Patterns and outcomes of breast reconstruction in older women – A systematic review of the literature

Patterns and outcomes of breast reconstruction in older women – A systematic review of the literature

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Patterns and outcomes of breast reconstruction in older women e A systematic review of the literature D.D. Oh a, K. Flitcroft a,b, M.E. Brennan a,b, A.J. Spillane a,b,c,* a

Breast and Surgical Oncology, The Poche Centre, 40 Rocklands Rd, North Sydney, New South Wales, Australia b Northern Clinical School, Sydney Medical School, The University of Sydney, Sydney, New South Wales, Australia c Royal North Shore and Mater Hospitals, Sydney, New South Wales, Australia Accepted 4 February 2016 Available online - - -

Abstract Purpose: Older age is associated with lower rates of breast reconstruction (BR) for women requiring mastectomy. The purpose was to assess the available evidence on uptake, outcome and quality of life (QoL) after BR in older women. Methods: A systematic literature review was performed via Medline, Embase and Cochrane databases using the search terms breast reconstruction, breast cancer, and mastectomy. Eligible studies reported rates of BR, rates of different reconstructive techniques, complication rates, and/or patient reported outcome measures (PROMs) of BR in women aged 60 years or older undergoing mastectomy for ductal carcinoma in situ or invasive carcinoma. Results: A total of 42 eligible studies were included, with 32 of these reporting BR rates, 10 reporting rates of different reconstructive techniques, 10 reporting rates of complications, and four reporting PROMs. The studies reported 24,746 cases of BR in 407,570 mastectomy patients aged 60 years or older from 1987 to 2012. Implant based BR was more common than autologous techniques. Mostly, complication rates were not higher in older women, and QoL outcomes were similar to younger women. Conclusions: This review confirms that BR rates are lower in older women despite recent studies demonstrating its efficacy. The perception among some surgeons and women requiring mastectomy that the potential risks of BR in older women outweigh the benefits needs to be revisited. Education of consumers and surgeons along with public advocacy for offering BR to all clinically eligible women are the most promising means of changing practice. Ó 2016 Elsevier Ltd. All rights reserved.

Keywords: Breast cancer; Breast reconstruction; Mastectomy; Elderly; Complications; Outcomes

Introduction Most women affected by breast cancer are over the age of 60 at diagnosis. In Australia, approximately 51% of the 13,567 women newly diagnosed with breast cancer in 2008 were aged 60 years or older.1 The United Kingdom (UK) reported even higher rates, with 59% of the average 49,557 new breast cancer cases per year between 2009 and 2011 being women aged 60 years or older.2 Breast * Corresponding author. Breast and Surgical Oncology, The Poche Centre, 40 Rocklands Rd, North Sydney, New South Wales, Australia. Tel.: þ61 2 9911 7250. E-mail address: [email protected] (A.J. Spillane).

cancer prevalence is projected to increase even further over time due to the ageing populations coupled with earlier detection through routine breast cancer screening.1,3,4 Furthermore, better treatments are resulting in older patients having improved survival rates with longer lives after the breast cancer diagnosis.5 Given these factors, breast reconstruction (BR) after mastectomy is an increasingly important consideration for older women (defined here as 60 years of age). Studies have shown the benefits of post-mastectomy reconstructive surgery on quality of life (QoL).6,7 Despite this, rates of BR vary between surgeons, centres and countries, ranging from <5% to 85%.8 Findings from the few

http://dx.doi.org/10.1016/j.ejso.2016.02.010 0748-7983/Ó 2016 Elsevier Ltd. All rights reserved. Please cite this article in press as: Oh DD, et al., Patterns and outcomes of breast reconstruction in older women e A systematic review of the literature, Eur J Surg Oncol (2016), http://dx.doi.org/10.1016/j.ejso.2016.02.010

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studies that report the proportion of women who are offered BR, in addition to the number who have BR, suggest that up to 50% would choose to undergo BR if offered it.8,9 Furthermore, the true rates of BR in patients aged 60 years or older are likely to be lower than the published figures as many studies exclude women over 60 or 65 years from their calculations.8 When addressed, the speculated reasons behind the differences in reconstruction rates in these older patients include: the patient’s suitability for reconstruction in terms of underlying health issues and tissue characteristics5; the surgeon’s personal bias against offering reconstruction to older patients10; and the patient’s reluctance to take up reconstruction.9 While older age has been as a factor contributing to lower rates of BR uptake,8,10 the current literature investigating this issue is relatively limited. Recent evidence generally suggests very little difference in outcomes or complications between young and older patients for both implant10,11 and autologous12,13 reconstructions. The purpose of this systematic review was to assess the rates of post-mastectomy BR (immediate or delayed) in women with breast malignancy aged 60 years or older, and to discuss the factors that may influence women of this age range to undergo BR. Review of the rates of different types of reconstruction, complications and patient-reported outcome measures (PROMs) in this age group are also reported. Materials and methods A literature search was conducted using three online databases via the Ovid SP search interface: Medline (1946 to August 2015), Embase (1947 to August 2015) and Cochrane Database (2005 to July 2015). The search terms used were breast cancer, combined with breast reconstruction and mastectomy. The search was limited to publications in English. The reference lists of identified studies were also reviewed for further relevant articles. While the aim was to evaluate BR in older women, the search terms did not specify age so that studies reporting a subgroup of older women would also be identified. Older age was defined as 60 years. Inclusion criteria:  Original studies reporting on BR in women aged 60 years or older treated with mastectomy for breast malignancy d ductal carcinoma in situ (DCIS) or invasive carcinoma (IC) d and specifically including information about any of the following: B

