Abstracts
The term Marine-Lenhart syndrome describes the association between Graves’ disease and autonomously functioning thyroid nodules (AFTN), such as toxic adenoma or toxic multinodular goiter. The two diseases may coexist or may be present at different moments in the same patient. In the literature, there are many reports on the development of Graves’ disease after radioiodine treatment for AFTN, but very little information may be found on the occurrence of AFTN after radioiodine therapy for Graves’ disease. We describe here the case of a female patient with Graves’ disease who was successfully treated with radioiodine for Graves’ disease, returning to normal thyroid function. Three years later, biochemical analysis and ultrasound examination identified a thyroid nodule that progressively increased in size. The 99mTc-pertechnetate scintigraphy showed avid uptake in the right lobule, which corresponded to a nodular lesion consistent with AFTN.
O termo “síndrome de Marine-Lenhart” descreve a associação da doença de Graves e nódulos tireoidianos de funcionamento autônomo (AFTN), como no adenoma tóxico ou bócio multinodular tóxico. As duas doenças podem coexistir ou podem estar presentes em diferentes momentos no mesmo paciente. Na literatura, existem muitos relatos sobre o desenvolvimento da doença de Graves após radioiodoterapia para AFTN, mas muito poucos dados podem ser encontrados em relação ao aparecimento de AFTN após radioiodoterapia para doença de Graves. Descrevemos o caso de uma paciente do sexo feminino com doença de Graves que realizou com sucesso o tratamento com iodo radioativo, com a normalização da função da tireoide. Três anos depois, uma análise bioquímica e um exame de ultrassonografia identificaram o aparecimento de um nódulo na tireoide que progressivamente aumentou de tamanho. A cintilografia com 99mTc-pertecnetato revelou uma captação ávida no lóbulo direito, correspondente à lesão nodular, consistente com uma AFTN.
INTRODUCTION
Graves’ disease and autonomously-functioning thyroid nodules (AFTN) both cause
thyrotoxicosis by different pathophysiological mechanisms (11 Kahaly GJ, Bartalena L, Hegedüs L. The American Thyroid
Association/American Association of Clinical Endocrinologists guidelines for
hyperthyroidism and other causes of thyrotoxicosis: an European perspective. Thyroid.
2011;21:585-91.,22 Krohn K, Paschke R. Progress in understanding the etiology of thyroid
autonomy. J Clin Endocrinol Metab. 2001;86:3336-45.). The coexistence of both diseases has
been termed “Marine-Lenhart syndrome”. Since the first description in 1911 by Marine and
Lenhart (33 Marine D, Lenhart CH. Pathological anatomy of exophthalmic goiter. Arch
Intern Med. 1911;8:265-316.), the presence of focal autonomy in
patients with Graves’ disease has been reported by numerous authors, and with different
presentations (44 Charkes ND. Graves’ disease with functioning nodules (Marine-Lenhart
syndrome). J Nucl Med. 1972;13:885-92.
5 Nishikawa M, Yoshimura M, Yoshikawa N, Toyoda N, Yonemoto T, Ogawa Y, et
al. Coexistence of an autonomously functioning thyroid nodule in a patient with Graves’
disease: an unusual presentation of Marine-Lenhart syndrome. Endocr J.
1997;44(4):571-4.
6 Waldherr C, Otte A, Haldemann A, Müller-Brand J. Marine-Lenhart syndrome:
a case observation upon 18 years. Nuklearmedizin. 1999;38(8):345-8.
7 Braga-Basaria M, Basaria S. Marine-Lenhart syndrome. Thyroid.
2003;13:991.
8 El-Kaissi S, Kotowicz MA, Goodear M, Wall JR. An unusual case of
Marine-Lenhart syndrome. Thyroid. 2003;13:993-4.
9 Paunkovic N, Paunkovic J. Associated Graves’ disease and Plummer disease.
Hellenic J Nucl Med. 2003;6:44-7.
