Arch Gynecol Obstet (2015) 291:525–530 DOI 10.1007/s00404-014-3418-y
MATERNAL-FETAL MEDICINE
The effect of physical exercise on postpartum fitness, hormone and lipid levels: a randomized controlled trial in primiparous, lactating women A. Zourladani • M. Zafrakas • B. Chatzigiannis P. Papasozomenou • D. Vavilis • C. Matziari
•
Received: 24 May 2014 / Accepted: 8 August 2014 / Published online: 20 August 2014 Ó Springer-Verlag Berlin Heidelberg 2014
Abstract Purpose To evaluate the effect of an exercise training program combining low-impact dance aerobic, resistance and stretching exercise on physical fitness, hormone and lipid levels of postpartum, primiparous, lactating women. Methods Thirty seven primiparous, lactating women were randomly assigned at 4-6 weeks postpartum to either follow an exercise training program of 50-60 min aerobic, strengthening and stretching exercise, 3 days a week, for 12 weeks (interventional group; n = 20) or no training program at all (control group; n = 17). The following parameters were measured at baseline and 12 weeks later: (1) for evaluation of physical fitness: VO2max, muscular endurance, joint mobility and body fat; (2) for evaluation of the lipidemic profile: triglyceride, total cholesterol, HDL and LDL levels, and (3) levels of hormones associated with lactation: prolactin, estradiol, cortisol, TSH, fT3 and fT4. Results After completion of the exercise training program, comparisons between the interventional and the control group showed statistically significant mean changes in VO2max (p = 0.003), muscular endurance of the upper
A. Zourladani B. Chatzigiannis C. Matziari School of Physical Education and Sport Science, Aristotle University of Thessaloniki, Thessaloniki, Greece M. Zafrakas School of Health and Medical Care, Alexander Technological Educational Institute of Thessaloniki, Thessaloniki, Greece M. Zafrakas (&) Ethnikis Antistatseos 81, 55134 Thessaloniki, Greece e-mail: [email protected] P. Papasozomenou D. Vavilis 1st Department of Obstetrics and Gynecology, Medical School, Aristotle University of Thessaloniki, Thessaloniki, Greece
extremities (p \ 0.001), and the abdomen (p \ 0.001), flexibility (p = 0.042), and body fat (p = 0.007). There were no significant differences between the two groups in mean changes of lipid and hormone levels. Conclusion Implementation of a low-impact exercise training program appears to improve physical fitness of postpartum women, while it does not seem to affect lipid levels and lactation-associated hormone levels. Hence, implementation of an exercise training program combining low-impact dance aerobic, resistance and stretching exercise is feasible in postpartum, primiparous, lactating women. Keywords VO2max Muscular endurance Joint mobility Body fat Lipidemic profile Hormone levels
Introduction A woman’s body undergoes remarkable changes after childbirth, regardless of the mode of delivery, and it may take up to 1 year for these changes to be completed [1]. Evidence suggests that, the aerobic capacity and strength of women decline in the early postpartum period [2]. Furthermore, physical complaints, such as backache, emotional problems, including increased anxiety, and functional limitations related to childcare, everyday household activities and work are common after birth, and all tend to increase over time [3]. Physical activity and exercise are well-established factors promoting lifelong physical health and enhancing wellness in the general population [4, 5]. Health-related components of physical fitness, including aerobic capacity, muscular endurance, flexibility, and body composition, are characterized by an ability to perform daily activities with
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vigor, and demonstrate the traits and capacities associated with low risk of premature development of hypokinetic disease [4]. It is noteworthy that women are less likely to participate in a physical exercise program than men [5]. Moreover, childbearing may further compromise a woman’s ability to participate in physical exercise programs [6]. Healthcare providers rarely incorporate exercise programs into postpartum care plans [7]. More research results are needed to create effective evidence-based exercise programs and fitness plans for postpartum women. Low-impact aerobics aim to provide cardiovascular and muscle-toning workout without risking injury to a person, due to intense stress on joints, tendons and muscles [8]. The relative importance of strengthening and flexibility to activities of daily living requires the inclusion of such exercises in an exercise routine [4]. In most studies, the effect of vigorous exercise programs on milk volume and composition has been evaluated [9, 10]. In few studies, the effect of a long-term exercise program on some of the parameters of postpartum physical fitness has been assessed [9, 11], while others have just recorded physical exercise of their subjects without the implementation of an exercise program [2, 12]. In some research projects, the effect of different types of aerobic exercise on postpartum health was evaluated [9, 10, 13], while others examined the effect of aerobic and resistance exercise on bone mineral density during lactation [14]. In addition, only few studies have examined the effects of exercise on the lipid profile of postpartum women [13], and on hormones associated with lactation [9, 13]. Given that women in western countries are increasingly asking for postpartum exercise programs, the purpose of this study was to investigate the effect of an exercise program combining low-impact dance aerobic, resistance and stretching exercises on the physical fitness of postpartum women. Additionally, given that abnormal plasma lipid and hormone concentrations are associated with increased risk of cardiovascular disease and the metabolic syndrome, their levels were compared between exercising and non-exercising women, to determine whether moderate exercise may affect the physical health of postpartum women.
