Pituitary adenomas with onset during puberty

Features and treatment

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✓ From a series of 207 patients with pituitary adenoma operated on by microsurgical technique from 1973 to February, 1982, the cases of nine young people whose symptoms had appeared between the ages of 11 and 15 years are presented. The most important data are that all the children were pubertal and that in seven the tumor was, or later became, invasive. By contrast, the tumor was enclosed in eight of nine other patients whose symptoms manifested between the ages of 16 and 20 years, and in 152 of the remaining 189 patients whose symptoms appeared after the age of 20 years. Considering the gravity of the disease treated, the results in this series may be termed encouraging. The treatment was multidisciplinary: starting with surgery, followed by radiotherapy, endocrine replacement therapy, and, in adenomas secreting prolactin and/or growth hormone, medical therapy with bromocriptine. The divergence between authors on the subject of childhood adenomas, especially as to whether they are more often invasive or enclosed, could be overcome, at least in part, if the term “pediatric age” were unequivocally defined and if there were an agreed distinction between puberty and childhood on the one hand and puberty and adolescence on the other.

Abstract

✓ From a series of 207 patients with pituitary adenoma operated on by microsurgical technique from 1973 to February, 1982, the cases of nine young people whose symptoms had appeared between the ages of 11 and 15 years are presented. The most important data are that all the children were pubertal and that in seven the tumor was, or later became, invasive. By contrast, the tumor was enclosed in eight of nine other patients whose symptoms manifested between the ages of 16 and 20 years, and in 152 of the remaining 189 patients whose symptoms appeared after the age of 20 years. Considering the gravity of the disease treated, the results in this series may be termed encouraging. The treatment was multidisciplinary: starting with surgery, followed by radiotherapy, endocrine replacement therapy, and, in adenomas secreting prolactin and/or growth hormone, medical therapy with bromocriptine. The divergence between authors on the subject of childhood adenomas, especially as to whether they are more often invasive or enclosed, could be overcome, at least in part, if the term “pediatric age” were unequivocally defined and if there were an agreed distinction between puberty and childhood on the one hand and puberty and adolescence on the other.

Numerous publications have appeared in recent years on pituitary adenomas in patients of pediatric age,2,6–8,12,13,18,22,24,30 so it seems that these tumors are less rare than was previously suspected. There is at present, however, no agreement on the biological behavior of adenomas in this age group. Richmond and Wilson24 reported a higher incidence of intrasellar and enclosed adenomas “in childhood and adolescence,” and explicitly contested earlier findings of Ortiz-Suarez and Erickson22 that adenomas of “adolescents” tend more often to be extrasellar and invasive. The experience of other authors also seems to vary from enclosed adenomas2,6,18,30 to invasive adenomas.7,8,12,13

In our view, this diversity of opinion arises, at least in part, from fuzziness about the term “pediatric age,” which should be divided into childhood, puberty, and adolescence. For example, of the 25 cases reported by Richmond and Wilson24 the onset of symptoms was probably prepubertal (from 5 to 12 years) in nine, and probably postpubertal (from 17 to 20 years) in another seven; in nine patients the age at onset ranged from 13 to 16 years. Thus, in the majority of these last nine cases, onset probably occurred in one of the phases of puberty. If the 36% of adenomas with “significant suprasellar extension or invasiveness” reported by these authors occurred mainly in the nine probably pubertal patients, there would be no discrepancy between their findings and those of Ortiz-Suarez and Erickson,22 who reported four patients operated on for invasive adenomas that probably occurred during puberty: at 14 years old in one case, at 13 years in another, “before” 15 years in a third, and “before” 17 years in the fourth.

This study is based on a review of 207 consecutive patients operated on for pituitary adenoma from 1973 to February, 1982. Of these, 189 were adults; nine were adolescents, in whom the onset of symptoms occurred between the ages of 16 and 20 years; and nine were classed as children, in whom onset occurred between the ages of 11 and 15 years. These last patients constituted, in our view, a singular group, both because all were in the pubertal period and because in seven of them (77.7%) the tumor was invasive, at least at the time of diagnosis. The clinical features of these nine patients and the treatment they received are analyzed and discussed.

