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Original Studies |
Department of Endocrinology (S.M.O., P.E.B.), The General Infirmary at Leeds, The Leukemia Research Fund (R.J.Q.M., R.A.C.), Center for Clinical Epidemiology, University of Leeds, Leeds, United Kingdom
Address all correspondence and requests for reprints to: Dr. S. M. Orme, Department of Endocrinology, The General Infirmary at Leeds, Great George Street, Leeds, United Kingdom LS1 3EX.
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Abstract |
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The overall cancer incidence rate [standardized incidence ratio, 0.76; 95% confidence interval (CI), 0.60–0.95] was lower than that in the general population of the United Kingdom, and there was no significant increase in site-specific cancer incidence rates. The overall cancer mortality rate was not increased, but the colon cancer mortality rate (standardized mortality ratio, 2.47; 95% CI, 1.31–4.22) was higher than expected. Mortality rates due to colon cancer, all malignant disease, cardiovascular disease and overall mortality were increased with higher posttreatment GH levels (P for trends, <0.02, <0.05, <0.02, and <0.0001). The overall mortality rate in patients with acromegaly with posttreatment GH levels less than 2.5 ng/mL (5 mU/L) was comparable to that in the general population of the United Kingdom (standardized mortality ratio, 1.10; 95% CI, 0.89–1.35).
We conclude that high posttreatment GH levels are associated with an increased overall mortality rate and increased mortality rates due to colon cancer, cardiovascular disease, and all malignant disease. Posttreatment GH levels less than 2.5 ng/mL (5 mU/L) result in an overall mortality rate similar to that in the general population.
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Introduction |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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A number of series have demonstrated an increased mortality rate in patients with acromegaly; the main cause of these excess deaths is vascular and respiratory disease (11, 12, 13). An increased mortality from malignant disease in acromegaly has been reported in elderly females (11), all females (13), and males (12). A recent small study has reported an excess overall mortality occurring only in patients whose GH level persists above 2.5 ng/mL (5 mU/L) after treatment (14). Other studies have reported a lower mortality in treated compared with untreated subjects (11, 12).
Previous studies have lacked the statistical power, due to small sample size, to determine reliably whether there is an excess cancer incidence or mortality in acromegaly. They have used different methods of ascertainment for morbidity and mortality data in cases and comparison groups (11, 12, 13) (hospital records and postmortem vs. general population data). Except for two small studies (14, 15), they have not had access to GH levels for the patients studied. To establish whether there is an excess cancer incidence and higher mortality in patients with acromegaly (and, if so, to determine if these are related to duration of disease, age at diagnosis, or degree of GH hypersecretion), we performed a large retrospective multicenter epidemiological cohort study that was larger in terms of cases and years of exposure than previous studies.
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Subjects and Methods |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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After ethical committee approval, we approached 15 tertiary referral centers, and a single observer (S.M.O.) was given access to the case notes of patients with acromegaly. Demographic and clinical data were collected on all available subjects, current and deceased, from each center with acromegaly diagnosed by standard biochemical criteria (16). Before the advent of the GH assay, radiological, clinical, and pathological evidence consistent with a diagnosis of acromegaly was accepted. Subjects with multiple endocrine neoplasia type 1, McCune-Albright syndrome, and ectopic GHRH syndrome were excluded.
Demographic information was used to trace subjects through the National Health Service Central Register at the Office for National Statistics (ONS) for England and Wales, the Scottish Central Register, and the Northern Ireland Central Services Agency and Registrar of Births and Deaths. The ONS supplied copies of death certificates, cancer registrations, or evidence of exit from the Register (i.e. emigration or entry into the armed services).
The ONS was able to identify 1362 subjects who represented 95% of the original number and thus formed the cohort that was analyzed for causes of death. Serial pretreatment GH levels were available in 78% of subjects, and posttreatment GH levels were available in 90% of subjects (fasting, mean of a day curve, or random level). For the purposes of analysis, we used pretreatment (at diagnosis) and last known (posttreatment) GH level. Depending on the assays used, the conversion factor between GH measured in milliunits per L and nanograms per mL ranges from about 2–2.5 (17) (Ellis, A., EQAS scheme, Edinburgh, U.K., personal communication), and we have chosen to adopt the commonly used convention of 1 ng/mL = 2 mU/L.
Methods
Causes of death and cancer registrations were coded using the International Classification of Diseases ICD-9, ninth edition, 1978 (18), and the ICD-0, second edition, 1990 (19), respectively. For each cohort member, person-years at risk were calculated by age, sex, and calendar year, commencing on the date of diagnosis of acromegaly and finishing on the date of cancer registration or death (for cancer incidence and mortality analysis, respectively), exit from the ONS Registry, 85th birthday, or end of December 1995 when the dataset was frozen. As there was no reliable cancer registry for Northern Ireland, all subjects from there were excluded from the cancer incidence analysis. Person-years of exposure to acromegaly before 1958 in England and Wales and before 1962 in Scotland were not used to calculate expected cancer incidence because cancer registries did not exist before these dates. Population disease and death rates for England and Wales were applied to the whole United Kingdom.
