Shoulder function following oncoplastic breast conserving surgery—a narrative review

Introduction

The high prevalence of breast cancer (BC) survivors makes it highly relevant to investigate late morbidity following the treatment. During the last decades, increased focus has been on late effects following the treatment of BC (1,2). The most important and prevalent late effects following BC surgery are lymphoedema, pain, as well as shoulder and arm morbidity (3-10). Besides, the cosmetic outcome is important to the women (11,12).

The risk of shoulder and arm morbidity following mastectomy with or without reconstruction is described in a recent review by Klein et al. (10). They found increased risk of locoregional morbidity following mastectomy compared to breast conserving surgery (BCS), and a risk of pain and functional deficits following mastectomy with reconstruction. Lauridsen et al. compared Constant Shoulder Score in patients having a mastectomy to patients having BCS. A higher risk of shoulder disability was seen among the group of mastectomized women, but the difference was non-significant unless the mastectomy was followed by radiation therapy (RT) to the chest wall (13).

Axillary surgery, especially axillary lymph node dissection (ALND), is known to be a risk factor for shoulder morbidity (1,14). Especially if followed by radiotherapy (4,10). Axillary surgery has been de-escalated during the last decades, and RT has been optimized by improved targeting and dose reduction. De-escalation of axillary surgery decrease the risk of late effects (14), but with the very good prognosis and many long-term survivors of BC, we must still focus on planning optimal surgery with as few late effects as possible, not only to the axilla, but also surgery of the breast.

Evidence-based knowledge assess a better overall survival of patients undergoing BCS vs. mastectomy, recommending BCS as the best treatment option for early BC. Indications to mastectomy for instance locally advanced BC still remain valid (15,16). The reason for the better prognosis is not fully understood, but it is speculated that the reason might be the RT following BCS leading to the abscopal effect (17). Another explanation might be the less invasive trauma of BCS compared to mastectomy, where the risk of triggering dormant tumour cells thereby facilitating relapse, is believed to be increased (18).

With the broad spectrum of oncoplastic breast conserving surgery (OPS) techniques, the possibilities of performing BCS as an alternative to mastectomy increases (19). If not only the survival benefit but also the risk of locoregional morbidity is as good or maybe even better for OPS, we should advise the patient to opt for BCS with oncoplastic techniques even if the lesion is large.

BCS means that only the cancer is removed (lumpectomy) with a margin of non-affected breast tissue followed by minor intramammary corrections. OPS covers a broad spectrum of different surgical techniques based on the integration of plastic surgery. A consensus from The American Society of Breast Surgeons was established in 2019, where OPS was divided in two main categories (20):

• Volume displacement—lumpectomy including redistribution of the resection volume over the preserved breast. Divided into two levels: level I, where less than 20% breast tissue is removed; level II, where 20–50% of breast tissue is removed.
• Volume replacement—lumpectomy, where volume is added using flaps or implants to correct the defect.

The evidence of the oncological safety and re-resection rate following OPS has been established in several studies (21-28). They report high overall survival rates and disease-free survival after OPS. Re-excision rates in the range 2.7% to 6.0% have been reported in OPS (25,29).

The overall risk of complications following OPS, which seem to be related to larger resection size, displacement of larger volumes, and longer scars, has been estimated to range from 9% to 38% (30-32). A meta-analysis from 2014 showed no significant difference in complication rates whether BCS was performed with or without OPS (21). It has been reported that some complications may delay and negatively affect subsequent adjuvant RT (33). On the other hand, delayed onset of chemotherapy has not been demonstrated (34,35).

A high level of excellent cosmetic outcome for BCS as well as OPS was demonstrated by Santos et al. with best results for OPS (36). Cosmetic results favoured OPS compared to mastectomy with immediate reconstruction (MxIR) (11).

The knowledge of late effects following BCS with and without oncoplastic surgery followed by RT is limited. If simple BCS is not possible the alternative has traditionally most often been mastectomy with or without immediate reconstruction.

The key question is if OPS causes late effects to the shoulder and arm on an acceptable level when compared to other surgical techniques of the breast. The main focus in this narrative review is shoulder function including restrictions in mobility, reduced strength, as well as functional impairment. We present this article in accordance with the Narrative Review reporting checklist (available at https://gs.amegroups.com/article/view/10.21037/gs-23-530/rc).

Methods

This narrative review aimed to examine the evidence on late effects following OPS focusing on shoulder morbidity.

Using the MeSH Terms “Breast Neoplasms”, “shoulder”, “oncoplast*”, and “reconstruct*”, the PubMed database was searched for relevant literature on the 6^th of June 2023 and a similar search was done in Embase and Scopus. An update was made on November 28^th, with no further results. All study types were eligible and at first there was no language restrictions or definite period of time.