Rates of BR

B

Rates of different reconstructive techniques

B

B

PROMs

Exclusion criteria:  No data specific for patients 60 years old  Articles published as abstracts only  Articles not published in English  Review articles that did not contain original data Studies identified via the online databases were screened by title to exclude ineligible or duplicate articles. Further screening was then performed by examining abstracts. The remaining articles were fully reviewed to ensure they met the inclusion criteria, and were then examined for their findings. Results Literature search The literature search identified 4115 publications, and 63 articles were identified for full-text review. Thirty-four met the inclusion criteria, and a further eight studies were included after examining the reference lists of these articles. Hence, a total of 42 articles met the inclusion criteria for further analysis (see Fig. 1 and Table 1). Study characteristics Of the 42 studies, 37 were retrospective and five were prospective.6,12,13,15,16 Thirty-one studies were from the United States of America (USA) and three were from the United Kingdom (UK).17e19 Both Italy20,21 and Canada7,22 had two studies each. Australia,23 France,24 the

4115 articles identified through Medline, Embase and Cochrane Databases

8 additional articles identified via reference lists

4123 titles/abstracts screened 4060 articles excluded

63 full-text articles assessed for eligibility

42 articles included in review

21 articles excluded. Reasons: • No data specific to patients ≥60 years old (16) • Full study not published (2) • Review article (3)

Figure 1. PRISMA flowchart.14

Rates of complications

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D.D. Oh et al. / EJSO xx (2016) 1e12

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Table 1 Studies reporting the rates of breast reconstruction, rates of different reconstructive techniques, rates of complications and/or patient reported outcome measures in mastectomy patients 60 years or older ordered by study size (i.e. number of mastectomies included). Author (year)

Country (study design)

Age Study period Mastectomy Reconstruction Reconstruction (years) (years) (n) (n) (%)

Hershman30 (2012) USA (R)

60

2000e2010

Lang28 (2013)

USA (R)

60

1998e2008

Morrow47 (2001)

USA (R)

70

National Health Service17 (2009) Agarwal49 (2015)

UK (R)

60

1985e1990 1994e1995 1998e2004

USA (R)

Jeevan19 (2010)

57,238 IC; 6741 DCIS 52 512

7065 IC; 1305 DCIS 2968

71e80 2000e2010

47,586 21,612 30,850 IC; 1489 DCIS 25,286

256 280 3 IC; 11 DCIS 901

UK (R)

60

2006e2009

23,885

1389

Agarwal39 (2011)

USA (R)

65

1998e2002

21,745

919

In40 (2013)

USA (R)

65

1999e2006

19,234

1212

Bezuhly48 (2009)

USA (R)

70

1998e2003

15,445

787

Butz42 (2015)

USA (R)

65

2005e2012

15,093

1624

Fischer44 (2014)

USA (R)

65

2005e2011

13,162

1799

Joslyn38 (2004)

USA (R)

65

1998e2000

12,029

494

Jeevan18 (2014)

UK (R)

60

2008e2009

9108

712 IBR; 364 DBR

Roder23 (2013)

Australia (R)

60

1998e2010

7381

223

Zhong22 (2014)

Canada (R)

65e74 2002e2012

7015

186

Kruper31 (2011)

USA (R)

60

2003e2007

5800

707

Alderman37 (2003)

USA (R)

65

1998

4515

178

Jagsi32 (2014)

USA (R)

60

1998e2007

2388

797

Polednak41 (2000)

USA (R)

65

1992e1996

2156

41

Kruper33 (2013)

USA (R)

60

2006e2009

1714

77

Stover43 (2005)

USA (R)

65

1994e2004

1414

156

Details (patient source; cancer type; reconstruction types included)

12.3 IC; 19.4 DCIS; Perspective database review; 13.1 overall IC and DCIS; IBR only 5.7 SEER database review; IC only; IBR only 0.5 National Cancer Database review; 1.3 IC and DCIS; IBR only 0.01 IC; 0.7 DCIS; National database review; 0.04 overall IC and DCIS; IBR and DBR 3.6 SEER database review; IC only; IBR and early DBR within 4 months of receiving mastectomy 5.8 Health Episode Statistics database review; IC only; IBR only 4.2 SEER database review; IC only; IBR only 6.3 SEER database review; IC and DCIS; IBR only 3.2 SEER database review; IC only; IBR only 10.8 American College of Surgeons National Surgical Quality Improvement Program Participant Use Files review; IC and DCIS; IBR only 13.7 American College of Surgeons National Surgical Quality Improvement Program database review; N/R; IBR only 4.1 SEER database review; IC and DCIS; IBR only 21 IBR; 21 DBR Review of all National Health Service hospital groups that provided mastectomy or BR; IC and DCIS; IBR and DBR 3 Quality Audit review; IC only; IBR only 2.7 Canadian Institute for Health Information database review; IC and DCIS; IBR only 12.2 California Office of State-wide Health Planning and Development inpatient database review; IC and DCIS; IBR only 4.1 SEER database review; IC only; IBR only 33.4 MarketScan Commercial Claims and Encounters database; IC and DCIS; IBR and DBR 1.9 Review of two state-wide Connecticut databases; IC and DCIS; IBR and DBR 4.3 California Office of State-wide Health Planning and Development inpatient database review; IC and DCIS; IBR only 11 Single centre patient records review; N/R; IBR only (continued on next page)