Statistical analysis
Cause-specific death rates (20) (Office of Population, Censuses,
and Surveys Mortality Statistics Series DH2) and cancer incidence rates
(21) (Cancer Statistics Series MB1) for England and Wales were obtained
by age, sex, and time period from 0–85 yr for the duration of the
study. Expected deaths or cancer incidences by cause in the cohort were
calculated by multiplying age-, sex-, and period-specific person-years
at risk within the cohort by corresponding national cause-specific
mortality rates or site-specific cancer rates using the computer
program PYRS (22). Standardized mortality ratios (SMRs) and
standardized incidence ratios (SIRs) were calculated, and significantly
excess mortality or cancer incidence was determined by calculating a
one-sided Poisson probability. Ninety-five percent confidence intervals
(CIs) for the SIRs and SMRs were calculated using Byar’s approximation
(23). We investigated linear trends in risk (pre- and posttreatment GH
level, age at diagnosis, and duration of disease) using a
2 test for linear trends (23). Significance was assumed
when P < 0.05. A one-sided Poisson probability was
calculated as we were testing a number of prior hypotheses relating to
increased cancer incidence and mortality in acromegaly (see
Introduction). Mortality or cancer incidence rates significantly lower
than the general population of the United Kingdom have a
P > 0.95; this can also be noted from the two-sided
confidence intervals.
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Results |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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We observed 79 cancer incidence registrations in our analysis
cohort of 1,239 subjects with acromegaly (16,778 person-years). Sixteen
subject registrations occurred before the date of diagnosis of
acromegaly and were therefore excluded from analysis. There was a
nonsignificant increase in colon cancer incidence (SIR, 1.68;
P = 0.06), whereas the rectal cancer incidence (SIR,
0.86; 95% CI, 0.23–2.20) and female breast cancer incidence (SIR,
0.93; 95% CI, 0.51–1.56) were similar to those in the general
population of the United Kingdom. Cancer incidence rates due to all
malignancies (SIR, 0.76; 95% CI, 0.60–0.95) and bronchial cancer
incidence (SIR, 0.33; 95% CI, 0.12–0.72) were reduced (Table 1
). There were no relationships among
cancer incidence and pre- or posttreatment GH levels, age at diagnosis,
or duration of disease (not shown).
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The colon cancer mortality rate was higher than expected (SMR,
2.47; 95% CI, 1.31–4.22), and there was a nonsignificant increase in
female breast cancer mortality (SMR, 1.60; P = 0.07;
Table 2). Mortality rates due to all
malignant disease (SMR, 1.16; 95% CI, 0.92–1.44), carcinoma of the
bronchus (SMR, 0.69; 95% CI, 0.37–1.18), and carcinoma of the rectum
(SMR, 1.09; 95% CI, 0.22–3.19) were similar to those in the general
population of the United Kingdom (Table 2). Mortality rates due to all
malignant disease and colon cancer were increased with higher
posttreatment GH levels (P for trends, <0.05 and
<0.02; Tables 4 and 5).
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) or age at diagnosis (Table 7).
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Three hundred and sixty-six deaths occurred in the 1,362 subjects
of our analysis cohort, representing 19,323 person-years of exposure to
acromegaly. We found an increase in all cause mortality rate (SMR, 1.6;
95% CI, 1.44–1.77) and in cardiovascular (SMR, 1.76; 95% CI,
1.47–2.07), cerebrovascular (SMR, 2.06; 95% CI, 1.50–2.76), and
respiratory (SMR, 1.85; 95% CI, 1.34–2.49) mortality rates (Table 3). All cause mortality rate and
cardiovascular mortality rate were increased with higher posttreatment
GH levels (P for trends, <0.0001 and <0.02; Table 4
).
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).
The overall mortality rate was higher in subjects in whom acromegaly
was diagnosed at a younger age (P for trend, 0.004), with
deaths from cerebrovascular disease being the main cause of this
increase (P for trend, <0.001; Table 7).
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Discussion |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Rajasoorya et al. (15) has shown that the predominant determinant of outcome (morbidity and mortality) in acromegaly is the final serum GH level after treatment. A multivariate analysis of that cohort showed that survival was significantly influenced by the last known GH level (P = 0.0001), but not by the GH level at diagnosis (P = 0.1). These findings are confirmed by the present study. We stratified posttreatment GH levels into three broad categories using evidence from previous published work. Bates et al. (14) reported that mortality in patients with acromegaly whose mean posttreatment GH level was below 2.5 ng/mL (5 mU/L) was the same as that in the general population (SMR, 1.42; 95% CI, 0.46–3.31). This notional safe level for posttreatment GH is supported by an earlier study that showed normalization of total body water and total exchangeable sodium in acromegalic patients with posttreatment GH levels below 2.5 ng/mL (5 mU/L) (24). The higher cut-off level of 10 ng/mL (20 mU/L) was derived from early surgical series that considered this level to represent the normalization of GH secretion (25, 26). We felt that using a fasting GH, random GH, or mean of a day curve was appropriate, as these are highly predictive of biochemically active acromegaly, as shown by elevated insulin-like growth factor I levels (27). The vast majority of GH levels used were fasting 0900 h GH levels, which closely correlate to mean 24-h GH levels and insulin-like growth factor I levels in acromegaly (15, 28).
