ORIGINAL ARTICLE

What happens to the thymus in childrenwho have undergone a median sternotomy?

Kelly MacDonald & Stephanie Mackenzie

Received: 27 July 2008 /Revised: 31 December 2008 /Accepted: 14 January 2009 /Published online: 11 March 2009# Springer-Verlag 2009

AbstractBackground The thymus grows rapidly during fetal life andcontinues to grow during childhood. When a child undergoesa median sternotomy during cardiac surgery, most of thethymus is removed to gain access to the mediastinum. Whathappens to the residual thymic tissue in the long term?Objective To test the hypothesis that residual thymic tissueleft after sternotomy regenerates into an identifiable thymusand is visible on MRI.Materials and methods We retrospectively reviewed thecardiac MR images obtained over a 14-month period in allchildren under the age of 17 years who had undergone amedian sternotomy (n=62) to establish the presence/absence of a thymus. We also reviewed the cardiac MRimages obtained over the same time period in children whohad never undergone open cardiac surgery (n=37).Results In the sternotomy group, 18 patients (29%) had anidentifiable thymus on MR images, compared to 92%(n=34) in the nonsternotomy group. This difference wasstatistically significant.Conclusions The majority of children in the study groupdid not have a visible thymus on MR images, whichsuggests that in these children any residual thymic tissueleft postoperatively does not regenerate.

Keywords Thymus . Sternotomy .MRI . Children

Introduction

The thymus is located in the anterior superior mediastinum.It is the site of T-lymphocyte maturation for the immunesystem [1]. The thymus grows rapidly throughout fetal life,weighing between 10 g and 15 g at birth [2]. It continues togrow during childhood, reaching its maximum weight andsize at puberty (30–40 g) [2]. During adulthood, the thymusinvolutes and, with advancing age, is replaced by adiposetissue. However, although there is a trend for rapid thymicgrowth prior to adulthood, it is recognized that there isconsiderable variation between individuals in the size andmorphology of the thymus gland in childhood [3, 4], andthus paediatric radiologists learn very early on in theirtraining the importance of considering the thymus gland inthe differential diagnosis of anterior mediastinal masses.

Premature involution of the thymus gland in prepubertalchildren is another recognized entity, occurring particularlyat times of illness, stress and chemotherapy, and in Cushingsyndrome. However, following a period of recovery thethymus usually regrows and in some cases this reboundgrowth results in thymic hyperplasia.

Children undergoing surgery for congenital cardiacabnormalities via a median sternotomy approach have mostof their thymus gland removed to gain access to themediastinum and to facilitate cannulation in cardiopulmonarybypass. However, what happens to residual thymic tissuewithin the mediastinum postoperatively is unknown. It is notclear whether residual thymic tissue is capable of regeneratingpostoperatively, or whether any remaining thymic tissueundergoes rebound hyperplasia.

Immunological studies performed in children undergoingopen cardiac surgery during infancy have found that T-lymphocyte maturation remains impaired years after surgery,with patients having significantly lower total lymphocyte

Pediatr Radiol (2009) 39:616–621DOI 10.1007/s00247-009-1202-0

K. MacDonald : S. MackenzieDepartment of Paediatric Radiology,Bristol Royal Hospital for Children,Bristol, UK

K. MacDonald (*)9 Devonshire Buildings,Bath BA2 4SP, UKe-mail: agatha@doctors.org.uk

counts, reflected in a reduced number of T cells peripherallycompared to matched control groups [5, 6]. In addition, otherimmunological studies have suggested that T-cell maturationin this group of children occurs instead at extrathymic sitespostoperatively [7].

However, what happens to any residual thymic tissue inthe long term has not to our knowledge been investigatedanatomically. We therefore investigated this question byanalysing follow-up cardiac MR examinations that areperformed at our institution in many of these childrenyears after surgery. We wished to investigate the hypoth-esis that residual thymic tissue left after sternotomyregenerates into an identifiable thymus visible on MRimaging.