Summary of Cases
Stage of Puberty and Presenting Symptoms

The state of puberty of the patients at the onset of the presenting symptoms ranged from the 2nd to the 5th stage of puberty described by Penny23 in the male and by Marshall and Tanner19 in the female (Table 1). Three of the five males (Cases 4, 5, and 8) were in puberty Stage 4, with penis and testes at an advanced stage of growth, and pubic hair even if not yet of the adult type. Their primary symptoms were, respectively, gigantism and acromegaly, gynecomastia, and obesity, and hirsutism. The other two patients (Cases 6 and 9) were in Stage 2, with only incipient development of penis and testes. The primary symptom in both cases was failure of sexual maturation.

TABLE 1

Preoperative features of pituitary adenomas with onset of symptoms during puberty*

Case No., & SexClinical OnsetAge at Surgery (yrs)Preoperative SymptomsAbnormal Hormonal LevelsSella TypeRadiological ExaminationsMorphology of Tumor
Age (yrs)Stage       
1, F 11 212 gigantism, headache, upper bitemporal defectGH 75 ng/ml, PRL 600 ng/ml2CT, angiographyenclosed with suprasellar extension
   
2, F 14.5 516 acromegalic gigantism, amenorrhea, galactorrhea; rt eye: 1/10, lt eye: 0.5/10; bitemporal hemianopsiaGH 160 ng/ml, PRL 2000 ng/ml4CT, angiographyinvasive with suprasellar extension
   
3, F 12 219 acromegalic gigantism, obesity, diabetes insipidus, bitemporal hemianopsia, sudden headache; rt eye: 4/10, lt eye: 6/10; rt ophthalmoplegiaGH 140 ng/ml, hypopituitarism4angiography, PEGinvasive with supraretrolaterosellar extension
   
4, M 14 431 acromegalic gigantism, diabetes insipidus; rt eye: 3/10, lt eye: 4/10; bitemporal hemianopsiaGH 110 ng/ml2PEGenclosed with supraretrosellar extension
   
5, M 15 415.2 gynecomastia, bitemporal hemianopsia; sudden visual loss, lt eye: 0.5/10, rt eye: 8/10PRL 830 ng/ml, hypopituitarism4CT, angiographyinvasive with supraretrosellar extension
   
6, M 12.5 214.5 gynecomastia, small testes, failure of pubic hair growth; rt eye: 6/10, lt eye: 3/10; bitemporal hemianopsiaPRL 6000 ng/ml, hypopituitarism4CT, angiographyinvasive with suprasellar extension, later extended to sphenoidal & both cavernous sinuses
   
7, F 14 529 amenorrhea, headache, lt homonymous hemianopsia; cobalt therapy at 24 yrs; 5 yrs later: headache, drowsiness, papilledema, lt hemiparesis; sudden right ophthalmoplegia; lt eye: 3/10, amaurosis on rtendocrine status not available4CT, angiographyinvasive with extension to retropharynx, rt middle cranial fossa & rt frontal ventricles
   
8, M 15 418 obesity, hirsutism, arterial hypertensionACTH 180 pg/ml, biorhythm of cortisol absent3CT, angiographyinvasive with extension to sphenoidal sinus
   
9, M 12 215 gynecomastia, small testes, failure of pubic hair growth, diabetes insipidus; rt eye: 7/10, lt eye: 5/10; bitemporal hemianopsia; papilledemahypopituitarism (nonsecreting adenoma)4angiography, PEGinvasive with retrosuprasellar extension

Abbreviations: GH = growth hormone; PRL = prolactin; ACTH = adrenocorticotropic hormone; CT = computerized tomography; PEG = pneumoencephalography.

Stage of puberty.

Classification according to Vezina and Maltais.29

Of the four females, two (Cases 1 and 3) were in puberty Stage 2, with projection of the areola and mammary papilla and incipient pubic hair growth. The other two (Cases 2 and 7) were in Stage 5; for some months both had presented mammary development and growth of adult pubic hair and both had menstruated for the first time, one 2 months before and the other 3 months before. The presenting symptoms in these four patients were, respectively, gigantism, acromegalic gigantism, acromegalic gigantism and amenorrhea-galactorrhea, and amenorrhea.