Arch Gynecol Obstet (2015) 291:525–530
of their predicted maximal heart rate, strengthening and stretching for 50-60 min per day, 3 days a week for 12 weeks. The maximal number of women in each exercise session was 6-7 participants. In the second group (control group, n = 20), women did not undertake physical exercise during the study period. The method of randomization was alternating sequence. Two authors (ZA and CB) generated the random allocation sequence, enrolled participants, and assigned participants to interventions. Blinding of participants and care providers after assignment to interventions was not possible, due to the nature of the study. After randomization, five women, two from the experimental and three from the control group dropped out of the study, leaving 20 participants in the interventional and 17 in the control group. Women dropped out of the study for the following reasons: (a) two women from the experimental group failed to follow the exercise program, by missing the pre-scheduled appointments; (b) two women from the control group did not show up at the end of the study period, to repeat physical measurements and blood tests; (c) one woman from the control group was diagnosed with colon cancer during the study period. Power analysis was conducted (with one-way fixed effects analysis of covariance) and the sample size of the study was considered to be adequate (effect size f = 0.4, power = 0.693). The following inclusion criteria were used: healthy, primiparous, lactating women. The following exclusion criteria were used: obstetrical complications during pregnancy (i.e., preterm birth, bleeding in any trimester, intrauterine growth restriction, intrauterine infection, and fetal anatomic and chromosomal anomalies), multiple gestation, pregnancy-induced hypertension, severe heart disease, chronic renal disease, chronic pulmonary disease, drug abuse and alcoholism, and serious mental and psychiatric illness. All women were informed of risks involved (i.e., physical trauma during exercise and triggering of previously undiagnosed cardiovascular or respiratory disease by exercise) and signed a consent form prior to participation. All interventions were in accordance with the Helsinki declaration of 1975 for experimentation in humans and the study was approved by the Ethics Committee of the Medical School of the Aristotle University of Thessaloniki. Physical exercise protocol
Materials and methods Recruitment and randomization Initially, 42 healthy, primiparous, lactating women were recruited at 4-6 weeks postpartum, and randomly assigned in two groups. In the first group (interventional group, n = 22), participants were engaged in an exercise program, consisting of aerobic exercise at an intensity of 60-70 %
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As previously described [15], the exercise program was in accordance with the American Council on Exercise (ACE) guidelines, and consisted of four parts: (a) warm-up, (b) low-impact aerobics, (c) muscle strengthening and (d) relaxation. The first part was a 10-min warm-up, including low-impact dance aerobics and stretching of main muscle groups, followed by the second part of 2025 min of low-impact aerobics. The intensity of exercise
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was consistent with the guidelines issued in 2003 by the American College of Obstetricians and Gynecologists (ACOG) [16]. Exercise intensity was tailored according to each participant’s fitness level limited to up to approximately 70 % of her maximal heart rate. The intensity of exercise was 140.4 ± 14.1 pulses per minute according to a heart rate monitor, and 12.1 ± 1.1 according to Borg’s scale of fatigue [17]. The third part of the exercise program was 15-20 min of muscle strengthening, consisting of exercises for all major muscle groups. Emphasis was given to the upper and lower back muscles, the abdominal muscles, and the pelvic floor. Each exercise program initially consisted of 1-3 sets, with 8-12 repetitions per set, which gradually increased. The fourth