Thoracoscopic Thymectomy Mid-Term Results

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DOI: 10.1016/j.athoracsur.2006.04.092 2006;82:1003-1007 Ann Thorac Surg

Victor Tomulescu, Virginia Ion, Andras Kosa, Olivia Sgarbura and Irinel Popescu Thoracoscopic Thymectomy Mid-Term Results

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ORIGINAL ARTICLES: GENERAL THORACIC

horacoscopic Thymectomy Mid-Term Resultsictor Tomulescu, MD, Virginia Ion, MD, PhD, Andras Kosa, MD, Olivia Sgarbura, and

rinel Popescu, MD, PhDepartments of General Surgery and Liver Transplantation and Neurology, Fundeni Clinical Institute, and the Department of

ealth Psychology and Psychosomatics, “Carol Davila” University of Medicine and Pharmacy, Bucharest, Romania

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Background. Results of thymectomy in patients withyasthenia gravis need to be reported in a standardizeday to allow accurate comparison.Methods. A retrospective study was conducted of 107

atients with myasthenia gravis without thymoma. Pa-ients were followed-up for more than 12 months afterhoracoscopic thymectomy and analyzed according to

yasthenia Gravis Foundation of America Recommen-ations for Clinical Research Standards.Results. The study population was aged 8 to 60 years

ld and included 15 men (14%) and 92 women (86%). Aight-side approach was used in 36 patients, and theemaining 71 patients had a left-side approach. Mortalityas 0% and morbidity was 9.34%. The mean operative

ime was 90 � 45 minutes. The histologic diagnosis of theesected thymus was hyperplasia (78.5%), atrophy (15%),

nd normal status (6.5%). The mean length of hospital-

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zation was 2.3 days (range, 2 to 6 days). The meanollow-up was 36.4 months (range, 12 to 74 months). Theate of complete stable remission was 59.5% by the end ofostoperative year 6. An earlier onset age and earlyperation were significantly associated with completetable remission and pharmacologic remission. A com-arison of right side versus left side approach showedimilarities in mean operative time, mean length ofospitalization, histopathologic results, and remissionates.

Conclusions. Outcomes of the thoracoscopic approachn myasthenia gravis without thymoma were similar tohose provided by open surgery, with the acknowledgedenefits of minimally invasive surgery and good patientcceptance.

(Ann Thorac Surg 2006;82:1003–8)

© 2006 by The Society of Thoracic Surgeons

ideo assisted thymectomy was introduced in 1992 asa minimally invasive alternative to thymectomy in

atients with myasthenia gravis. Our preliminary resultsave been previously reported [1]. The purpose of thiseport is to provide results from a wider range of patientsith longer follow-up periods to enable a more accurate

valuation of the approach. Given the heterogeneity ofhe disease and its unpredictable progress, comparisonsf different therapeutic outcomes proved to be veryifficult, if not impossible. The Task Force of the Myas-

henia Gravis Foundation of America (MGFA) has there-ore issued new classifications for the clinical, therapeu-ic, and postinterventional status [2], which we also usedo stratify the participants in our study as a landmark foromparison by future research.

aterial and Methods

ur study was approved by the Fundeni Clinical Insti-ute Ethics Committee, and the need for informed con-ent from patients was waved because of its retrospectiveesign. Since April 1999, a thoracoscopic approach haseen used in all patients admitted in the Department ofeneral Surgery and Liver Transplantation of Fundenilinical Institute with either nonthymomatous myasthe-

ccepted for publication April 27, 2006.

ddress correspondence to Dr Popescu, Department of General Surgery

ia gravis or stage I thymoma, defined as a tumor size ofess than 4 cm with no signs of invasiveness on computedomography (CT). Those with stage II or III thymomaeceived the transsternal approach. Between April 1999nd April 2005, the thoracoscopic approach was used in60 patients with myasthenia gravis without thymoma.According to the MGFA Recommendations for Clinical

esearch Standards in the assessment of the postopera-ive status—complete stable remission (CSR) and phar-

acologic remission (PR) of patients—was calculated athe end of a minimal period of 12 months’ follow-up. Weestricted our study population to patients undergoingurgery between April 1999 and May 2004. We excluded7 participants with less than 12 months’ follow-up, 9atients with incomplete preoperative recorded datarovided by the Department of Neurology, and 17 pa-

