Diabetes mellitus/impaired glucose tolerance/hormonal disorders
take any surgical process  Neuromuscular disorders (Guillain barre syndrome, Myasthenia gravis)
 When decision is needed for the diabetic patient who underwent an etc.
amputation
Monitoring indications
 Assess the therapeutic intervention related to respiratory illness in dia-
diabetic patients, all parts of the lung are equally affected, and the
betic patients
 Describe the course of diseases that affect lung function and associated thickening of the basal lamina is of the same order of magnitude in
structures both the lung and the kidney [10]. Pulmonary damage at an early
 Monitor diabetic patients who are exposed to occupational/industrial stage in most patients with diabetes mellitus is subclinical, and
hazardous agents rarely present with complaints [17]. Spirometry noninvasively
Disability/impairment evaluations quantifies the physiological reserves in a large micro-vascular
 Assess diabetic patients as a part of a rehabilitation program
bed that is not clinically affected by diabetes. Lung function may
 Assess diabetic patients as part of an insurance evaluation
 Assess diabetic patients for social security and legal reasons
provide useful measures of the progression of systemic micro-
angiopathy in diabetic patients [17].
In normal healthy non smokers after the age of 35, the expected
Advances in science and technology have made spirometry a much decline in lung function (FEV1) is 25–30 ml/year. However, the
more reliable, valid and relatively simple tool to incorporate into average rate of decline of lung function in diabetic patients, as
routine clinical visits. Spirometry is a basic, widely used pulmonary measured by Forced Expiratory Volume in 1 s (FEV1), is 71 ml/year.
function test (PFT). It typically assesses the lung volumes and [18] McKeever et al. [19] have observed that an increase in mean
flows, and is ideally suited to describing the effects of obstruction HbA1c is associated with a decrease in the lung function parame-
or restriction on lung function [12]. It is now regarded as an inte- ters FVC and FEV1. They hypothesize that impaired glucose auto-
gral component of any respiratory medical surveillance program. regulation is associated with impaired lung function. Asanuma et
PFT has assumed a key role in epidemiological studies investigat- al. [20], Lange et al. [21] and Boulbou et al. [22], have reported that
ing the incidence, natural history and causality of lung disease FVC and FEV1 are reduced in diabetic subjects, as compared to the
[13]. Although there is no substitute for spirometry, and even in control subjects. Similarly, Cazzato et al. [23], conducted a cross-
countries where it is not widely available as a standardized clinical sectional study to assess pulmonary function in children with insu-
algorithm or diagnostic pathway, yet, it can greatly assist in the lin-dependent diabetes mellitus (IDDM), and reported that FVC and
diagnosis of common airway diseases. Spirometry is essential for FEV1 were significantly lower in diabetics than in controls. Simi-
diagnosing respiratory illnesses, assessing their severity, determin- larly, Makkar et al. [24], performed spirometry on patients with
ing response to treatment and tracking patients’ progress over time IDDM, and reported that the IDDM patients had reduced FVC,
[14]. The utility of spirometry was further recognized when its FEV1 and MEF 25–75%, as compared to their matched control.
applications were highlighted in diabetic patients [15] inhaled Moreover, Rosenecker et al. [25] demonstrated that in patients
insulin was introduced for the treatment of diabetes mellitus and with diabetes, FVC and FEV1 declined significantly over the five
researchers discussed its applications in association with inhaled year study period, whereas patients without diabetes did not show
insulin at various scientific gatherings [16] (see Tables 2 and 3). a significant decline during this period. Davis et al. [26] have re-
ported that the Forced Vital Capacity (FVC), Forced Expiratory Vol-
ume in 1 s (FEV1), Vital Capacity (VC) and Peak Expiratory Flow
3. Diabetes mellitus and lung function (PEF) were reduced in diabetic patients. Similarly, Meo et al.
[15,27] reported that lung function parameters Forced Vital Capac-
Diabetic mellitus targets lungs and its associated structures, as ity (FVC) and Forced Expiratory Volume in 1 s (FEV1), and Peak
it does other organs. Electron microscopic study has shown that in Expiratory Flow (PEF) in type 1 and type 2 diabetic patients were
impaired, as compared to their matched controls. Stratification of
Table 2
Contraindications of Spirometry in diabetic patients.
results by years of disease showed a duration of disease-response
effect on lung function.