Materials and methods

Before commencing this study, the North Somerset andSouth Bristol Research Ethics Committee was contactedand approval was given. A retrospective study wasperformed and the images of all patients under the age of17 years who had undergone a cardiac MR examination atour institution over a 14-month period commencingOctober 2006 were reviewed.

Imaging was performed routinely as part of a standardcardiac series protocol that included a contiguous axial HASTEsequence through the thorax. Images were obtained on a 1.5-TMR system (Symphony, Siemens, Erlangen, Germany).

Each set of electronic images was reviewed on aworkstation and the axial HASTE sequence was specificallyexamined by two radiologists (a specialist registrar inradiology and a consultant paediatric radiologist). Theimages was specifically scrutinized for the presence of athymus and agreement was reached by consensus. Where thequality of the MR images was suboptimal (for examplebecause of movement artefact), the patient was excludedfrom the study.

Although both radiologists were unaware of whichchildren had previously undergone open cardiac surgery,evidence of a sternotomy was often visible on imaging, andthis study cannot, therefore, be described as “blinded”.After reviewing all MR examinations performed over this14-month period, the clinical notes of each patient werereviewed and the following documented:

1. Details of any previous cardiac surgery2. Age at the time of the last sternotomy (some children

had multiple sternotomies for cardiac surgery)3. Details of any noncardiac illness/therapy, e.g. radiotherapy4. Age at the time of MR examination5. Time interval between last sternotomy andMR examination6. Gender

The patients were divided into study or control groupsaccording to whether they had previously had a sternotomy.The control group consisted of patients who had notundergone an open cardiac procedure, but either werebeing investigated (e.g. for coarctation) or had undergoneprocedures such as balloon valvuloplasty. The results foreach group were then analysed to identify:

1. What proportion of children in each group had a visiblethymus on MR imaging.

2. Whether the presence of a visible thymus in the studygroup was related to any other factors, such as age attime of sternotomy, or time interval between surgeryand imaging.

The results were analysed using Fisher’s exact test.

Results

A total of 122 consecutive patients younger than 17 yearsunderwent a cardiac MR examination over the 14-monthstudy period, and 77 of these children had previously had asternotomy during cardiac surgery and 45 had not. Of the122 children, 23 (19%) were excluded from the studybecause either their hospital notes could not be located orbecause the axial HASTE sequence was suboptimal and itwas felt that the images could not be accurately interpreted.Of the remaining 62 children in the sternotomy group, 41were boys and 21 were girls. The age at which the childrenunderwent a sternotomy varied from younger than12 months to 10 years. However, the majority (68%) wereyounger than 4 years of age at the time of surgery (Table 1).The age at which the children underwent MRI over the14-month study period ranged from 1 year to 16 years, andthe time interval between the children’s sternotomy andimaging also varied widely from 1 year to 16 years.

In the sternotomy group, a thymus gland could beidentified on the MR images in 18 of the 62 children (29%).A visible thymus on the MR images was more likely to bepresent in those children who had undergone a sternotomy at ayoung age (36% for those younger than 4 years of age,compared to 15% for those 4 years or older; Fig. 1). However,this difference was not statistically significant (P=0.14).

Further analysis of these data by time between surgeryand imaging showed no clear relationship between durationof follow-up and the presence/absence of a thymus.

There were 37 children (21 boys, 16 girls) in the controlgroup. The age at time of MR imaging ranged fromyounger than 12 months to 16 years. In 34 of the 37children (92%), the thymus could be clearly seen on theaxial HASTE sequence, compared to 29% in the studygroup. This difference was found to be highly significant(P<0.0001). The three children in whom the thymus could

Pediatr Radiol (2009) 39:616–621 617

Table 1 Data for the sternotomy study group.