10 Cakir M. Marine-Lenhart syndrome. J Natl Med Assoc.
2005;97:1036-8.
11 Chatzopoulos D, Iakovou I, Moralidis E. Images in thyroidology:
Marine-Lenhart syndrome and radioiodine-131 treatment. Thyroid.
2007;17:373-4.
12 Brahma A, Beadsmoore C, Dhatariya K. The oldest case of Marine-Lenhart
syndrome? JRSM Short Rep. 2012;3:21.
13 Damle N, Mishra R. Identifying Marine-Lenhart syndrome on a
99mTc-pertechnetate thyroid scan. Indian J Endocrinol Metab.
2013;17(2):366.-1414 Scherer T, Wohlschlaeger-Krenn E, Bayerle-Eder M, Passler C, Reiner-Concin
A, Krebs M, et al. A case of simultaneous occurrence of Marine-Lenhart syndrome and a
papillary thyroid microcarcinoma. BMC Endocrine Disorders. 2013;13:16.), with an overall prevalence of such association ranging from 2.7% to 4.1%
(44 Charkes ND. Graves’ disease with functioning nodules (Marine-Lenhart
syndrome). J Nucl Med. 1972;13:885-92.). Moreover, during the last years, several papers
have been published on the development of Graves’ disease shortly after radioiodine therapy
for AFTNs (1515 Chiovato L, Santini F, Vitti P, Bendinelli G, Pinchera A. Appearance of
thyroid stimulating antibody and Graves’ disease after radioiodine therapy for toxic
nodular goiter. Clin Endocrinol (Oxf). 1994;40:803-6.
16 Schmidt M, Gorbauch E, Dietlein M, Faust M, Stützer H, Eschner W, et al.
Incidence of postradioiodine immunogenic hyperthyroidism/Graves’ disease in relation to a
temporary increase in thyrotropin receptor antibodies after radioiodine therapy for
autonomous thyroid disease. Thyroid. 2006;16:281-8.
17 Boddenberg B, Voth E, Schicha H. Immunogenic hyperthyroidism following
radioiodine ablation of a focal autonomy. Nuklearmedizin. 1993;32:18-22.-1818 Custro N, Ganci A, Scafidi V. Relapses of hyperthyroidism in patients
treated with radioiodine for nodular toxic goiter: relation to thyroid autoimmunity. J
Endocrinol Invest. 2003;26:106-10.). The incidence of this event is significantly higher, especially in patients
with elevated serum thyroid peroxidase antibodies (TPO-Ab) levels at baseline (1515 Chiovato L, Santini F, Vitti P, Bendinelli G, Pinchera A. Appearance of
thyroid stimulating antibody and Graves’ disease after radioiodine therapy for toxic
nodular goiter. Clin Endocrinol (Oxf). 1994;40:803-6.,1616 Schmidt M, Gorbauch E, Dietlein M, Faust M, Stützer H, Eschner W, et al.
Incidence of postradioiodine immunogenic hyperthyroidism/Graves’ disease in relation to a
temporary increase in thyrotropin receptor antibodies after radioiodine therapy for
autonomous thyroid disease. Thyroid. 2006;16:281-8.), as well as
in patients TPOAb-negative at baseline who became TPOAb-positive after treatment (1717 Boddenberg B, Voth E, Schicha H. Immunogenic hyperthyroidism following
radioiodine ablation of a focal autonomy. Nuklearmedizin. 1993;32:18-22.,1818 Custro N, Ganci A, Scafidi V. Relapses of hyperthyroidism in patients
treated with radioiodine for nodular toxic goiter: relation to thyroid autoimmunity. J
Endocrinol Invest. 2003;26:106-10.).
Here, we report an unusual case of Marine-Lenhart syndrome, in which an AFTN developed after radioiodine therapy for Graves’ disease.