ients who were lost to follow-up. Our study finallyvaluated 107 patients with myasthenia gravis withouthymoma who were followed-up for more than 12

onths after thoracoscopic thymectomy.All of the patients received specific treatment for at

east 3 months before surgery in the Department ofeurology of the Fundeni Clinical Institute. Patientsere considered suitable for a surgical procedure onlyhen evidence showed good treatment tolerance and aecrease of the quantitative myasthenia gravis score to at

east 10. Preoperative clinical staging was assessed by theGFA clinical classification [2]. Preoperative diagnostic

ests included spirometry and a CT scan. Patients were

ransferred to our department on the morning of the

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cheduled operation. The surgical technique that wesed has been described elsewhere [1, 3].Patients were extubated immediately and remained in

he intensive care unit for 24 hours. They were evaluatedy the same neurologist just after surgery and every 6onths during the 6 years of follow-up. Data were

ollected and analyzed using medical records and tele-hone interviews. Treatment, morbidity, mortality, andostinterventional status at follow-up were also beenssessed according to the MGFA Recommendations forlinical Research Standards.The databases were compiled and analyzed using

xcel 2002 (Microsoft, Redmond, WA), SPSS 10.0 (SPSS,nc, Chicago IL), and Epi Info 6.0 software (Centers forisease Control, Atlanta, GA). The normal sample distri-ution was measured by using the Kolmogorov-Smirnov

K-S) test. Univariate analysis of variables potentiallyffecting complete stable remission (CSR) and pharma-ological remission (PR), including age at operation,ender, disease duration, and histology were calculatedy using the Kaplan-Meier method. We used the log-ank test to compare survival curves, and univariatenalysis and �2 test were used to calculate the relativeisk (RR) with a 95% confidence interval (CI). The Stu-ent t test was also used. Values of p � 0.05 wereonsidered statistically significant.

esults

he study cohort included 15 men (14%) and 92 women86%). The average age at the time of the operation was of8.06 � 9.97 years (range, 8 to 60 years). The normalistribution of the study population was determinedsing the K-S test that yielded a nonsignificant p value

K-S Z � 1.284, p � 0.07) showing a normal distribution ofhe data. The mean duration of the disease was 21.20

onths, and it had variations within the study group. Noender-related significant differences were found.According to the MGFA clinical classification of theaximal severity level in the history of the disease before

urgery, 18 patients (16.85%) were stratified in class IIa,6 (33.74%) in class IIb, 16 (14.86%) in class IIIa, 1816.85%) in class IIIb, 16 (14.86%) in class IV, and 3 (2.84%)n class V.

The 107 participants received preoperative steroidherapy. Additional treatment with anticholinesteraseas required in 43 patients (40.19%), and 28 (26.17%)

equired immunosuppressive drugs.We initially performed a left-side surgical approach for

he first 30 patients, followed by right-side thoracoscopys an alternative intervention. Our decision on whethero use the right-side or left-side approach depended onhe CT status of the thymus. Only 2 patients needed theombined cervical and thoracoscopic approach becausef the cervical extension of the thymus. There was noonversion to open thymectomy. The mean operativeime was 90 � 45 minutes.

No patients died. Postoperative morbidity occurred in0 patients (9.24%), consisting of severe postoperative

yasthenia crisis in 1 patient who needed mechanical c

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entilation for 5 days, 2 with contralateral pneumothoraxfter removal of the drains, 3 with hemothorax thatequired emergent reoperation, and 4 patients with pro-onged pleural drainage.

The three cases of hemothorax were resolved by tho-acoscopic reoperation. In 1 patient, bleeding caused by aesion of the internal mammary vein from the oppositeite was stopped with clips applied on the bleedingessel. Bleeding at the level of the trocar port occurred inpatients, one of which required extension of the trocaround and ligation of the intercostal artery.The most frequent histologic diagnosis was hyperplas-

ic thymus (78.5%); involuted thymus was found in 15%.he remaining 7 patients (6.5%) in the study had aormal thymus.The mean length of hospitalization was 2.3 days (range,to 6 days). The average postoperative stay included 2

ays in our department and an additional day in theepartment of Neurology. The mean follow-up periodas 36.4 months (range, 12 to 74 months).Our study aimed to achieve CSR and PR as defined by

