Abstract

A maximal aerobic capacity below the 20th percentile is associated with an increased risk of all-cause mortality (Blair 1995). Adult Adult burn survivors have a lower aerobic capacity compared with nonburned adults when evaluated 38 ± 23 days postinjury (deLateur 2007). However, it is unknown whether burn survivors with well-healed skin grafts (ie, multiple years postinjury) also have low aerobic capacity. This project tested the hypothesis that aerobic fitness, as measured by maximal aerobic capacity (VO2max), is reduced in well-healed adult burn survivors when compared with normative values from nonburned individuals. Twenty-five burn survivors (36 ± 12 years old; 13 females) with well-healed split-thickness grafts (median, 16 years postinjury; range, 1–51 years) covering at least 17% of their BSA (mean, 40 ± 16%; range, 17–75%) performed a graded cycle ergometry exercise to test volitional fatigue. Expired gases and minute ventilation were measured via a metabolic cart for the determination of VO2max. Each subject's VO2max was compared with sex- and age-matched normative values from population data published by the American College of Sports Medicine, the American Heart Association, and recent epidemiological data (Aspenes 2011). Subjects had a VO2max of 29.4 ± 10.1 ml O2/kg body mass/min (median, 27.5; range, 15.9–53.3). The use of American College of Sports Medicine normative values showed that mean VO2max of the subjects was in the lower 24th percentile (median, 10th percentile). A total of 88% of the subjects had a VO2max below American Heart Association age-adjusted normative values. Similarly, 20 of the 25 subjects had a VO2max in the lower 25% percentile of recent epidemiological data. Relative to nongrafted subjects, 80 to 88% of the evaluated skin-graft subjects had a very low aerobic capacity. On the basis of these findings, adult burn survivors are disproportionally unfit relative to the general U.S. population, and this puts them at an increased risk of all-cause mortality (Blair 1995).

Each year ∼1.4 million people in the United States sustain burn injuries.1 Because of medical advances, survival rates of individuals with severe burns have dramatically increased. The psychological and physical recovery process from severe burns is multifactorial and can take months to years.2

Physical inactivity leads to poor cardiovascular fitness, and poor fitness is highly correlated with increased all-cause mortality.3 Physical and psychological impairments, similar to those associated with burn recovery, can lead to sustained periods of physical inactivity.4 Thus, an individual with burn injuries can suffer from a decrease in cardiovascular fitness during their recovery. Relatively little is known about the cardiovascular fitness of adults who previously sustained severe burn injuries. De Lateur et al5 examined maximal aerobic capacity (VO2max, the standard measure of cardiovascular fitness) in adults with 19 ± 16% of their TBSA burned 38 ± 23 days (range, 9–122 days) postinjury. Although VO2max was low (21.7 ± 7.0 ml/kg/min) when compared with age-matched norms, the relatively short time period between injury and testing makes it difficult to speculate on the cause of poor cardiovascular fitness. Willis et al6 observed reductions in VO2max in adults 5.1 ± 1.8 years postinjury; however, the small sample size (n = 8) and limited range of injury severity (ie, only one subject had >40% TBSA grafted) limits the interpretation of those findings. Given this paucity of data regarding cardiovascular fitness in adults with well-healed skin grafts, the current study extends previous findings by examining adults ~15 years postinjury (range, 1–51 years) with a wide range of % TBSA grafted (ie, 17–75% TBSA). We hypothesized that cardiovascular fitness, quantified by VO2max, is lower in adults with well-healed burn injuries compared with that in age- and sex-matched normative population values. Further, we hypothesize that the extent of the compromised cardiovascular fitness is independent of years postinjury and % TBSA grafted.

METHODS

Twenty-five burn survivors (36 ± 12 years old; 13 females) with well-healed split-thickness grafts covering at least 17% of their BSA (mean, 40 ± 16%; range, 17–75%) participated in the study. Subjects must have been at least 1 year postinjury, however, no upper-range postinjury was imposed, resulting in a median postinjury of ~–16 years with a range of 1 to 51 years. Subjects were excluded if they had cardiovascular, metabolic, or neurological diseases and thus subjects were generally healthy. The rule of Nine's7 was used to calculate the area of skin covered by split-thickness grafts. Although individuals with at least 15% of their TBSA covered with grafts were eligible for participation, subject recruitment focused on inclusion of individuals across a wide range of TBSA grafted. Subjects refrained from alcohol and exercise 24 hours, food 4 hours, and caffeine 12 hours before testing. Written informed consent was obtained from all subjects before participating in this study. Study procedures and the informed consent were approved by the Institutional Review Boards of the University of Texas Southwestern Medical Center and Texas Health Presbyterian Hospital Dallas.