This study gives some support to previous series (2, 3, 4) that have shown an increased incidence of colonic carcinomas. We found no excess incidence of rectal carcinoma, which is in line with the largest previously reported study (8619 person-years of follow-up) (3). The neoplasms arose uniformly throughout the large bowel, with five cancer registrations in the right or proximal colon, five in the left or distal colon, and two from unspecified sites. We did not confirm the overall increase in incidence of neoplasms or female carcinomas of the breast reported by Nabarro (1). In fact, we found a lower than expected overall cancer incidence and a particularly low incidence of carcinoma of the bronchus. Environmental factors such as smoking habits and exposure to pollution and ionizing radiation, which are major etiological factors in the development of lung cancer (29, 30), may have been different in the acromegalic cohort and the general population. The majority of nonmalignant respiratory deaths were due to bronchopneumonia or pneumonia (thirty-one), which may have been smoking related. Deaths directly attributable to smoking, i.e. chronic bronchitis, emphysema, and chronic airways obstruction (eleven), represented a minority. These data do not give further insight into smoking rates or the etiology of the reduced incidence of carcinoma of the bronchus observed in this cohort.
There was no increase in mortality rate from malignant disease in general, but there was a significant increase in the colon cancer mortality rate and a nonsignificant increase in mortality due to breast cancer. Nabarro (1) reported no excess cancer mortality or breast cancer mortality, but found a marked excess breast cancer incidence (SIR, 4.23; P < 0.0001). We found the opposite pattern of malignancies in our cohort, with a low or normal cancer incidence rate and a normal or raised cancer mortality rate. Mortality due to all malignant disease and colon cancer were increased with higher posttreatment GH levels, but not duration of disease. These data suggest that GH hypersecretion modifies the progression of existing malignancies, particularly colonic carcinoma. This may explain the discrepancy between the cancer incidence and cancer mortality rates observed, which could be of importance outside the management of acromegaly.
Mortality rates due to cardiovascular, cerebrovascular, and respiratory disease were increased, which is broadly in line with previous series (11, 12, 13). Overall and cardiovascular mortality rates were increased with high posttreatment GH levels. Mortality due to cerebrovascular and respiratory disease was not related to posttreatment GH levels. We confirmed the work of Bates et al. (14) and showed that the overall mortality rate in those acromegalic patients with posttreatment GH levels below 2.5 ng/mL (5 mU/L) is comparable to that in the general population of the United Kingdom (SMR, 1.10; 95% CI, 0.89–1.35). The present study lends substantial support to efforts to reduce GH secretion to below 2.5 ng/mL (5 mU/L). The achievement of this postoperatively is less with large tumors and high GH levels (31). Radiotherapy requires up to 10 yr to achieve maximum reduction in GH secretion (32). Of the medical modalities available, somatostatin analogs (33) more frequently achieve this target than dopamine agonists (34).
Mortality in acromegaly and particularly mortality due to cerebrovascular disease rise with decreasing age at diagnosis. This supports the long held clinical impression that acromegaly occurring in the elderly has a more indolent course, whereas an early presentation is associated with more aggressive disease. The high cerebrovascular mortality occurring in acromegalic patients diagnosed under 35 yr of age (SMR, 7.36; 95% CI, 3.18–14.51) may be due to structural changes in the vascular system, such as hypertension (35), that are not ameliorated by lowering GH levels. This is supported by the positive relationship between cerebrovascular mortality and duration of acromegaly.
In summary, we have performed a large retrospective epidemiological cohort study that has shown increased mortality rates from colon cancer, cardiovascular disease, cerebrovascular disease, and respiratory disease in patients with acromegaly. Mortality rates due to colon cancer, all malignant disease, and cardiovascular disease were increased with higher posttreatment GH levels. Posttreatment GH levels below 2.5 ng/mL (5 mU/L) were associated with an overall mortality rate similar to that of the general population of the United Kingdom.
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Footnotes |
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2 Members of the United Kingdom Acromegaly Study Group: A. B.
Atkinson and D. R. Hadden (Royal Victoria Hospital, Belfast,
Northern Ireland); P. H. Baylis and P. Kendall-Taylor (University
of Newcastle-Upon-Tyne, Newcastle Upon-Tyne, UK); C. G. Beardwell
and S. M. Shalet (Christie Hospital, Manchester, UK); G. Beastall
and G. M. Teasdale (University of Glasgow, Glasgow, Scotland);
P.-M. G. Bouloux (Royal Free Hospital, London, UK); C. W.