he Clinical Research Standards of MGFA [2]. The pre-perative status evaluated according to the Clinical Re-earch Standards of MGFA during the 6 years of theollow-up period is shown in Figure 1. The CSR and PRurves have an ascending pattern pointing to the goodostoperative outcome.The CSR rate in our study group was only 5% at the

nd of the first year after surgery but increased to 15% athe end of the second year. For patients undergoing earlyhymectomy, a rate of 32.87% was calculated at the end ofhe third year (74 patients), 42% at the end of the fourthear (50 patients), and 42.85% at the end of the fifth year42 patients). A sudden increase of the CSR rate to 59.5%y the end of the sixth year was seen, but the estimatead involved only the 37 patients who had completed the

ollow-up period. The Kaplan-Meier method was used tohow the evolution of the remission rates (Fig 2).

The correlation coefficient between the average quan-itative myasthenia gravis scores and the median corti-osteroid doses within the 6 years after surgery was

ig 1. The postoperative status (complete stable remission [CSR],harmacologic remission [PR]) during the 6 years after surgery (x-xis � time in years; y-axis � percentage).

alculated by means of the Pearson correlation, consid-

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ring the values of the 6-month estimates. A significantlytrong association between the two variables was dem-nstrated (r � 0.956, p � 0.0001) (Fig 3). Univariatenalysis aimed to identify whether the clinical, histologic,nd surgical factors might play a role in the achievementf CSR and subsequently, CSR and PR.We also compared the left-side surgical approach (71

atients) versus the right-side approach (36 patients) andound similar patterns of average operating time, meanength of hospitalization, and rates of remission (p valuesot significant).

omment

lthough total thymectomy has always been consideredo be the goal of surgery in myasthenia gravis, andeveral studies comparing aggressive with limited resec-ions support the prerequisite that the less thymus leftehind, the higher the remission rate [4], the optimalpproach that balances the extent of resection, morbidity,atient acceptance, and results remain controversial.inimally invasive thymectomy techniques do not nec-

ssarily equate with poorer outcomes.Only patients with generalized myasthenia gravis were

uitable for surgery. The procedure was not provided toatients with ocular symptoms alone or for those classi-ed with a MGFA clinical status class I, although about0% of these patients are known to further developeneralized myasthenia gravis [5]. More importantly, inur opinion, surgical intervention should not be imposedn the remaining 70% of these, who would have noenefit; instead, consistent follow-up could enable rapidiscovery of those who are going to develop generalizedyasthenia gravis. Surgery has also been the therapeutic

ption for patients with late-onset myasthenia gravis, butnly if they were younger than 70 years old or hadhymomatous myasthenia gravis, or both.

We believe that surgery is merely one link in theomplex chain of myasthenia gravis treatment, and the

ig 2. Kaplan-Meier curve for our rates of complete stable remis-ion. MG � myasthenia gravis.

est outcomes are therefore most likely to be provided 0

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nly by a coordinated approach of medical and surgicalherapies. Practically all the study participants were re-eiving prednisone at the time of the operation. In ourpinion, the very low rate of severe postoperative myas-henia crises (0.93%) is closely associated with the preop-rative intensive treatment and with the lower extent ofhest trauma related to thoracoscopy.

Yim and colleagues [6] favor the right thoracoscopicpproach because (1) identification of the vena cava is aandmark for easier dissection of innominate vein, (2) theonfluence of the innominate veins is easier to dissect bysing a right approach, and (3) ergonomically, it is easier

or right-hand surgeons to dissect the thymus fromnferior horns to upper horns with a right approach. Tohis we would add that the right approach allows a betteriew in the cervical area.Irrespective of the patient’s anatomic characteristics,

very effort is made to perform a full removal of thehymic tissue by clearing the innominate vein and ante-ior pericardium from all mediastinal fat. We believe aeft-side approach facilitates the procedure because mostf the mediastinal fat is located on the left side of thenterior mediastinum. The use of a 30° endoscope (Karltorz-Endoscopy, Culver City, CA) provides significantelp. Although we share the opinion of Mineo andolleagues [7] that thymectomy can be performed byither a left-side or a right-side approach, we believe theeft-side approach has some advantages. In our experi-nce, the dissection maneuvers are safer when per-ormed on the left side because the right phrenic nerve isituated outside the surgical field, thus reducing the riskf an incidental lesion. It is also easier to perform aissection of the right side of the thymus by a leftpproach than a dissection of the left side of the thymusy right approach, especially for the aortopulmonaryindow.We have not performed a pneumomediastinum to

acilitate thymectomy as have Mineo and colleagues [8],ut we have observed that insufflation of up to 8 mm Hgnables pulmonary collapse and enlarges the operatingeld between the heart and sternum by almost 2 cm,

ig 3. Comparative evolution of average quantitative myastheniaravis (QMG) score and average corticosteroids (CS) doses duringhe 6 years after surgery (Pearson’s correlation, r � 0.956, p �

.0001).