Preoperative Features

Table 1 lists the preoperative features of the nine patients. In four, symptoms were related to mixed adenomas secreting growth hormone and prolactin (PRL) (Cases 1 and 2) or to GH-secreting adenomas (Cases 3 and 4). All four presented gigantism or acromegalic gigantism, three complained of bitemporal hemianopsia, and one of upper bitemporal defect. Three had marked bilateral reduction of visual acuity, combined in one case with unilateral ophthalmoplegia of acute onset. Two patients also had diabetes insipidus, associated in one with obesity, and one patient had primary amenorrhea and galactorrhea. Only one patient reported headache.

Plain x-ray films and pluridirectional tomography showed global widening of the sella turcica in two patients (Cases 1 and 4: Type 2 sella according to the classification of Vezina and Maltais29) and diffuse destruction (Type 4 sella29) in two others (Cases 2 and 3). On the evidence of the morphology and neuroradiological examinations (Table 1), the two patients with Type 2 sella were classified as suffering from enclosed adenoma, with suprasellar extension in one case and supraretrosellar extension in the other. The two patients with Type 4 sella pathology were classified as suffering from invasive adenoma, one with suprasellar and the other with supraretrolaterosellar extension.

Hormone assays showed that both the GH and the PRL levels were considerably higher in the invasive than in the enclosed adenomas. Another point worth noting is that the clinical history was considerably shorter in adenomas secreting both GH and PRL than in those secreting GH only. Two patients (Cases 5 and 6) had PRL-secreting adenomas, and the levels of the hormone before operation were very high. Both adenomas were invasive and at a very advanced stage, notwithstanding a clinical history of only 2 months in one case and 2 years in the other. Another patient (Case 7) had an exceptionally advanced invasive adenoma, due to a very late diagnosis at the time of her first treatment with cobalt and a subsequent delay in referral to us. She was operated on as an emergency without any preoperative hormonal study. However, the adenoma was classified as PRL-secreting on the evidence of the postoperative assays.

In both of the last two patients (Cases 8 and 9) the duration of symptoms was 3 years; the former patient had an invasive adenoma without suprasellar extension that secreted adrenocorticotropic hormone (ACTH), and the latter had a nonsecreting invasive adenoma with supraretrosellar extension.

Treatment and Results

Transsphenoidal Surgery. Six patients were operated on by the transsphenoidal route; removal was subtotal in five and apparently total in one. Table 2 (Cases 1, 2, 4, 5, 8, and 9) gives in detail the results of surgery and of postoperative radiotherapy and medical treatment. As will be noted, there was definite improvement in some symptoms in the first weeks after the operation in all the patients. Visual acuity improved in all five patients who presented visual deficits before operation (Cases 1, 2, 4, 5, and 9), and papilledema receded within a few weeks in Case 7. The visual field normalized in three patients (Cases 1, 2, and 5) and improved in three (Cases 4, 5, and 9).

TABLE 2

Results after surgery, radiotherapy, and continuing medical treatment in pituitary adenomas with onset of symptoms during puberty*

Case No., & SexSurgical Approach & Tumor RemovalHistological FeaturesSignificant Postoperative ResultsAfter Postop RadiotherapyLong-Term ResultsFollow-Up Results
Hormone LevelsMedical Treatment      
1, F transsphenoidal, apparently totalchromophobic, moderate anaplasiaheadache resolved, visual field normal; GH 18 ng/ml, PRL 85 ng/mlGH 15 ng/ml, PRL 42 ng/mlbromocriptinenormal growth & visual field; GH 4.2 ng/ml, PRL 6 ng/ml; CT negativenormal at 3 yrs
 
2, F 1st: transsphenoidal, subtotal; relapse after 9 mos; 2nd: transsphenoidalacidophilic & chromophobicafter reop: rt eye: 8/10, lt eye: 7/10; visual field normal; GH 30 ng/ml, PRL 180 ng/mlGH 21 ng/ml, PRL 30 ng/mlbromocriptineacromegaly much improved, regular menses; continued improved vision; GH 5 ng/ml, PRL 11 ng/ml; CT negativegood at 5.9 yrs
 