Patient no. Gender Age (years) at timeof last/only sternotomy

Age (years) attime of MRI

Interval (years) betweenlast/only sternotomy and MRI

Thymic remnantidentified on MRI

1 F <1 1 1 Yes

2 M <1 2 1 No

3 M 1 4 3 No

4 F <1 4 4 Yes

5 M 4 6 2 No

6 M 3 6 2 No

7 F 4 6 2 No

8 M <1 6 6 No

9 M 2 7 5 No

10 M <1 7 7 Yes

11 F 4 7 3 No

12 M 5 8 3 Yes

13 M <1 8 8 No

14 F <1 8 7 No

15 M 6 9 2 Yes

16 M 6 9 3 No

17 M <1 9 9 No

18 F <1 9 9 No

19 F 8 10 1 Yes

20 M 1 10 9 No

21 M 4 10 6 No

22 M <1 10 9 No

23 M <1 10 10 Yes

24 M <1 11 11 No

25 F 10 11 1 No

26 M 7 11 3 No

27 M <1 11 11 No

28 F 8 11 3 No

29 F <1 11 11 No

30 M 1 11 10 Yes

31 M 1 12 11 No

32 M 7 12 4 No

33 M <1 12 12 Yes

34 M 3 12 8 No

35 F <1 13 13 No

36 M 8 13 4 No

37 M 2 13 11 Yes

38 F 3 13 10 No

39 M 5 13 8 No

40 M <1 14 13 No

41 F 3 14 10 No

42 F <1 14 13 Yes

43 M 2 14 12 No

44 M 2 14 12 No

45 M 4 14 9 No

46 M 8 14 6 No

47 M 2 14 12 Yes

48 M 2 15 13 Yes

618 Pediatr Radiol (2009) 39:616–621

not be identified were aged 8, 15 and 16 years, and theanterior mediastinum could be clearly visualized. Onreview of the case notes of these three children, an obviouscause (e.g. recent significant illness prior to imaging) forthe absence of a visible thymus could not be identified.

Discussion

In over 90% of the children in the control group comprisingthose younger than 17 years who had not undergone anopen cardiac procedure, the thymus was easily identifiable

on the axial HASTE images obtained as part of a congenitalcardiac MRI protocol (Fig. 2). The presence of congenitalcardiac disease by itself did not appear to alter the grossmorphology of the thymus.

During congenital cardiac surgery via a median sternotomyapproach most of the thymus is routinely removed to gainaccess to mediastinal structures. Among the children in thesternotomy group, only 29% (18/62) had a visible thymus onthe contiguous axial HASTE images obtained after surgery,suggesting that less than a third of children have either apersisting or regenerated thymus after open cardiac surgery(Fig. 3). Thus, most children following open cardiac surgery

0

5

10

15

20

25

<1 yr 1-3 yrs 4-6 yrs 7-10 yrs

No thymus

Thymus

Num

ber

of c

hild

ren

Fig. 1 Proportion of children in the study group who had anidentifiable thymus on MR images, categorized according to age attime of surgery

Fig. 2 An 11-year-old child from the control group. Axial HASTE imageshows the thymus gland (arrow) within the anterior superior mediastinum

Table 1 (continued).

Patient no. Gender Age (years) at timeof last/only sternotomy

Age (years) attime of MRI

Interval (years) betweenlast/only sternotomy and MRI

Thymic remnantidentified on MRI

49 F 2 15 13 No

50 F 5 16 11 No

51 M <1 16 15 Yes

52 F 3 16 13 Yes

53 F 3 16 12 No

54 M 1 16 15 No

55 M 1 16 15 Yes

56 F 2 16 14 Yes

57 F 8 16 9 No

58 M 1 16 14 No

59 F <1 16 16 No

60 M 6 16 10 No

61 M 6 16 10 No

62 M <1 16 16 Yes

Pediatr Radiol (2009) 39:616–621 619

are left with a persistently altered contour to their superiormediastinum on any subsequent chest imaging (Fig. 4).

In this study we also found no radiological evidence ofthymic hyperplasia. However, we acknowledge that theinterval between sternotomy and imaging was more than1 year in all patients and thus we may have missed thosechildren with transient hyperplasia that might have occurredin the first few months following surgery.