CASE REPORT
A 42-year-old woman came to our outpatient clinic in December 2008 because of fatigue,
palpitations, tremors, nervousness and irritability, insomnia, oligo-amenorrhea, sweating,
and weight loss for three months. Graves’ disease was diagnosed based on clinical
symptoms/signs, a TSH level of < 0.001 mIU/L (normal values, 0.27-4.2) with elevated free
triiodothyronine (FT3, 17.39 pg/mL, n.v. 2-4.4) and free thyroxine (FT4, 38.3 pmol/L; n.v.
12-22), and positivity for TSH receptor antibodies (TRAb, 19 IU/L, n.v. < 1.5), as well
as thyroid peroxidase antibodies (TPOAb, 158 U/L; n.v. < 35). Thyroid ultrasound (US)
examination showed a diffuse enlargement of the gland, associated with hypoechogenicity and
increased vascularity. The 131I thyroid scan revealed an enlarged gland with
diffuse increased uptake of radioiodine at 6 and 24 hours (Figure 1). Therapy with methimazole (MMI, 30 mg/day) was started, and the patient
was referred for radioactive iodine treatment (RIT) in March 2009. Within six weeks from
RIT, her thyroid function tests normalized with TSH of 1.64 mIU/L and FT4 of 16 pm/L. TPO-Ab
were 364 UI/L. Six months later, thyroid US examination showed a 7-mm hypoechoic nodule with
regular margins and an increased intranodular blood flow in color-Doppler in the upper
portion of the right lobe. Over the next 18 months, the nodule increased in size up to a
maximum diameter of 12 mm (Figure 2). Changes in serum
TSH levels during the follow-up after radioiodine treatment are shown in figure 3. In the last evaluation, serum TSH was low-normal
(0.67 mIU/L) with normal levels of FT3 and FT4. TRAb were negative.
99mTc-Pertechnetate scintigraphy revealed an avid tracer uptake in the right
lobe, corresponding to the nodular lesion demonstrated by US, consistently with an AFTN
(Figure 4). Thus, our patient developed an AFTN
three years after the onset of hyperthyroidism due to Graves’ disease that was successfully
treated with radioiodine. Looking at the pertinent literature (1515 Chiovato L, Santini F, Vitti P, Bendinelli G, Pinchera A. Appearance of
thyroid stimulating antibody and Graves’ disease after radioiodine therapy for toxic
nodular goiter. Clin Endocrinol (Oxf). 1994;40:803-6.
16 Schmidt M, Gorbauch E, Dietlein M, Faust M, Stützer H, Eschner W, et al.
Incidence of postradioiodine immunogenic hyperthyroidism/Graves’ disease in relation to a
temporary increase in thyrotropin receptor antibodies after radioiodine therapy for
autonomous thyroid disease. Thyroid. 2006;16:281-8.
17 Boddenberg B, Voth E, Schicha H. Immunogenic hyperthyroidism following
radioiodine ablation of a focal autonomy. Nuklearmedizin. 1993;32:18-22.-1818 Custro N, Ganci A, Scafidi V. Relapses of hyperthyroidism in patients
treated with radioiodine for nodular toxic goiter: relation to thyroid autoimmunity. J
Endocrinol Invest. 2003;26:106-10.), we present our case as a
variant of classic Marine-Lenhart syndrome. When the “hot” nodule was discovered, there was
no diffuse increase in radiotracer uptake by the gland and TRAb were negative, because
hyperthyroidism due to Graves’ disease – diagnosed three years before – was successfully
cured by radioiodine. On the other hand, the two diseases developed in the same individual
and there was a close temporal relationship between radioiodine treatment of Graves’ disease
and the occurrence of the “hot” thyroid nodule.
The 131I thyroid scan revealed an enlarged gland with diffuse, increased uptake of radioiodine at 6 (left panel) and 24 (right panel) hours.
