Journal of Plastic, Reconstructive & Aesthetic Surgery (2014) 67, 797e803
Preoperative anemia impacts early postoperative recovery following autologous breast reconstruction* Jonas A. Nelson a,*, John P. Fischer a, Cyndi U. Chung a, Joshua Fosnot a, Jesse C. Selber b, Joseph M. Serletti a, Liza C. Wu a a b
Division of Plastic Surgery, Hospital of the University of Pennsylvania, Philadelphia, PA, USA Department of Plastic Surgery, MD Anderson Cancer Center, Houston, TX, USA
Received 26 October 2013; accepted 11 February 2014
KEYWORDS Abdominal wall strength; Free flap breast reconstruction; Anemia; TRAM; Function; Outcomes
Summary Introduction: Preoperative anemia impacts a significant portion of breast reconstruction patients, though this does not appear to affect surgical outcomes. The impact of anemia on postoperative physical and mental health, however, is unknown. This study aimed to prospectively evaluate the role of preoperative anemia in recovery after autologous reconstruction. Methods: From 2005 to 2010, we prospectively assessed autologous breast reconstruction patients with satisfaction surveys, strength and functional tests, and the short form 36 (SF36). Data was collected preoperatively and at early (<90d), intermediate (90e365d), and late (>365d) follow-up. We stratified patients by presence or lack of preoperative anemia (hemoglobin<12 g/dL). Results: Of 399 patients undergoing reconstruction, 179 enrolled in the study. Anemic patients (n Z 31, 17%) had higher rates of preoperative chemotherapy (p Z 0.02) and lower rates of radiation (p Z 0.001). Preoperatively, anemic patients reported worse physical (p < 0.001), mental (p Z 0.003) and overall health (p Z 0.0003). These scores worsened postoperatively for anemic and nonanemic patients, though anemic patients had lower average scores in all SF36 categories. This was significant only for early follow-up physical health (p Z 0.02). Change in SF36 scores and objective physical exam assessments did not differ between the two cohorts.
*
This study was presented at the 59th Annual Meeting of the Robert H Ivy Society of Plastic Surgeons, March 9th, 2013, Bethelem, PA. * Corresponding author. Division of Plastic Surgery, Perelman School of Medicine, University of Pennsylvania, 3400 Spruce Street, Philadelphia, PA 19104, USA. E-mail address:
[email protected] (J.A. Nelson). http://dx.doi.org/10.1016/j.bjps.2014.02.017 1748-6815/ª 2014 British Association of Plastic, Reconstructive and Aesthetic Surgeons. Published by Elsevier Ltd. All rights reserved.
798
J.A. Nelson et al. Conclusions: Though preoperative anemia may not impact surgical outcomes, it adversely impacts the recovery of breast reconstruction patients. Subjective physical health differences were significant in early follow-up, though this did not translate to differences in mental health or satisfaction. We advocate for preoperative optimization of hemoglobin to enhance the early recovery potential of breast reconstruction patients. ª 2014 British Association of Plastic, Reconstructive and Aesthetic Surgeons. Published by Elsevier Ltd. All rights reserved.
Introduction Anemia impacts a significant proportion of the breast cancer population, with estimates ranging from 18 to 75%.1e3 Our group has recently demonstrated that preoperative anemia does not impact major surgical outcomes after autologous reconstruction,4 a finding which has been echoed in other recent studies.2,5 However, there is a dearth of literature exploring the impact of anemia on postoperative recovery. This question is particularly important in autologous breast reconstruction, which involves large incisions and considerable involvement of the abdominal musculature. Patients undergoing this procedure would benefit greatly if they could be identified and counseled in advance about their risk for longer postoperative recovery. The purpose of our study was to assess the impact of anemia on postoperative functional recovery in patients undergoing autologous breast reconstruction via objective and subjective functional assessments.
