December 5, 2003

Renaming papillary microcarcinoma of the thyroid gland: The Porto proposal

The 12th Annual Cancer Meeting held at the Institute of Molecular Pathology and Immunology of the University of Porto (IPATIMUP), Porto, Portugal, on March 3-5, 2003, was devoted to carcinomas of thyroid follicular cells. During the course of 3 days, a group of basic scientists, pathologists, and clinicians interested in thyroid neoplasia exchanged views about several important aspects of the biology, pathology, and behavior of these tumors. One of the items was the thyroid neoplasm that is currently designated as papillary microcarcinoma. Pollowing a general discussion on the subject and the conclusion that a change in terminology ought to be considered, a working group composed of the 4 individuals listed as authors of this article met for the purpose of exploring the issue in more detail. A consensus was reached by the group to propose a new term for the entity. We would like to present to our fellow pathologists and to the medical community at large the rationale behind our choice, which we refer to as"the Porto proposal."

Papillary carcinoma is the most common malignant tumor of the thyroid gland. In addition to the clinically detectable cases, the size of which ranges widely, there is a variant currently designated papillary marocamMOWza (PMiC), which has been defined as a papillary carcinoma measuring 1 cm or less in diameter [1,2]. This variant, also known as occult papillary carcinoma, latent papillary carcinoma, small papillary carcinoma, nonencapsulaled thyroid tumor, and occult sclerosing carcinoma [3,4], is an extremely common condition, to the point of having been regarded as "a normal finding" [5]. It practically always represents an incidental finding at autopsy or in thyroid glands removed for other reasons. Its prevalence in the various systematic autopsy studies that have been carried out has ranged between 5.6% and 35.6% [5-10]. The latter figure is from Finland and is based on a detailed study of 101 cases [5]. The authors of that paper estimated that if serial sections of the glands had been taken, the total number of detected tumors would have been no less than 308. These studies have also shown that the prevalence of this tumor increases steeply from birth to adulthood and that it remains relatively constant afterward. When coupled with the known marked differences in incidence that exist between PMiC and clinically detectable papillary carcinoma, this observation suggests that most PMiCs develop in adolescence and young adulthood and that they tend to remain stable afterward, in the sense of growing at a similar rate to the normal gland, unless an additional event were to occur causing the tumor to speed up its rate of growth and become clinically apparent. Taking into account the frequency of PMiC and the rarity of clinically significant papillary carcinoma, the chance of this additional event taking place is obviously very low.

The fact that PMiC shares architectural, cytologic, immunohistochemical, and behavioral features with its larger counterpart has been well documented. In particular, it has been demonstrated that it has the capability to spread to the regional lymph nodes and that under exceptional circumstances it can even metastasize to distant sites [II]. These very rare cases, however, generally precent with metastases. In the case of tumors discovered incidentally, the chances of later metastases developing are extremely low. Indeed, it has been repeatedly demonstrated that under these circumstances the overwhelming majority of these tumors are of no clinical significance. As a corollary, the conclusion has been reached by several groups that no additional therapy is necessary if a PMiC is detected incidentally in a thyroid gland [12,13]. We fully agree with this recommendation and have often made it ourselves in cases that have been sent to us in consultation. However, we are conscious of the fact that the use of the term carcmowza in a pathology report sends to both surgeon and patient a message with a considerable therapeutic, prognostic, psychologic, and financial impact, and we are also aware that these implications are not necessarily tempered by whatever qualifiers and comments one may choose to include in the report. As a result, whenever the diagnosis of PMiC is made, the definite possibility exists that the repercussions of this diagnosis will be far greater that those justified by the biologic potential of the neoplasm. The proposal was therefore discussed at the Porto meeting to rename this entity in a way that would avoid these potential untoward effects while still accurately reflecting its nature. After considering and discarding several alternatives, the term papillary microtumor (PMiT) was chosen, since it was felt that it was the one coming closer to the fulfillment of these requirements. To wit, it indicates the fact that the lesion is of small size, that it is a neoplastic process (remaining purposefully noncommittal about its malignant potential, because while the tumor may show microscopic local invasion, it is clinically benign), and that it belongs to the papillary family of neoplasms.