 Nausea, vomiting, headache, dizziness (these disorders affect the test
performance)
 Hemoptysis of unknown origin 4. Impaired lung function can cause diabetes mellitus
 Current history of any abdominal or thoracic surgery
 Current history of any limb amputation Diabetes mellitus and lung function have a two way cause effect
 Current history of glaucoma or any eye surgery
 Recent history of severe chest pain, unstable angina or myocardial
relationship. It is pertinent to assess respiratory dysfunction
infarction caused by diabetes mellitus, and it is even more pertinent, in
 Thoracic aneurysms/pneumothorax non-diabetic subjects, to assess the risk of diabetes mellitus. The
 Diabetic patients with a history of HIV/hepatitis B/hepatitis C (because impaired lung function may be forecast quite reliably many years
of high risk of transmission of infection. However, spirometry can be
before the actual diagnosis of diabetes mellitus. Subjects with re-
performed after taking high standard sterilizing measures)
duced lung function are at a higher risk of developing insulin
S.A. Meo / International Journal of Diabetes Mellitus 2 (2010) 47–50 49

resistance and hyperinsulinemia. Impaired pulmonary function normal physiological reserves that allow alveolar oxygen uptake to
may increase the risk of developing diabetes mellitus. Subjects increase in accordance with metabolic demand and exertional
who are predisposed to developing diabetes have decreased spiro- dyspnea may not develop until 40–50% of alveolar gas exchange
metric indices many years prior to the diagnosis, compared with capacity is lost. Diabetic lung involvement is best characterized
those who do not develop diabetes. This decrement in spirometric as a loss of physiological reserves, and it become a cause of exer-
parameters remains after the development of diabetes; however, tional dyspnea in diabetic patients [9].
the mechanism involved is most probably that of insulin resistance
[28–31]. 7. Diabetes mellitus and respiratory muscles strength

5. Impaired lung function is emerging risk factor for type 2 Respiratory muscle endurance is of interest in pulmonary criti-
diabetes mellitus cal care and many other areas of medicine. Reduced muscle
strength has been reported in diabetic patients. Bilateral or unilat-
Impaired lung function, especially FVC and FEV1, has attracted eral diaphragmatic paralysis has been observed in diabetic patients
mounting attention as a potentially novel risk factor for glucose [40]. In addition [41] conducted a study, and determined respira-
intolerance [32], insulin resistance 33 and type 2 diabetes mellitus tory muscles endurance by means of a direct MVV test during
[28–31]. The most probable mechanisms include effects of hypox- the inspiratory and expiratory phases of respiration, by using a
emia on glucose and insulin regulation [33], lung-related inflam- MP-100 student Bio Pac system. They reported that the respiratory
matory mediators and their effects on insulin signaling [32]. Yeh muscles endurance was impaired, and a greater perception of
et al. [34] analyzed longitudinal data of a large sample of middle- respiratory exertion was noticed in diabetic patients relative to
aged adults from a community-based study, and tested the their matched controls. Moreover, breathlessness on exertion and
hypothesis that decreased lung function (FVC and FEV1) is cross- orthopnea in association with type 2 diabetes mellitus has been
sectionally associated with features of insulin resistance, and is also reported. Investigation showed that bilateral diaphragmatic
an independent predictor of the incidence of type 2 diabetes mel- paralysis due to phrenic neuropathy may be an important, if rare
litus. Moreover, they also reported that adults with impaired FVC complication of diabetes, and diaphragmatic function should be
(% predicted) had various features of insulin resistance, including considered in any patient with unexplained breathlessness and
higher levels of blood glucose, insulin, triglycerides, lower HDL orthopnoea [40].
cholesterol and higher systolic blood pressure.
Lazarus et al. [33] found that the decrease in FVC, FEV1 and 8. Diabetes mellitus and pulmonary infection
maximal midexpiratory flow rate at the baseline forecast hyperin-
sulinemia and estimated insulin resistance over 20 years of follow- The frequency and enhanced severity of pulmonary tract infec-
up, independent of age, adiposity and cigarette smoking. Similarly, tions in uncontrolled diabetes have been well known for a long
Eriksson and Lindgarde [35] found that non-diabetic middle-aged time. The availability of antibiotics has made a significant differ-
subjects with a 10% decrease in mean vital capacity developed dia- ence, but infection is probably a more serious threat to life in a dia-
betes mellitus during a 6-year follow-up. Engstrom and Janzon betic than in a non-diabetic individual. Diabetes mellitus is
[28] demonstrated that decreased FVC and FEV1 predicted the recognized as an independent risk factor for developing lower
presence of diabetes. Ford and Mannino [30] reported that FVC respiratory tract infections [42,43]. The mechanism for increased
and FEV1 were significantly and inversely associated with the susceptibility to infection is due to an alteration in the chemotac-
prevalence of diabetes. They also found that restrictive lung dis- tic, phagocytic and bactericidal activity of polymorphonuclear leu-
ease was significantly associated with the incidence of diabetes; kocytes [44]. The impaired phagocytic function is also one of the
however, this association was not observed in subjects with major causes of pulmonary infection in diabetic patients.
obstructive lung disease.