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Table 1 (continued ) Author (year)

Country (study design)

Age Study period Mastectomy Reconstruction Reconstruction (years) (years) (n) (n) (%)

Details (patient source; cancer type; reconstruction types included)

Arrington29 (2014)

USA (R)

60

1998e2010

525

66

12.6

Sisco45 (2015)

USA (R)

65

2005e2011

214

77

36

Morrow15 (2005)

USA (P)

65

2001e2003

200

17

8.3

Escriba26 (2014)

Spain (R)

70

2005 2008 2011

163 225 200

8 9 8

4.9 4 4

Miller16 (2012)

USA (P)

60

2006e2010

158

34

21.5

Ganz36 (1998)

USA (R)

60

1994e1995

153

17

11.1

O’Brien35 (1993)

USA (R)

60

1987e1991

116

12

10.3

Levine34 (2012)

USA (R)

60

2001e2009

89

17

19.1

Petit21 (2008)

Italy (R)

65

1997e2001

82

20

24.4

van Vuuren25 (2015)

Netherlands (R) 60e70 2008e2011

47

15

31.9

Albornoz27 (2014)

USA (R)

60

1998e2011

N/R

N/R

De Gournay24 (2010)

France (R)

60

1990e2008

N/R

N/R

1.54e5.09 AR; 1.04e6.42 IR N/R

Selber13 (2009)

USA (P)

65

1992e2007

N/R

55

N/R

Howard-McNatt11 (2011)

USA (R)

60e74 1998e2008

N/R

89

N/R

Girotto6 (2003)

USA (P)

<65 65

1997e2001

N/R

28

N/R

Albornoz50 (2012)

USA (R)

60

2008

N/R

1568

N/R

Lipa46 (2003)

USA (R)

65

1987e2000

N/R

84

N/R

Bowman7 (2006)

Canada (R)

60e77 1997e2005

N/R

75

N/R

Chang12 (2011)

USA (P)

60

N/R

122

N/R

SEER database review; IC only; IBR only Review of NorthShore University HealthSystem patient records; IC and DCIS; IBR only Questionnaire-based study on SEER-reported cases; IC and DCIS; IBR only Review of all inpatient records from hospitals in Catalonia via the Acute Hospital Discharge Dataset; IC only; IBR only Review of Saint Agnes Hospital (Baltimore) patient records; IC and DCIS; IBR only Review of two large metropolitan centres; IC only; IBR only Review of Breast Consultation Centre (Cincinnati) patient records; IC and DCIS; IBR only Review of Bellevue Hospital (New York) patient records; IC and DCIs; IBR and DBR Review of European Institute of Oncology (Milan) patient records; IC only; IBR only Review of Atrium Medical Centre patient records (Heerlen); N/R; IBR only National Cancer Database review; N/R; IBR only Review of Georges Francois Leclerc Cancer Care Centre (Dijon) patient records; IC and DCIS; IBR and DBR Review of University of Pennsylvania Hospital (Philadelphia) patient records; N/R; IBR and DBR Review of Wake Forest University Baptist Medical Centre (WinstoneSalem) patient records; IC and DCIS; IBR and DBR Review of Johns Hopkins Hospital (Baltimore) patient records; N/R; IBR and DBR Nationwide Inpatient Sample review; IC and DCIS; IBR and DBR Review of M.D. Anderson Cancer Centre (Houston) patient records; IC and DCIS; IBR and DBR Review of patient records from two surgeons’ practices; N/R; IBR and DBR Review of University of California Los Angeles Medical Centre (Los Angeles) patient records; N/R; IBR and DBR

2002e2009

(continued on next page)

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Table 1 (continued ) Author (year)

Country (study design)

Age Study period Mastectomy Reconstruction Reconstruction (years) (years) (n) (n) (%)

Details (patient source; cancer type; reconstruction types included)

August51 (1994)

USA (R)

60

1980e1991

N/R

18

N/R

De Lorenzi20 (2010)

Italy (R)

>65

1999e2004

N/R

51

N/R

Review of University of Michigan Breast Care Centre (Ann Arbor) patient records; N/R; IBR and DBR Review of European Institute of Oncology (Milan) patient records; IC only; IBR only

N/R ¼ not reported; R ¼ retrospective study design; P ¼ prospective study design; IC ¼ invasive carcinoma; DCIS ¼ ductal carcinoma in situ; IR ¼ implant reconstruction; AR ¼ autologous reconstruction; IBR ¼ immediate breast reconstruction; DBR ¼ delayed breast reconstruction.