Methods This study was part of a prospective, blinded, cohort study assessing abdominal strength, physical health, mental health, and patient satisfaction in patients undergoing abdomen-based free flap breast reconstruction.15,16 All patients scheduled for autologous free flap breast reconstruction utilizing abdominal tissue by the senior author (JMS) between 2005 and 2010 were eligible to enroll in this IRB approved prospective study. Enrolled patients completed a preoperative evaluation, which included an abdominal strength functional assessment, a version of the Short Form 36 (SF-36). The abdominal evaluation examined three aspects of the abdominal wall: upper abdominal strength, lower abdominal strength, and a measure of functional independence, which assessed a patient’s ability to sit up from a supine position (Figure 1). This current study limited analysis to upper abdominal strength and functional independence. The SF-36 is a health survey asking thirty-six questions to produce eight scales, which are then aggregated to produce a summary physical health score and a summary mental health score. Following surgery, participants were examined at each subsequent postoperative visit by abdominal strength exam and SF-36. Patients also completed a satisfaction survey in order to assess postoperative cosmetic and functional satisfaction. Data was obtained at preoperative, early follow-up (<90 days), intermediate follow-up (90e365 days), and long-term follow-up visits (>365 days). Patients who had
multiple visits within a given follow-up interval had their data averaged for that timeframe. All enrolled women who underwent deep inferior epigastric artery perforator flap (DIEP), superficial inferior epigastric artery flap (SIEA), or muscle-sparing free transverse rectus abdominis myocutaneous flap (msfTRAM) procedures between September 2005 and August 2010 in addition to preoperative and follow-up data were included in this analysis. Patients without follow-up were excluded. A detailed review of hospital and office records was performed for each enrolled patient and included the following: preoperative history and physical, operative reports, discharge summaries, outpatient clinic notes, and laboratory data. An institutional hospital database was queried for medical complications associated with each patient’s initial reconstructive hospitalization. Additionally, we limited the study cohort to patients undergoing operations at the main teaching hospital of the health system. Patients were divided into two cohorts based on the WHO classification of anemia: those with HgB 12 g/dL and those with HgB < 12 g/dL. These patients were subsequently analyzed by unilateral and bilateral reconstruction. Three analyses were performed on the data collected: intercohort comparisons of mental and physical health measures for each follow-up time interval; intracohort comparisons of mental and physical health measures over time; and intercohort comparisons of those changes in scores over time. All data were entered into an Access database and an Excel workbook (Microsoft Corp., Redmond, WA). Statistical analysis included Chi Square and Fisher’s exact tests (where appropriate) for categorical variables and the Wilcoxon Rank Sum test and Wilcoxon Signed Rank tests (where appropriate) for continuous variables. All tests were twotailed, and statistical significance was defined as p < 0.05. All analyses were performed using STATA IC 10.0 (StataCorp, College Station, TX). Table 1
Demographics. HgB < 12 n Z 31
Age Race White Black Hispanic Asian Other
%
48.2 (9.9) 26 4 1 0 0
HgB e hemoglobin.
HgB 12 n Z 143
%
51.5 (7.6) 83.9% 12.9% 3.2% 0.0% 0.0%
120 18 0 1 2
p value 0.08
83.9% 12.6% 0.0% 0.7% 1.4%
0.43
Preoperative anemia impacts early recovery
799
Results
Table 3
Surgical characteristics. Hgb < 12 % n Z 31
General characteristics Overall, 399 women underwent autologous breast reconstruction by the senior author between 2005 and 2010 at the main teaching hospital of our health system. Of those patients, 174 women enrolled in our prospective study. Preoperative anemia was present in 31 patients (17.8%), who had an average HgB of 11.1(0.7 g/dL). Among nonanemic patients, the average HgB was 13.5(0.9) g/dL. The anemic and nonanemic cohorts were similar in terms of ethnicity and past medical history (Tables 1 and 2). Anemic patients tended to be younger (48.2 (9.9) vs. 51.5(7.6) years, p Z 0.08). In addition, anemic patients were significantly more likely to have had preoperative chemotherapy (71.0% vs. 48.3%, p Z 0.02) and significantly less likely to have had preoperative radiation (16.1% vs. 47.6%, p Z 0.001). No significant differences were noted with regard to the laterality of the reconstruction, although a greater proportion of anemic patients had bilateral reconstruction (64.5% vs. 55.2%, p Z 0.35) (Table 3). Proportionally more anemic patients also had immediate reconstruction, though this only neared significance (80.6% vs. 58.0%, p Z 0.051). The breakdown of msfTRAM, DIEP, and SIEA flaps was not significantly different between the two patient cohorts. Medical and surgical complications after surgery did not differ consistently or significantly between anemic and nonanemic patients (Table 4).