Burke and J. A. H. Wass (The Radcliffe Infirmary, Oxford,
UK); R. N. Clayton (Stoke on Trent, UK); D. R. Cullen and
A. P. Weetman (Royal Hallamshire and Northern General Hospitals,
Sheffield, UK); T. A. Howlett (Leicester Royal Infirmary); L.
Hipkin, B. A. Walker, and M. C. White (deceased) (Royal
Liverpool University Hospital, Liverpool, UK); H. S. Jacobs
(Middlesex Hospital, London, UK); W. J. Jeffcoate (City Hospital,
Nottingham, UK); J. P. Monson (The Royal Hospital National Health
Service Trust, London, UK); M. C. Sheppard and P. M. Stewart
(University of Birmingham, Birmingham, UK); and A. Staines
(LRF, University of Leeds, Leeds, UK).
Received January 5, 1998.
Revised April 7, 1998.
Accepted April 24, 1998.
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 E. R. Schwarz, P. Jammula, R. Gupta, and S. Rosanio A Case and Review of Acromegaly-Induced Cardiomyopathy and the Relationship Between Growth Hormone and Heart Failure: Cause or Cure or Neither or Both? Journal of Cardiovascular Pharmacology and Therapeutics, December 1, 2006; 11(4): 232 - 244. [Abstract] [PDF]
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P. Mulatero, F. Veglio, P. Maffei, M. Bondanelli, S. Bovio, F. Daffara, G. Leotta, A. Angeli, C. Calvo, C. Martini, et al. CYP11B2 -344T/C Gene Polymorphism and Blood Pressure in Patients with Acromegaly J. Clin. Endocrinol. Metab., December 1, 2006; 91(12): 5008 - 5012. [Abstract] [Full Text] [PDF]
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S. Cannavo, B. Almoto, G. Cavalli, S. Squadrito, G. Romanello, M. T. Vigo, F. Fiumara, S. Benvenga, and F. Trimarchi Acromegaly and Coronary Disease: An Integrated Evaluation of Conventional Coronary Risk Factors and Coronary Calcifications Detected by Computed Tomography J. Clin. Endocrinol. Metab., October 1, 2006; 91(10): 3766 - 3772. [Abstract] [Full Text] [PDF]
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R. Kauppinen-Makelin, T. Sane, H. Sintonen, H. Markkanen, M. J. Valimaki, E. Loyttyniemi, L. Niskanen, A. Reunanen, U.-H. Stenman, and and the Finnish Acromegaly Study Group Quality of Life in Treated Patients with Acromegaly J. Clin. Endocrinol. Metab., October 1, 2006; 91(10): 3891 - 3896. [Abstract] [Full Text] [PDF]
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P. J. Jenkins, P. Bates, M. N. Carson, P. M. Stewart, J. A. H. Wass, and on behalf of the UK National Acromegaly Register S Conventional Pituitary Irradiation Is Effective in Lowering Serum Growth Hormone and Insulin-Like Growth Factor-I in Patients with Acromegaly J. Clin. Endocrinol. Metab., April 1, 2006; 91(4): 1239 - 1245. [Abstract] [Full Text] [PDF]
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R. Cozzi, M. Montini, R. Attanasio, M. Albizzi, G. Lasio, S. Lodrini, P. Doneda, L. Cortesi, and G. Pagani Primary Treatment of Acromegaly with Octreotide LAR: A Long-Term (Up to Nine Years) Prospective Study of Its Efficacy in the Control of Disease Activity and Tumor Shrinkage J. Clin. Endocrinol. Metab., April 1, 2006; 91(4): 1397 - 1403. [Abstract] [Full Text] [PDF]
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 H. Markkanen, T. Pekkarinen, M. J. Valimaki, H. Alfthan, R. Kauppinen-Makelin, T. Sane, and U.-H. Stenman Effect of Sex and Assay Method on Serum Concentrations of Growth Hormone in Patients with Acromegaly and in Healthy Controls Clin. Chem., March 1, 2006; 52(3): 468 - 473. [Abstract] [Full Text] [PDF]
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A. Pokrajac, A. G Claridge, S K A. Shakoor, and P. J Trainer The octreotide test dose is not a reliable predictor of the subsequent response to somatostatin analogue therapy in patients with acromegaly Eur. J. Endocrinol., February 1, 2006; 154(2): 267 - 274. [Abstract] [Full Text] [PDF]
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A. Colao, R. Attanasio, R. Pivonello, P. Cappabianca, L. M. Cavallo, G. Lasio, A. Lodrini, G. Lombardi, and R. Cozzi Partial Surgical Removal of Growth Hormone-Secreting Pituitary Tumors Enhances the Response to Somatostatin Analogs in Acromegaly J. Clin. Endocrinol. Metab., January 1, 2006; 91(1): 85 - 92. [Abstract] [Full Text] [PDF]
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E. Resmini, M. Casu, V. Patrone, G. Murialdo, F. Bianchi, M. Giusti, D. Ferone, and F. Minuto Sympathovagal Imbalance in Acromegalic Patients J. Clin. Endocrinol. Metab., January 1, 2006; 91(1): 115 - 120. [Abstract] [Full Text] [PDF]