It should be emphasized that this proposed change in terminology was specifically discussed in connection with the most common situation, i.e., that of a single focus of papillary carcinoma measuring 1. Patient's age. The recommendation made in this document excludes tumors detected in children and adolescents under the age of 19 years. As pointed out in this journal some years ago in a Guest Editorial written by the Chernobyl Pathologists Group (which included 2 of the authors of the current paper) [14], a significant number of papillary carcinomas with a diameter of less than 1 cm in diameter occurring in this age group show direct extrathyroidal invasion and are associated with distant metastases. It was therefore suggested in that document that the term papillary microcarcinoma (here replaced by PMiT) be employed only for adult patients and that papillary neoplasms occurring in children be designated as papillary carcinomas regardless of size until a study has been carried out in them correlating size and other features to prognosis. We agree with this recommendation, and add that the age limit we have arbitrarily adopted (under 19 years) should be reviewed when further information on adolescents becomes available.

2. Number of tumors. Whenever 2 or more lesions with the appearance of PMiT are detected, the possibility must be considered that they represent intrathyroid spread from a separate primary thyroid carcinoma. If no such primary can be found and the lesions are morphologically typical of PMiT, a diagnosis of multicentric PMiT can be made. More evidence is needed on the appropriate diagnosis and management of cases where 2 or more lesions are present, each individually less than 1 centimeter in diameter, but greater than 1 centimeter when taken together; until such evidence is available, it would be safer not to use the term PMiT under these circumstances.

3. Unusual microscopic appearances. The proposal here outlined applies to the typical case of PMiT and excludes-for the time being and until further information is obtained-those rare instances in which the tumor has features that may be indicative of a potential for an aggressive behavior. This includes cases accompanied by invasion of the thyroid capsule, blood vessel permeation, or tall cell features [15].

4. PMiTs occurring within a benign lesion. Occasionally, lesions fulfilling the criteria for PMiT are found entirely confined within benign thyroid nodules having otherwise typical features of follicular adenoma or hyperplastic (adenomatoid) nodule. It is proposed that these lesions be designated as "PMiT within . . .". This term should be reserved for those cases in which the PMiT appears as a sharply outlined focus within the benign nodule, rather than the more common situation in which ill-defined multiple areas of nuclear clearing are encountered, the significance of which is beyond the scope of this communication.

5. PMiT found at ultrasound, computed tomography, or magnetic resonance imaging. If a papillary carcinoma of less than 1 cm diameter is found incidentally at radiologie examination performed for some other reason, we believe that it should still be classified as PMiT. Conversely, if the tumor were to be found in the course of an investigation carried out because of the presence or suspected presence of metastases, we do not recommend the use of the term.

We would be remiss if we failed to mention that 2 very similar proposals have been made in the past using the same reasoning and aiming at the same goals. Hazard et al. [3] proposed to designate this lesion as nonencapsulated thyroid tumor because "the surgeon may become unduly alarmed when the pathologist reports the presence of carcinoma." They added that "this may lead to reoperation, radical dissection of the neck or extensive irradiation, all of which are unnecessary and undesirable." Harach et al. [5] proposed the term occult papillary tumor "in order to avoid unnecessary operations an\d serious psychologic effects on patients." However, the tumors are not necessarily nonencapsulated, and are increasingly being found at ultrasound examination and therefore not always "occult." Semantics aside, it is hoped that the "Porto proposal" here presented, which is an elaboration and reaffirmation of those earlier recommendations, will be considered by the setters of tumor nomenclature in this field and ultimately accepted by the pathology community. It is our expectation that the adoption of this terminology will decrease the danger of overtreatment, minimize the psychologic anxiety engendered by a diagnosis of carcinoma, and maintain unchanged the patient's eligibility for life insurance. Needless to say, the pathologist should use discretion in applying the term to any tumor with unusual features. Furthermore, the renaming of this tumor as here proposed should not prevent the pathologist from reinforcing the message regarding the generally innocuous nature of PMiT in the form of a written or verbal comment to the clinician whenever such reinforcement is felt necessary.


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juan Rosai, MD,* Virginia A. LiVolsi, MD,[dagger] Manuel Sobrinho- Simoes, MD,[double dagger] and E. D. Williams, MD[sec]

From the * DepartmcnL of Pathology, National Cancer Institute, Milan, Italy; [dagger] Departmenl of Pathology, University of Pennsylvania Medical School; [double dagger] Medical Faculty of Porto and Institute of Molecular Pathology and Immunology of the University of Porto (IPATIMUP), Porto, Portugal; and the [sec]Thyroid Cardnogcnesis Group, Strangeways Research Laboratory, University of Cambridge, Cambridge, England.

Copyright Westminster Publications, Inc. Oct 2003