part of the exercise program was 10 min of relaxation, often including yoga. Emphasis was given on stretching of the thoracic muscles to relieve stress caused by extra breast weight and/or constant muscle contraction from breastfeeding and infant cuddling. All stretches were performed both on an active and static basis, and lasted 10-20 s each. The same 35-year-old instructor, certified by the Aerobics and Fitness Association of America (AFAA), with extensive experience in this field, supervised all classes [1]. The following physical fitness parameters were measured: (1) body weight and body fat. The body weight was evaluated electronically, using a special monitor (Tanita InnerScan body composition monitor BC-533, Sindelfingen, Germany). Body fat was evaluated by measuring the skinfold thickness with a skinfold caliper (Lange Skinfold Calliper, Beta Technology Incorporated, Cambridge, Maryland) at the following sites: the triceps, thigh, subscapular, chest, mid-axillary, supra-iliac, and abdominal area. Body density and body fat were calculated using the equation of Jackson & Pollock [18]. (2) VO2max: the Astrand-Rhyming cycle ergometer test was used to estimate VO2max from simple heart rate measurements [19]. The exercise protocol involved constant power output (50-100 W) for 6 min; the pedal rate was set at 50 rpm; the heart rate was measured during the 5th and 6th min of work. (3) Muscular endurance: muscular endurance of the upper extremities was assessed by the YMCA bench press endurance test [4]. Abdominal muscular endurance was assessed by the abdominal bent-knee curl up test [4]. (4) Flexibility: for low back and posterior thigh flexibility the modified sit and reach test [20] was used. Plasma lipid and hormone analyses Blood samples were collected from all women at 68 weeks postpartum (baseline), between 08:00 and 09:00 AM, at least 12 h after the last meal, 1.5 h after breastfeeding, and before exercise. Plasma concentrations
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Fig. 1 Investigational protocol
of total cholesterol, high-density lipoproteins (HDL), lowdensity lipoproteins (LDL), and total triglycerides were measured using a clinical chemistry analyzer (Instrumentation Laboratory ILab 600, Brussels, Belgium). Concentrations of T3, T4, TSH and prolactin were measured by chemiluminescence enzyme immunoassay (CLIA), using the ADVIA CentaurÒ CP Immunoassay System (Siemens, Germany). Estradiol and cortisol were measured by the Electrochemiluminescence (ECL) assay, using E170 Modular Analytics (Roche diagnostics, Greece). Samples were transported in a cooler to the laboratory for separation after centrifugation, and plasma was frozen immediately at –20 °C. Two days after the last exercise session, all physical fitness measurements and plasma lipid and hormone tests were repeated for both the interventional and the control group. An overview of the investigational protocol is presented as a flow chart in Fig. 1. Statistical analysis Descriptive data are presented as minimum and maximum values, means, standard deviations or standard error of the mean. The assumption of normality was tested by the Shapiro–Wilk test (N \ 50). The Pearson’s Correlation Coefficient r was calculated between baseline and followup for normally distributed measurements. When r \ 0.5, differences between groups at baseline were analyzed by the two independent samples t test; the one-way ANCOVA
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model (including baseline measurements as a covariate at each case) was used to compare mean changes between the two groups, while differences between baseline and followup for both groups were analyzed with the paired t test. When r C 0.5, a Linear Mixed model was used. The Mann–Whitney U test for two independent groups and the Wilcoxon test for paired data were used for not normally distributed measurements. Computation of p values was done by the Monte Carlo method. The SPSS 15.0 software was used (IBM Corp, New York, USA), and the level of statistical significance was set at p \ 0.05.