Assessment results FIM scores The average preoperative FIM scores were similar between cohorts (6.9(0.2) in anemic patients, 6.8(0.3) in nonanemic
Table 2
Patient Medical History. HgB < 12 % n Z 31
Preoperative HgB Body mass index Obesity Chronic Obstructive Pulmonary Disease Diabetes Hypertension Dyslipidemia Smoking e current Smoking e past Preoperative radiation Preoperative chemotherapy HgB e hemoglobin.
HgB 12 % n Z 143
p value
11.1 (0.7) 13.5 (0.9) <0.0001 30.0 (6.5) 28.3 (5.2) 0.23 14 45.2% 45 31.5% 0.14 0 0.0% 3 2.1% 1.00
Unilateral 11 Bilateral 20 Immediate 25 reconstruction Delayed 6 reconstruction Bilateral 0 combination Flap type (unilateral) TRAM 7 DIEP 4 SIEA 0 Flap type (bilateral) msfTRAM/ 15 msfTRAM DIEP/DIEP 0 msfTRAM/DIEP 3 SIEA/SIEA 0 SIEA/msfTRAM 0 SIEA/DIEP 2
9.7% 32.3% 19.4% 12.9%
7 37 35 20
4.9% 25.9% 24.5% 14.0%
0.39 0.47 0.54 0.15
7 5
22.6% 57 16.1% 68
39.9% 47.6%
0.001
22
71.0% 69
48.3%
0.02
p value
35.5% 64 64.5% 79 80.6% 83
44.8% 0.35 55.2% 58.0% 0.051
19.4% 53
37.1%
0.0% 7
4.9%
63.6% 44 36.4% 18 0.0% 2
68.8% 0.74 28.1% 3.1%
75.0% 41
51.9% 0.29
0.0% 15.0% 0.0% 0.0% 10.0%
11.4% 25.3% 2.5% 3.8% 6.3%
9 20 2 3 5
patients, p Z 0.56) (Table 5). In early postoperative followup, FIM scores in anemic and nonanemic patients continued to be similar, (5.5(1.8) vs. 6.0(1.1), p Z 0.26), a trend which continued into intermediate and long-term followup. Furthermore, changes in scores from the preoperative to postoperative periods were not significantly different between the two patient cohorts. Upper abdominal strength scores Average preoperative strength scores were 4.7(0.7) and 4.6(0.8) in anemic and nonanemic patients, respectively (p Z 0.62) (Table 5). These values were 3.1(1.4) and 3.3(1.1) (p Z 0.57) in early follow-up, 4.0(0.9) and 4.1(0.9) (p Z 0.43) in intermediate follow-up, and 4.1(1.1) and 4.2(1.0) (p Z 0.93) in long-term follow-up. Changes in scores were significant only when comparing preoperative scores to intermediate follow-up scores in bilateral cases ( 0.8(1.1) vs. 0.5(1.0), p Z 0.03).
Table 4
3 10 6 4
HgB 12 % n Z 143
Surgical complications. HgB < 12 % n Z 31
Major immediate surgical complication Major delayed surgical complication Minor surgical complication Medical complication
HgB 12 % n Z 143
p value
3
9.7% 3
2.1% 0.07
1
3.2% 13
9.1% 0.47
17
54.8% 78
54.5% 0.98
2
6.5% 11
7.7% 1.00
800 Table 5
J.A. Nelson et al. Scores for functional independence measure, upper abdominal strength.