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C. L. Ronchi, V. Varca, P. Beck-Peccoz, E. Orsi, F. Donadio, A. Baccarelli, C. Giavoli, E. Ferrante, A. Lania, A. Spada, et al. Comparison between Six-Year Therapy with Long-Acting Somatostatin Analogs and Successful Surgery in Acromegaly: Effects on Cardiovascular Risk Factors J. Clin. Endocrinol. Metab., January 1, 2006; 91(1): 121 - 128. [Abstract] [Full Text] [PDF]
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J Ayuk and M C Sheppard Growth hormone and its disorders Postgrad. Med. J., January 1, 2006; 82(963): 24 - 30. [Abstract] [Full Text] [PDF]
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W. H T Smith, R U. Nair, D. Adamson, M. T Kearney, S. G Ball, and A. J Balmforth Somatostatin receptor subtype expression in the human heart: differential expression by myocytes and fibroblasts J. Endocrinol., December 1, 2005; 187(3): 379 - 386. [Abstract] [Full Text] [PDF]
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P Cabanas, T Garcia-Caballero, J Barreiro, L Castro-Feijoo, R Gallego, T Arevalo, R Canete, and M Pombo Papillary thyroid carcinoma after recombinant GH therapy for Turner syndrome Eur. J. Endocrinol., October 1, 2005; 153(4): 499 - 502. [Abstract] [Full Text] [PDF]
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A. Bartke Minireview: Role of the Growth Hormone/Insulin-Like Growth Factor System in Mammalian Aging Endocrinology, September 1, 2005; 146(9): 3718 - 3723. [Abstract] [Full Text] [PDF]
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R. Kauppinen-Makelin, T. Sane, A. Reunanen, M. J. Valimaki, L. Niskanen, H. Markkanen, E. Loyttyniemi, T. Ebeling, P. Jaatinen, H. Laine, et al. A Nationwide Survey of Mortality in Acromegaly J. Clin. Endocrinol. Metab., July 1, 2005; 90(7): 4081 - 4086. [Abstract] [Full Text] [PDF]
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N. R. Biermasz, A. M. Pereira, J. W. A. Smit, J. A. Romijn, and F. Roelfsema Morbidity after Long-Term Remission for Acromegaly: Persisting Joint-Related Complaints Cause Reduced Quality of Life J. Clin. Endocrinol. Metab., May 1, 2005; 90(5): 2731 - 2739. [Abstract] [Full Text] [PDF]
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D. Selvarajah, J. Webster, R. Ross, and J. Newell-Price Effectiveness of adding dopamine agonist therapy to long-acting somatostatin analogues in the management of acromegaly Eur. J. Endocrinol., April 1, 2005; 152(4): 569 - 574. [Abstract] [Full Text] [PDF]
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J. J. Puder, S. Nilavar, K. D. Post, and P. U. Freda Relationship between Disease-Related Morbidity and Biochemical Markers of Activity in Patients with Acromegaly J. Clin. Endocrinol. Metab., April 1, 2005; 90(4): 1972 - 1978. [Abstract] [Full Text] [PDF]
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P. Nomikos, M. Buchfelder, and R. Fahlbusch The outcome of surgery in 668 patients with acromegaly using current criteria of biochemical 'cure' Eur. J. Endocrinol., March 1, 2005; 152(3): 379 - 387. [Abstract] [Full Text] [PDF]
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I. E Bonapart, R. van Domburg, S. M T H ten Have, W. W de Herder, R. A M Erdman, J. A M J L Janssen, and A. J. van der Lely The 'bio-assay' quality of life might be a better marker of disease activity in acromegalic patients than serum total IGF-I concentrations Eur. J. Endocrinol., February 1, 2005; 152(2): 217 - 224. [Abstract] [Full Text] [PDF]
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G. Minniti, D. Traish, S. Ashley, A. Gonsalves, and M. Brada Risk of Second Brain Tumor after Conservative Surgery and Radiotherapy for Pituitary Adenoma: Update after an Additional 10 Years J. Clin. Endocrinol. Metab., February 1, 2005; 90(2): 800 - 804. [Abstract] [Full Text] [PDF]
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M. Terzolo, G. Reimondo, M. Gasperi, R. Cozzi, R. Pivonello, G. Vitale, A. Scillitani, R. Attanasio, E. Cecconi, F. Daffara, et al. Colonoscopic Screening and Follow-Up in Patients with Acromegaly: A Multicenter Study in Italy J. Clin. Endocrinol. Metab., January 1, 2005; 90(1): 84 - 90. [Abstract] [Full Text] [PDF]
