Touch sensibility in the breast after subcutaneous mastectomy and immediate reconstruction with a prosthesis

British Journal,o~ Phric Surgery (1997). 50, 443-449 8 1997 The Bntlsh Association of Plastlc Surge&

Touch sensibility in the breast after subcutaneous mastectomy and immediate reconstruction with a prosthesis

K. P. Benediktsson,* L. Perbeck,’ E. Geigant+ and G. Solders’

*Departments of Surgery and ‘Clinical Neurophysiology, Kurolinska Institute at Huddinge University Hospital, Huddinge, Sweden

SUMMA RX Touch sensibility was assessed with von Frey’s monofilaments in the breasts of 10 healthy women (controls) and of 80 women with breast cancer who at least 1 year previously had undergone subcutaneous mastectomy and immediate reconstruction with a prosthesis. Touch thresholds were measured at nine positions on each breast.

Low threshold values (< 3.2 mN) and good reproducibility were found in the controls. In the patients’ surgi- cally treated breasts normal (< 3.2 mN) or subnormal (< 20 mN) median threshold values were found outside the areola. Higher median values were noted on the areola and nipple; on the nipple, however, one third of the patients had normal sensibility while 14% lacked sensibility.

The only factors found to influence the results were simultaneous subcutaneous reduction mammaplasty (lower touch thresholds) and the localisation of the incision (slightly lower thresholds for lazy-S than inframammary incision).

These results confirm the clinical impression that touch sensibility is substantially retained after subcutaneous mastectomy and immediate reconstruction with a prosthesis.

Sensory innervation of the breast is supplied primarily by the lateral and anterior cutaneous branches of the second to the fifth or sixth intercostal nerves. The lateral cutaneous branches innervate the skin of the breast laterally through their anterior rami, also known as lateral mammary branches, while the anterior cutaneous branches innervate the medial parts through their medial rami. sometimes called medial mammary branches. A limited region of the skin covering the upper portion of the breast is supplied by nerves arising from the cervical plexus, specifically branches of the supraclavicular nerves. There appears to be no crossover of innervation from the contralateral side.’ The nipple and areola are mainly innervated by the anterior ramus of the lateral cutaneous branch of the fourth intercostal nerve.’ 6

Miller and Kasahara’ have demonstrated that the most superficial layers (the epidermis and the immedi- ately underlying part of the dermis) of the nipple- areola complex are poorly innervated, while the deeper layers of the dermis are richly innervated, mostly by free nerve fibre endings. The skin outside the areola is richer in superficial nerve endings, which often are associated with hair follicles.

Loss of skin sensibility has been reported after most kinds of breast surgery, particularly after breast reconstruction.‘,’ i.i: ” Since December 1988 we have performed subcutaneous mastectomy and immediate reconstruction with a prosthesis in patients with breast cancer not suitable for lumpectomy but without involvement of the skin or nipple-areola complex. The operation usually takes less than 2 hours, even with axillary dissection. Other authors have reported good

cosmetic results and an acceptable recurrence rate after this operation for breast cancer.‘G’8 Our operative methods have undergone some changes, partly as a result of the development of saline-filled implants with textured surfaces. In contrast to silicone-tilled implants, these can be placed subcutaneously instead of submuscularly without getting a significant increase in the frequency of capsular contraction.‘9,“’ From a cosmetic point of view the subcutaneous location is usually preferable, as most women with breast cancer are over 40 years old and have developed some ptosis of the breasts.

The purpose of the present study was to determine the frequency and degree of sensibility loss after this operation and to correlate the sensibility loss to different types of treatment, particularly surgical techniques.

Patients and methods

Patients and controls

Women with breast cancer who had undergone subcutaneous mastectomy and immediate reconstruction with a prosthesis at least 1 year before the time of examination and who did not fullil any of the exclu- sion criteria listed below were included in the study. The original series consisted of 125 consecutive patients, 40 (32%) of whom were excluded. Ten patients were excluded because of a new operation on the same breast during the year before the study, 11 because they had no nipple and 7 because both breasts had been operated on. Seven patients had moved away, and 5 had died (3 from metastases, 2 from other causes).