The standard measure for aerobic capacity is a VO2max test.8,9 The used VO2max protocol consisted of cycling on an electronically braked ergometer (Lode Excalibur Sport; Lode B.V., Groningen, NL) with the power output starting at 25 or 50 W and progressively increasing 25 W every 2 minutes until volitional fatigue. Oxygen uptake and related gas exchange measures were obtained by open-circuit indirect calorimetry using a PARVO Medics TrueOne 2400 Metabolic Measurement System (Parvo Medics, Inc., Salt Lake City, UT) calibrated before use. Heart rate (HR) and rating of perceived exertion (RPE) were measured at rest, every 2 minutes, and at the end of the VO2max test. HR was measured from ECG and a Polar® Vantage XL HR monitor (model 145900; Polar Electro, Inc., Woodbury, NY). RPE was measured by the Borg 15-point category scale using standardized instructions.10 For some subjects (n = 13), a capillary finger-stick blood sample was obtained 3 min after completion of the test for determination of blood lactate concentration. Peak oxygen uptake was objectively identified based upon an HR within 10 beats per minute of age-predicted maximum (220 − age), an RPE score of 19 to 20, and/or a respiratory exchange ratio (RER) of >1.0.9

Interpretation of Data

Data are presented as mean ± SD. Subjects were grouped into one of three classifications according to the % TBSA grafted: 17 to 35%, 40 to 55%, and >60%. Differences between groups were analyzed with a one-way analysis of variance (ANOVA). Alpha was set at .05 and Bonferroni post hoc tests were conducted if a significant main effect occurred. The relationship between VO2max and % TBSA and years since injury were examined using a Pearson-Product Moment correlation.

The obtained VO2max data were compared against three published normative data sets, each of which is based upon observations from thousands of healthy and presumably nonburned individuals. Population normative data published by the American Heart Association (AHA)8 were used to classify each subject as having a VO2max above or below their sex- and age-matched norm. Similarly, each subject's VO2max percentile was identified using age- and sex-matched normative values published by the American College of Sports Medicine (ACSM).11 Last, the number of subjects in each quartile of fitness (ie, low to high fitness) were identified using epidemiological data12 in which fitness, as quantified with a VO2max test, was correlated to cardiovascular risk factors.

RESULTS

Subject demographics are presented in Table 1. The median and range of % TBSA grafted was 34% and 17 to 75%, respectively. The median time since the burn injury was 15.7 years. Because of the study design, stratification of subjects into groups resulted in differences between % TBSA grafted in each group (17–35%, 40–55%, and >60%; P < .001). There were no differences between groups in length of time postinjury (P = .295), age (P = .488), height (P = .437), or body mass (P = .277).

Table 1.

Participant characteristics

Table 1.

Participant characteristics

All subjects achieved a VO2max based on values obtained at the end of the incremental test to exhaustion (ie, HRmax, RPE, RER, and blood lactate; Table 2). There were no differences between groups in absolute VO2max (ie, oxygen uptake in L/min; P = .885), relative VO2max (oxygen uptake in ml/kg body mass/min; P = .260), HRmax (P = .990), RPE (P = .945), and RER (P = .393), whereas lactate approached significance (P = .052).

Table 2.

Values at the end of the incremental bike test to exhaustion

Table 2.

Values at the end of the incremental bike test to exhaustion

Table 3 shows VO2max responses of the evaluated subjects when compared with normative data sets. When referenced against AHA normative data,8 88% of the subjects had a VO2max below the age-/sex-matched normative values. When VO2max of the subjects was classified into population percentiles, based on normative data from the ACSM,11 the median percentile for VO2max was the lowest 10th percentile (range, 10th–90th percentile; mean, 24 ± 25 percentile). Notably, 76% of the subjects were in the lowest 20th percentile for VO2max when compared against this data set.11 Similar to those observations, relatively recent epidemiological data12 showed that 80% of the subjects had a VO2max that was in the lowest quartile. VO2max was not correlated with years since injury (r = .003; P = .987; Figure 1) or % BSA grafted (r = .190; P = .363; Figure 2).

Table 3.

Classification of VO2max values relative to three population normative data sets

Table 3.

Classification of VO2max values relative to three population normative data sets

Maximal oxygen uptake (VO2max) was not correlated to duration since injury (r = .003; P = .987).
Figure 1.

Maximal oxygen uptake (VO2max) was not correlated to duration since injury (r = .003; P = .987).

Maximal oxygen uptake (VO2max) was not correlated to BSA grafted (%; r = 0.190; P = .363).
Figure 2.

Maximal oxygen uptake (VO2max) was not correlated to BSA grafted (%; r = 0.190; P = .363).