Netherlands25 and Spain26 had one study each. The majority of studies reported on women aged 60 years (19 studies).16e19,23,24,27e36 Fifteen studies reported on women aged 65 years,6,13,15,20,21,37e46 and three studies reported on women 70 years.26,47,48 The remaining five studies reported on various smaller age groups between 60 and 80 years old.7,11,22,25,49 Nineteen studies included both IC and DCIS patients, 14 studies included IC patients only, and nine studies did not specify a type of cancer. Twentyseven studies reported immediate breast reconstruction (IBR),15,16,19e23,25e31,33,35e40,42e45,47,48 15 studies reported both IBR and delayed breast reconstruction (DBR),6,7,11e13,17,18,24,32,34,41,46,49e51 and no studies reported only DBR.

Breast reconstruction rates Thirty-two papers reported the rates of post-mastectomy BR in women aged 60 years or older15e46 (see Table 1). Thirty studies were retrospective while two were prospective.15,16 Twenty-four studies were from the USA and three from the UK.17e19 Australia,23 Canada,22 Italy,21 the Netherlands25 and Spain26 had a study each. The majority of studies reported rates of women aged 60 years (15 out of 32).16e19,23,27e36 Eleven studies reported BR rates in women aged 65 years,15,21,37e45 while three studies reported BR rates in women 70 years.26,47,48 Three studies had focussed on other age ranges older than 60 years.22,25,49 Altogether, the studies reported 24,746 cases of BR in 407,570 mastectomy patients aged 60 years or older. This corresponded to a pooled BR rate of 6.1%. The seven largest studies, all with more than 20,000 mastectomy patients aged 60 or over, reported reconstruction rates ranging from 0.04 to 13.1%.17,19,28,30,39,47,49 In comparison, the smallest seven studies, all with less than 200 cases of mastectomy, reported relatively higher rates ranging from 8.3 to 31.9%.15,16,21,25,34e36,52,53 Rates of reconstruction were relatively high in studies reviewing their own institution’s databases. A median reconstruction rate of 21.5% (range 11e31.9%) was reported by the seven studies of this kind.16,21,25,34,35,43,45

Twelve of these 32 studies 16e19,23,28,29,34,37e40 provided data about BR rates for specific age groups (see Table 2). Type of breast reconstruction Ten papers reported the rates of different BR techniques undertaken in mastectomy patients aged 60 years or older (see Table 3) 6,11,37,38,42,43,45,46,48,50. In Girotto et al.’s study of 28 breast cancer patients who were at least 65 years old, 22 (79%) underwent IBR.6 The most common reconstructive technique was implant-based reconstruction at 50% (n ¼ 14), followed by free transverse rectus abdominis musculocutaneous (TRAM) and deep inferior epigastric perforator (DIEP) flaps (25%, n ¼ 7), and pedicled TRAM flap (14%, n ¼ 4). The least common was the latissimus dorsi (LD) flap at 11% (n ¼ 3). These rates were in contrast to the patients 64 years and younger (n ¼ 372) from the same study, where free TRAM/DIEP flaps were more common (45%, n ¼ 167) and implants were less common (33%, n ¼ 123). The study also found that the rate of nippleeareola complex reconstruction was much lower in women aged 65 years or over than in those younger than 65 (42.9% vs. 71.4%).6 Albornoz et al.’s study of 1568 BR patients aged 60 years and older reported implant reconstruction as the most common technique at 63.3%. This was followed by pedicled flaps at 32.5% and microsurgical flaps at 4.0%.50 Howard-McNatt et al.’s study of 89 BR patients aged between 60 and 74 years reported 82% undergoing implantbased reconstruction, followed by TRAM (14%), LD with implant (3%), and DIEP flap (1%).11 Lipa et al.’s study of 84 BR cases in women aged 65 and over reported TRAM flap as the most popular technique at 40.48%, followed by implantation at 30.95%, and LD flap at 28.57%.46 Bezuhly et al. in their study of the SEER registry between 1998 and 2003 reported combined reconstruction (of implant and autologous techniques) as the most common in their group of patients 70 years and over.48 Hence, the majority of studies were conducted in the USA and favoured implant reconstruction for those aged 60 or over.6,11,42,43,45,50 Even in the studies that reported autologous as a popular option, implant reconstruction became more likely as women aged.37,48

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Table 2 Studies reporting the breast reconstruction rates of specific age groups over 60. Author (year)

Age group (years)

Mastectomy (n)

Reconstruction (n)

Reconstruction (%)

Lang28 (2013)

60e69 70e79 80þ 60e69 70e79 80þ 65e74 >75 60e69 70e79 80þ 65e70 70e75 75e80 80þ 65e74 75e84 85þ 60e69 70e79 80þ 60e69 70e79 80þ 65e74 75þ 60e69 70e79 80þ 60e69 70þ 60e69 70e79 80e89

22,294 19,038 11,180 13,258 13,694 5387 10,622 11,123 10,867 8410 4608 4454 4724 4703 5353 5858 4868 1303 4372 3097 1639 3184 2317 1880 2260 2255 364 344 210 66 92 59 25 5

2251 628 89 461 4 0 717 202 1195 176 18 626 349 177 60 388 95 11 955 120 0 186 29 8 144 38 35 25 6 25 9 14 3 0