The most credible explanation for the link between low FVC and 9. Diabetes mellitus and pulmonary tuberculosis
FEV1 and diabetes risk is related to hypoxemia-induced insulin
resistance. The animal model studies also reported that experi- The association between diabetes mellitus and tuberculosis (TB)
mental hypoxia produces insulin resistance and hyperinsulinemia has been discussed in the literature for a long time. Pulmonary
in animals [36]. Moreover, exposure to high altitude hypoxia [32] tuberculosis and diabetes mellitus frequently coexist [45]. It has
or hypobaric hypoxia can reduce insulin sensitivity and lead to a been also reported that there is a high prevalence of TB disease
predisposition for the development of type 2 diabetes. Impaired vi- in diabetic children and adolescents [46]. The frequency of tuber-
tal capacity and the risk of diabetes are partially determined by ad- culosis was 4–5 times more than in non-diabetics. The disease
verse fetal or early-life conditions, and inflammatory precursors was more aggressive in poorly controlled diabetics, and is signifi-
may also favor resistance to insulin action [37]. The main sugges- cantly associated with the development of pleural effusion [47]. In-
tion of the study by Yeh et al. is that impaired lung function (FVC creased reactivation of tuberculosis lesions has also been recorded
and FEV1) deserves high attention as an emerging novel risk factor in diabetics. It has also been reported that the development of
for type 2 diabetes mellitus. FVC might still be a useful risk predic- tuberculosis occurred more frequently in juvenile diabetes and
tor, and the FVC-diabetes link could suggest explanations for other the occurrence of tuberculosis increased with the duration of dia-
phenomena such as an increased risk of coronary artery disease, betes, causing a significantly greater mortality rate. In various
along with impaired lung function. infectious conditions of the lung, along with other related investi-
gations, spirometry may also provide reliable information about
6. Diabetes mellitus and alveolar gas exchange the health of the lung.

Diabetic patients showed impaired alveolar gas exchange 10. Conclusion


capacity and reduced pulmonary elastic recoil, as compared with
healthy controls [38]. It has also been found that the impairment Spirometry is a simple, reliable, valid and powerful tool that can
of the pulmonary diffusion capacity for carbon monoxide was com- be used to assess, differentiate, follow-up and manage patients
mon in type 2 diabetes mellitus in Asian Indian patients [39]. The with pulmonary disorders. Diabetes mellitus is a major public
50 S.A. Meo / International Journal of Diabetes Mellitus 2 (2010) 47–50

health care problem with increasing incidence and long term com- [21] Lange P, Groth S, Kastrup J, Mortensen J, Appleyard M, Nyboe J, et al. Diabetes
mellitus, plasma glucose and lung function in a cross-sectional population
plications and is a leading cause of illness and death across the
study. Eur Respir J 1989;2(1):14–9.
world. Diabetes mellitus is associated with continuing damage, [22] Boulbou MS, Gourgoulianis KI, Klisiaris VK, Tsikrikas TS, Stathakis NE,
dysfunction and failure of various organs, including the lungs. Molyvdas PA. Diabetes mellitus and lung function. Med Princ Pract
Therefore, when the question of the management of diabetes mel- 2003;12(2):87–91.
[23] Cazzato S, Bernardi F, Salardi S, Tassinari D, Corsini I, Ragni L, et al. Lung
litus arises, physicians should be aware of the size of the problem function in children with diabetes mellitus. Pediatr Pulmonol
of pulmonary complications, and must consider the lung as being 2004;37(1):17–23.
as serious as other complications of diabetes mellitus. The im- [24] Makkar P, Gandhi M, Agrawal RP, Sabir M, Kothari RP. Ventilatory pulmonary
function tests in type 1 diabetes mellitus. J Assoc Physicians India
paired lung functions (FVC and FEV1) reflects a causative role 2000;48(10):962–6.
played by the lungs in developing diabetes, then optimizing the [25] Rosenecker J, Hofler R, Steinkamp G, Eichler I, Smaczny C, Ballmann M, et al.