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444 British Journal of Plastic Surgery

A consent form with information about the examination was sent to the remaining 85 patients. Five declined to participate. Thus, 80 patients were examined. Their mean age was 54 years (range 40-80). Forty five patients (56%) had a scar after a previous lumpectomy when admitted for subcutaneous mastectomy. Axillary dissection was performed in 69 patients (86%) either before or at the mastectomy. Post- operatively 17 patients (21%) were given radiotherapy (48 Gy) to the thoracic wall and lymph nodes. Chemotherapy (cyclophosphamide, methotrexate and 5-fluorouracil) was given to 19 patients (24%) 7 of whom also received radiotherapy.

On the basis of the operative method, the patients were grouped as follows:

Group A (n = 15). Lazy-S shaped horizontal incision (above and lateral to the areola)*’ and a submuscularly located prosthesis.

Group B (n = 13). Subcutaneous reduction mammaplasty through a keyhole skin incision with a wide vertical pedicle of skin and fat*’ and a submuscularly located prosthesis, and a reduction mammaplasty or mastopexy of the contralateral breast.

Group C (n = 24). Lazy-S incision and a subcutaneously located prosthesis.

Group D (n = 28). Inframammary incision and a subcutaneously located prosthesis.

Table 1 Patient details.

There were no significant differences between the groups for the other treatments given (Table 1).

Ten healthy volunteers from the hospital staff, with a mean age of 38 years (range 26-63) were included as controls. Nine were tested twice with an interval of 6-12 months to evaluate the reproducibility of the test. For analysis of the results each control’s right breast served as the ‘treated’ one and the left breast as the contralateral one. Besides the 10 healthy controls, the patient’s ‘healthy’ breast (the untreated side) served as control in each case.

All 80 patients and the 10 controls gave their informed consent to participate in the study, which was approved by the hospital ethics committee.

Assessment of touch thresholds

Tactile thresholds were assessed with von Frey’s hairs. With the patient in a semisupine position with closed eyes in a warm room (23”Q a series of 20 nylon filaments (Stoelting Co., Wood Dale, IL, USA) with bending thresholds of 0.035-2052 milliNewton (mN) (0.0036-209.2 g) were applied perpendicularly to the skin at nine positions on each breast (Fig. 1): on the nipple (test site 3), at 9, 3, 12 and 6 o’clock just inside the areola (sites 2, 4, 7 and 8 respectively) and at four corresponding sites 1.5-2.5 cm outside the areolar edge, depending on breast size (sites 1, 5, 6 and 9 respectively). The threshold was defined as the minimal

Group Number Mean age Months between op. and exam. Radiotherapy Chemotherapy Previous lumpectomy Axillary dissection (years) Mean (SD) n (“9) n (x) n (“96) n (5)

A 15 48 31.8 (9.8) 5 (10) 4 (27) 9 (60) 14 (93) B 13 54 30.5 (6.0) 2 (15) 4 (31) 5 (38) 12 (92) C 24 55 20.8 (4.2) 5 (21) 5 (21) 15 (63) 19 (79) D 28 58 19.1 (4.8) 5 (18) 6 C-21) 16 (57) 24 (86)

Total 80 54 23.9 (8.2) 17 (21) 19 (24) 45 (56) 69 (86)

SD: standard deviation.

Fig. 1

Figure l-(A) Touch sensibility being tested with a von Frey hair on a right breast. Test sites marked with ink. (B) Test sites on a right breast.

Breast sensibility after subcutaneous mastectomy 445

bending force (in mN) of the thinnest filament sensed by the subject in a descending series of applications (‘no value’) at four trials. When none of the filaments was sensed the sensibility was registered as 2000 mN.

All 20 filaments were calibrated exclusively for this study on a microscopic balance. The values of the mass in grams required to bend the tip of the filament were converted to force units (milliNewtons) by the formula F = m x g (g = 9.818).

The following were done to minimise errors:

1. The same instrument was used for all measurements after calibrating its filaments on a microbalance.

2. The same investigator (EG) performed all the measurements in the same surroundings and at the same room temperature and took care to apply the filaments in the same way every time.