10.1 3.3 0.8 3.5 0.03 0 6.8 1.8 11 2.1 0.4 14 7 4 1 6.6 2.0 0.8 22 3.9 0 5.8 1.3 0.4 6.4 1.7 9.6 7.3 2.9 38 9.8 24 12 0

National Health Service17 (2009)

Agarwal39 (2011) Jeevan19 (2010)

In40 (2013)

Joslyn38 (2004)

Jeevan18 (2014)

Roder23 (2013)

Alderman37 (2003) Arrington29 (2014)

Miller16 (2012) Levine34 (2012)

Complication rates of breast reconstruction Ten studies reported the complication rates of women aged 60 years or older (see Table 4)6,7,11e13,20,42,43,46,51 Girotto et al. reported an overall complication rate (i.e. both surgical and medical) of 18% in 28 BR patients older than 65 years, which was not significantly different to the rate of younger patients at 11%.6 Another study reported a surgical complication rate of 29.1% and medical complication rate of 5.4% in those aged 65 years and older, which were very similar to the rates observed for women younger than 65 included in the study.13 Several papers looked at older reconstruction patients only, reporting overall complication rates ranging from 11.2% to 38.7%11,20,43 and a surgical complication rate as high as 50.6%.7 Chang et al., in his study of microvascular reconstruction procedures, reported a complication rate of 26.2% in women aged between 60 and 69 years, which was lower than the rate of 29% in women younger than 50. However, a rate of 42.6% was observed in those aged 70 and older.12 August et al. reported a lower overall complication rate

amongst women aged 60 years and over compared to women younger than 60 years (31.8% vs 49.8%).51 Butz et al. found that women aged 65 years and over had higher rates of complication from post-mastectomy reconstruction than those younger than 65 (6.8% vs. 5.2%), although this was not statistically significant.42 Lipa et al. reported significantly higher rates of complication for implant-based reconstruction in patients aged over 65 years compared to patients of all ages (77% vs. 37%). However, complication rates for autologous procedures were similar between the two groups (35.3% vs. 33.9%).46 Patient reported outcomes of breast reconstruction Four studies investigated the QoL of older BR patients using PROMs.6,7,24,45 Sisco et al. used a combination of the Duke Health Profile, the Holmes-Rovner Satisfaction with Decision Scale, and the BREAST-Q to study the QoL and satisfaction of reconstruction patients aged 65 years and over.45 In comparison to the patients of the same age-range who received mastectomy only, the reconstruction patients had significantly better scores in breast-

Please cite this article in press as: Oh DD, et al., Patterns and outcomes of breast reconstruction in older women e A systematic review of the literature, Eur J Surg Oncol (2016), http://dx.doi.org/10.1016/j.ejso.2016.02.010

D.D. Oh et al. / EJSO xx (2016) 1e12

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Table 3 Studies reporting the type of breast reconstruction undertaken by women aged 60 years or older. Author (year)

Country (study design)

6

Girotto (2003)

USA (P)

Albornoz50 (2012)

USA (R)

Howard-McNatt11 (2011) Butz42 (2015)b

USA (R) USA (R)

Stover43 (2005)

USA (R)

Sisco45 (2015)

USA (R)

Alderman37 (2003)

USA (R)

Bezuhly48 (2009)

USA (R)

Lipa46 (2003)

USA (R)

Age (years) <65 65 <39 40e49 50e59 60 60e74 <65 65 >65 <65 <65 65 35e44 45e54 55e64 65e74 75 <50 50e69 70 65

Type of reconstruction undertaken by study cohorta % Implant

% Autologous

% Combined

33 50 66.4 60.2 56.9 63.3 82 78.8 83.5 92 84 58.6 69 40.9 27.8 30.0 42.6 45.5 23.0 22.4 26.8 30.95

67 50 33.6 39.3 43.0 36.5 15 15.2e21.3 8.6e16.5 8 16 20.2 15.5 59.1 72.2 70.0 57.4 54.5 43.3 43.4 31.9 69.05

0 0 0 0 0 0 3 0e6.1 0e7.9 0 0 21.2 15.5 0 0 0 0 0 33.7 34.2 41.3 0

a

Percentages may not add up to 100% due to rounding. All figures provided are what were reported by the original studies. b Study reported ‘Latissimus flap (with or without tissue expander or implant)’ as a type of reconstruction without further stratification. Due to this, only a range is provided for % Autologous and % Combined.

Table 4 Studies reporting the complication rates of breast reconstruction in women aged 60 years or older. Author (year)

Country (study design)

Age (years)

Howard-McNatt11 (2011) Girotto6 (2003) Bowman7 (2006) Chang12 (2011) Selber13 (2009) Butz42 (2015) Stover43 (2005)

USA (R)

>60

USA (P) Canada (R) USA (P) USA (P) USA (R) USA (R)

65 60e77 60 65 65 >65

Lipa46 (2003) August51 (1994) De Lorenzi20 (2012)

USA (R) USA (R) Italy (R)

65 60 >65

Reconstruction (n) 89 28 83 156 69 1624 150 84 22 51

Complication (n)

Overall rate of complication (%)

Reoperation (n)

Hospital stay (days)a

7 surgical; 3 implant loss

11.2

4

N/R

4 surgical; 1 medical 42 surgical 34 surgical 19 surgical; 3 medical 110 surgical 46 surgical; 1 medical; 11 implant loss 42 surgical; 4 medical 7 surgical 9 surgical