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hich makes mediastinal dissection easier. Positive pres-ure is also very useful during the dissection, particularlyn the cervical area.

Our reported surgical procedure is not a “maximal”hymectomy as has been shown by Jaretzki [9] or Zielin-ki and colleagues [10], but it closely matches otherublished thoracoscopic approaches [11–16] and thestandard extended transsternal thymectomy” [17]. Theranscervical approach is also associated with minimalccess trauma, and the use of the current technique hasielded remission rates equivalent to the results of moreggressive and extensive techniques [18]. A thoraco-copic approach can provide a better view (thymus isarticularly a mediastinal gland) and an easier way oferforming the procedure compared with extension of

he thymectomy and ergonomics (too many instrumentsn a single narrow cervical incision).

The postoperative evolution was satisfactory in 2259.5%) of the 37 patients who were in CSR by the end ofhe follow-up period. Throughout the 6 years, curves foroth CSR and PR had an ascending trend, with a 97.19%tatus improvement at the end of the follow-up. The goodutcome after thymectomy was confirmed by the Kaplan-eier pattern. A comparison of our results with those

eported by Jaretzki and colleagues [19] showed that ouremission rates were consistent with the estimates re-orted by other authors at 3, 4, and 5 follow-up years (Fig). Our rough rate of achieving CSR was 39.25%, whichas in accordance to similar data reported by Savcenko

nd associates (14%) [20], Mineo and associates (36%)12], and even with the 33.3% rate of bilateral video-ssisted extended thoracoscopic thymectomy publishedy Mantegazza and associates [21].Our low remission rates during the first 2 years of

ollow-up could be explained by the constant use oforticosteroids. The steroid medication dosage has to berogressively lowered, which means that a longer time iseeded to get total exclusion and achievement of CSRith a high rate of PR. The slope of the remissioniagram shows a sudden increase between years 5 and 6,uggesting that a longer follow-up period might beeeded to determine all the beneficial effects of thoraco-copic thymectomy. However, the small number of pa-ients (37) who completed the follow-up period limitedhe statistical power of our study.

No gender-related differences in achieving CSR ex-sted in our study group. Patients with an earlier onsetge had better chances of achieving remission (CSR �R) after operation than the others (p � 0.04), but theR 95% CI is not reliable as it ranges from 0.8 to 10.8

Fig 4). This might become an important issue in theelection of participants for further studies. Patientsndergoing surgery shortly after the disease onsetight have twice as many chances to achieve remis-

ion than the remaining patients (p � 0.03, RR, 1.56,5% CI, 0.94 to 1.59). Although higher rates of remis-ion in patients with hyperplastic thymus have beeneported [21–23], our results did not point to any

dvantage for this histologic finding, similar to the a

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MPC study [24]. We therefore believe that the role ofistology should be further investigated.Even if our study patients were not randomized for the

eft-side and right-side approaches, respectively, theirimilar characteristics in terms of average age and sex-atio enabled us to conclude that the two approaches arequally reliable as far as postoperative evolution, remis-ion, and status rates are concerned.

The mean duration of the disease until patients under-ent surgery in our series was 18.8 months, which

avorably compares with the mean duration of 42.2onths in our historical series. This suggests that the

horacoscopic approach has a high patient complianceith surgery (we have tripled our experience performedithin a similar time interval) because of its better

osmetic results, with the same medical outcomes.We believe that the thoracoscopic approach in non-

umoral myasthenia gravis has several clearly definedharacteristics: it has a higher rate of acceptance anday therefore benefit an increased number of patients;

he left-side and right-side approaches are similar inerms of postoperative evolution, remission, and statusates; earlier onset age of the disease and early oper-tion are important favorable prognostic factors; thentervention is associated with a very low rate oframatic postoperative myasthenia crises in patientsith preoperative intensive treatment; it provides sim-

lar benefits to those of the “standard extended trans-ternal thymectomy” as it is currently performed, inorrelation to the extension of the thymic tissue re-oval; and, as measured by CSR rates, the thoraco-

copic approach proved to be as effective as openxtended surgery, with the acknowledged benefit ofinimal invasive surgery.It is important to note that the achievement of favor-

ble outcomes requires highly coordinated teamworknvolving a strong collaboration between neurologists,urgeons, and anesthesiologists in making appropriateecisions on selection of patients, therapeutic options,

ig 4. Kaplan-Meier curves depending on the age of onset. Solidine � age 40 years or younger; broken line � age older than 40ears.

nd timing of surgery.