Preoperative FIM Early FIM Intermediate FIM Long-term FIM Preoperative UA Early UA Intermediate UA Long-term UA
HgB < 12
HgB 12
Overall p value
Unilateral p value
Bilateral p value
6.9 5.5 6.8 6.7 4.7 3.1 4.0 4.1
6.9 6.0 6.7 6.7 4.6 3.3 4.1 4.2
0.56 0.26 0.56 0.97 0.62 0.57 0.43 0.93
0.83 0.87 0.92 0.48 0.88 0.78 0.66 0.56
0.29 0.28 0.48 0.55 0.67 0.8 0.19 0.76
(0.2) (1.8) (0.4) (0.5) (0.7) (1.4) (0.9) (1.1)
(0.3) (1.1) (0.7) (0.6) (0.8) (1.1) (0.9) (1.0)
FIM e functional independence measure, UA e upper abdominal strength, Hgb e Hemoglobin.
SF-36 scores Preoperatively, anemic patients reported significantly lower physical health scores (52.1(12.4) vs. 63.9(11.6), p < 0.001) (Table 6). Upon analysis by laterality, this was significant only for bilateral reconstruction (p < 0.0001). Anemic patients also reported significantly lower physical health scores in the early postoperative period (45.7(6.8) vs. 52.0(11.6), p Z 0.02). Average scores were also lower in anemic patients upon intermediate (59.7(14.9) and 64.4(11.8) and long-term follow-up (60.9(18.0) vs. 65.0(12.7), though this was only significant for unilateral cases in long-term follow-up (p Z 0.04). Change in physical health scores from preoperative to postoperative periods was not significantly different between the two patient cohorts (Table 7). Anemic patients also had significantly lower preoperative subjective mental health scores (65.5(17.4) vs. 75.1(16.7), p Z 0.003) (Table 6). Upon analysis by laterality, this was statistically significant in bilateral cases only (p Z 0.003). Though not statistically significant, anemic patients had slightly lower early postoperative scores (61.2(18.6) vs. 66.2(18.3), p Z 0.21), intermediate followup scores (71.8(20.4) vs. 75.9(19.1), p Z 0.4), and longterm follow-up scores (65.2(12.7) vs. 77.1(20.8), p Z 0.15). Change in subjective mental health scores from preoperative baseline to postoperative follow-up was not significantly different between the two patient cohorts (Table 7). Satisfaction scores When asked to rate their overall cosmetic results, their sense of wholeness and femininity, and the degree to which the surgery changed their lives, patients reported neither
Table 6
consistent nor significant differences between the two patient cohorts (Table 8).
Discussion Anemia continues to impact a significant proportion of women presenting for breast reconstruction. The goal of this study was to elucidate the role of anemia on functional outcomes after autologous breast reconstruction. We demonstrate that preoperatively, anemic patients have lower, average subjective physical and mental health scores compared to nonanemic patients. Postoperatively, this discrepancy is significant only in the early follow-up period, though the discrepancy persists throughout followup. Importantly, this finding is not accompanied by differences in objective functional measures or satisfaction rates. The authors previously analyzed this patient population as part of a more comprehensive outcomes analysis to establish the prevalence and impact of anemia on outcomes after autologous breast reconstruction.4 This study found that 18% of patients had preoperative anemia by the World Health Organization definition (HgB < 12 g/ dL), which is lower than the 25e75% estimates published in the breast cancer population.1e3 No significant differences in surgical outcomes were noted between anemic and nonanemic patients, though medical complications were more common in those with HgB < 10 g/dL (p Z 0.018). This data echoed recently published, prospectively maintained data from the American College of Surgeons National Surgical Quality Improvement project, which looked at 30-day outcomes in just over 800
Absolute scores, physical and mental health.
Preoperative physical health Preoperative mental health Early physical health Early mental health Intermediate physical health Intermediate mental health Long-term physical health Long-term mental health
HgB < 12
HgB 12
Overall p value
Unilateral p value
Bilateral p value
52.1 65.3 45.7 61.2 59.7 71.8 60.9 65.2
63.9 75.1 52.0 66.2 64.4 75.9 65.0 77.1
<0.001 0.003 0.02 0.21 0.23 0.40 0.46 0.15
0.15 0.26 0.09 0.17 0.41 0.76 0.04 0.04
<0.0001 0.003 0.12 0.65 0.31 0.35 0.42 0.89
(12.4) (17.4) (6.8) (18.6) (14.9) (20.4) (18.0) (12.7)
(11.6) (16.7) (11.6) (18.3) (11.8) (19.1) (12.7) (20.8)
Preoperative anemia impacts early recovery Table 7 health.
