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Ann Thorac Surg 2000;70:327-334
© 2000 The Society of Thoracic Surgeons

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Special report

Myasthenia gravis: recommendations for clinical research standards¹

^a Department of Surgery, Columbia Presbyterian Medical Center, New York, New York, USA
^b Department of Neurology, University of Texas Southwestern Medical Center, Dallas, Texas, USA
^c Neurology Service, William Beaumont Hospital, Royal Oak, Michigan, USA
^d Departments of Neurology and Neurosciences, Case Western Reserve University, Department of Veterans Affairs Medical Center, University Hospitals of Cleveland, Cleveland, Ohio, USA
^e Department of Neurology, University of California at Los Angeles, Los Angeles, California, USA
^f National Institute for Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland, USA
^g Department of Medicine, Duke University Medical Center, Durham, North Carolina, USA

Address reprint requests to The Myasthenia Gravis Foundation of America, Inc, 123 West Madison, Suite 800, Chicago, IL 60602
e-mail: myastheniagravis{at}msn.com

The need for universally accepted classifications, grading systems, and methods of analysis for patients undergoing therapy for MG is widely recognized and is particularly needed for therapeutic research trials. The Medical Scientific Advisory Board (MSAB) of the Myasthenia Gravis Foundation of America (MGFA) formed a Task Force in May 1997 to address these issues. Initially, the Task Force planned to develop classifications and outcome measures pertaining only to standardizing thymectomy trials. However, it quickly became apparent that their efforts should apply to all therapeutic trials for MG, and thus the scope of the mission was expanded.

During the development of these recommendations, the Task Force faced numerous dilemmas for which no universally satisfactory solution was available. Dilemmas were defined as "situations that require one to choose between two equally balanced alternatives or predicaments that seemingly defy satisfactory solutions." The Task Force members agreed at the outset, however, that their primary goal was to develop a uniform set of classifications to be used in the comparative analysis of the various therapeutic interventions for MG. With this as the primary goal, a consensus was gradually developed. In developing a consensus, at least two meetings were held each year during a 3-year period. Between meetings there was exchange of all proposals by electronic and surface mail, consultation with national and international experts in the field, critical analysis of all proposals, and many revisions. All conflicts (both minor and major) were resolved by vote. Virtually all issues were eventually approved unanimously; a few received a plurality of six.

This report presents the work of the Task Force and proposes classification systems and definitions of response to therapy designed to achieve more uniformity in recording and reporting clinical trials and outcomes research. Although designed primarily for research purposes, we think physicians may find some of the recommendations useful in the clinical management of patients with MG.

MGFA clinical classification

This classification (Table 1) is designed to identify subgroups of patients with MG who share distinct clinical features or severity of disease that may indicate different prognoses or responses to therapy. It should not be used to measure outcome. It defers quantitative assessment of muscle weakness to the more precise Quantitative MG Score for Disease Severity, defers response to therapy to the MGFA Postintervention Status and the Quantitative MG Score, and defers the status of medication to the Therapy Status classification.

In general, these classifications use subjective assessments and lack quantification. What one physician may regard as "mild," another might regard as "moderate" or "severe." Furthermore, some experienced clinicians believe that oropharyngeal involvement is more dangerous, and perhaps different than limb weakness, and thus should be identified by the classification system. Some feel that "crisis" (respiratory insufficiency necessitating intubation and assisted ventilation) is the result of coincidental infection or other stress in susceptible patients, whereas others regard crisis as defining the ultimate in disease severity.

The Task Force discussed these issues at length, and the members think that a uniform classification is necessary if meaningful comparison of data is to be achieved. The Task Force sees no alternative but to accept the inherent imprecision of a clinical classification, and it recommends that the MGFA Clinical Classification be used to supplement or to replace the classifications now in use. It also recommends that the most severely affected muscles be employed to define the patient’s Class and that the "maximum severity" designation be used to identify the most severe pretreatment clinical classification status. The "maximum severity" designation may be made historically and is employed as a point of reference. The maximum severity remains the point of reference thereafter, with any worsening of the MG being reflected in the postintervention status determination.

The quantitative MG score for disease severity

A quantitative MG scoring system (QMG Score) is essential in the objective evaluation of therapy for MG. This scoring system is based on quantitative testing of sentinel muscle groups. The QMG Score should be used in conjunction with the Clinical Classification and the Postintervention Status. It does not replace the clinical evaluation of the patient and should not be used to compare severity between patients. To assess the effect of treatment, the QMG Score should be determined before beginning the treatment under study and at appropriate intervals thereafter. As with all patient evaluations, the time of the examination in relation to therapy, and the presence of factors that may alter the clinical course, should be recorded.