Statistical methods

Values for touch thresholds are given in mN as medians and interquartile range. Because of skewness of the data from the breast cancer subjects all results were log transformed and then analysed according to a factorial experiment analysis of variance with one independent factor and two dependent factors. The independent factor was group (operative method) with five levels (A-D and controls), and the dependent factors were side with two levels (treated and untreated breast) and test site with nine levels. In case of significant interactions between the factors in the model, simple main effects were examined with multiple com- parisons test according to Bonferroni/Dunn. P < 0.05 was accepted as significant.

Results

In the healthy controls we found an even distribution of threshold values and no significant differences between sides. The mean values for the right and left side were therefore used for calculation of normal limits (Table 2). In the nine controls that were tested twice, no significant differences in touch thresholds were found between the two occasions. Lower threshold values were noted on the skin outside the areola than on the areola and nipple. Significant differences (P < 0.05) were observed when site 4 was compared with sites 1, 5, 6 or 9 and when site 8 was compared with sites 1 or 6. Based on the data from the controls, threshold values < 3.2 mN were considered as normal, 3.2-20 mN as moderately raised and 20.1-200 mN as highly raised. Values exceeding 200 mN were judged to represent loss of touch sensation.

Table 2 Touch thresholds in healthy controls

In all four patient groups the touch threshold values on the treated breast were generally high and unevenly distributed on the nipple-areola complex (sites 2, 3, 4, 7 and S), but much lower and more evenly distributed outside the areola (sites 1,5,6 and 9), where the highest median touch thresholds were found laterally and inferiorly (sites 1 and 9; range 2.5-l 1.6 mN) and the lowest ones (P < 0.001 compared to any other site in groups A-D together) medially (site 5; range 1.5- 1.8 mN). There were significant interactions between groups regarding the differences in touch thresholds between sides and also regarding differences between test sites on the operated breast but not on the contralateral breast. There were significant differences between sides regarding differences in touch thresholds between test sites, the distribution between sites of touch threshold values being much more uneven on the treated breast than the untreated one.

The distribution of touch threshold values on the nipple is shown for all groups in Fig. 2 (logarithmic scale) and Table 3 (percentage distribution). The values were higher in group D than in the other patient groups, but the differences were not significant.

Median values for different test sites in the different groups are given in Table 4. Patient groups A, C and D showed significantly higher touch thresholds as compared with the controls on all test sites except site 5 for group A and site 4 for group C. In group B (patients who had undergone subcutaneous reduction mammaplasty) no significant differences were found in touch thresholds as compared with the controls except on site 9 (inferiorly on the skin).

In Figure 3 the means of the medians for all nine test sites in the different groups (Table 4) are compared. When all test sites were combined, there were no significant differences between the results for group A (implant located submuscularly) and group C (subcutaneous location of implant). In the controls the median touch threshold values for all test sites combined were significantly lower than in any of the patient groups except group B.

In group B the touch thresholds were generally lower than in the other patient groups, but the difference was significant only in comparison with group D (patients operated through an inframammary incision), both when all nine test sites were considered together and when considering only sites 2, 7 or 8 (all on the areola) but not when considering only sites 1, 3,4, 5,6 or 9. Only one of the patients in group B lacked sensibility of her nipple (she had suffered epidermal necro- sis of the nipple postoperatively).

The inframammary incision (group D) resulted in slightly more impaired sensibility than the lazy-S incision (group C), but the difference was significant only

Tut site I 2 3 4 5 6 7 8 9

Mean 0.52 1.02 1.04 1.91 0.47 0.43 1.30 1.36 0.81 Standard deviation 0.81 1.32 0.85 1.84 0.54 0.60 1.32 1.18 0.81

Results are given in milliNewtons as the mean of the mean threshold values of the right and left breast for each of the nine test sites in all ten controls.


: 2395 76 0 m 881 0

..-- E 324 5 '1 119 (D F 44 a; Ei 16 a .- c 6 al 5 2 2

2 8E-1

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; lE-1

; 4E-2 5

0 8 0

0 8

0

0 :

0 8 0 8 0

4- 1 0 8 0 e-

0

0

0 0

0 0 0 0

A B C D Controls Group

Fig. 2

Figure 2-Touch thresholds (mN) on the nipple of the treated breast in the four groups of patients (A-D) and in the controls. Grid line at zero. Median value is indicated with a bar.