3, F subfrontal, subtotalacidophilicheadache resolved, visual acuity normal; partial regression of ophthalmoplegia, acromegaly, & obesity; GH 56 ng/ml, hypopituitarism unchangedGH 31 ng/mlbromocriptine, thyroid, cortisone, Pitressinnormal vision, acromegaly much improved; improvement of obesity, diabetes insipidus, & ophthalmoplegia; GH 16 ng/ml; CT: small amount of lateroretrosellar tumorfair at 6.2 yrs
 
4, M transsphenoidal, subtotalacidophilicrt eye: 5/10, lt eye: 7/10; improvement of visual field; partial regression of acromegaly; GH 43 ng/mlGH 41 ng/mlbromocriptine, thyroid, Pitressinacromegaly, diabetes insipidus, & vision improved; bitemporal hemianopsia improved; GH 21 ng/ml; CT: small amount of retrosellar tumorfair at 6 yrs
 
5, M transsphenoidal, subtotalchromophobicboth eyes: 9/10, visual field normal; PRL 85 ng/ml; partial regression of hypopituitarismPRL 50 ng/ml, unchanged hypopituitarismbromocriptine, thyroidimprovement of obesity & gynecomastia; normal sexual development; continued improved vision; PRL 9.5 ng/ml; CT negativenormal at 3.3 yrs
 
6, M 1st: subfrontal, subtotal 2nd: transsphenoidal, subtotalacidophilic & chromophobic1st: visual acuity & field improved, 8 mos later rhinorrhea and bilatophthalmoplegia; 2nd: regression of rhinorrhea & ophthalmoplegia, unchanged hypopituitarism; PRL 1000 ng/mlPRL 600 ng/ml, unchanged hypopituitarismbromocriptine, thyroid, cortisone, carbamazepineregression of rhinorrhea & ophthalmoplegia; normal sexual development; normal visual acuity & field; diabetes insipidus improved & controlled; PRL 36 ng/ml; CT: small amount of laterosellar tumorgood at 4 yrs
 
7, F subfrontal, subtotalchromophobicregression of hypertension; worsening of hemiparesis; unchanged ophthalmoplegia & vision; PRL 2600 ng/mlno postop radiotherapybromocriptine, thyroid, cortisoneunchanged ophthalmoplegia, obesity, amenorrhea, vision & visual field; severe lt hemiparesis; PRL 700 ng/ml; hypopituitarismpoor at 4 yrs
 
8, M transsphenoidal, apparently totalbasophilicpartial regression of hypertension, obesity, hirsutism; ACTH 40 pg/ml, biorhythm of cortisol presentACTH 25 pg/ml, biorhythm of cortisol normalizedregression of obesity, hirsutism & hypertension; normal endocrine status; CT negativegood at 2 yrs
 
9, M transsphenoidal, subtotalchromophobicregression of papilledema; rt eye: 8/10, lt eye: 6/10; improvement of visual fieldunchanged hypopituitarismPitressin, cortisone, thyroidvision & visual field improved; partial regression of diabetes insipidus; partial sexual maturation, hypopituitarismfair at 2 yrs

Abbreviations: GH = growth hormone; PRL = prolactin; ACTH = adrenocorticotropic hormone; CT = computerized tomography.