DISCUSSION

The purpose of this study was to examine the aerobic capacity, as indexed from VO2max, of individuals with well-healed skin grafts (ie, at least 1 year after the initial burn injury) covering 17 to 75% of their TBS. Using AHA norms,8 we show that 88% of the evaluated subjects were below age- and sex-matched normative values. With respect to population norms published by the ACSM,11 the VO2max from subjects in the current investigation averaged in the ~25% percentile, although the data were not normally distributed; thus a median of the lowest 10th percentile (range, 10th–90th percentile) is more reflective of the evaluated subjects. This is further supported by data from the study by Aspenes et al,12 in which 80% of the evaluated subjects fall in the lowest fitness quartile when compared with values from more than 4000 nongrafted individuals. Therefore, the primary finding of this study is that 80% or more of the evaluated skin-grafted individuals have an aerobic capacity that is disproportionally lower than age-matched nongrafted individuals.

Because the obtained values were compared with normative VO2max data sets from thousands of individuals, it was important that a true maximum (or peak) oxygen uptake be achieved in the evaluated subjects. To that end, there is strong evidence that these subjects obtained a VO2max. For example, at test termination the subjects had HRs at or near age-predicted max, had RPE values of 19 or 20, had RER values >1.0, and the 13 subjects assessed had lactate concentrations that were near or above 7 mmol/L (Table 2). The use of these standard thresholds for evidence that subjects achieved a true VO2max allows us to make comparisons to the aforementioned normative datasets.9

The observed findings are consistent with prior findings suggesting that adults with skin grafts have a low VO2max.5,6 We extend those findings in three distinct and important ways: 1) we examined individuals across a longer duration postinjury (ie, 17.3 ± 13.5 years), relative to the duration postinjury, as studied by de Lateur et al5 (38 ± 23 days) and Willis et al6 (5.1 ± 1.8 years); 2) approximately half of the examined individuals had skin grafts covering 40% or more of their TBSA, in contrast to only 1 subject with greater than 40% TBSA burned examined by Willis et al6; and 3) the overall number of subjects in the present investigation (25 subjects) is appreciably greater than the 8 subjects evaluated by Willis et al,6 thereby allowing for correlative analyses between VO2max and demographic data.

The mechanism(s) by which burn survivors have such low aerobic capacities remains unclear. Acute burn injury results in a catabolic state in which resting metabolic rate is increased for a period of time directly correlated to amount of TBSA burned.13 In the most severe cases (>75% TBSA burned), increased resting metabolic rate may persist for 1 year or more.13,14 This acute hypermetabolic state can lead to substantial skeletal muscle loss.15 A lower skeletal muscle mass, relative to preburn injury, leads to a reduction in the amount of aerobically active muscle mass. This will decrease maximal oxygen extraction across that muscle, and according to the Fick equation (VO2max = cardiac outputmax × [arterial − venous oxygen contentmax]), VO2max will be reduced. Because the subjects in the present study were at least 1 year postinjury, it is unknown whether in the subsequent years after the injury these subjects were able to rebuild the muscle loss that occurred during this hypermetabolic state. Given a lack of correlation between VO2max and duration since injury (Figure 1), and if reduced muscle mass is contributing to reduced VO2max, these data suggest that restitution of muscle mass was unlikely to occur despite many years postinjury. That said, we cannot distinguish whether a sustained loss of muscle mass, if in fact that occurred in the observed subjects, is because of an inability to increase muscle mass or simply a lack of physical training.

Decreased physical activity independently will reduce physical fitness (ie, VO2max).16 Every 1% TBSA burned results in approximately 1 day of hospitalization.17 The cardiovascular detraining that occurs with bed rest alone can lead to a 15% reduction in VO2max in as little as 10 days.16 Therefore, it is likely that hospitalization associated with a burn injury causes an acute reduction in cardiovascular fitness secondary to bed rest deconditioning. This is particularly evident in the low VO2max values (21.7 ± 7.0 ml/kg/min) reported by de Lateur et al5 in subjects 37.4 ± 23.3 days postinjury.5 Thus, on leaving the hospital, skin-grafted individuals' VO2max is profoundly reduced. If that level of aerobic fitness is not returned to a preinjured state, then the aerobic capacity of severely burned individuals is “reset” downward. This event, along with well-known age-related decreases in aerobic fitness18 would result in skin-graft patients having persistently low VO2max values even decades postinjury (Figure 1).