801
Change in absolute scores, physical and mental HgB < 12
Preoperative to early physical health Preoperative to early mental health Preoperative to intermediate physical health Preoperative to intermediate mental health Preoperative to long-term physical health Preoperative to long-term mental health
HgB 12
p value
8.8 (15.6)
12.8 (11.8) 0.3
9.4 (14.4)
10.6 (16.8) 0.9
4.6 (18.2)
0.7 (10.2) 0.2
4.5 (22.1)
1.1 (16.1) 0.2
10.1 (24.2)
0.8 (10.4) 0.3
1.8 (23.3)
4.0 (16.4) 0.6
patients.6 However, though this data also examined a large cohort of patients, the NSQIP dataset is limited beyond its ability to examine early flap loss and early postoperative complications. Table 8
Satisfaction scores. n
HgB < 12 n
HgB 12 p value
Early Follow-up: How has surgery. Affected your life? 20 4.2 (1.6) 109 4.4 Affected your 20 3.9 (1.9) 109 4.2 feeling of wholeness? Affected your 20 3.8 (2.0) 109 4.0 feeling of femininity? Affected overall 20 5.0 (1.3) 109 4.5 cosmetic results? Intermediate Follow-up: How has surgery. Affected your life? 19 4.7 (1.5) 105 4.3 Affected your 19 4.6 (1.7) 105 4.1 feeling of wholeness? Affected your 19 4.6 (1.6) 105 4.1 feeling of femininity? Affected overall 19 4.1 (1.9) 105 4.6 cosmetic results? Long-term Follow-up: How has surgery. Affected your life? 7 3.9 (1.2) 46 4.4 Affected your 7 4.6 (1.6) 46 4.3 feeling of wholeness? Affected your 7 4.3 (1.8) 46 4.3 feeling of femininity? Affected overall 7 4.1 (1.5) 46 4.9 cosmetic results?
(1.5) (1.7)
0.58 0.46
(1.8)
0.81
(1.6)
0.17
(1.4) (1.8)
0.27 0.18
(1.3)
0.21
(1.3)
0.47
(1.7) (1.7)
0.37 0.74
(1.7)
0.98
(1.2)
0.36
Though anemia may not significantly affect flaprelated outcomes, the impact of anemia on postoperative functional recovery in breast reconstruction has previously not been examined. Recent studies in the orthopedic literature have extensively examined the effect of anemia on functional outcomes. These studies tend to use postoperative HgB levels as the basis for comparison rather than preoperative HgB. In a prospective observational study, Conlon et al. evaluated 79 patients undergoing primary hip arthroplasties with SF-36 and Functional Assessment of Cancer Therapy Anemia (FACT-Anemia) surveys.7 Scores were compared between the preoperative and 2-month postoperative periods. The authors found a statistically significant, positive correlation between Day 8 postoperative hemoglobin and change in survey scores. Specifically, improvement in postoperative SF-36 score was 8.6 points for every HgB increase of 1 g/ dL and 2.9 points for the same increase in the FACTAnemia score. This supports our finding that anemic patients experience postoperative functional improvement at slightly slower rates. Other authors reporting a positive correlation include Lawrence et al., who performed a retrospective cohort study with 5793 patients undergoing hip fracture repair.8 The authors found that the distance their patients walked at discharge increased with higher postoperative HgB levels. This remained statistically significant after adjusting for age, level of dependence in activities of daily living, and neurological comorbidities. Similarly, in a prospective study of 487 hip fracture patients, Foss et al. found that during the first three postoperative days, there was a significant positive correlation between daily HgB and daily Cumulated Ambulation Score (CAS) (0.12 and p Z 0.02, 0.18 and p < 0.001, 0.18 and p < 0.001, respectively).9 These studies are notable in that the authors found a positive correlation in objective functional tests. In contrast, we did not observe a significant difference in objective strength assessments. However, the application of these findings comparing postoperative Hgb is again limited given our focus on preoperative HgB. These positive findings are balanced, however, by an equal if not greater number of negative studies in the orthopedic literature. Gruson et al. looked specifically at preoperative anemia in their prospective study of 395 patients, all of whom had operatively treated femoral neck or intertrochanteric fractures.10 They found that anemic and nonanemic patients displayed no difference in recovery of mobility and basic and instrumental activities of daily living at three, six, or twelve months after surgery e a conclusion very different from ours. We note, however, that Gruson et al. used a telephone survey in order to assess their patients postoperatively, as opposed to the in-person clinical evaluation and survey utilized in this study. Patients may be more likely to diminish their complaints on the phone rather than in the office, which could have factored into the authors’ finding of nonsignificance. In contrast to Gruson et al., all other studies examined perioperative or postoperative anemia. In a follow-up observational study, Cormier-Lavoie et al. examined 160 patients who received major hip or knee arthroplasty at least six months prior.11 No significant correlation was
802
J.A. Nelson et al.