health of the lung through cessation of smoking habits, avoidance Diabetes mellitus in patients with cystic fibrosis: the impact of diabetes
mellitus on pulmonary function and clinical outcome. Eur J Med Res 2001;27
of irritants and toxic exposure, control of underlying airway 6(8):345–50.
inflammation and the promotion of physical activity seem war- [26] Davis T, Knuiman M, Kendall P, Vu H, Davis WA. Reduced pulmonary function
ranted. Indeed, it seems time to add the spirometer to the tools and its associations in type 2 diabetes: the Fremantle diabetes study. Diab Res
Clin Pract 2000;50:153–9.
available for monitoring diabetes mellitus and its important seque- [27] Meo SA, Abdul Majeed Al Drees, Muhammad Arif, Sayed Fayaz Ahmed Shah,
lae. Moreover, physicians must fully utilize Spirometry in the man- Khalid Al-Rubean. Lung function in type 1 diabetic patients. Saudi Med J
agement of diabetes mellitus. 2005;26(11):1728–33.
[28] Engstrom G, Janzon L. Risk of developing diabetes is inversely related to lung
function: a population-based cohort study. Diab Med 2002;19:167–70.
Conflict of interest statement [29] Engstrom G, Hedblad B, Nilsson P, Wollmer P, Berglund G, Janzon L. Lung
function, insulin resistance and incidence of cardiovascular disease: a
longitudinal cohort study. J Int Med 2003;253:574–81.
None declared. [30] Ford ES, Mannino DM. Prospective association between lung function and the
incidence of diabetes: findings from the national health and nutrition
References examination survey epidemiologic follow-up study. Diab Care
2004;27:2966–70.
[31] Litonjua AA, Lazarus R, Sparrow D, Demolles D, Weiss ST. Lung function in type
[1] Meo SA. Diabetes mellitus: health and wealth threat. Int J Diab Mellitus
2 diabetes: the normative aging study. Respir Med 2005;99(12):1583–90.
2009;1(1):42.
[32] Hjalmarsen A, Aasebo U, Birkeland K, Sager G, Jorde R. Impaired glucose
[2] James RG, Alberti KGMM, Mayer BD, Ralph AD, Allan D, Steven G, et al. Report
tolerance in patients with chronic hypoxic pulmonary disease. Diab Metab
on the expert committee on the diagnosis and classification of diabetes
1996;22:37–42.
mellitus. Diab Care 2002;25:S5–20.
[33] Lazarus R, Sparrow D, Weiss ST. Baseline ventilatory function predicts the
[3] Arnalich F, Hernanz A, Lopez-Maderuelo D. Enhanced acute-phase response
development of higher levels of fasting insulin and fasting insulin resistance
and oxidative stress in older adults with type II diabetes. Horm Metab Res
index: the normative aging study. Eur Respir J 1998;12:641–5.
2000;32:407–12.
[34] Yeh HC, Punjabi NM, Wang NY, Pankow JS, Duncan BB, Brancati FL. Vital
[4] Walter R, Beiser A, Givelber R. The association between glycemic state and lung
capacity as a predictor of incident type 2 diabetes: the atherosclerosis risk in
function: the Framingham heart study. Am J Respir Crit Care Med
communities study. Diab Care 2005;28(6):1472–9.
2003;167:911–6.
[35] Eriksson KF. Lindgarde F: poor physical fitness, and impaired early insulin
[5] Cirillo D, Agrawal Y, Cassano P. Lipids and pulmonary function in the third
response but late hyperinsulinaemia, as predictors of NIDDM in middle-aged
national health and nutrition examination survey. Am J Epidemiol
Swedish men. Diabetologia 1996;39:573–9.
2002;155:842–8.
[36] Cheng N, Cai W, Jiang M, Wu S. Effect of hypoxia on blood glucose, hormones,
[6] Brownlee M. Biochemistry and molecular cell biology of diabetic
and insulin receptor functions in newborn calves. Pediatr Res 1997;41:852–6.
complications. Nature 2001;414:813–20.
[37] Schmidt MI, Duncan BB, Sharrett AR, Lindberg G, Savage PJ, Offenbacher S,
[7] Sandler M, Bunn AE, Stewart RI. Pulmonary function in young insulin-
et al. Markers of inflammation and prediction of diabetes mellitus in adults
dependent. Chest 1986;90(5):670–5.
(atherosclerosis risk in communities study): a cohort study. Lancet
[8] Matsubara T, Hara F. The pulmonary function and histopathological studies of
1999;353:1649–52.
the lung in diabetes mellitus. Nippon Ika Daigaku Zasshi 1991;58(5):528–36.