The reason why a small proportion of children in thisstudy had a visible thymus after sternotomy is not clear. Itmay be because of varying surgical techniques, with somesurgeons excising less thymic tissue than others to gainaccess to the mediastinum. This potential variable is difficultto identify retrospectively when reviewing operative notesbecause the precise details and extent of the routinely

performed incidental thymectomy at the time of sternotomywas never described in detail in the operative notes.

This study does appear to show a weak, although notstatistically significant, link between undergoing cardiacsurgery at a younger age and having a visible thymus onsubsequent imaging. This could be explained by the fact thatthe thymus in younger children shows a greater lateralextent, and as this part of the thymus is less likely to affectaccess to the mediastinum intraoperatively, it may be lesslikely to be removed by the surgeon at the time ofsternotomy. Therefore, in younger children more thymictissue may be left behind within the mediastinum at the timeof surgery, which has a greater capacity for regeneration intoa visible structure on imaging. In addition, it may be thatresidual thymic tissue, regardless of the volume remaining,

Fig. 3 A 16-year-old patient who had previously had open cardiac surgery at the age of 7 years. Axial HASTE images (a, b) demonstrate noidentifiable thymic tissue within the anterior mediastinum

Fig. 4 Chest radiographs in a child before (a) and after (b) cardiac surgery demonstrate the presence and subsequent loss of the thymic shadowon the contour of the superior mediastinum

620 Pediatr Radiol (2009) 39:616–621

in younger children has a greater intrinsic regenerativecapacity than in older children. This hypothesis has, to ourknowledge, never been formally investigated.

Most children (71%), regardless of their age at sternotomy,did not have an identifiable thymus on MR imaging aftersurgery. This finding is consistent with previous immunolog-ical studies [5, 6] showing that children undergoing opencardiac surgery during infancy continue to have long-termdecreased peripheral T-cell count and impaired T-lymphocyte maturation years after surgery.

The consequence of having a reduced volume offunctioning thymic tissue in the infant and child, as wellas a reduced peripheral T-cell count, is unknown. In thefetus, absence of the thymus is known to be associated withcomplete absence of T-cell development and profoundimmunodeficiency (as seen in complete DiGeorge syn-drome). In our patient group it may be that minimal residualthymic tissue after sternotomy was, in fact, sufficient forimmune function, or it could be that extrathymic maturationcontributes to the well-being of these children [5, 7]. Thelong-term risk of reduced/absent thymic tissue in thispopulation with regard to infectious disease or malignancyhas yet to be fully evaluated and further prospective studiescorrelating a lack of visible thymic tissue with immunolog-

ical parameters, as well as assessing the long-term clinicalconsequences of reduced/absent thymic tissue, are required.

References

1. Janeway CA, Travers P, Walport M et al (2001) Immunobiology:the immune system in health and disease, 5th edn. GarlandPublishing, New York

2. Boyd E (1932) The weight of the thymus gland in health anddisease. Am J Dis Child 43:1162–1214

3. Baron RL, Lee JK, Sagel SS et al (1982) Computed tomography ofthe normal thymus. Radiology 142:121–125

4. Francis IR, Glazer GM, Bookstein FL et al (1985) The thymus:reexamination of age-related changes in size and shape. AJR 145:249–254

5. Eysteinsdottir JH, Freysdottir J, Haraldsson A et al (2004) Theinfluence of partial or total thymectomy during open heart surgeryin infants on the immune function later in life. Clin Exp Immunol136:349–355

6. Halnon NJ, Jamieson B, Plunkett M et al (2005) Thymic functionand impaired maintenance of peripheral T cell populations inchildren with congenital heart disease and surgical thymectomy.Pediatr Res 57:42–48

7. Torfadottir H, Freysdottir J, Skaftddottir I et al (2006) Evidence forextrathymic T cell maturation after thymectomy in infancy. ClinExp Immunol 145:407–412

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