Table 3 Percentage distribution of touch thresholds on the nipple

Group A B c D A-D Controls

Normal (< 3.2 mN) 33.3 38.5 45.9 14.3 31.3 100 Moderately raised (3.2-20 mN) 40.0 53.8 29.1 28.6 35.0 0 Highly raised (20.1-200 mN) 6.1 7.7 8.3 42.9 20.0 0 Lack of sensibility (> 200 mN) 20.0 0 16.1 14.3 13.8 0 Median threshold (mN) 9.1 3.5 9.1 33.8 9.1 1.2

Table 4 Median touch thresholds on the treated breast and in the controls

Group Test sites Mean of medians for sites

I 2 3 4 5 6 7 8 9 I-9

A 11.6 11.6 9.1 19.8 1.9 9.1 11.6 9.1 9.1 10.3 (176.4) (552.9) (114.8) (60.5) (3.4) (28.4) (41.7) (59.9) (32.8)

B 2.5 (i::) 3.5 3.5 1.8 1.8 9.1 3.5 2.5 3.5 (7.6) (1.6) (11.7) (1.5) (3.3) (17.5) (9.9) (21.9)

C 6.3 19.8 9.1 9.1 1.9 3.5 33.8 19.8 6.3 12.2 (104.1) (64.1) (31.8) (13.3) (2.5) (38.8) (148.9) (3 1.4) (33.4)

D 11.6 57.6 33.8 19.8 1.9 2.7 26.8 67.6 11.6 25.9 (148.9) (167.8) (106.2) (141.1) (11.5) (25.6) (90.1) (140.3) (37.2)

Total 9.1 19.8 9.1 10.4 1.9 3.0 19.8 19.8 9.1 11.3

A-D (141.1) (148.4) (45.4) (30.8) (3.0) (18.0) (61.3) (64.1) (31.9)

Controls 0.2 0.3 1.2 1.7 0.1 0.2 1.0 1.5 0.6 0.8 (0.3) (1.8) (1.8) (2.9) (0.9) (0.3) (2.7) (2.4) (1.7)

All values are in mN. Figures in parentheses are the interquartile ranges (IQR = 9’3’).


35 ,

Fig. 3

Figure 3-Mean values (bar: standard error) of the median touch thresholds for all test sites (1-9) of the treated breast in each patient group (A-D) and in the controls. There are significant differences (P c 0.05) only between the patient groups B and D, and between the controls and patient groups A, C and D.

for sites 4 and 8 (both on the areola) and not for all nine test sites combined.

When the patients who had undergone axillary dissection (n = 69) were compared with those who had not (n = 1 I), no differences were found at the nipple- areola complex, but the threshold values were slightly higher at test sites outside the areola (sites 1, 5, 6 and 9; P < 0.05) in the axillary dissection group. Neither radiotherapy, chemotherapy nor previous lumpectomy affected the results significantly; however, few patients had radiotherapy or chemotherapy. No correlation was found with the patients’ age or with the interval between operation and examination.

In the contralateral (untreated) breasts the results obtained from all test sites were within our normal limits. Compared to the controls there were no significant differences in touch thresholds for any of the patient groups when all test sites were considered together. In group D we found significantly higher touch thresholds as compared to the controls when sites 2 and 7 (both on the areola) were considered alone. In group B (in which the contralateral breast had been treated with a conventional reduction mammaplasty), significantly higher touch thresholds than in the controls were found at site 7 (superiorly on the areola). The touch thresholds in the contralateral breasts were not significantly higher in group B than in the other patient groups. Compared to the treated breasts significantly lower touch thresholds were found in the contralateral breasts at all test sites in groups A and D and at all except site 4 in group C, but in group B the differences were significant only for sites 4, 5, 6 and 9.

Discussion

In most patients we found normal or only moderately raised touch thresholds outside the areola, especially on the medial side. On the areola and nipple higher

thresholds were generally found but only 14% lacked touch sensibility (> 200 mN) on the nipple and 31% had normal values (< 3.2 mN). The lazy-S incision resulted in slightly better preserved sensibility on the medial and inferior part of the areola when compared to the inframammary incision. The location of the prosthesis (submuscular or subcutaneous) did not influence the results. The best sensibility was found in the group that underwent subcutaneous reduction mammaplasty (group B). In this group only one patient lacked sensibility on the nipple, and the median touch thresholds were within our normal limits at most test sites.

