Intima-media thickness in cardiovascularly asymptomatic hypopituitary adults with growth hormone deficiency: relation to body mass index, gender, and other cardiovascular risk factors
Abstract
OBJECTIVE: Increased cardiovascular mortality and carotid atherosclerosis have been observed in hypopituitary patients with untreated GH deficiency (GHD), but results are contradictory and relations to cardiovascular risk factors are not clear. The aim of this study was to investigate intima-media thickness (IMT) in relation to cardiovascular risk factors in adults with GHD. DESIGN: Cross-sectional observational study of 21 men and 13 women with GHD, but without cardiovascular disease, compared to two healthy control groups matched for age, sex and smoking habits. One control group was matched for body mass index (BMI) and the other group was nonobese. MEASUREMENTS: IMT of the carotid and femoral arteries, blood pressure, blood samples and anthropometric data. RESULTS: Patients had 12% thicker composite carotid IMT [(IMT of common carotid artery + IMT of bulb)/2] compared to nonobese controls (P = 0.022), but IMT was not different compared to BMI-matched controls. Femoral IMT did not differ between patients and controls. Patients had higher waist : hip ratio (WHR), heart rate, serum triglycerides and fasting insulin concentrations in combination with lower high-density lipoprotein (HDL) cholesterol and smaller low-density lipoprotein (LDL) peak particle size compared to both nonobese and to BMI-matched controls. This cardiovascular risk pattern was more pronounced in female patients than in male patients compared to their gender controls. Carotid IMT was related to age, serum cholesterol, LDL cholesterol and smoking in the patient group. Only age was independently related to carotid IMT in multivariate analysis. CONCLUSIONS: These results indicate that high BMI in GH-deficient patients contribute to their increased intima-media thickness. However, several cardiovascular risk factors are present in this patient group independent of their increased BMI, especially in women.
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Altered body composition, insulin resistance, hypertension, unfavorable lipid profile, endothelial dysfunction and atherosclerosis have been found in several studies on patients with long-term GHD.
“Altered body composition, insulin resistance, hypertension, unfavorable lipid profile, endothelial dysfunction and atherosclerosis have been found in several studies on patients with long-term GHD (74,76,77,(82)(83)(84)(85)(86)(87).”
From Pituitary Dysfunction After Traumatic Brain Injury: A Clinical and Pathophysiological Approach (2015) · cites this paper as [83]
Cites
Matthews, D. R., Hosker, J. P., Rudenski, A. S., Naylor, B. A., Treacher, D. F., & Turner, R. C. (1985) · Diabetologia · doi:10.1007/bf00280883 · Cited by 31,502 · see citing works
Role of Insulin Resistance in Human Disease
Reaven, G. M. (1988) · Diabetes · doi:10.2337/diab.37.12.1595 · Cited by 12,154 · see citing works
O'Leary, D. H., Polak, J. F., Kronmal, R. A., Manolio, T. A., Burke, G. L., & Wolfson, S. K. (1999) · New England Journal of Medicine · doi:10.1056/nejm199901073400103 · Cited by 4,685 · see citing works
Hubert, H. B., Feinleib, M., McNamara, P. M., & Castelli, W. P. (1983) · Circulation · doi:10.1161/01.cir.67.5.968 · Cited by 4,241 · see citing works
Premature mortality due to cardiovascular disease in hypopituitarism
Rosén, T., & Bengtsson, B.-Å. (1990) · The Lancet · doi:10.1016/0140-6736(90)91812-o · Cited by 1,402 · see citing works
Self-citationHeart rate and cardiovascular mortality: The Framingham study
Kannel, W. B., Kannel, C., Paffenbarger, R. S., & Cupples, L. A. (1987) · American Heart Journal · doi:10.1016/0002-8703(87)90666-1 · Cited by 1,292 · see citing works
"Portal" adipose tissue as a generator of risk factors for cardiovascular disease and diabetes.
Björntorp, P. A. (1990) · Arteriosclerosis An Official Journal of the American Heart Association Inc · doi:10.1161/01.atv.10.4.493 · Cited by 1,115 · see citing works
Treatment of adults with growth hormone (GH) deficiency with recombinant human GH.