Ultrasonographic appearance of a hypoechoic nodule with regular margins in the upper portion of the right lobe: over 18 months, it increased in size from 7 mm originally to a maximum diameter of about 12 mm.
99mTc-Pertechnetate thyroid scintigraphy revealed an avid tracer uptake in the right lobe, corresponding to the nodular lesion demonstrated by the US consistent with an AFTN.
DISCUSSION
Coexistence of Graves’ disease and AFTN was first described by Marine and Lenhart, in a
study about thyroid histopathology and iodine content in exophthalmic goiter (33 Marine D, Lenhart CH. Pathological anatomy of exophthalmic goiter. Arch
Intern Med. 1911;8:265-316.). Additional reports followed, and most of these
articles describe only one or few patients (44 Charkes ND. Graves’ disease with functioning nodules (Marine-Lenhart
syndrome). J Nucl Med. 1972;13:885-92.
5 Nishikawa M, Yoshimura M, Yoshikawa N, Toyoda N, Yonemoto T, Ogawa Y, et
al. Coexistence of an autonomously functioning thyroid nodule in a patient with Graves’
disease: an unusual presentation of Marine-Lenhart syndrome. Endocr J.
1997;44(4):571-4.
6 Waldherr C, Otte A, Haldemann A, Müller-Brand J. Marine-Lenhart syndrome:
a case observation upon 18 years. Nuklearmedizin. 1999;38(8):345-8.
7 Braga-Basaria M, Basaria S. Marine-Lenhart syndrome. Thyroid.
2003;13:991.
8 El-Kaissi S, Kotowicz MA, Goodear M, Wall JR. An unusual case of
Marine-Lenhart syndrome. Thyroid. 2003;13:993-4.
9 Paunkovic N, Paunkovic J. Associated Graves’ disease and Plummer disease.
Hellenic J Nucl Med. 2003;6:44-7.
10 Cakir M. Marine-Lenhart syndrome. J Natl Med Assoc.
2005;97:1036-8.
11 Chatzopoulos D, Iakovou I, Moralidis E. Images in thyroidology:
Marine-Lenhart syndrome and radioiodine-131 treatment. Thyroid.
2007;17:373-4.
12 Brahma A, Beadsmoore C, Dhatariya K. The oldest case of Marine-Lenhart
syndrome? JRSM Short Rep. 2012;3:21.
13 Damle N, Mishra R. Identifying Marine-Lenhart syndrome on a
99mTc-pertechnetate thyroid scan. Indian J Endocrinol Metab.
2013;17(2):366.-1414 Scherer T, Wohlschlaeger-Krenn E, Bayerle-Eder M, Passler C, Reiner-Concin
A, Krebs M, et al. A case of simultaneous occurrence of Marine-Lenhart syndrome and a
papillary thyroid microcarcinoma. BMC Endocrine Disorders. 2013;13:16.). The overall prevalence of such association was
reported between 2.7% to 4.1% (44 Charkes ND. Graves’ disease with functioning nodules (Marine-Lenhart
syndrome). J Nucl Med. 1972;13:885-92.). Different
mechanisms are implicated in the pathogenesis of Graves’ disease and in the nodular
formation of thyroid tissue with functional autonomy. Graves’ disease is caused by an
autoimmune process that involves the whole thyroid gland and is characterized by the
presence of stimulating TSH receptor antibodies (11 Kahaly GJ, Bartalena L, Hegedüs L. The American Thyroid
Association/American Association of Clinical Endocrinologists guidelines for
hyperthyroidism and other causes of thyrotoxicosis: an European perspective. Thyroid.
2011;21:585-91.).