The Task Force recommends that a QMG Score be used in all prospective studies of therapy for MG. The specific scoring system recommended (Table 2) [2] is a modification of earlier systems developed for this purpose [3–6]. Its interexaminer reliability has been confirmed. A manual and a demonstration video of this system are available from the MGFA [7].

MGFA therapy status

The MGFA Therapy Status (Table 3) defines the treatment regimen of the patient at a given time and is most useful when used with the MGFA Postintervention Status. The Therapy Status, at any point in time, is defined by using a single designation or a combination of the designations. In addition, the duration of this status, the current doses of all pertinent medications, and the schedule of plasma exchanges and IV immunoglobulin (Ig) should be recorded.

The Postintervention Status (Table 4) is designed to assess the clinical state of MG patients at any time after institution of treatment for MG. Use of this classification requires that specific forms of therapy be recorded separately in the Therapy Status section.

Isolated weakness of eyelid closure was thought not to be a sign of active disease and therefore was not considered an exclusionary criteria from CSR or PR status. In contrast, patients receiving cholinesterase inhibitors are excluded from PR and MM-1 status because these medications mask myasthenic symptoms.

Grouping by age, sex, race, and geography

The sex, race, age at onset, and geographic distribution of patients may be important variables in assessing response to treatment of MG [11, 12]. Accordingly, these variables should be identified in all studies and their effect on response to treatment should be evaluated.

At this time, definitions of the age limits of childhood, adolescence, or onset of puberty have not been universally accepted or applied [11, 13]. Appropriate age subdivision in children needs to be defined for universal use. Until such time as these age groups can be agreed on, it is recommended that age grouping occur by decade (ie, up to 10 years, 11 to 20 years, 21 to 30 years, etc).

Thymic pathology

There are no comprehensive guidelines for the evaluation of the nonthymomatous thymus removed from patients with MG. Incomplete and variable sampling techniques [14] and the lack of comprehensive diagnostic guidelines may account for the conflicting reports regarding the relationship between the histologic changes in the thymus and the response to thymectomy.

To determine the prognostic and therapeutic importance of pathologic changes in the thymus removed during thymectomy, uniform criteria for specimen management, sampling techniques, criteria for the diagnosis of hyperplasia and involution, characterization of immunocytochemical changes, and other determinants need to be defined and standardized [12, 15, 16].

The histologic classification and grading of thymic neoplasms, including the identification of noninvasive and invasive thymomas, other neoplasms of the thymus, and their relation to MG results, also need to be standardized [15, 17–24]. Patients with thymoma undergoing thymectomy for MG should be analyzed separately from those without thymoma, because combining these patient cohorts has made it difficult to determine whether the presence of a thymoma, even when noninvasive, alters the prognosis.

The Task Force recommends that the multiple issues involved be addressed with the development of guidelines for the evaluation of the nonthymomatous thymus in MG and a universally acceptable single classification of thymic neoplasms.

MGFA thymectomy classification

Multiple techniques are described for removal of the thymus in MG. The debate regarding which technique is preferable is not resolved. Although, classically, "total thymectomy" is considered the goal of surgery, it has not been demonstrated unequivocally that this is necessary, nor is it clear that all the resectional techniques do achieve this goal.

To resolve the issues regarding the choice of thymectomy technique and whether there is a relationship between the resectional technique employed and the rate of remission and improvement, the type of thymic resection used needs to be defined in as objective terms as possible. In addition, multiple resectional techniques should not be reported as a single cohort.

The Thymectomy Classification (Table 5) is based on published reports. The techniques are grouped according to the primary approach (transcervical, videoscopic, transsternal, or combinations) and are described briefly. Referenced reports are recommended for details. Because, within each category, there may be variations in the extent of the resection from surgeon to surgeon, the extent of the resection for each patient cohort must be recorded. In all prospective studies it is recommended that detailed descriptions of the operative technique be supplied, accompanied by drawings and photographs of typical specimens. Ideally, a video of the technique should also be available.

View larger version (67K): [in this window] [in a new window]   Fig 1. Anatomy of the thymus. This illustration represents what is now generally accepted as the surgical anatomy of the thymus [41]. The frequencies (percent occurrence) of the variations are noted. Black = thymus; gray = fat that may contain islands of thymus and microscopic thymus. A-P window = aorto-pulmonary window. Source: Neurology 1997;48(suppl 5):S52–S63.

There are several variations to the Transsternal Thymectomy approach. The "Standard" technique was originally designed to remove the well-defined central cervical–mediastinal lobes. At this time, although a complete or partial [34–36] sternotomy may be performed, the resection is more extensive than originally described, with removal of all visible mediastinal thymus. Mediastinal fat, varying in extent, may or may not be removed. The cervical extensions of the thymus are removed from below, with or without some adjacent cervical fat. Variations of this technique include a video-assisted technique using a complete median sternotomy via a limited lower sternal transverse skin incision [37]. The "Extended" [38] procedure is also known as Aggressive Transsternal Thymectomy [39] and Transsternal Radical Thymectomy [40]. These resections remove the entire mediastinal thymus and most of the mediastinal perithymic fat. They vary somewhat in extent in the mediastinum and may or may not include all tissue removed by the T-4 techniques. The cervical extensions are removed from below, with or without additional tissue, but without a formal neck dissection.