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W. M. Cao, K. Murao, H. Imachi, X. Yu, H. Dobashi, K. Yoshida, T. Muraoka, N. Kotsuna, S. Nagao, N. C. W. Wong, et al. Insulin-Like Growth Factor-I Regulation of Hepatic Scavenger Receptor Class BI Endocrinology, December 1, 2004; 145(12): 5540 - 5547. [Abstract] [Full Text] [PDF]
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D. R. Clemmons and C. Strasburger Monitoring the Response to Treatment in Acromegaly J. Clin. Endocrinol. Metab., November 1, 2004; 89(11): 5289 - 5291. [Full Text] [PDF]
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K. S.-L. Lam, A. Xu, K. C.-B. Tan, L.-C. Wong, S.-C. Tiu, and S. Tam Serum Adiponectin Is Reduced in Acromegaly and Normalized after Correction of Growth Hormone Excess J. Clin. Endocrinol. Metab., November 1, 2004; 89(11): 5448 - 5453. [Abstract] [Full Text] [PDF]
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 A Levy Pituitary disease: presentation, diagnosis, and management J. Neurol. Neurosurg. Psychiatry, September 1, 2004; 75(suppl_3): iii47 - iii52. [Full Text] [PDF]
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J. Svensson, B.-A. Bengtsson, T. Rosen, A. Oden, and G. Johannsson Malignant Disease and Cardiovascular Morbidity in Hypopituitary Adults with or without Growth Hormone Replacement Therapy J. Clin. Endocrinol. Metab., July 1, 2004; 89(7): 3306 - 3312. [Abstract] [Full Text] [PDF]
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N. R. Biermasz, F. W. Dekker, A. M. Pereira, S. W. van Thiel, P. J. Schutte, H. van Dulken, J. A. Romijn, and F. Roelfsema Determinants of Survival in Treated Acromegaly in a Single Center: Predictive Value of Serial Insulin-Like Growth Factor I Measurements J. Clin. Endocrinol. Metab., June 1, 2004; 89(6): 2789 - 2796. [Abstract] [Full Text] [PDF]
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N. M. Neary, C. J. Small, A. M. Wren, J. L. Lee, M. R. Druce, C. Palmieri, G. S. Frost, M. A. Ghatei, R. C. Coombes, and S. R. Bloom Ghrelin Increases Energy Intake in Cancer Patients with Impaired Appetite: Acute, Randomized, Placebo-Controlled Trial J. Clin. Endocrinol. Metab., June 1, 2004; 89(6): 2832 - 2836. [Abstract] [Full Text] [PDF]
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A. F. Muller, J. J. Kopchick, A. Flyvbjerg, and A. J. van der Lely Growth Hormone Receptor Antagonists J. Clin. Endocrinol. Metab., April 1, 2004; 89(4): 1503 - 1511. [Full Text] [PDF]
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J. Ayuk, R. N. Clayton, G. Holder, M. C. Sheppard, P. M. Stewart, and A. S. Bates Growth Hormone and Pituitary Radiotherapy, But Not Serum Insulin-Like Growth Factor-I Concentrations, Predict Excess Mortality in Patients with Acromegaly J. Clin. Endocrinol. Metab., April 1, 2004; 89(4): 1613 - 1617. [Abstract] [Full Text] [PDF]
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A. Colao, D. Ferone, P. Marzullo, and G. Lombardi Systemic Complications of Acromegaly: Epidemiology, Pathogenesis, and Management Endocr. Rev., February 1, 2004; 25(1): 102 - 152. [Abstract] [Full Text] [PDF]
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O. Serri, C. Beauregard, and J. Hardy Long-Term Biochemical Status and Disease-Related Morbidity in 53 Postoperative Patients with Acromegaly J. Clin. Endocrinol. Metab., February 1, 2004; 89(2): 658 - 661. [Abstract] [Full Text] [PDF]
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I. M. Holdaway, R. C. Rajasoorya, and G. D. Gamble Factors Influencing Mortality in Acromegaly J. Clin. Endocrinol. Metab., February 1, 2004; 89(2): 667 - 674. [Abstract] [Full Text] [PDF]
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 E. Giovannucci, E. B Rimm, Y. Liu, and W. C Willett Height, predictors of C-peptide and cancer risk in men Int. J. Epidemiol., February 1, 2004; 33(1): 217 - 225. [Abstract] [Full Text] [PDF]
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 D. E. Meyers and R. C. Cuneo Controversies Regarding the Effects of Growth Hormone on the Heart Mayo Clin. Proc., December 1, 2003; 78(12): 1521 - 1526. [Abstract] [PDF]
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D. R. Clemmons, K. Chihara, P. U. Freda, K. K. Y. Ho, A. Klibanski, S. Melmed, S. M. Shalet, C. J. Strasburger, P. J. Trainer, and M. O. Thorner Optimizing Control of Acromegaly: Integrating a Growth Hormone Receptor Antagonist into the Treatment Algorithm J. Clin. Endocrinol. Metab., October 1, 2003; 88(10): 4759 - 4767. [Abstract] [Full Text] [PDF]