AFTNs are clonal in origin and virtually independent from TSH for growth and function (22 Krohn K, Paschke R. Progress in understanding the etiology of thyroid
autonomy. J Clin Endocrinol Metab. 2001;86:3336-45.). When a thyroid nodule is recorded in the context of
Graves’ disease, it is assumed to be scintigraphically “cold”. As it emerges from some data
in the literature, a nodular variant of Graves’ disease can be defined as Marine-Lenhart
syndrome when the following criteria are met: (i) the thyroid scan shows an enlarged gland
and one or more poorly functioning nodules; (ii) the nodule is TSH-dependent and the
peri-nodular tissue is TSH-independent; (iii) after endogenous or exogenous TSH stimulation,
the return of function can be demonstrated in the nodule; and (iv) the nodule is
histologically benign (44 Charkes ND. Graves’ disease with functioning nodules (Marine-Lenhart
syndrome). J Nucl Med. 1972;13:885-92.). In this case, if one or
more autonomous nodules are present in the context of Graves’ disease, they are suppressed
by the over-activity of the remaining gland and, therefore, there is no radioiodine uptake.
Once the most part of the gland has been treated with oral medication or radioiodine and, as
a consequence, has become progressively less active, the nodules increase their activity in
a TSH-dependent way (1111 Chatzopoulos D, Iakovou I, Moralidis E. Images in thyroidology:
Marine-Lenhart syndrome and radioiodine-131 treatment. Thyroid.
2007;17:373-4.). In a unifying pathogenetic
hypothesis, it has also been proposed that autoimmunity, such as presence, intrinsic
function and concentration of TRAb may influence the preferential development of diffuse or
nodular follicular hyperplasia (1919 Studer H, Huber G, Derwahl M, Frey P. Die Umwandlung von Basedowstrumen in
Knotenkroepfe. Schweiz Med Wochenschr. 1989;119:203-8.), and further
enhance nodules activity (2020 Poertl S, Kirner J, Saller B, Mann K, Hoermann R. T3-release from
autonomously functioning thyroid nodules in vitro. Exp Clin Endocrinol Diabetes.
1998;106:489-93.). But several authors
believe that Marine-Lenhart syndrome may be due to different pathological mechanisms that
occur independently of each other in the same patients, without any relationship between
TRAb positivity, and nodular growth and/or function (2121 Biersack HJ, Biermann K. The Marine-Lenhart syndrome revisited. Wien Klin
Wochenschr. 2011;123:459-62.). Therefore, the diagnosis of Marine-Lenhart syndrome remains difficult to be
determined, and the simultaneous occurrence of the two diseases is still matter of debate
(2121 Biersack HJ, Biermann K. The Marine-Lenhart syndrome revisited. Wien Klin
Wochenschr. 2011;123:459-62.,2222 Cakir M. Diagnosis of Marine-Lenhart syndrome. Letter to the Editor.
Thyroid. 2004;14:555.). As
it occurred in some case reports (77 Braga-Basaria M, Basaria S. Marine-Lenhart syndrome. Thyroid.
2003;13:991.,88 El-Kaissi S, Kotowicz MA, Goodear M, Wall JR. An unusual case of
Marine-Lenhart syndrome. Thyroid. 2003;13:993-4.,2222 Cakir M. Diagnosis of Marine-Lenhart syndrome. Letter to the Editor.
Thyroid. 2004;14:555.), there has
been also controversy regarding how to diagnose Marine-Lenhart syndrome, depending on which
imaging techniques have been used to identify the thyroid nodule. In fact, although
palpation is highly suggestive, it needs confirmation by ultrasonography, in order to
exclude an asymmetrical enlargement of one lobe that may give the false sensation of a
nodular lesion (2323 Wiest PW, Hartshorne MF, Inskip PD, Crooks LA, Vela BS, Telepak RJ, et al.
Thyroid palpation versus high-resolution thyroid ultrasonography in the detection of
nodules. J Ultrasound Med. 1998;17:487-96.). Moreover, although there is
ultrasound detection, it is necessary to determine nodule uptake in a thyroid scan. In most
cases, a 99mTc-pertechnetate thyroid scan enables the identification of focal
abnormal uptake of the tracer, corresponding to the AFTN, even in the context of a diffuse,
intense uptake by the gland (77 Braga-Basaria M, Basaria S. Marine-Lenhart syndrome. Thyroid.