The test method

Von Frey’s method of measuring touch sensibility thresholds is simple to use but easy to misinterpret. Its use necessitates good understanding of the factors that can influence the results. The buckling force for individual filaments may differ considerably between different instruments, and the probe numbers provided by the manufacturers, representing the logarithm of 10 times the buckling force in milligrams, cannot be taken for granted.” After taking the precautions described above in the methods section, however, we believe our results to be reliable. The results obtained for the nine controls that were examined twice give credit to the method’s reproducibility. The perception of von Frey’s hairs is probably an expression of both touch, pressure and pain, which makes them suitable for our purpose. Vibration instruments are likely to affect a more limited range of receptors, and the stimulus is dampened by the fat and connective tissue. The two-point discrimi- nation test is inappropriate, because of the limited area of the nipple and areola and the relatively large receptor fields of the skin covering them.

Anatomical considerations

Our results correlate well with the anatomy of the nerves of the breast.’ h The final touch perception after a breast operation is of course a combination of the sensibility maintained and that regained by reinnervation postoperatively. Clearly it must be difficult to per- form a subcutaneous mastectomy without severing the anterior ramus of the lateral cutaneous branch of the fourth intercostal nerve at its entrance into the breast or elsewhere during its course to the nipple-areola complex. As the rest of the breast skin is more richly and more superficially innervated, it retains its sensibility better than the nipple-areola complex, which is mainly innervated by the fourth intercostal nerve. The differences in the distribution of sensory nerve endings may also explain the higher touch thresholds on the nipple-areola complex compared to the surrounding skin among our controls.

Subcutaneous reduction mastectomy

The more peripherally in the breast the nerves are severed during a breast operation, the more difficult will be the reinnervation of the nipple-areola complex. One would therefore expect the reinnervation of the


nipple-areola complex to be less complete after subcutaneous mastectomy than after reduction mammaplasty, when it can begin at the edge of the areola. Courtiss and Goldwyn’ found unchanged sensation in the nipple and areola in 65% of their patients after reduction mammaplasty (transposition methods) but ‘reasonable’ sensation in the nipple and areola in only 25% of patients after subcutaneous mastectomy. They observed that the sensibility returned in the peripheral skin before it did in the nipple and areola. Other investigators have found that the sensibility often returns completely in breasts after pedicled reduction mammaplasty.4,5,21 Even following breast reduction and free nipple transplantation, Townsend’ found a return of sensation in the transplants in 82% of breasts 1 year or more postoperatively. In gigantomastia the sensibility may even be improved postoperatively, both after pedicled and amputation/free-nipple-graft reductionz3 After augmentation mammaplasty, Courtiss and Goldwyn’ found decreased sensation in the nipple and areola in 15% of 249 patients 2 years postoperatively. There was no difference in sensation whether the implant was inserted through an inframammary incision or through or around the areola. Farina et al.’ found no significant reduction in sensibility in 20 patients after augmentation mammaplasty, 10 of whom were operated by the periareolar route and 10 by the inframammary route. Great care was taken to spare the nerves to the nipple-areola complex.’

We performed subcutaneous reduction mammaplasty with a wide inferiorly based pedicle of skin and fat engaging the area at 4 o’clock in the left breast and 8 o’clock in the right. We believe that this explains the relatively good sensibility postoperatively in this group of patients (group B). By sparing as much as possible of the subcutaneous fat in the pedicle, we have probably minimised the trauma to the anterior ramus of the lateral branch of the fourth intercostal nerve. It is not surprising that the differences in touch thresholds between sides were the lowest in this group, as both breasts in every patient had surgery (conventional reduction mammaplasty in the contralateral breast). In group B site 9 (inferior site on the skin) is located at the meeting point of the lateral and medial flaps, which were thinner in the breasts subjected to subcutaneous mastectomy than in the contralateral breasts. This may well explain why the difference was greatest at this test site.