The results from the literature search were managed in Covidence (www.covidence.org). After initial removal of duplicates (N=153), a total of 188 papers were left. Their titles and abstracts were screened for relevance by at least two of the authors, leaving 39 papers for a full text review. Eligibility criteria was: studies examining OPS reporting results concerning shoulder and arm function. Furthermore, only studies with full text available in English were included. We excluded non-human studies, conference abstracts, pilot studies, and papers where OPS was a part of total breast reconstruction. The full text review resulted in inclusion of seven papers. During the process, the reference lists of relevant publications were screened for supplementary studies, and two more articles were added (Figure 1, Table 1).

Figure 1 Flow chart regarding selection of included studies.

Each step of the screening was done by at least two independent authors, and the findings were compared. Discussion solved disagreements.

Key contents and findings

In general, OPS has limited postoperative complications (11,30,37), low re-resection rates (25,29), and the cosmetic outcome is acceptable with high patients’ satisfaction (11,36-38). Furthermore, OPS is safe with high overall and disease-free survival rates (21,23-25).

The knowledge of shoulder morbidity following OPS in general is limited, and few studies focus on the issue. In the present literature search, only nine relevant papers were identified (Table 2). Only two of them, Hauerslev et al. and Rose et al., included volume displacement. Both of them included volume replacement too, and did not differentiate between the surgical techniques (38,39). The rest of the studies only described volume replacement.

In an observational study, Zhou et al. compared shoulder morbidity in two groups: latissimus dorsi (LD) mini-flap vs. conventional BCS (depending on the need for replacement of volume) and found the LD mini-flap an excellent additional technique to conventional BCS according to shoulder morbidity (40). With a follow-up of 1 year, the Disabilities of the Arm, Shoulder, and Hand (DASH) questionnaire was used, and an objective evaluation of range of motion (ROM) and muscle strength was made. In their conclusion, the patients having a LD mini-flap OPS enabling larger excision had a low risk of postoperative complications, a high level of aesthetics, and minimal functional impairment. All the patients had received ALND and RT, and no description of the extent of RT was given, which makes it difficult to judge the effect of the breast surgery, as the axillary surgery and RT is assumed to affect the shoulder function and thereby blurring the effect of the breast surgery.

In the small cohort study by Hamdi et al. 63% of the 22 included patients had ALND—RT was not consequent in all patients. This reduce the strength of the conclusion, saying donor site morbidity following thoracodorsal artery perforator (TDAP) flap was reduced to a minimum (41). They focused on donor site morbidity and compared the operated sides to the non-operated sides by measuring strength, LD thickness and shoulder mobility by ROM. The ROM was equal on both sides in most directions except active and passive forward elevation and passive abduction. The muscle strength and thickness of LD was preserved.

The systematic review from Mangialardi et al. was based on studies reporting on the use of the TDAP and included among others the study by Hamdi et al. and a randomised controlled trial (RCT) by Abdelrahman et al. (37,41,42). Five of the 12 included studies reported on shoulder function following oncoplastic surgery. None of them reported severe shoulder morbidity. A broad spectrum of evaluation methods was used in the studies, but despite that, the review concluded that OPS with TDAP is safe and has low morbidity.

The cross-sectional study by Rose et al. compared 96 BC patients treated with OPS to 631 BC patients treated with conventional BCS (39). Of the 96 OPS patients, 32 had level I and 64 had level II OPS surgery. Level I was defined as adaption and minor mobilisation of glandular tissue with or without repositioning of the nipple-areola-complex. Level II OPS comprised reduction mammoplasty, volume displacement, and volume replacement techniques. The patients were identified from the Danish Breast Cancer Cooperative Group (DBCG) registry and evaluated by patient-reported outcome measure (PROM) using the Breast-Q and a study-specific questionnaire. The response rate was 48.3%. They found no clear difference in physical well-being evaluated by the health-related quality of life (HRQoL) even though it was indicated that the OPS group comprised BC patients with a more advanced disease stage.

Another cross-sectional study including 174 patients divided into four groups with difference in axillary surgery [ALND vs. sentinel node (SN)] as well as in breast surgery (BCS vs. LD mini-flap reconstruction) found a negative impact on shoulder function for the group treated by the combination of ALND and LD mini-flap (43). This may speak to the favour of conventional BCS over LD mini-flap OPS in combination with ALND. The shoulder function was evaluated by Quick-DASH (Q-DASH) and the median follow-up time was 24 months with a very wide range of 3–108 months making the results difficult to compare.

The mean follow-up time in the cross-sectional study by Aristokleous et al. was 24 months and, like in the above-mentioned study, with a wide range (2–55 months) (44). They compared OPS and BCS in 215 BC patients and found for both surgery types that they affected physical function evaluated by DASH and Breast-Q, without any difference between surgery types. RT and SN did not adversely affect the outcome but was however not described in detail. The performed OPS was therapeutic mammaplasties, reductions, or volume replacement by chest wall perforator flaps (CWPF). The aim of the study was to compare the difference in PROMs when the patients were submitted to preoperative standardized surgical assessment and shared decision-making and the conclusion supported that these tools may de-escalate OPS.