2003;13:991.
8 El-Kaissi S, Kotowicz MA, Goodear M, Wall JR. An unusual case of
Marine-Lenhart syndrome. Thyroid. 2003;13:993-4.
9 Paunkovic N, Paunkovic J. Associated Graves’ disease and Plummer disease.
Hellenic J Nucl Med. 2003;6:44-7.
10 Cakir M. Marine-Lenhart syndrome. J Natl Med Assoc.
2005;97:1036-8.
11 Chatzopoulos D, Iakovou I, Moralidis E. Images in thyroidology:
Marine-Lenhart syndrome and radioiodine-131 treatment. Thyroid.
2007;17:373-4.
12 Brahma A, Beadsmoore C, Dhatariya K. The oldest case of Marine-Lenhart
syndrome? JRSM Short Rep. 2012;3:21.
13 Damle N, Mishra R. Identifying Marine-Lenhart syndrome on a
99mTc-pertechnetate thyroid scan. Indian J Endocrinol Metab.
2013;17(2):366.-1414 Scherer T, Wohlschlaeger-Krenn E, Bayerle-Eder M, Passler C, Reiner-Concin
A, Krebs M, et al. A case of simultaneous occurrence of Marine-Lenhart syndrome and a
papillary thyroid microcarcinoma. BMC Endocrine Disorders. 2013;13:16.).
Besides the coexistence of thyroid autonomy (Plummer’s disease) and Graves’ disease, which
is sometimes questionable (2121 Biersack HJ, Biermann K. The Marine-Lenhart syndrome revisited. Wien Klin
Wochenschr. 2011;123:459-62.,2222 Cakir M. Diagnosis of Marine-Lenhart syndrome. Letter to the Editor.
Thyroid. 2004;14:555.), it is also possible that the two diseases may occur in the same
patient years apart. There is literature on the risk that Graves-like hyperthyroidism may
develop after radioiodine treatment in patients with elevated serum TPO-Ab levels at
baseline (1515 Chiovato L, Santini F, Vitti P, Bendinelli G, Pinchera A. Appearance of
thyroid stimulating antibody and Graves’ disease after radioiodine therapy for toxic
nodular goiter. Clin Endocrinol (Oxf). 1994;40:803-6.,1616 Schmidt M, Gorbauch E, Dietlein M, Faust M, Stützer H, Eschner W, et al.
Incidence of postradioiodine immunogenic hyperthyroidism/Graves’ disease in relation to a
temporary increase in thyrotropin receptor antibodies after radioiodine therapy for
autonomous thyroid disease. Thyroid. 2006;16:281-8.), as well as in TPOAb-negative patients at baseline who became TPOAb-positive
after treatment (1717 Boddenberg B, Voth E, Schicha H. Immunogenic hyperthyroidism following
radioiodine ablation of a focal autonomy. Nuklearmedizin. 1993;32:18-22.,1818 Custro N, Ganci A, Scafidi V. Relapses of hyperthyroidism in patients
treated with radioiodine for nodular toxic goiter: relation to thyroid autoimmunity. J
Endocrinol Invest. 2003;26:106-10.). Therefore, it could be hypothesized that, in a subject genetically
susceptible to thyroid autoimmunity, follicular cell damage caused by radioiodine could
trigger an autoimmune response against TSH receptors, thus explaining the occurrence of
Graves’ disease after radioiodine therapy (1515 Chiovato L, Santini F, Vitti P, Bendinelli G, Pinchera A. Appearance of
thyroid stimulating antibody and Graves’ disease after radioiodine therapy for toxic
nodular goiter. Clin Endocrinol (Oxf). 1994;40:803-6.