Figure 1
Grading scale for abdominal functional assessment.
found between postoperative hemoglobin and Functional Status Index score, SF-36 score, or adverse events. It is possible that the authors missed seeing an effect because they examined patients long after surgery. This finding was echoed by other authors.12e14 Meanwhile, the effect we found was most significant in the early postoperative period, or less than 90 days following surgery. As demonstrated above, the effect of anemia on postoperative functional outcome is highly debated in orthopedics. However, to date there have been few studies that examine the same question in autologous breast reconstruction. Though it is reasonable to assume that some aspect of orthopedic outcomes would translate to plastic surgery, this is likely not the case, as our patient population possesses demographics, comorbidities, and oncologic histories drastically different from orthopedic patients. In contrast to many of the studies cited in orthopedic surgery, we used a combination of objective and subjective measures to assess health. We note that all discrepancies were detected upon subjective assessment only. The objective strength assessment did not differ consistently between anemic and nonanemic patients over time. Why anemic patients consistently self-report lower health scores and why these differences did not translate to the objective measures is unclear. It may however be related to the impact of anemia on the psychological state. Furthermore, of note in subjective physical health scores, a general trend in change of score over time was noted. Anemic patients tended to have a smaller decrease in scores into the early period, and a more pronounced increase in score over time. However, due to small numbers in follow up, such differences were not significant. This study is additionally notable for analyzing patient satisfaction. Anemic patients displayed no consistent patterns in higher or lower averages for self-reported
satisfaction, despite self-reported differences in physical and mental health scores. A number of limitations should be acknowledged. The first and most significant limitation is the sample size of patients included in the study, and related to this the attrition in study participation which was noted. While some attrition would be expected over time, it is unclear why some patients chose to continue to participate in the study and others did not. Additionally, secondary to the small numbers within the anemic/non-anemic cohorts, we chose to combine several types of flaps within the analysis cohorts as subdividing these flaps would have potentially produced meaningless results secondary to the small numbers of SIEA flaps. This is certainly not without concern. However, the flap-type distribution was not significantly different. Additionally, based on our previous studies, only small differences based on flap type exist in abdominal strength. However, we believe that the strengths of this study outweigh the potential criticisms. It is a prospective, blinded study of abdominal wall strength, performed on patients of a single surgeon at a single institution to decrease variability in surgical and perioperative management. We have attempted to examine the data from multiple angles to gain the most insight possible, with both objective and subjective variables assessed. Our results do not suggest that autologous breast reconstruction should be restricted from anemic patients. Instead, our findings suggest that patients undergoing this surgery should be appropriately screened for preoperative anemia and counseled accordingly. The surgeon should assess patients’ preoperative physical and mental health and emphasize that functional recovery may be more gradual in anemic patients. The surgeon should also consider having a lower threshold in recommending physical therapy to anemic patients. We advocate for
Preoperative anemia impacts early recovery preoperative optimization of hemoglobin to enhance early recovery potential after breast reconstruction.