Results According to self-reported data about the course of pregnancy, 20 % of women in the interventional and 22 % in the control group were rarely engaged in low-intensity physical activity (walking) during pregnancy; 35 % in the interventional and 55 % in the control group had attended antenatal classes for 1-3 weeks; 35 % of women in the interventional and 45 % in the control group gave birth by cesarean section. The majority of participants were breastfeeding almost exclusively throughout the study period. By the beginning of the study, three women in each group combined breastfeeding with one or two meals with a milk formula, while by the end of the study five women in the interventional and six in the control group did so. Table 1 provides descriptive data for each group. At baseline, by the beginning of the study, there were no differences between the interventional and the control group in any of the parameters measured, i.e., physical fitness, lipid and hormone levels. After completion of the exercise training program, 12 weeks later, measurements were repeated, and the following statistically significant differences were found in the interventional group as compared with initial measurements: (1) VO2max (p \ 0.001), (2) muscular endurance of the upper extremities (p \ 0.001), (3) abdominal muscular endurance (p \ 0.001), (4) Table 1 Descriptive data of women participating in the study Interventional group (n = 20) (Mean ± SD)
Control group (n = 17) (Mean ± SD)
Age (years)
30.9 ± 2.5
31.7 ± 2.5
Height (cm)
166.7 ± 5.3
168.3 ± 6.0
Body weight before pregnancy (kg)
61.0 ± 10.52
60.8 ± 9.1
Body weight at baseline (kg)
65.1 ± 9.6
65.7 ± 10.8
Body weight at follow-up (kg)
61.8 ± 10.0
64.4 ± 10.7
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flexibility (p \ 0.001), and (5) body fat (p \ 0.001). Likewise, statistically significant changes in the interventional group were found regarding blood levels of cholesterol (p = 0.022), LDL (p = 0.032), prolactin (p = 0.006) and estradiol (p = 0.045). Similar comparisons between baseline and 12 weeks later in the control group showed statistically significant changes in the following parameters: body fat (p = 0.006), flexibility (p = 0.001), cholesterol (p = 0.029), T4 (p = 0.035), and estradiol (p = 0.030). Comparisons between the two groups at follow-up showed differences in VO2max (p = 0.012), muscular endurance of the upper extremities (p \ 0.001) and muscular endurance of the abdominal muscles (p = 0.001). Furthermore, comparisons between the interventional and the control group showed statistically significant mean changes in the following parameters: (1) VO2max (p = 0.003), (2) muscular endurance of the upper extremities (p \ 0.001), (3) abdominal muscle endurance (p \ 0.001), (4) flexibility (p = 0.042), and (5) body fat (p = 0.007). There were no significant differences between the two groups in mean changes of lipid and hormone levels. An overview of results regarding physical fitness, lipid and hormone levels between and within the two groups of women is presented in Table 2.
Discussion This study was prompted by the lack of detailed practice guidelines regarding physical exercise in postpartum women; in general, gradual resumption of activity as tolerated is advised, however, more evidence about the type, frequency and duration of exercise is needed. In the present study, a physical exercise program was planned specifically for postpartum, lactating women and proved to be effective in improving physical fitness, without any adverse effects on lactation. In particular, in respect to cardio-pulmonary function, the VO2max increased significantly in women participating in the exercise program, as compared with the control group. Consistently, similar increases of the VO2max between 13 [21] and 25 % [9] have been previously reported. This finding is particularly important, given that women appear to have physiologically decreased aerobic capacity after childbirth as compared with that before pregnancy [2, 22]. In the present study, muscular endurance of the upper extremities and the abdomen increased significantly after physical exercise, whereas no changes were found in the control group. These findings are consistent with those previously published in a small study, including ten postpartum women engaged in exercise and ten controls [14]. Interestingly, muscular endurance is known to decrease physiologically after childbirth [2, 23, 24].
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Table 2 Overview of comparisons (p values) regarding physical fitness, lipid and hormone levels between and within the two groups of women
Ns not statistically significant a
Results from Linear Mixed Model
b
Results from one-way ANCOVA and t test
c
Results from Mann–Whitney and Wilcoxon tests
Interventional (n = 20) vs. control group at baseline (n = 17)
Interventional (n = 20) vs. control group at follow-up (n = 17)
Comparison of means
Body weighta
Ns
Ns
Ns
Ns
Ns
Body fata
Ns
Ns
0.007
\0.001
0.006
Upper extremity endurancea
Ns
\0.001
\0.001
\0.001