[38] Guvener N, Tutuncu NB, Akcay S, Eyuboglu F, Gokcel A. Alveolar gas exchange
[9] Ljubić S, Metelko Z, Car N, Roglić G, Drazić Z. Reduction of diffusion capacity for
in patients with type 2 diabetes mellitus. Endocr J 2003;50(6):663–7.
carbon monoxide in diabetic patients. Chest 1998;114(4):1033–5.
[39] Sinha S, Guleria R, Misra A, Pandey RM, Yadav R, Tiwari S. Pulmonary functions
[10] Weynand B, Jonckheere A, Frans A, Rahier J. Diabetes mellitus induces a
in patients with type 2 diabetes mellitus and correlation with anthropometry
thickening of the pulmonary basal lamina. Respiration 1999;66(1):14–9.
and microvascular complications. Indian J Med Res 2004;119(2):66–71.
[11] Thomas R Gildea. Pulmonary function testing, 2009. Available from:
[40] White JE, Bullock RE, Hudgson P, Home PD, Gibson GJ. Phrenic neuropathy in
http://www.clevelandclinicmeded.com/medicalpubs/diseasemanagement/
association with diabetes. Diab Med 1992;9(10):954–6.
pulmonary/pulmonary-function-testing/#cesec36, cited date; Oct, 2009.
[41] Meo SA, Abdul Majeed Al Drees, Muhammad Arif, Khalid Al-Rubean.
[12] Ruppel GL. Pulmonary function testing. Trends and techniques. Respir Care
Assessment of respiratory muscles endurance in diabetic patients. Saudi
Clinics North America 1997;3:155–81.
Med J 2006;27(2):223–6.
[13] McKay, Ray T, Horvath Edward. Pulmonary function testing in industry. In:
[42] Bhansali A, Suresh V, Chaudhry D, Vaiphei K, Dash RJ, Kotwal N. Diabetes and
Carl Zenz O, Dickerson Bruca, Horvath Edward P, editors. Occupational
rapidly advancing pneumonia. Postgrad Med J 2001;77(913):734–45.
medicine. London: Mosby; 1984. p. 229.
[43] Ardigo D, Valtuena S, Zavaroni I, Baroni MC, Delsignore R. Pulmonary
[14] Christine Jenkinsa. Spirometry performance in primary care: the problem, and
complications in diabetes mellitus: the role of glycemic control. Curr Drug
possible solutions. Primary Care Respir J 2009;18(3):128–9.
Targets Inflamm Allergy 2004;3(4):455–8.
[15] Meo SA, Al Drees AM, Arif M, Al-Rubean K. Lung function in type 2 Saudi
[44] Marvisi M, Marani G, Brianti M, Della Porta R. Pulmonary complications in
diabetic patients. Saudi Med J 2006;27(3):338–43.
diabetes mellitus. Recent Prog Med 1996;87(12):623–37.
[16] Meo SA. In: Sixth international conference in diabetes science and technology,
[45] Jabbar A, Hussain SF, Khan AA. Clinical characteristics of pulmonary
Atlanta, USA; 2006.
tuberculosis in adult Pakistani patients with co-existing diabetes mellitus.
[17] Hsia CC. Recruitment of lung diffusing capacity: update of concept and
Health J 2006;12(5):552–7.
application. Chest 2002;122:1774–83.
[46] Webb EA, Hesseling AC, Schaaf HS, Gie RP, Lombard CJ, Spitaels A, et al. High
[18] Davis WA, Knuiman M, Kendall P, Grange V, Davis TM. Fremantle diabetes
prevalence of Mycobacterium tuberculosis infection and disease in children and
study: glycemic exposure is associated with reduced pulmonary function in
adolescents with type 1 diabetes mellitus. Int J Tuberc Lung Dis
type 2 diabetes: the Fremantle diabetes study. Diab Care 2004;27(3):752–7.
2009;13(7):868–74.
[19] McKeever TM, Weston PJ, Hubbard R, Fogarty A. Lung function and glucose
[47] Falguera M, Pifarre R, Martin A, Sheikh A, Moreno A. Etiology and outcome of
metabolism: an analysis of data from the third national health and nutrition
community-acquired pneumonia in patients with diabetes mellitus. Chest
examination survey. Am J Epidemiol 2005;161(6):546–56.
2005;128(5):3233–9.
[20] Asanuma Y, Fujiya S, Ide H, Agishi Y. Characteristics of pulmonary function in
patients with diabetes mellitus. Diab Res Clin Pract 1985;1(2):95–101.

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