Type of incision

The differences we found between patients with an inframammary incision and those with a lazy-S incision may be explained similarly. The inframammary incision often has to be extended quite far laterally to reach the axillary tail of the mammary gland. The route of dissection then obviously leads through the subcutaneous tissue at the entry of the important branch from the fourth intercostal nerve into the breast. We did not make any special effort to spare this nerve, simply because at that time we were not aware of its importance. There may also have been a ten- dency to remove more of the subcutaneous fat in the inferior part of the breast when operating through an

inframammary incision than when the dissection was made from above. Thirdly, the operations through a lazy-S incision were mostly performed by the same surgeon, while a few different surgeons (including some with less experience in this kind of surgery) performed the operations through an inframammary incision. They may have been more reluctant to leave subcutaneous fat, as the first priority was to remove all glandular tissue. Altogether we find that these reasons sufficiently explain the significantly higher touch threshold values found in the medial and inferior parts of the areola in patients with an inframammary incision. These differences could at least be partly avoided in future operations, bearing these reasons in mind. In our opinion the inframammary incision is still a better choice, unless the patient already has a scar near the areola. Why axillary dissection affected the sensibility only of the breast skin outside the areola may be explained by the depth, in its lateral part, of the main nerve to the nipple-areola complex.

Other factors

We found no significant correlation between breast sensibility and age. This does not mean that age is of no importance for the sensibility. Most likely skin sensibility in the breast diminishes with increasing age, as has been shown for some other regions,24x25 although our series of patients is too small and too heteroge- neous (because of differences in operative methods) to show this. Quite possibly this is the main reason why the controls had slightly better sensibility than that found in the patients’ untreated breasts. Evaluating the possible effects of radiotherapy and chemotherapy was not the main purpose of this study, and the patients receiving such adjuvant therapy were too few to allow any valid conclusions.

Comparison with other methods for breast reconstruction

Several investigators have used von Frey’s instrument to measure breast sensibility after reconstruction with musculocutaneous flaps. Slezak et a1.9 examined ten patients after breast reconstruction with a pedicled transverse rectus abdominis musculocutaneous (TRAM) flap and found no sensibility in two flaps and ten times higher touch thresholds than normal in the rest of the flaps. Lapatto et al.” studied 39 patients after breast reconstruction with free TRAM flaps and found little or no sensibility in more than 75% of the flaps. Liew et al.13 found a measurable sensory recovery in 16 of 28 patients (76%) 7-68 months following reconstruction with TRAM flaps with median values ranging from 2-10 times higher than those of normal controls. Peltoniemi et al” studied 44 patients after latissimus dorsi breast reconstruction with an endo- prosthesis and found some degree of sensibility in some part of the flap in 64% of the patients but normal sensibility, according to their definition (C 49 mN), in some part of the flap in only about one quarter of the patients. None of these authors report any sensibility in the nipple-areola complex of their patients’ breasts.


Conclusion

After subcutaneous mastectomy and immediate reconstruction with a prosthesis in breast cancer, touch sensibility is normal or subnormal in the skin outside the areola in most patients, but considerably reduced in the nipple-areola complex. As far as postoperative sensibility is concerned, the method is superior to modified radical mastectomy followed by breast reconstruction with a musculocutaneous flap. By taking care to preserve the lateral mammary branch of the fourth intercostal nerve while performing the subcutaneous mastectomy, it is probably possible to minimise the loss of sensibility in the nipple-areola complex without affecting the radical extent of the operation.

Acknowledgements

The authors wish to thank Mrs Elisabeth Berg, statistician at the Karolinska Institute. for her help with the statistical analysis of the results,

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The Authors Kristinn I? Benediktsson MD, General Surgeon.

Department of Surgery

Leif Perbeck MD, BSc, Associate Professor, Department of Surgery

Evy Geigant RN. Department of Clinical Neurophysiology

Giiran Solders MD, BSc, Associate Professor. Departments of Neurology and Clinical Neurophysiology

Karolinska Institute at Huddinge University Hospital, Huddinge. Sweden.

Correspondence to Kristinn Benediktsson. Department of Surgery, OSS, 7300 Orkanger. Norway.

Paper received 29 July 1996 Accepted 2 April 1997, after revision

Documents

Touch sensibility in the breast after subcutaneous mastectomy and immediate reconstruction with a prosthesis