Ns
Flexibilitya
Ns
Ns
0.042
\0.001
0.001
VO2maxc
Ns
0.012
0.003
\0.001
Ns
Abdominal muscle endurancea
Ns
0.001
\0.001
\0.001
Ns
Cholesterolb
Ns
Ns
Ns
0.022
0.029
Triglyceridesc
Ns
Ns
Ns
Ns
Ns
LDLb
Ns
Ns
Ns
0.032
Ns
HDLa
Ns
Ns
Ns
Ns
Ns
Ns
Ns
Ns
Ns
Ns
Prolactin
Ns
Ns
Ns
0.006
Ns
TSHc T3c
Ns Ns
Ns Ns
Ns Ns
Ns Ns
Ns Ns
T4c
Ns
Ns
Ns
Ns
0.035
Estradiolc
Ns
Ns
Ns
0.045
0.030
Cortisolb c
Another finding in the present study was that flexibility of the posterior muscles of the thigh and the lower back were increased significantly in the interventional and the control group, and this difference between the two groups was statistically significant. The improvement of flexibility in the control group could be one of the physiological changes after childbirth. To the best of our knowledge, there are no published data regarding flexibility in postpartum women. A further finding in the present study was that body fat decreased significantly in the interventional and the control group. This decrease could be attributed to the fact that women in both groups were breastfeeding, since lactation is well known to reduce body fat [25], while physical exercise appears to have an additional effect. Similar findings have been previously reported in one study [11], whereas other studies reported in part contradictory results [9, 26]. Interestingly, despite its effect on body fat, exercise did not appear to have an effect on body weight reduction, in the present study. This could be due to the combination of aerobic and muscle-strengthening exercises, which both tend to increase non-fatty body mass and metabolic rate [15] without affecting body weight [27, 28]. Among its other positive effects on physiological functions and metabolism, physical exercise seems to have a favorable effect on the lipidemic profile of individuals [29] with further positive effects in the prevention of
Interventional group (n = 20): baseline vs. follow-up
Control group (n = 17): baseline vs. follow-up
cardiovascular disease [30]. It is also well known that the lipidemic profile of women changes in parallel with other physiological changes during pregnancy and postpartum [31]. In the present study, exercise did not appear to have any significant effect on total cholesterol, LDL, HDL and triglyceride levels, despite postpartum physiological reductions in these parameters. Similar results have been previously reported [16, 17], with one exception of increasing HDL levels following a program of aerobic exercise [13], which could be possibly explained by a reduction of other daily activities [13]. The lipidemic profile seems to change during the postpartum period by a combination of exercise with a special diet [17] or by diet only [16]. It is well established that during lactation and the postpartum period, a series of hormonal changes take place [32]. In the present study, such changes were found within the two groups, between baseline and after the 12-week period of either exercise or no intervention, and these findings could be attributed to physiological changes of the postpartum period. In contrast, no such changes were found between the interventional and the control group, and thus exercise did not seem to have any effect on prolactin, estradiol, cortisol, TSH, fT3, and fS4 levels. These findings are in line with those of previous studies, which did not show any effect of moderate [13] or intensive [10] exercise on hormone levels of postpartum women.
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The main strengths of the present study are prospective, randomized control study design, and use of strict inclusion and exclusion criteria. On the other hand, the main limitation is that only primiparous, breastfeeding, and healthy women were included. Future studies should include multiparous women and gradually more intensive exercise programs. In conclusion, implementation of a low-impact exercise training program appears to improve the overall physical fitness of postpartum women, including improvements of cardio-respiratory function (VO2max), muscle strength and endurance of the upper extremities and the abdomen, musculoskeletal stretching of the back and thighs, and reduction of total body fat. On the other hand, a low-impact exercise training program does not seem to be enough to improve the lipid profile of postpartum, lactating women beyond the physiological changes after childbirth.
Conflict of interest interest.
The authors declare no relevant conflict of