Acromegaly improved early in one patient (Case 4), and symptoms in the patient with Cushing's disease (Case 8) improved within a few weeks of operation. The hormone levels fell, but did not reach normal levels, in all five patients with hormone-secreting tumors (Cases 1, 2, 4, 5, and 8), whereas the pituitary deficiency of the patient with an nonsecreting pituitary adenoma (Case 9) was unchanged. All six patients then received radiotherapy, five having cobalt therapy and one highenergy treatment with a linear accelerator. Four of these patients (Cases 1, 2, 4, and 6) exhibited further lowering but not normalization of the hormone levels. In the patient operated on for Cushing's disease, on the other hand, the biorhythm of plasma cortisol and ACTH returned to normal. In the patient operated on for a nonsecreting adenoma, the hypopituitarism was unchanged. Four patients were then treated with bromocriptine at doses ranging from 5 to 7 mg daily, with the following results: PRL and GH levels became normal in two patients (Cases 1 and 2), the PRL level returned to normal in one patient (Case 5), and GH levels were reduced but not to normal in another patient (Case 4). Three patients (Cases 4, 5, and 9) also received endocrine replacement therapy. In an average follow-up period of 3.7 years, the quality of life is normal in two of these patients, good in two, and fair in the other two. Follow-up computerized tomography (CT) scanning in five of these six cases proved negative in four, and revealed a small quantity of retrosellar tumor in one (Case 4).

Subfrontal Surgery. The other three patients (Cases 3, 6, and 7) were operated on by a subfrontal route, with subtotal removal in all. As shown in Table 2, the results were generally good, especially considering the type and extent of the tumors. One patient, however, had to undergo a second operation after 8 months because of regrowth of the basal portion of the tumor, which had caused bilateral ophthalmoplegia and cerebrospinal fluid (CSF) rhinorrhea. It is noteworthy that this patient had not accepted the offer of postoperative radiotherapy. Postoperative blood levels of PRL and of GH fell considerably but did not normalize in any cases. Two patients (Cases 3 and 6) were then given radiotherapy, and the levels were reduced still further but not to normal. The third patient (Case 7), already irradiated preoperatively, was treated with bromocriptine only, which further lowered but did not normalize the PRL level. The other two patients (Cases 3 and 6) are still receiving bromocriptine, with a resulting normalization of the PRL in one and near-normalization of the GH in the other. These two patients also received endocrine replacement therapy; the quality of their life has improved and is fair in one and good in the other after an average follow-up period of 5.1 years. A recent CT scan showed only tiny fragments of residual tumor in these two patients, in the laterosellar region in one and in the lateroretrosellar region in the other. On the other hand, the quality of life was poor 4 years after surgery in the patient operated on for giant invasive adenoma (Case 7). She has not been examined for the past 2 years.

Operative Complications

The only complication associated with the transsphenoidal route was an intraoperative CSF fistula in two patients, successfully closed during the same operation in one patient and at reoperation in the other. In the latter case, a carboxylate cement, previously used by others4 and ourselves,11 was employed for reconstruction of the floor of the sella turcica. The same cement proved useful in closure of the CSF fistula in Case 6 (Tables 1 and 2).

In the course of the subfrontal operation on the patient with the giant invasive adenoma (Case 7), the tumor-infiltrated right carotid artery ruptured, necessitating closure of the vessel. This aggravated the left hemiparesis that the patient already had before operation.

Discussion

From the reports of Guiot, et al.,14,15 and others,1,16,25–29 as well as from our own experience, it may be inferred that the difference between invasive and enclosed adenomas has nothing to do with size. We therefore do not think it matters that in some of our patients the enclosed/invasive classification was based on neuroradiological investigations done some time after the onset of symptoms. In any event, our experience suggests that most pituitary adenomas arising in puberty are or will become invasive. This point seems to be borne out by analysis of the experience of other workers,7,8,13,22 and does not appear to conflict with the experience of those who have found a higher percentage of enclosed adenomas in the pediatric age group.2,6,16,24 On sifting through the cases reported by authors who apparently disagree with this suggestion, we find that most of their patients were probably prepubertal or postpubertal, but not pubertal.

Our experience confirms the findings of other workers1,10,21,27 that an invasive adenoma may have a very rapid or very long history, but is subject at any time to sudden worsening of symptoms with acute reduction of visual acuity and/or ophthalmoplegia. It is therefore clear that, in tumors with these biological characteristics, surgical intervention must be the first step in treatment. We think that this applies even in adenomas secreting PRL and/or GH, which respond to medical treatment with bromocriptine3,17 or lisuride,5,9 because, although medical treatment normalizes or lowers the blood levels of the overproduced hormones (especially of prolactin), its effectiveness in reducing the tumor mass has yet to be proved. Surgical intervention is especially important in invasive adenomas: a case was recently reported of cerebellar metastasis from an invasive prolactinoma during treatment with bromocriptine.20

The choice of surgical approach took into account the size and extent of the tumor, as already stated by other authors.31 The transsphenoidal route proved to be effective in intrasellar and intrasphenoidal adenomas as well as in tumors with moderate suprasellar development. The subfrontal route also yielded broadly satisfactory results in two patients with invasive adenomas developing mainly above and along the sella and in one patient with giant adenoma.