Bengtsson, B. Å., Edén, S., Lönn, L., Kvist, H., Stokland, A. M., Lindstedt, G., Bosaeus, I. G., Tölli, J., Sjöström, L., & Isaksson, O. G. P. (1993) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.76.2.8432773 · Cited by 780 · see citing works
Self-citationSalonen, R. M., & Salonen, J. T. (1991) · Journal of Internal Medicine · doi:10.1111/j.1365-2796.1991.tb00336.x · Cited by 568 · see citing works
<b>Increased cerebrovascular mortality in patients with hypopituitarism</b>
Bülow, B., Hagmar, L., Mikoczy, Z., Nordström, C., & Erfurth, E. M. (1997) · Clinical Endocrinology · doi:10.1046/j.1365-2265.1997.d01-1749.x · Cited by 542 · see citing works
Wendelhag, I., Gustavsson, T., Suurküla, M. B., Berglund, G., & Wikstrand, J. (1991) · Clinical Physiology · doi:10.1111/j.1475-097x.1991.tb00676.x · Cited by 515 · see citing works
Self-citationCampbell, M. J., Julious, S. A., & Altman, D. G. (1995) · BMJ · doi:10.1136/bmj.311.7013.1145 · Cited by 476 · see citing works
Carotid artery intima‐media thickness as an indicator of generalized atherosclerosis
Grobbee, D. E., & Bots, M. L. (1994) · Journal of Internal Medicine · doi:10.1111/j.1365-2796.1994.tb00847.x · Cited by 437 · see citing works
Pulse rate, coronary heart disease, and death: The NHANES I Epidemiologic Follow-up Study
Gillum, R. F., Makuc, D. M., & Feldman, J. J. (1991) · American Heart Journal · doi:10.1016/0002-8703(91)90970-s · Cited by 405 · see citing works
Markussis, V., Beshyah, S. A., Johnston, D. G., Fisher, C., Nicolaides, A. N., & Sharp, P. (1992) · The Lancet · doi:10.1016/0140-6736(92)92892-j · Cited by 390 · see citing works
Wendelhag, I., Liang, Q., Gustavsson, T., et al. (1997) · Stroke · doi:10.1161/01.str.28.11.2195 · Cited by 376 · see citing works
Self-citationLandin‐Wllhelmsen, K., Wllhelmsen, L., Lappast, G., Rosén, T., Lindstedt, G., Lundberg, P., & Bengtsson, B. (1994) · Clinical Endocrinology · doi:10.1111/j.1365-2265.1994.tb02556.x · Cited by 340 · see citing works
Self-citationCardiovascular risk factors in adult patients with growth hormone deficiency
Rosén, T., Edén, S., Larson, G., Wilhelmsen, L., & Bengtsson, B. (1993) · European Journal of Endocrinology · doi:10.1530/acta.0.1290195 · Cited by 338 · see citing works
Self-citationWofford, J. L., Kahl, F. R., Howard, G., McKinney, W. M., Toole, J. F., & Crouse, J. R. (1991) · Arteriosclerosis and Thrombosis A Journal of Vascular Biology · doi:10.1161/01.atv.11.6.1786 · Cited by 335 · see citing works
Prevalence of carotid atherosclerosis and serum cholesterol levels in eastern Finland.
Salonen, R. M., Seppänen, K., Rauramaa, R., & Salonen, J. T. (1988) · Arteriosclerosis An Official Journal of the American Heart Association Inc · doi:10.1161/01.atv.8.6.788 · Cited by 315 · see citing works
Treatment of adults with growth hormone (GH) deficiency with recombinant human GH
Bengtsson, B. A. (1993) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.76.2.309 · Cited by 309 · see citing works
Self-citationGrowth hormone-deficient adults are insulin-resistant
Johansson, J.-O., Fowelin, J., Landin, K., Lager, I., & Bengtsson, B.-Å. (1995) · Metabolism · doi:10.1016/0026-0495(95)90004-7 · Cited by 275 · see citing works
Self-citationGrowth Hormone (GH) Treatment Reverses Early Atherosclerotic Changes in GH-Deficient Adults1
Pfeifer, M., Verhovec, R., Žižek, B., Preželj, J., Poredoš, P., & Clayton, R. N. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.84.2.5456 · Cited by 266 · see citing works
Rosén, T., Bosaeus, I. G., TöIli, J., Lindstedt, G., & Bengtsson, B. (1993) · Clinical Endocrinology · doi:10.1111/j.1365-2265.1993.tb00974.x · Cited by 255 · see citing works
Self-citationCuneo, R. C., Salomon, F., Watts, G. F., Hesp, R., & Sönksen, P. H. (1993) · Metabolism · doi:10.1016/0026-0495(93)90145-e · Cited by 252 · see citing works
Serum Total IGF-I, Free IGF-I, and IGFBP-1 Levels in an Elderly Population
Janssen, J. A. M. J. L., Stolk, R. P., Pols, H. A. P., Grobbee, D. E., & Lamberts, S. W. J. (1998) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.18.2.277 · Cited by 243 · see citing works
Wendelhag, I., Wiklund, O., & Wikstrand, J. (1993) · Arteriosclerosis and Thrombosis A Journal of Vascular Biology · doi:10.1161/01.atv.13.10.1404 · Cited by 225 · see citing works
Self-citationObesity, lipids, and glucose intolerance The Framingham Study
Kannel, W. B., Gordon, T., & Castelli, W. P. (1979) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/32.6.1238 · Cited by 207 · see citing works
Serum lipid levels in growth hormone-deficient men
de Boer, H., Blok, G. J., Voerman, H. J., Phillips, M., & Schouten, J. A. (1994) · Metabolism · doi:10.1016/0026-0495(94)90245-3 · Cited by 198 · see citing works
Hulthe, J., Wikstrand, J., Emanuelsson, H., Wiklund, O., de Feyter, P. J., & Wendelhag, I. (1997) · Stroke · doi:10.1161/01.str.28.6.1189 · Cited by 197 · see citing works
Self-citationHigh fibrinogen and plasminogen activator inhibitor activity in growth hormone-deficient adults.