In the present data set VO2max was not correlated to the duration postinjury (Figure 1) or the percent of TBSA grafted (Figure 2). These observations suggest that the decrements in aerobic capacity years after an injury are unrelated to the extent of the injury and accompanying TBSA grafted or the period of time after the injury. Regarding the former, greater TBSA burned results in longer hospitalization and recovery times,17 and thus it would be reasonable to hypothesize a greater loss of aerobic fitness.16 On the contrary, one could hypothesize that the longer the duration postinjury the more time one would have to improve aerobic fitness after hospitalization, although this apparently is not the case with the present data set. It is possible that the lack of relationships between VO2max and TBSA grafted, as well as years after the injury, is substantially influenced by level of physical activity after full recovery. Similarly, fitness level before the injury may also play a role in an individual's ability to maintain or improve fitness during recovery. Unfortunately, an assessment of the level of physical activity before the injury, and from the time of recovery until we assessed the subject, was not obtained. Thus, we cannot identify whether in the present data set the few subjects showing normal (and even increased) VO2max values had a higher level of physical activity before their injury or since their injury, relative to their lower fit counterparts. It is interesting to note that there were three subjects with VO2max values in the 80th to 90th percentiles of age- and sex-matched normative values. On the basis of this very small sample size, it is possible that subjects who are more physically active before their injury (ie, greater VO2max), and/or are more physically active after their injury, have increased VO2max values relative to less-active burned individuals. Prospective research will be required to address those questions.

A key question is whether low aerobic fitness years after the injury is based on physiological mechanisms (ie, an inability to improve VO2max for physiological reasons, inclusive of the aforementioned muscle atrophy) and/or perhaps psychological barriers associated with burn injury that lead to reduced desire to participate in physical activity. For example, years after a burn injury, fatigue is an “almost universal complaint” as a major barrier preventing such individuals from returning to work and performing activities of daily living.19 A total of 59% of burned individuals report problems with fatigue an average of 17 years postinjury.20 Other perceived or real barriers to physical activity may include impaired temperature regulation, hypertrophic scars, and contractures that may limit range of motion, hyperpigmentation, psychosocial barriers, decreased cutaneous sensation, and a lower quality of life.4,21,27

Even if these barriers can be overcome, the exercise training response in burned adults is relatively unknown. Grisbrook et al28 showed similar improvements in VO2max (compared with nonburned subjects) when previously burned adults participated in a 12-week aerobic/resistance training program. However, these results should be viewed in the context of a small sample size (n = 9), the absence of a difference in VO2max between groups at baseline, and peak HRs that are appreciably less than age-predicted maximums (pretraining peak HRs ~166 beats per minute for ~39-year olds). However, in burned children (~–10 years old), there is growing evidence that 12 weeks of aerobic/resistance training significantly improves lean body mass, muscle strength, and VO2max compared with burned children who do not undergo training.29,30 Future studies are warranted to investigate the extent to which a large group of severely burned adults, across a wide range of TBSA, has the capacity to improve aerobic fitness with exercise training.

By design, the present study did not include a nonburned control group from which VO2max could be compared relative to the burned group. To eliminate selection bias we chose to use normative data representative of large population sets (upward to thousands of individuals from three unique data sets), an approach that is routinely used in clinical exercise and pulmonary function testing.31,35 Therefore, the used comparisons are more representative of the nonburned population, relative to if we assessed 25 nonburned individuals. Last, by making comparisons with several data sets (AHA, ACSM, etc) we show that the results are consistent independent of the epidemiological data set used.

Regardless of the cause, a lower physical fitness compared with age-matched normative values puts skin-grafted individuals at an increased cardiovascular risk. Every 5 ml/kg/min decrement in VO2max corresponds to a ~56% higher prevalence of a cardiovascular risk factor,12 and a maximal aerobic capacity below the 20th percentile (of which 76% of the investigated cohort resides) is associated with an increased risk of death from all causes.36 Importantly, improving aerobic fitness decreases one's risk of all-cause mortality,36 with the strongest reduction in death being from a cardiovascular event.3 With the number of burn survivors escalating because of improved medical treatment, it is important that future studies investigate the barriers to physical activity and subsequent methods to improve physical fitness, which in turn can improve mortality and morbidity in skin-graft patients years after the injury.

In conclusion, the present findings clearly show that a substantial percentage of skin-graft patients have a disproportionally low VO2max many years after their injury relative to nonburned individuals. The reasons for this lower aerobic fitness are unknown, although it may be the result of reduced physical activity and perhaps associated physiological and/or psychological barriers. Alternatively, comparable levels of physical activity in skin-grafted individuals may not result in the same improvements in cardiovascular fitness relative to nonburned individuals. Regardless of the mechanism(s), the present data show that individuals with well-healed skin grafts have lower cardiovascular fitness many years after injury, which will increase their risk of all-cause mortality.

This work was supported by the National Institutes of General Medical Sciences Grant GM068865.

ACKNOWLEDGMENTS

We thank the subjects for their participation. We also thank Kim Hubing, Jena Langlois, and Gary Purdue for their assistance. This work was supported by the National Institutes of General Medical Sciences Grant GM068865.

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Author notes

1

The authors declare no conflict of interest.