16 Schmidt M, Gorbauch E, Dietlein M, Faust M, Stützer H, Eschner W, et al.
Incidence of postradioiodine immunogenic hyperthyroidism/Graves’ disease in relation to a
temporary increase in thyrotropin receptor antibodies after radioiodine therapy for
autonomous thyroid disease. Thyroid. 2006;16:281-8.
17 Boddenberg B, Voth E, Schicha H. Immunogenic hyperthyroidism following
radioiodine ablation of a focal autonomy. Nuklearmedizin. 1993;32:18-22.-1818 Custro N, Ganci A, Scafidi V. Relapses of hyperthyroidism in patients
treated with radioiodine for nodular toxic goiter: relation to thyroid autoimmunity. J
Endocrinol Invest. 2003;26:106-10.). Unlike most cases reported in the literature, our
particular case of Marine-Lenhart syndrome shows the appearance of an AFTN as a consequence
of Graves’ disease treatment with radioiodine. First, Waldherr and cols. described a
46-year-old woman who developed AFTNs within 13 years of radioiodine treatment for Graves’
disease, with strongly positive thyroid antibodies. The authors suggested that the
autonomous nodules were a consequence of Graves’ disease treatment with radioiodine (66 Waldherr C, Otte A, Haldemann A, Müller-Brand J. Marine-Lenhart syndrome:
a case observation upon 18 years. Nuklearmedizin. 1999;38(8):345-8.). Similarly, our patient developed an AFTN three years
after the onset of a hyperthyroidism due to Graves’ disease successfully treated with
radioiodine. A 99mTc thyroid scan showed an area of increased focal uptake in the
right lobe, corresponding to the palpable nodule, and the existence of the nodule was
confirmed by thyroid ultrasonography. The nodule developed in the context of the thyroid
gland few months after the radioiodine treatment had been performed, as TSH level started to
rise.
In conclusion, the possibility of an association between autoimmune thyroid diseases, namely Graves’ disease, and AFTN emerges from several data in the literature (44 Charkes ND. Graves’ disease with functioning nodules (Marine-Lenhart syndrome). J Nucl Med. 1972;13:885-92.,2424 Ruggeri RM, Campennì A, Sindoni A, Baldari S, Trimarchi F, Benvenga S. Association of autonomously functioning thyroid nodules with Hashimoto’s thyroiditis: study on a large series of patients. Exp Clin Endocrinol Diabetes. 2011;119:621-7.). The most intriguing and interesting aspect of this association is represented not so much by the co-existence of the two diseases, often not easy to ascertain, as by the possibility that they can develop in the same patient over a lifetime. Clinicians should be aware of such a possibility, especially in those patients who are candidate to radioiodine treatment.
REFERENCES
-
1Kahaly GJ, Bartalena L, Hegedüs L. The American Thyroid Association/American Association of Clinical Endocrinologists guidelines for hyperthyroidism and other causes of thyrotoxicosis: an European perspective. Thyroid. 2011;21:585-91.
-
2Krohn K, Paschke R. Progress in understanding the etiology of thyroid autonomy. J Clin Endocrinol Metab. 2001;86:3336-45.
-
3Marine D, Lenhart CH. Pathological anatomy of exophthalmic goiter. Arch Intern Med. 1911;8:265-316.
-
4Charkes ND. Graves’ disease with functioning nodules (Marine-Lenhart syndrome). J Nucl Med. 1972;13:885-92.
-
5Nishikawa M, Yoshimura M, Yoshikawa N, Toyoda N, Yonemoto T, Ogawa Y, et al. Coexistence of an autonomously functioning thyroid nodule in a patient with Graves’ disease: an unusual presentation of Marine-Lenhart syndrome. Endocr J. 1997;44(4):571-4.
-
6Waldherr C, Otte A, Haldemann A, Müller-Brand J. Marine-Lenhart syndrome: a case observation upon 18 years. Nuklearmedizin. 1999;38(8):345-8.