Postoperative radiotherapy, whether with cobalt or with high-energy treatment using a linear accelerator, proved to be useful, without complications. In six out of eight patients, the plasma levels of the overproduced hormones underwent a further significant reduction but not normalization. Postoperative medical therapy with bromocriptine proved advantageous in all seven patients operated on for PRL- and/or GH-secreting adenoma, inducing normalization or further reduction of the hormone levels. Endocrine replacement therapy for hypopituitarism is being taken by six of our nine patients, and it is undoubtedly responsible in part for the currently satisfactory quality of life enjoyed by the majority of our patients. The outcome is normal in two, good in three, fair in three, and poor in one.

The generally encouraging results we have observed following the multidisciplinary treatment schedule presented in this paper might, if confirmed by other workers, constitute a valid therapeutic protocol for invasive adenomas with onset during puberty and, perhaps, for invasive adenomas in general.

Addendum

After this paper was submitted, another child was operated on. He was a 14-year-old boy, who for 1 year exhibited gigantism, polyphagia, diabetes insipidus and, for a few weeks, headache. His visual acuity was 6/10 on the left and 10/10 on the right. He had an upper bitemporal defect, and GH levels of 90 ng/ml. Pluridirectional tomography showed erosion of the floor of the sella turcica. Computerized tomography scanning and angiography revealed a sellar tumor with supraretrosellar extension. The patient was successfully operated on by a transsphenoidal approach, and the tumor was histologically classified as acidophilic. At the operation, we were able to observe the invasive behavior of the tumor, which had clearly infiltrated the perihypophyseal dura mater and the floor of the sella turcica.

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    Robert F: L'adénome hypophysaire dans l'acromégaliegigantisme. Étude macroscopique, histologique et ultrastructurale in Hardy JRobert FSomma Met al: Acromégalie-gigantisme. Neurochirurgie 19 (Suppl 2):1171721973Robert F: L'adénome hypophysaire dans l'acromégaliegigantisme. Étude macroscopique histologique et ultrastructurale in Hardy J Robert F Somma M et al: Acromégalie-gigantisme. Neurochirurgie 19 (Suppl 2):117–172 1973

  • 26.

    Robert F: Le prolactinome. Aspects pathologiques. Neurochirurgie 27 (Suppl 1):61731981Robert F: Le prolactinome. Aspects pathologiques. Neurochirurgie 27 (Suppl 1):61–73 1981

  • 27.

    Somma MLanthier A: Évaluation clinique et biologique post opératoire et résultats thérapeutiques in Hardy JRobert FSomma Met al: Acromégalie-gigantisme. Neurochirurgie 19 (Suppl 2):1011161973Somma M Lanthier A: Évaluation clinique et biologique post opératoire et résultats thérapeutiques in Hardy J Robert F Somma M et al: Acromégalie-gigantisme. Neurochirurgie 19 (Suppl 2):101–116 1973

  • 28.

    Vezina JL: Le prolactinome. Aspects radiologiques de la selle turcique. Neurochirurgie 27 (Suppl 1):19281981Vezina JL: Le prolactinome. Aspects radiologiques de la selle turcique. Neurochirurgie 27 (Suppl 1):19–28 1981

  • 29.

    Vezina JLMaltais R: La selle turcique dans l'acromégalie. Étude radiologique in Hardy JRobert FSomma Met al: Acromégalie-gigantisme. Neurochirurgie 19 (Suppl 2):35561973Vezina JL Maltais R: La selle turcique dans l'acromégalie. Étude radiologique in Hardy J Robert F Somma M et al: Acromégalie-gigantisme. Neurochirurgie 19 (Suppl 2):35–56 1973

  • 30.