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2. Jaretzki A 3rd, Barohn RJ, Ernstoff RM, et al. Myastheniagravis: recommendations for clinical research standards.Task Force of the Medical Scientific Advisory Board of theMyasthenia Gravis Foundation of America. Ann ThoracSurg 2000;70:327–34.

3. Tomulescu V, Ion V, Ciurea S, Tulbure D, Popescu I. [Video-assisted thoracoscopic thymectomy—preliminary results].Chirurgia (Bucuresti) 2000;95:215–20.

4. Jaretzki A, Steinglass KM, Sonett JR. Thymectomy in themanagement of myasthenia gravis. Semin Neurol 2004;24:49–62.

5. Evoli A, Batocchi AP, Minisci C, Di Schino C, Tonali P.Therapeutic options in ocular myasthenia gravis. Neuro-muscul Disord 2001;11:208–16.

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7. Mineo TC, Pompeo E, Ambrogi V. Video-assisted thoraco-scopic thymectomy: from the right or from the left? J ThoracCardiovasc Surg 1997;114:516–7.

8. Mineo TC, Pompeo E, Ambrogi V, Sabato AF, Bernardi G,Casciani CU. Adjuvant pneumomediastinum in thoraco-scopic thymectomy for myasthenia gravis. Ann Thorac Surg1996;62:1210–2.

9. Jaretzki A 3rd. Video-assisted thoracoscopic extendedthymectomy and extended transsternal thymectomy in non-thymomatous myasthenia gravis patients. J Neurol Sci 2004;217:233–4.

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asthesia: results of left-sided approach. Ann Thorac Surg2000;69:1537–41.

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NVITED COMMENTARY

he article by Tomulescu and colleagues [1] underlineshe persistence in the controversy between those whoromote “maximal” thymectomy during the course of

reating myasthenia gravis and those who do not. Theuthors state that their procedure is equivalent tostandard extended” transsternal thymectomy, an oper-tion which is said to remove about 85% of thymic tissuen the mediastinum.

A survey of the current literature further emphasizeshe nub of the issue. Reproof being cast on those who doot espouse removal of as much thymus and ectopic

hymus as possible is becoming more apparent. Theocus is more and more on maximal thymectomy as thetandard of care, even by thoracoscopic approaches, andarallels the attention to the maximal operation pro-oted by others [2, 3]. Maximal is generally defined as en

loc removal of thymus and all perithymic fat from theeck to the diaphragm and between the phrenic nerves.The choice of video-assisted surgery is attractive to

atients with nonthymomatous myasthenia gravis. Theurgery is cosmetically acceptable and seems to have less

hat mean that we, as surgeons recommending the bestvailable treatment for this disease, should promoteeaving residual thymic rests to achieve general accep-ance over a maximal transsternal operation that is ex-ected to improve remission, diminish the incidence ofeoperation, and lessen dependence on pharmacologicntervention in the long term? Somewhere, the twopproaches should intersect in all clinical aspects.Twenty years ago, Jareztki and colleagues [2] illus-

rated that there were adverse consequences to non-aximal thymectomy. In the authors’ reference to

aretzki and colleagues, they choose to focus on thymicistology rather than the point that Jaretzki and col-

eagues were making, which is a lesson emphasizing asuch removal of thymic tissue as possible. Other more

ontemporary studies that have used thoracoscopic pro-edures promote the notion of maximal thymectomy withesults that are comparable with the transsternal maximalperation [4, 5].For Tomulescu and colleagues, the devil is in the

etails. The remission rates with or without depen-

ence on drugs may be similar in the intermediate

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Victor Tomulescu, Virginia Ion, Andras Kosa, Olivia Sgarbura and Irinel Popescu Thoracoscopic Thymectomy Mid-Term Results

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