Conclusion Though preoperative anemia may not impact surgical outcomes, it adversely impacts the recovery of breast reconstruction patients. Subjective physical health differences were significant in early follow-up, though this did not translate to differences in mental health or satisfaction rates. We advocate for preoperative optimization of hemoglobin with iron supplementation to optimize the early recovery potential of breast reconstruction patients.
Disclosure None of the authors listed have any conflicts of interest to report.
Funding No internal or external funding was utilized for the preparation of this work.
References 1. Weber RS, Jabbour N, Martin 2nd RC. Anemia and transfusions in patients undergoing surgery for cancer. Ann Surg Oncol 2008; 15(1):34e45. 2. Shander A, Knight K, Thurer R, et al. Prevalence and outcomes of anemia in surgery: a systematic review of the literature. Am J Med 2004;116(Suppl. 7A):58Se69S. 3. Tas F, Eralp Y, Basaran M, et al. Anemia in oncology practice: relation to diseases and their therapies. Am J Clin Oncol 2002; 25(4):371e9. 4. Nelson JA, Fischer JP, Grover R, et al. The impact of anemia on microsurgical breast reconstruction complications andoutcomes. Microsurgery; 2013 Nov 4. http://dx.doi.org/10.1002/micr.22202 [Epub ahead ofprint] PubMed PMID: 24436188.
803 5. Windhofer C, Gruber S, Hofer E, et al. Free flap survival despite severe anemia after fourth degree hand burn. Burns 2006; 32(2):261e5. 6. Mlodinow AS, Ver Halen JP, Rambachan A, et al. Anemia is not a predictor of free flap failure: a review of NSQIP data. Microsurgery 2013;33(6):432e8. 7. Conlon NP, Bale EP, Herbison GP, et al. Postoperative anemia and quality of life after primary hip arthroplasty in patients over 65 years old. Anesth Analg 2008;106(4):1056e61. 8. Lawrence VA, Silverstein JH, Cornell JE, et al. Higher Hb level is associated with better early functional recovery after hip fracture repair. Transfusion 2003;43(12):1717e22. 9. Foss NB, Kristensen MT, Kehlet H. Anaemia impedes functional mobility after hip fracture surgery. Age Ageing 2008;37(2): 173e8. 10. Gruson KI, Aharonoff GB, Egol KA, et al. The relationship between admission hemoglobin level and outcome after hip fracture. J Orthop Trauma 2002;16(1):39e44. 11. Cormier-Lavoie A, Ruel M, Sylvestre M, et al. Effect of postoperative anemia on functional outcome and quality of life after hip and knee arthroplasties: a long term follow-up. F1000Research 2013;2:61. See more at: http://dx.doi.org/10. 12688/f1000research.2-61.v1 http://f1000research.com/ articles/2-61/v1#sthash.1yIOlEAo.dpuf. 12. So-Osman C, Nelissen R, Brand R, et al. Postoperative anemia after joint replacement surgery is not related to quality of life during the two weeks postoperatively. Transfusion 2011;51(1): 71e81. 13. Wallis JP, Wells AW, Whitehead S, et al. Recovery from postoperative anaemia. Transfus Med 2005;15(5):413e8. 14. Vuille-Lessard E, Boudreault D, Girard F, et al. Postoperative anemia does not impede functional outcome and quality of life early after hip and knee arthroplasties. Transfusion 2012; 52(2):261e70. 15. Selber JC, Nelson J, Fosnot J, et al. A prospective study comparing the functional impact of SIEA, DIEP, and musclesparing free TRAM flaps on the abdominal wall: part I. unilateral reconstruction. Plast Reconstr Surg. 2010 Oct;126(4):1142e53 http://dx.doi.org/10.1097/PRS.0b013e3181f02520.16. 16. Selber JC, Fosnot J, Nelson J, et al. A prospective study comparing the functional impact of SIEA, DIEP, and musclesparing free TRAM flaps on the abdominal wall: Part II. Bilateral reconstruction. Plast Reconstr Surg 2010 Nov;126(5):1438e53. http://dx.doi.org/10.1097/PRS.0b013e3181ea42ed.