Johansson, J. O., Landin‐Wilhelmsen, K., Tengborn, L., Rosén, T., & Bengtsson, B. Å. (1994) · Arteriosclerosis and Thrombosis A Journal of Vascular Biology · doi:10.1161/01.atv.14.3.434 · Cited by 167 · see citing works
Self-citationGrowth Hormone (GH) Treatment Reverses Early Atherosclerotic Changes in GH-Deficient Adults
Pfeifer, M. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.84.2.453 · Cited by 164 · see citing works
Bülow, B., Hagmar, L., ESKILSSON, J., & Erfurth, E. M. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.85.2.6346 · Cited by 144 · see citing works
Karason, K., Wikstrand, J., Sjöström, L., & Wendelhag, I. (1999) · International Journal of Obesity · doi:10.1038/sj.ijo.0801024 · Cited by 141 · see citing works
Self-citationStensland-Bugge, E., Bønaa, K. H., Joakimsen, O., & Njølstad, I. (2000) · Stroke · doi:10.1161/01.str.31.3.574 · Cited by 134 · see citing works
Schmidt, F., & Wendelhag (1999) · Clinical Physiology · doi:10.1046/j.1365-2281.1999.00145.x · Cited by 112 · see citing works
Riches, F. M., Watts, G. F., Hua, J., Stewart, G. R., Naoumova, R. P., & Barrett, P. H. R. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.84.8.5925 · Cited by 97 · see citing works
Sverrisdóttir, Y. B., Elam, M., Herlitz, H., Bengtsson, B., & Johannsson, G. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.83.6.4895 · Cited by 97 · see citing works
Self-citationBulow, B. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.85.2.574 · Cited by 92 · see citing works
Elhadd, T. A., Abdu, T. A. M., Oxtoby, J., Kennedy, G., McLaren, M., Neary, R. H., Belch, J. J. F., & Clayton, R. N. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.9.7813 · Cited by 88 · see citing works
Prevalence and Determinants of Carotid Atherosclerosis in Healthy Postmenopausal Women
Lassila, H. C., Tyrrell, K. S., Matthews, K. A., Wolfson, S. K., & Kuller, L. H. (1997) · Stroke · doi:10.1161/01.str.28.3.513 · Cited by 83 · see citing works
Determinants of femoral and carotid artery atherosclerosis
Joensuu, T., Salonen, R. M., Winblad, I., Korpela, H., & SALONEN, J. T. (1994) · Journal of Internal Medicine · doi:10.1111/j.1365-2796.1994.tb01123.x · Cited by 76 · see citing works
Alphalipoprotein cholesterol levels in relation to acute myocardial infarction and its risk factors
Wiklund, O., Fager, G., Craig, I. H., Wilhelmsson, C., VEDIN, A., Olofsson, S. ‐., Bondjers, G., & Wilhelmsen, L. (1980) · Scandinavian Journal of Clinical and Laboratory Investigation · doi:10.3109/00365518009095573 · Cited by 66 · see citing works
Sverrisdóttir, Y. B. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.83.6.1881 · Cited by 55 · see citing works
O'Neal, D., Hew, F. L., Sikaris, K. A., Ward, G. M., ALFORD, F. P., & Best, J. D. (1996) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.81.7.8675559 · Cited by 52 · see citing works
Riches, F. M. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.84.8.2854 · Cited by 38 · see citing works
Hulthe, J., Wiklund, O., Olsson, G., et al. (1999) · Scandinavian Journal of Clinical and Laboratory Investigation · doi:10.1080/00365519950185157 · Cited by 25 · see citing works
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Molitch, M. E., Clemmons, D. R., Malozowski, S., Merriam, G. R., & Vance, M. L. (2011) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2011-0179 · Cited by 1,047 · see citing works
Pituitary Dysfunction After Traumatic Brain Injury: A Clinical and Pathophysiological Approach
Tanriverdi, F., Schneider, H. J., Aimaretti, G., Masel, B. E., Casanueva, F. F., & Kelestimur, F. (2015) · Endocrine Reviews · doi:10.1210/er.2014-1065 · Cited by 218 · see citing works
Hormone Replacement Therapy and Physical Function in Healthy Older Men. Time to Talk Hormones?