Kelsall et al. compared mastectomy with MxIR (281 patients) including deep inferior epigastric perforator (DIEP) flap with OPS including therapeutic mammoplasty and CWPF (286 patients) in two unmatched and afterwards case-matched cohorts. An institution-specific questionnaire revealed favouring of OPS according to “return to full function and activity” (11). Even if the OPS group that received RT was compared to a MxIR group that required or did not require post-mastectomy RT the “return to full activity” was still faster in the OPS group. One of the forces in this study was the consideration and matching according to RT but also breast size.

In a large prospective study comparing OPS (105 patients) with BCS (229 patients), Hauerslev et al. found a comparable risk of shoulder morbidity in a follow-up period of 18 months—even though OPS was offered in patients with larger tumours and with a more advanced disease stage (38). The study mostly, but not exclusively, described volume displacement including reduction OPS. The study did not distinguish between volume displacement and volume replacement in the inclusion of patients nor in the reporting of the results. The shoulder morbidity was evaluated by a non-validated questionnaire including Visual Analogue Scale and Likert items.

Only one suitable RCT was identified in the literature search (42). The study was very small with only 42 included BC patients divided into two groups: partial breast reconstruction using LD flap or using TDAP. Follow-up was after 3, 6 and 12 months. The TDAP group had a significantly better functional outcome of the shoulder evaluated by Shoulder Pain and Disability Index (SPADI).

Agrawal recommends, in a review of how to plan oncoplastic and reconstructive breast surgery, how to select patients for the different procedures. Patient and case characteristics were divided into three categories (high, average, and low complexity) to aid selection in the complexity of a certain BC cases. One of the patient characteristics of importance for choosing the right kind of surgery was the patient’s shoulder limitations before surgery (45).

Following the Delphi consensus conference in 2019, Weber et al. reviewed the gaps in the knowledge of OPS. Their conclusion was that quality-of-life and surgical morbidity should be further investigated. They recommend to implement a prospective register based on a defined set of core variables for oncoplastic procedures in centers performing OPS. This register could facilitate further investigation by observational and RCT studies (46).

The heterogeneity in the selected studies was high—one publication was a systematic review, one an RCT, four were cohort studies, and three were cross-sectional studies (11,37-44). Some of the studies were small and there was a considerable variation in follow-up time. They described shoulder function following different kinds of OPS; primarily volume replacement techniques including CWPF. Only two studies included volume displacement too, but not separating the two techniques neither according to inclusion nor to reporting the results. Separating the two techniques would have been interesting, as one could imagine that volume replacement would affect the shoulder morbidity more than volume displacement. This review cannot answer the question whether the two techniques are comparable according to shoulder morbidity.

The assessment of shoulder function was based on several different evaluation methods. Among them, ROM, DASH, Q-DASH, SPADI, HRQoL and non-validated subjective questionnaires were used. Also, the variation in axillary surgery and RT within and between the studies made the comparison difficult.

With the use of Covidence to manage the literature search, the risk of missing important studies is low. At least two authors have systematically screened titles, abstracts and finally full text studies. The references in the selected full text studies were screened for relevance and the review was supplied with further studies. During the whole process the authors solved disagreements by discussion.

Conclusions

The requisite knowledge of late effects following OPS is still not available for unambiguous recommendations. This narrative review has elucidated the knowledge and has reached a conclusion based on review of the existing literature of this item.

We found that the risk of decreased shoulder function caused by OPS—volume displacement as well as volume replacement—does not exceed the risk of shoulder problems seen after BCS and mastectomy with or without immediate reconstruction. Therefore, OPS can be considered if conventional BCS is not possible. But the knowledge of shoulder function after OPS is limited, and studies comparing shoulder function after OPS, BCS and mastectomy with or without immediate reconstruction are warranted.

Acknowledgments

Funding: None.

Footnote

Provenance and Peer Review: This article was commissioned by the Guest Editors (Tine Engberg Damsgaard, C. Andrew Salzberg and Jørn Bo Thomsen) for the series “Hot Topics in Breast Reconstruction World Wide” published in Gland Surgery. The article has undergone external peer review.

Reporting Checklist: The authors have completed the Narrative Review reporting checklist. Available at https://gs.amegroups.com/article/view/10.21037/gs-23-530/rc

Peer Review File: Available at https://gs.amegroups.com/article/view/10.21037/gs-23-530/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://gs.amegroups.com/article/view/10.21037/gs-23-530/coif). The series “Hot Topics in Breast Reconstruction World Wide” was commissioned by the editorial office without any funding or sponsorship. M.D.L. and M.B.R. report that they receive honoraria for serving as the speakers of an educational arrangement for breast cancer specialists at Aarhus University Hospital financed by Pfizer, and they are the leaders of a course of breast surgery educating junior doctors, the course and their wage for arranging the course is paid by The Danish Health Authorities. The authors have no other conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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