    Werder EAGirard JZachmann Met al: Treatment of Cushing's disease in childhood by transsphenoidal resection of a pituitary microadenoma in: International Symposium on Pituitary MicroadenomasMilan1978. Milan: Universita de Milano1978 p 100 (Abstract)Werder EA Girard J Zachmann M et al: Treatment of Cushing's disease in childhood by transsphenoidal resection of a pituitary microadenoma in: International Symposium on Pituitary Microadenomas Milan 1978. Milan: Universita de Milano 1978 p 100 (Abstract)

  • 31.

    Wilson CBDempsey LC: Transsphenoidal microsurgical removal of 250 pituitary adenomas. J Neurosurg 48:13221978Wilson CB Dempsey LC: Transsphenoidal microsurgical removal of 250 pituitary adenomas. J Neurosurg 48:13–22 1978

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References

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Landolt AMWüthrich RFellmann H: Regression of pituitary prolactinoma after treatment with bromocriptine. Lancet 1:108210831979 (Letter)Landolt AM Wüthrich R Fellmann H: Regression of pituitary prolactinoma after treatment with bromocriptine. Lancet 1:1082–1083 1979 (Letter)

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Robert F: L'adénome hypophysaire dans l'acromégaliegigantisme. Étude macroscopique, histologique et ultrastructurale in Hardy JRobert FSomma Met al: Acromégalie-gigantisme. Neurochirurgie 19 (Suppl 2):1171721973Robert F: L'adénome hypophysaire dans l'acromégaliegigantisme. Étude macroscopique histologique et ultrastructurale in Hardy J Robert F Somma M et al: Acromégalie-gigantisme. Neurochirurgie 19 (Suppl 2):117–172 1973

26.

Robert F: Le prolactinome. Aspects pathologiques. Neurochirurgie 27 (Suppl 1):61731981Robert F: Le prolactinome. Aspects pathologiques. Neurochirurgie 27 (Suppl 1):61–73 1981

27.

Somma MLanthier A: Évaluation clinique et biologique post opératoire et résultats thérapeutiques in Hardy JRobert FSomma Met al: Acromégalie-gigantisme. Neurochirurgie 19 (Suppl 2):1011161973Somma M Lanthier A: Évaluation clinique et biologique post opératoire et résultats thérapeutiques in Hardy J Robert F Somma M et al: Acromégalie-gigantisme. Neurochirurgie 19 (Suppl 2):101–116 1973

28.

Vezina JL: Le prolactinome. Aspects radiologiques de la selle turcique. Neurochirurgie 27 (Suppl 1):19281981Vezina JL: Le prolactinome. Aspects radiologiques de la selle turcique. Neurochirurgie 27 (Suppl 1):19–28 1981

29.

Vezina JLMaltais R: La selle turcique dans l'acromégalie. Étude radiologique in Hardy JRobert FSomma Met al: Acromégalie-gigantisme. Neurochirurgie 19 (Suppl 2):35561973Vezina JL Maltais R: La selle turcique dans l'acromégalie. Étude radiologique in Hardy J Robert F Somma M et al: Acromégalie-gigantisme. Neurochirurgie 19 (Suppl 2):35–56 1973

30.

Werder EAGirard JZachmann Met al: Treatment of Cushing's disease in childhood by transsphenoidal resection of a pituitary microadenoma in: International Symposium on Pituitary MicroadenomasMilan1978. Milan: Universita de Milano1978 p 100 (Abstract)Werder EA Girard J Zachmann M et al: Treatment of Cushing's disease in childhood by transsphenoidal resection of a pituitary microadenoma in: International Symposium on Pituitary Microadenomas Milan 1978. Milan: Universita de Milano 1978 p 100 (Abstract)

31.

Wilson CBDempsey LC: Transsphenoidal microsurgical removal of 250 pituitary adenomas. J Neurosurg 48:13221978Wilson CB Dempsey LC: Transsphenoidal microsurgical removal of 250 pituitary adenomas. J Neurosurg 48:13–22 1978

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