Giannoulis, M. G., Martin, F. C., Nair, K. S., Umpleby, A. M., & Sonksen, P. (2012) · Endocrine Reviews · doi:10.1210/er.2012-1002 · Cited by 132 · see citing works
Adult growth hormone deficiency - benefits, side effects, and risks of growth hormone replacement
Reed, M. L., Merriam, G. R., & Kargi, A. Y. (2013) · Frontiers in Endocrinology · doi:10.3389/fendo.2013.00064 · Cited by 119 · see citing works
Mortality in adults with hypopituitarism: a systematic review and meta-analysis
Jasim, S., Alahdab, F., Ahmed, A. T., Tamhane, S., Prokop, L. J., Nippoldt, T. B., & Murad, M. H. (2017) · Endocrine · doi:10.1007/s12020-016-1159-3 · Cited by 112 · see citing works
Beauregard, C., Utz, A. L., Schaub, A. E., Nachtigall, L., Biller, B. M. K., Miller, K. K., & Klibanski, A. (2008) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-2371 · Cited by 99 · see citing works
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Verhelst, J., & Abs, R. (2009) · European Journal of Endocrinology · doi:10.1530/eje-09-0291 · Cited by 70 · see citing works
Metabolic alterations in patients who develop traumatic brain injury (TBI)-induced hypopituitarism
Prodam, F., Gasco, V., Caputo, M., Zavattaro, M., Pagano, L., Marzullo, P., Belcastro, S., Busti, A., Perino, C., Grottoli, S., et al. (2013) · Growth Hormone & IGF Research · doi:10.1016/j.ghir.2013.04.001 · Cited by 35 · see citing works
Murray, R. D., Wieringa, G., Lawrance, J. A., Adams, J. E., & Shalet, S. M. (2010) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2009.03754.x · Cited by 24 · see citing works
- Authors
- Leonsson, M., Hulthe, J., Oscarsson, J., Johannsson, G., Wendelhag, I., Wikstrand, J., & Bengtsson, B.
- Affiliations
- Sahlgrenska University Hospital (SE)
- University of Gothenburg (SE)
- Corresponding author
- Hulthe, Johannes
- Venue
- Clinical Endocrinology
- Publisher
- Wiley
- Published
- 2002-12
- Volume
- 57
- Issue
- 6
- Pages
- 751-759
- ISSN
- 0300-0664 (ISSN-L)
- 1365-2265
- OpenAlex
- W2167403780
- Cited by
- 49
- References
- 47
- Citations by year
- 2025: 1 · 2024: 2 · 2022: 1 · 2021: 1 · 2020: 2 · 2017: 1 · 2016: 2 · 2015: 2 · 2014: 3 · 2013: 3 · 2012: 3
- FWCI
- 1.52
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Clinical Endocrinology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Hjärt-Lungfonden
- Vetenskapsrådet
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Growth Hormone and Insulin-like Growth Factors
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Hormonal and reproductive studies
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiovascular Health and Disease Prevention
- Keywords
- growth hormone deficiency, hypopituitarism, intima-media thickness, carotid atherosclerosis, cardiovascular risk factors, body mass index, obesity, sex differences, LDL particle size, HDL cholesterol, triglycerides, insulin, waist-to-hip ratio, femoral artery
- MeSH terms
- Adult, Age Factors, Cardiovascular Diseases, Cholesterol, Cross-Sectional Studies, Female, Femoral Artery, Humans, Hypopituitarism, Cholesterol, LDL, Male, Middle Aged, Obesity, Risk Factors, Sex, Sex Factors, Smoking, Growth Hormone, Ultrasonography, Body Mass Index, Multivariate Analysis, Case-Control Studies, Carotid Artery, Common, Tunica Intima, Statistics, Nonparametric
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