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 I Perry, P M Stewart, K Kane, P J Jenkins, and P D Fairclough Colorectal screening guidelines in acromegaly Gut, September 1, 2003; 52(9): 1387 - 1387. [Full Text]
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P. De, D. A. Rees, N. Davies, R. John, J. Neal, R. G. Mills, J. Vafidis, J. S. Davies, and M. F. Scanlon Transsphenoidal Surgery for Acromegaly in Wales: Results Based on Stringent Criteria of Remission J. Clin. Endocrinol. Metab., August 1, 2003; 88(8): 3567 - 3572. [Abstract] [Full Text] [PDF]
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A. Colao, L. Spinelli, P. Marzullo, R. Pivonello, M. Petretta, C. Di Somma, G. Vitale, D. Bonaduce, and G. Lombardi High Prevalence of Cardiac Valve Disease in Acromegaly: An Observational, Analytical, Case-Control Study J. Clin. Endocrinol. Metab., July 1, 2003; 88(7): 3196 - 3201. [Abstract] [Full Text] [PDF]
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R. N. Clayton Cardiovascular Function in Acromegaly Endocr. Rev., June 1, 2003; 24(3): 272 - 277. [Abstract] [Full Text] [PDF]
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J. C. Smith, H. Lane, N. Davies, L. M. Evans, J. Cockcroft, M. F. Scanlon, and J. S. Davies The Effects of Depot Long-Acting Somatostatin Analog on Central Aortic Pressure and Arterial Stiffness in Acromegaly J. Clin. Endocrinol. Metab., June 1, 2003; 88(6): 2556 - 2561. [Abstract] [Full Text] [PDF]
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 D. Komninou, A. Ayonote, J. P. Richie Jr., and B. Rigas Insulin Resistance and Its Contribution to Colon Carcinogenesis Experimental Biology and Medicine, April 1, 2003; 228(4): 396 - 405. [Abstract] [Full Text] [PDF]
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A. Ben-Shlomo and S. Melmed The Role of Pharmacotherapy in Perioperative Management of Patients with Acromegaly J. Clin. Endocrinol. Metab., March 1, 2003; 88(3): 963 - 968. [Full Text] [PDF]
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 V. D. Longo and C. E. Finch Evolutionary Medicine: From Dwarf Model Systems to Healthy Centenarians? Science, February 28, 2003; 299(5611): 1342 - 1346. [Abstract] [Full Text] [PDF]
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 S. R. Rose Studies Reveal Minimal Cancer Risks with Growth Hormone Therapy AAP Grand Rounds, November 1, 2002; 8(5): 49 - 50. [Full Text] [PDF]
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E. M. Erfurth, B. Bulow, G. Svahn-Tapper, B. Norrving, K. Odh, Z. Mikoczy, J. Bjork, and L. Hagmar Risk Factors for Cerebrovascular Deaths in Patients Operated and Irradiated for Pituitary Tumors J. Clin. Endocrinol. Metab., November 1, 2002; 87(11): 4892 - 4899. [Abstract] [Full Text] [PDF]
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J. J. Kopchick, C. Parkinson, E. C. Stevens, and P. J. Trainer Growth Hormone Receptor Antagonists: Discovery, Development, and Use in Patients with Acromegaly Endocr. Rev., October 1, 2002; 23(5): 623 - 646. [Abstract] [Full Text] [PDF]
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J. S. Bevan, S. L. Atkin, A. B. Atkinson, P.-M. Bouloux, F. Hanna, P. E. Harris, R. A. James, M. McConnell, G. A. Roberts, M. F. Scanlon, et al. Primary Medical Therapy for Acromegaly: An Open, Prospective, Multicenter Study of the Effects of Subcutaneous and Intramuscular Slow-Release Octreotide on Growth Hormone, Insulin-Like Growth Factor-I, and Tumor Size J. Clin. Endocrinol. Metab., October 1, 2002; 87(10): 4554 - 4563. [Abstract] [Full Text] [PDF]
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P J Jenkins and P D Fairclough Screening guidelines for colorectal cancer and polyps in patients with acromegaly Gut, October 1, 2002; 51(90005): v13 - 14. [Full Text] [PDF]
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J. Ayuk, S. E. Stewart, P. M. Stewart, and M. C. Sheppard Long-Term Safety and Efficacy of Depot Long-Acting Somatostatin Analogs for the Treatment of Acromegaly J. Clin. Endocrinol. Metab., September 1, 2002; 87(9): 4142 - 4146. [Abstract] [Full Text] [PDF]