-
7Braga-Basaria M, Basaria S. Marine-Lenhart syndrome. Thyroid. 2003;13:991.
-
8El-Kaissi S, Kotowicz MA, Goodear M, Wall JR. An unusual case of Marine-Lenhart syndrome. Thyroid. 2003;13:993-4.
-
9Paunkovic N, Paunkovic J. Associated Graves’ disease and Plummer disease. Hellenic J Nucl Med. 2003;6:44-7.
-
10Cakir M. Marine-Lenhart syndrome. J Natl Med Assoc. 2005;97:1036-8.
-
11Chatzopoulos D, Iakovou I, Moralidis E. Images in thyroidology: Marine-Lenhart syndrome and radioiodine-131 treatment. Thyroid. 2007;17:373-4.
-
12Brahma A, Beadsmoore C, Dhatariya K. The oldest case of Marine-Lenhart syndrome? JRSM Short Rep. 2012;3:21.
-
13Damle N, Mishra R. Identifying Marine-Lenhart syndrome on a 99mTc-pertechnetate thyroid scan. Indian J Endocrinol Metab. 2013;17(2):366.
-
14Scherer T, Wohlschlaeger-Krenn E, Bayerle-Eder M, Passler C, Reiner-Concin A, Krebs M, et al. A case of simultaneous occurrence of Marine-Lenhart syndrome and a papillary thyroid microcarcinoma. BMC Endocrine Disorders. 2013;13:16.
-
15Chiovato L, Santini F, Vitti P, Bendinelli G, Pinchera A. Appearance of thyroid stimulating antibody and Graves’ disease after radioiodine therapy for toxic nodular goiter. Clin Endocrinol (Oxf). 1994;40:803-6.
-
16Schmidt M, Gorbauch E, Dietlein M, Faust M, Stützer H, Eschner W, et al. Incidence of postradioiodine immunogenic hyperthyroidism/Graves’ disease in relation to a temporary increase in thyrotropin receptor antibodies after radioiodine therapy for autonomous thyroid disease. Thyroid. 2006;16:281-8.
-
17Boddenberg B, Voth E, Schicha H. Immunogenic hyperthyroidism following radioiodine ablation of a focal autonomy. Nuklearmedizin. 1993;32:18-22.
-
18Custro N, Ganci A, Scafidi V. Relapses of hyperthyroidism in patients treated with radioiodine for nodular toxic goiter: relation to thyroid autoimmunity. J Endocrinol Invest. 2003;26:106-10.
-
19Studer H, Huber G, Derwahl M, Frey P. Die Umwandlung von Basedowstrumen in Knotenkroepfe. Schweiz Med Wochenschr. 1989;119:203-8.
-
20Poertl S, Kirner J, Saller B, Mann K, Hoermann R. T3-release from autonomously functioning thyroid nodules in vitro. Exp Clin Endocrinol Diabetes. 1998;106:489-93.
-
21Biersack HJ, Biermann K. The Marine-Lenhart syndrome revisited. Wien Klin Wochenschr. 2011;123:459-62.
-
22Cakir M. Diagnosis of Marine-Lenhart syndrome. Letter to the Editor. Thyroid. 2004;14:555.
-
23Wiest PW, Hartshorne MF, Inskip PD, Crooks LA, Vela BS, Telepak RJ, et al. Thyroid palpation versus high-resolution thyroid ultrasonography in the detection of nodules. J Ultrasound Med. 1998;17:487-96.
-
24Ruggeri RM, Campennì A, Sindoni A, Baldari S, Trimarchi F, Benvenga S. Association of autonomously functioning thyroid nodules with Hashimoto’s thyroiditis: study on a large series of patients. Exp Clin Endocrinol Diabetes. 2011;119:621-7.
-
Funding: this study was not supported by any grant.
Publication Dates
-
Publication in this collection
June 2014
History
-
Received
10 Dec 2013 -
Accepted
03 Mar 2014