18 50.6 21.8 31.9 6.8 38.7

N/R 17 N/R 0 N/R 13

N/R N/R 4.3, mean 3.5, mean 2, median 2.8, mean

54.8 31.8 16.7

N/R 6 6

N/R N/R N/R

N/R ¼ not reported; R ¼ retrospective study design; P ¼ prospective study design. a Studies used either mean or median only, as presented in this table. No studies reported both mean and median.

related body-image and breast-related psychosocial health. There were no statistically-significant differences in any other areas such as physical health, pain and disability between the two groups. Furthermore, the study found no significant correlation between the patient’s age and their selfreported outcome.45 Girotto et al. used the Short Form 36 questionnaire to study the health, body image and physical functioning of BR patients aged 65 and older.6 The patients reported better QoL in all three areas compared to their age-matched population controls and mastectomy-only patients.

Furthermore, the older patients who had received reconstruction scored better than younger reconstruction patients in questions related to mental health.6 Bowman et al. surveyed 75 BR patients aged 60 to 77 in regards to QoL and patient satisfaction.7 Around 70% of the women felt that their results were good or excellent, and 89% stated they would undergo the same treatment again. Over 90% believed that reconstruction should be offered regardless of patient age.7 De Gournay et al. used various questionaries from the European Organisation for Research and Treatment of

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Cancer and the Michigan Breast Reconstruction Outcome Study to compare the physical health, sexual health and body image of LD flap patients and mastectomy-only patients. However, no statistically-significant differences in these areas were found when these patients were older than 60.24

Discussion Overall, this systematic review has demonstrated four key points: women aged 60 and over generally have lower BR rates than those of other age groups and this relative difference increases with age (see Table 2); they tend to undergo more non-autologous reconstructions than younger women; they have similar rates of complications; and equivalent, if not better, QoL outcomes. These latter two points raise the question of whether steps should be taken to offer more BR options to older women. There was significant heterogeneity in results between the studies included in this review, particularly in BR rates. None of the reported studies contained control groups, as they all share either an audit-based or retrospective methodology, where analysis was undertaken of BR procedures performed in their respective centres (from patient records and/or patient surveys) or collected from particular databases (local, regional or national). The quality of the studies is best assessed by considering attributes such as the sample size (ranging from 47 to 63,979 mastectomy patients; 8 to 8370 BR patients), the representativeness of the participant population (in terms of demographic and clinical characteristics) and the type and detail of data reported. The quality of each study must be carefully considered when interpreting their individual results, with a greater weighting given to larger, representative studies with detailed reporting of findings. One of the larger and more representative studies that may offer a better insight was Lang et al.’s analysis of the SEER database, which contains data from approximately 28% of all breast cancer patients diagnosed annually in the USA.28 The study included patient data from an extensive period of 1998e2008, amassing 52,512 mastectomy patients aged 60 and over from various states. The study’s evaluation of patient data from 1998 onwards is noteworthy as the Women’s Health and Cancer Rights Act was passed that year. This law requires most health insurance plans that cover mastectomies to also cover BR, allowing greater accessibility to BR.55 This may explain why some of the studies that collected data from before 1998 reported relatively low BR rates.41,47 The only limitation of Lang et al.’s study was that the SEER database did not provide data on delayed reconstruction, adjuvant therapy, or other factors that could have influenced the decision to have BR including co-morbidities, smoking or patient preferences.28 This study found an IBR rate of 5.7% in women aged sixty or over.

Another robust study was the UK’s National Mastectomy and BR Audit,17 also reported in a summary paper by Jeevan et al.18 The Audit included all National Health Service (NHS) hospitals in England that provided mastectomy or BR, as well as six NHS hospitals in Wales and Scotland and another 114 independent hospitals. Additionally, the audit’s design as a prospective cohort study allowed all information collected to be appropriate and relevant to its objectives. The study included all types of mastectomies and BR then available (for both IBR and DBR), and differentiated IC patients from DCIS patients.18 By 2014, the UK’s BR rate had risen to 21% for both immediate and delayed BR in the 60 and over age group,18 demonstrating that significant change is possible over a short time-frame. Two of the highest reconstruction rates were 36%, reported by a USA retrospective study of 214 mastectomy patients aged 65 and older,45 and 31.9%, reported by a Dutch study of 47 mastectomy patients aged between 60 and 70. In both studies, patients were recruited retrospectively through mail surveys. This may have led to a selection bias favouring women with reconstruction. Another study from the USA also reported a high reconstruction rate of 33.4% in its analysis of 2388 mastectomy patients aged 60 and older.32 In this study, however, patients were identified via an employment-based database for medical insurance claims, and therefore sampled commercially-insured individuals only. Since 1998, most American women with health insurance plans have been covered for BR, but many disparities in access to BR remain.52 Uninsured women, the least likely to have BR, are excluded from this study, again raising the probability of overestimating the true BR rate in the general population. The lowest rate of 0.04% was reported by a UK NHS national database review of 32,339 mastectomy patients aged 60 and over.17 The low rate may be explained by the early study period of 1998e2004, as many other studies have shown higher rates of BR in more recent years.8 This is consistent with another study based in the early years of BR, as it also reported relatively low reconstruction rates of 0.5% from 1985 to 1990 and 1.3% from 1994 to 1995 in mastectomy patients aged 70 and over.47 Surgeon-related factors for lower BR rates in older women This review has shown that surgeons are less likely to offer BR to older patients.37,47,53 Age alone seems to have a great influence on a surgeon’s decision to offer reconstruction, mainly due to concerns that older patients undergoing surgery may have higher complication rates, longer hospital stays and poorer patient outcomes.7,54 However, numerous studies have shown that women do not have higher complication rates or longer stays after BR based on age alone, accepting that these patients may be more carefully selected.10e13,51 Walton et al. adds that surgeons