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 D. M. Cook Shouldn't Adults with Growth Hormone Deficiency Be Offered Growth Hormone Replacement Therapy? Ann Intern Med, August 6, 2002; 137(3): 197 - 201. [Abstract] [Full Text] [PDF]
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L. A. Frohman Controversy about Treatment of Growth Hormone-Deficient Adults: A Commentary Ann Intern Med, August 6, 2002; 137(3): 202 - 204. [Full Text] [PDF]
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P. J. Trainer Acromegaly--Consensus, What Consensus? J. Clin. Endocrinol. Metab., August 1, 2002; 87(8): 3534 - 3536. [Full Text] [PDF]
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 M. S. Sandhu, D. B. Dunger, and E. L. Giovannucci Insulin, Insulin-Like Growth Factor-I (IGF-I), IGF Binding Proteins, Their Biologic Interactions, and Colorectal Cancer J Natl Cancer Inst, July 3, 2002; 94(13): 972 - 980. [Abstract] [Full Text] [PDF]
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C. A. Sklar, A. C. Mertens, P. Mitby, G. Occhiogrosso, J. Qin, G. Heller, Y. Yasui, and L. L. Robison Risk of Disease Recurrence and Second Neoplasms in Survivors of Childhood Cancer Treated with Growth Hormone: A Report from the Childhood Cancer Survivor Study J. Clin. Endocrinol. Metab., July 1, 2002; 87(7): 3136 - 3141. [Abstract] [Full Text] [PDF]
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G. Brevetti, P. Marzullo, A. Silvestro, R. Pivonello, G. Oliva, C. di Somma, G. Lombardi, and A. Colao Early Vascular Alterations in Acromegaly J. Clin. Endocrinol. Metab., July 1, 2002; 87(7): 3174 - 3179. [Abstract] [Full Text] [PDF]
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R. J. Irving, M. N. Carson, D. J. Webb, and B. R. Walker Peripheral Vascular Structure and Function in Men with Contrasting GH Levels J. Clin. Endocrinol. Metab., July 1, 2002; 87(7): 3309 - 3314. [Abstract] [Full Text] [PDF]
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R Palmqvist, G Hallmans, S Rinaldi, C Biessy, R Stenling, E Riboli, and R Kaaks Plasma insulin-like growth factor 1, insulin-like growth factor binding protein 3, and risk of colorectal cancer: a prospective study in northern Sweden Gut, May 1, 2002; 50(5): 642 - 646. [Abstract] [Full Text] [PDF]
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 T. Shioi, J. R. McMullen, P. M. Kang, P. S. Douglas, T. Obata, T. F. Franke, L. C. Cantley, and S. Izumo Akt/Protein Kinase B Promotes Organ Growth in Transgenic Mice Mol. Cell. Biol., April 15, 2002; 22(8): 2799 - 2809. [Abstract] [Full Text] [PDF]
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C. Parkinson, W. M. Drake, M. E. Roberts, K. Meeran, G. M. Besser, and P. J. Trainer A Comparison of the Effects of Pegvisomant and Octreotide on Glucose, Insulin, Gastrin, Cholecystokinin, and Pancreatic Polypeptide Responses to Oral Glucose and a Standard Mixed Meal J. Clin. Endocrinol. Metab., April 1, 2002; 87(4): 1797 - 1804. [Abstract] [Full Text] [PDF]
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A. G. Renehan and S. M. Shalet Acromegaly and Colorectal Cancer: Risk Assessment Should Be Based on Population-Based Studies J. Clin. Endocrinol. Metab., April 1, 2002; 87(4): 1909 - 1909. [Full Text] [PDF]
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L. Le Marchand, T. Donlon, A. Seifried, R. Kaaks, S. Rinaldi, and L. R. Wilkens Association of a Common Polymorphism in the Human GH1 Gene with Colorectal Neoplasia J Natl Cancer Inst, March 20, 2002; 94(6): 454 - 460. [Abstract] [Full Text] [PDF]
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C. Parkinson, W. D. J. Ryder, and P. J. Trainer The Relationship between Serum GH and Serum IGF-I in Acromegaly Is Gender-Specific J. Clin. Endocrinol. Metab., November 1, 2001; 86(11): 5240 - 5244. [Abstract] [Full Text] [PDF]
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 E. Giovannucci Insulin, Insulin-Like Growth Factors and Colon Cancer: A Review of the Evidence J. Nutr., November 1, 2001; 131(11): 3109S - 3120. [Abstract] [Full Text] [PDF]
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J. Ma, E. Giovannucci, M. Pollak, J. M. Chan, J. M. Gaziano, W. Willett, and M. J. Stampfer Milk Intake, Circulating Levels of Insulin-Like Growth Factor-I, and Risk of Colorectal Cancer in Men J Natl Cancer Inst, September 5, 2001; 93(17): 1330 - 1336. [Abstract] [Full Text] [PDF]
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