The combined transcervical and transsternal thymectomy procedures are known as Transcervical–Transsternal Maximum Thymectomy [41] and Extended Cervical–Mediastinal Thymectomy [42]. These resections routinely use wide exposure in the neck and a complete median sternotomy with en bloc removal of all tissue in the neck and mediastinum that may contain gross or microscopic thymus anatomically. The resections include removal of both sheets of mediastinal pleura and sharp dissection of the pericardium. A similar procedure, although a less extensive resection in the neck and mediastinum, has been described by Lennquist and associates [43].

It is recommended that the thymectomy classification, with modifiers as necessary, be employed when reporting the results of thymectomy for MG.

MGFA morbidity and mortality classification

During the evaluation of therapeutic options, in addition to the determination of the remission and improvement status, quality of life and cost–benefit assessments should be performed [44]. This requires the analysis of, among other things, the number and duration of hospitalizations and intensive care unit stays, and complications related directly to each form of therapy (Table 6).

A prospective, randomized clinical trial remains the preferred method to evaluate therapy (Class I evidence in the American Academy of Neurology AAN nomenclature) [45]. When a randomized trial does not appear feasible, a prospective risk-adjusted outcome analysis of nonrandomly assigned treatment (Class II evidence in the AAN nomenclature) is recommended [46]. In prospective studies, in addition to the use of the classification, definitions, grading systems, and methods of analysis recommended herein, the CONSORT guidelines [47, 48] are recommended.

"Survival" instruments, which are used in the analysis of remissions, are fundamental in the comparative analysis of therapeutic programs for MG. Although different levels of clinical improvement should be evaluated in the analysis of all forms of therapy, Complete Stable Remission remains the primary focus of the analysis, at least in the assessment of thymectomy.

Qualify-of-life instruments should also be employed because therapy for MG is usually not innocuous and frequently does not produce a completely stable remission. Quality-of-life measures evaluate the impact of intermediate levels of clinical improvement and morbidity of therapy, and complement information provided by remission and clinical improvement analysis. Although a functional status instrument assessing activities of daily living has been developed for MG [49], there are no disease-specific quality-of-life instruments for MG at this time. The Task Force recommends that these be developed. The steps necessary to accomplish this have been defined [50].

An Outcomes Analysis guideline and an accompanying diagram defining their interrelationships were developed to provide background information on the available analytic techniques [44]. Experts in the field of biostatistics and outcomes analysis should be consulted in the design of all studies, and in the collection and evaluation of the data.

Data bank

Multi-institutional studies utilizing the data bank concept and fulfilling the requirements discussed next are recommended. This method of study should be particularly useful and practical for multiple institutions to compare the relative value of the many therapies, including various thymectomy techniques.

For a data bank program to be successful, it must be developed appropriately and monitored rigorously. Computer-based patient records, including the "human language" component [51], are required. Definitions, classifications, and standardized forms must be agreed on and used. Standardization of numeric grading for all important variables is required. Mechanisms must be in place to review all the clinical records and to monitor the quality of the database, including validation for completeness and accuracy through a rigid auditing process. The monitoring requirement involves a major commitment by the sponsoring institutions, professionals, and staffs. Mechanisms to defray costs would need to be developed.

Amendments

The MSAB of the MGFA has established a Standing Committee for review of the Clinical Research Standards. The goal of any proposed amendment is to improve the guidelines based on demonstrable errors in the existing guidelines, development of new data, and common sense. The Review Committee will review recommendations from national and international neurologic organizations and centers, journal editorial boards, neurologists, immunologists, surgeons, biostatisticians, nurses, respiratory therapists, and others working in the field of MG. The Review Committee will also serve as a clearinghouse for questions, as they arise, concerning the application of the Clinical Research Standards.

Please submit questions and proposals in writing to Chairperson, Clinical Research Standards Review Committee, Medical Scientific Advisory Board, Myasthenia Gravis Foundation of America, Inc, 123 West Madison, Suite 800, Chicago, IL 60602; e-mail: myastheniagravis@msn.com

Acknowledgments

Supported by the Ringel Foundation.

Footnotes

¹ Reprinted with permission from Neurology 2000;55:16–23 (© AAN Enterprises, Inc.). Additional material related to this article can be found on the Neurology Web site at www.neurology.org. Consult the Table of Contents for the July 12 issue to find the title link for this article. See also Neurology 2000;55:3–4, 7–15.

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