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should adopt a more accurate system of risk assessment that encompasses more than just the patient’s age,5 with other factors such as functional impairment and comorbid conditions being strongly linked to increased post-operative complications and poorer survival rates.55-57 Surgeons may also incorrectly assume that body image is not as important in older women and be reluctant to offer them BR.54 It has also been proposed in the past that IBR may hinder the detection of local recurrence and the provision of adjuvant therapy.62 Since then however, a number of publications have demonstrated that IBR does not affect the detection of local recurrence,59-61 nor the administration of adjuvant radiotherapy or chemotherapy.10,62 James et al., however, argue that the current studies supporting BR in older women are only based on small numbers and carry selection bias.54 Women in the older age brackets are frequently excluded in major studies; and if included, they are only represented by small numbers that are statistically weak.63 At least two studies on BR were found to exclude women over 65 years of age.64,65 In addition, larger primary and locally advanced breast cancers (especially stage II and III) often require neoadjuvant chemotherapy before surgical treatment and subsequent reconstruction. Although this is a feasible option for younger patients, older patients may experience greater toxicity from chemotherapy.66 For these reasons, many healthcare providers may still be reluctant to offer BR to older women post-mastectomy. Adding to this is the notion, reported in at least one study, that older women have a tendency to be more reserved when making decisions about their care, which gives doctors more influence in their management.67 Patient-related factors for lower BR rates in older women In addition to apparent reduced chances of being offered BR, older women also have lower rates of accepting the procedure in comparison to younger patients. In a survey of 87 breast cancer patients who decided against reconstruction (mean age 58.9 years), 40% stated age as the reason for their decision.9 This may be due to women not wanting to undergo any more surgery after their mastectomy. They may also feel that the effort and risks associated with a reconstructive procedure may fail to outweigh its positive effects on QoL. However, several studies have demonstrated the significant benefits BR can have on the QoL of older women by improving aesthetics, function and psychosocial health.6,7,68,69 Two studies on PROMs revealed that older reconstruction patients enjoyed similar if not better QoL outcomes than younger reconstruction patients.6,7 Poor patient education on BR may also be a contributing factor.47 Although some may argue that the significance of the breast may be less in older women, Goin and Goin claim that a woman’s feelings towards her breasts does

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not change significantly with age, and that older women still see psychological benefits from reconstruction.70 The impact of type of reconstruction The literature on the types of reconstruction undertaken by women aged 60 years or over is limited and is largely restricted to studies based in the USA. Overall in the USA, implant-based reconstruction was the most common type of reconstruction in older women.6,11,37,38,43,50 This could be due to autologous reconstructions being more complex and placing greater physical demands on the patient as well as involving longer hospital stays than implant procedures37 d even though some studies have reported lower complication rates.6,27,46 Bowman et al. reported a particularly high surgical complication rate of 50.6% in their study of 83 BR patients aged between 60 and 77. However, their study cohort had a higher proportion of more complex autologous procedures such as TRAM flap (n ¼ 43), compared with LD flap (n ¼ 8) or implant (n ¼ 31).7 August et al. reported a lower overall complication rate for BR patients aged 60 years and older compared to those younger than 60 (31.8% vs. 49.8%); but this study was from 1994, prior to the more technical BR procedures now available.51 These two studies, therefore, raise the question of whether it is a woman’s age, or the complexity of surgery, that is primarily responsible for higher complication rates in older women. Previously, the standard procedure for immediate implant-based reconstruction was two-staged, involving the placement of a tissue expander at the time of mastectomy, followed by an exchange of expanders for a permanent implant at a second operation.74 However, the increasing availability of one-stage ‘direct-to-implant’ IBR with acellular dermal matrices allows patients to undergo both mastectomy and reconstruction in a single procedure. One-stage reconstruction removes the extra risks, costs and inconvenience of a second procedure.71-73 This may make BR more attractive for older women in the future by reducing the possible negative attitudes older patients may have towards receiving more surgery.47 These technical developments may partially explain the recent small rise in BR rates in all age groups.74 However, as this is a relatively new surgical development, it is unknown whether the outcomes following one-stage reconstruction (including complication rates) are similarly low in older women. Limitations While the methodology of this systematic review was rigorous, there are some limitations, largely based on the heterogeneity of the included studies in terms of sample size, time period, patient cohorts and data presented. This raises numerous confounding variables that may affect

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the findings of this review. For example, it is evident that BR uptake rates have generally increased over time, and with this review’s inclusion of studies with cohorts sourced from as early as 1980, many of the reported BR rates may not reflect today’s rates. Additionally, some of the studies included may have overlapping patient cohorts (for example, the two Agarwal et al. studies from 2011 and 2015), which may further limit the value of results such as the pooled BR rate. The review contains sparse data on DBR, with only four studies including DBR patients in their series,26,33,35,41 and one study included ‘early DBR’ patients only (BR within four months of receiving mastectomy).23 This may be because DBR is often performed by surgeons outside the cancer centres that many of these studies recruit in, making data collection difficult. The review was also unable to link the rates of complication to the type of reconstruction as this data was not provided by most of the included studies. Furthermore, the results of the literature search were limited to English, which may have excluded some studies based in non-English speaking countries.

Conclusion Despite recent studies demonstrating the efficacy of BR in older women,6,7 this literature review confirms the lower rates in women aged 60 years or older. Older women with medical contraindications for BR will remain ineligible for this procedure. However, older women with no medical contraindications deserve to be considered as candidates for reconstruction, as it may improve their QoL as much as, if not more than, their younger counterparts.6 The perception among some healthcare providers, surgeons and women requiring mastectomy that the potential risks of BR in older women outweigh the benefits needs to be revisited. Studies have demonstrated the oncological safety of BR and complication rates are similar in those aged above or below 60 years old.6,13 Older women who require adjuvant treatment such as chemotherapy or radiotherapy can still be offered delayed reconstruction once they have recovered from any associated morbidity. Implant-based options may be more appropriate than autologous options for older women, and direct to implant techniques may increase the uptake of BR in these women provided it is offered. All women with breast cancer deserve choice. In the absence of medical contraindications, all women requiring mastectomy for breast cancer should be offered BR, regardless of age. Increasing access to BR will become even more important in the future as populations age, breast cancer is diagnosed earlier, treatments improve and more women are living longer following mastectomy. Education of consumers and surgeons, as well as public advocacy for offering BR to all clinically eligible women, are the most promising means of changing practice.

Conflicts of interest statement The authors have no conflicts of interest to declare. Funding This research is funded in part by The Friends of the Mater Foundation, North Sydney, Australia. The funding source played no role in study design, data collection, analysis and interpretation of data, writing of the manuscript or decision to submit the manuscript for publication. References 1. Australian Institute of Health Welfare Cancer Australia. Breast cancer in Australia: an overview. Australian Institute of Health and Welfare; 2012. 2. Cancer Research UK. Breast cancer statistics 2014 9th October 2015. Available from: http://www.cancerresearchuk.org/healthprofessional/cancer-statistics/statistics-by-cancer-type/breast-cancer. 3. Australian Demographic Statistics. Feature article: population by age and sex, Australia, states and territories. Australian Bureau of Statistics; 2014. 4. Ortman JM, Velkoff VA. An aging nation: the older population in the United States. United States Census Bureau; 2014. 5. Walton L, Ommen K, Audisio RA. Breast reconstruction in elderly women breast cancer: a review. Cancer Treat Rev 2011;37(5):353–7. 6. Girotto JA, Schreiber J, Nahabedian MY. Breast reconstruction in the elderly: preserving excellent quality of life. Ann Plastic Surg 2003; 50(6):572–8. 7. Bowman CC, Lennox PA, Clugston PA, Courtemanche DJ. Breast reconstruction in older women: should age be an exclusion criterion? Plastic Reconstr Surg 2006;118(1):16–22. 8. Brennan ME, Spillane AJ. Uptake and predictors of post-mastectomy reconstruction in women with breast malignancyesystematic review. Eur J Surg Oncol 2013;39(6):527–41. 9. Handel N, Silverstein MJ, Waisman E, Waisman JR. Reasons why mastectomy patients do not have breast reconstruction. Plastic Reconstr Surg 1990;86(6):1118–22. discussion 23e5. 10. Wong A, Snook K, Brennan M, et al. Increasing breast reconstruction rates by offering more women a choice. ANZ J Surg 2014;84(1e2): 31–6. 11. Howard-McNatt M, Forsberg C, Levine EA, et al. Breast cancer reconstruction in the elderly. Am Surg 2011;77(12):1640–3. 12. Chang EI, Vaca L, DaLio AL, Festekjian JH, Crisera CA. Assessment of advanced age as a risk factor in microvascular breast reconstruction. Ann Plastic Surg 2011;67(3):255–9. 13. Selber JC, Bergey M, Sonnad SS, et al. Free flap breast reconstruction in advanced age: is it safe? Plastic Reconstr Surg 2009; 124(4):1015–22. 14. Liberati A, Altman DG, Tetzlaff J, et al. The PRISMA Statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration PRISMA: explanation and elaboration. Ann Intern Med 2009; 151(4):W-65. 15. Morrow M, Mujahid M, Lantz PM, et al. Correlates of breast reconstruction: results from a population-based study. Cancer 2005; 104(11):2340–6. 16. Miller A, Chandru Kowdley G. Breast reconstruction after mastectomy at an urban community-based program. Am Surg 2012; 78(11):1281–4. 17. NHS Information Centre for Health and Social Care. National mastectomy and breast reconstruction audit. Second Annual Report. Leeds: NHS Information Centre for Health and Social Care; 2009.

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