References 1. Zourladani A, Tsaloglidou A, Tzetzis G, Tsorbatzoudis CH, Matziari CH (2012) The effect of a low impact exercise training programme on the well-being of Greek postpartum women: a randomised controlled trial. Int Sport Med J 12:30–38 2. Treuth M, Butte N, Puyau M (2005) Pregnancy-related changes n physical activity, fitness, and strength. Med Sci Sports Exerc 37:832–837 3. Web DA, Bloch JR, Coyne JC, Chung EK, Benett IM, Culhane JF (2008) Postpartum physical symptoms in new mothers: their relationship to functional limitations and emotional well-being. Birth 35:179–187 4. American College of Sports Medicine (2006) ACSM’s guidelines for exercise testing and prescription, 7th edn. Lippincott Williams & Wilkins, USA 5. Trost SG, Owen N, Bauman AE, Sallis JF, Brown W (2002) Correlates of adults’ participation in physical activity: review and update. Med Sci Sports Exerc 34:1996–2001 6. Miller YD, Trost SG, Brown WJ (2002) Mediators of physical activity behavior change among women with young children. Am J Prev Med 23:98–103 7. Mottola MF (2002) Exercise in the postpartum period: practical applications. Curr Sports Med Rep 1:362–368 8. Ryan AS, Nicklas BJ, Dennis KE (1998) Aerobics exercise maintains regional bone mineral density during weight loss in postmenopausal women. J Appl Physiol 84:1305–1310 9. Dewey KG, Lovelady CA, Nommsen-Rivers LA, McCrory MA, Lonnerdal B (1994) A randomized study of the effects of aerobic exercise by lactating women on breast-milk volume and composition. N Engl J Med 330:449–454 10. Quin T, Carey GB (1999) Does exercise intensity or diet influence lactic acid accumulation in breast milk? Med Sci Sports Exerc 31:105–110 11. Lovelady CA, Lonnerdahl B, Dewey KG (1990) Lactation performance of exercising women. Am J Cl Nutr 52:103–109
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12. Sampselle CM, Seng J, Yeo S, Killion C, Oakley D (1999) Physical activity and postpartum well-being. J Obstet Gynecol Neonatal Nurs 28:41–49 13. Lovelady CA, Nommsen-Rivers LA, Mc-Grory MA, Dewey KG (1995) Effects of exercise on plasma lipids and metabolism of lactating women. Med Sci Sports Exerc 27:22–28 14. Lovelady CA, Bopp MJ, Colleran HL, Mackie HK, Wideman L (2009) Effect of exercise training on loss of bone mineral density during lactation. Med Sci Sports Exerc 41:1902–1907 15. Callaway C (1997) Low impact aerobics. In: Peg J (ed) Aerobics instructor manual, the resource for group fitness instructors. American Council on Exercise, San Diego, CA, pp 357–381 16. Artal R, O’Toole M (2003) Exercise in pregnancy: guidelines of the American College of Obstetricians and Gynaecologists for exercise during pregnancy and the postpartum period. Br J Sports Med 37:6–12 17. Edvardsen E, Hem E, Anderssen SA (2014) End criteria for reaching maximal oxygen uptake must be strict and adjusted to sex and age: a cross—sectional study. PLoS One 14:9e85276 18. Jackson AS, Pollock ML (1985) Practical assessment of body composition. Physician Sport Med 13:76–90 ˚ strand PO, Rhyming IA (1954) A nomogram for calculation of 19. A aerobic capacity (physical fitness) from pulse rate during submaximal work. J Appl Physiol 7:218–221 20. Hoeger WWK, Hopkins DR (1992) A comparison of the sit and reach and the modified sit and reach in the measurement of flexibility in women. Res Q Exerc Sport 63:191–195 21. Lovelady CA, Garner KE, Moreno KL, Williams JP (2000) The effect of weight loss in overweight, lactating women on the growth of their infants. N Engl J Med 342:449–453 22. Clapp JF 3rd, Capeless E (1997) Cardiovascular function before, during, and after the first and subsequent pregnancies. Am J Cardiol 80:1469–1473 23. McCrory M (2000) Aerobic exercise during lactation: safe, healthful, and compatible. J Hum Lact 16:95–98 24. Larson-Mayer DE (2002) Effect of postpartum exercise on mothers and their offspring, a review of the literature. Obes Res 10:841–853 25. Kramer FM, Stunkard AJ, Marshall KA, McKinney S, Liebschutz J (1993) Breast-feeding reduces maternal lower-body fat. J Am Diet Assoc 93:429–433 26. Little KD, Clapp JF (1998) Self-selected recreational exercise has no impact on early postpartum lactation—induced bone loss. Med Sci Sports Exerc 30:831–836 27. Schmitz KH, Jensen MD, Kugler KC, Jeffery RW, Leon AS (2003) Strength training for obesity prevention in midlife women. Int J Obes Relat Metab Disord 27:326–333 28. Velthuis MJ, Schuit AJ, Peeters PH, Twisk JW, Schuit AJ (2009) Exercise program affects body composition but not weight in postmenopausal women. Menopause 16:777–784 29. Leon AS, Sanchez OA (2001) Response of blood lipids to exercise training alone or combined with dietary intervention. Med Sci Sports Exerc 33:S502–S515 30. American Heart Association (2003) Exercise and physical activity in the prevention and treatment of atherosclerotic cardiovascular disease. A statement from the Council on Clinical Cardiology (subcommittee on exercise, rehabilitation, and prevention) and the Council on Nutrition, Physical Activity, and Metabolism (subcommittee on physical activity). Circulation 107:3109–3116 31. Quresi IA, Xi XR, Limbu YR, Bin HY, Chen MI (1999) Hyperlipidaemia during normal pregnancy, parturition and lactation. Ann Acad Med Singapore 28:217–221 32. Altemus M, Deuster P, Galliven E, Carter CS, Gold PW (1995) Suppression of hypothalamic—pituitary—adrenal axis. J Clin Endocrinol Metab 80:2954–2959
MATERNAL-FETAL MEDICINE
The effect of physical exercise on postpartum fitness, hormone and lipid levels: a randomized controlled trial in primiparous, lactating women A. Zourladani • M. Zafrakas • B. Chatzigiannis P. Papasozomenou • D. Vavilis • C. Matziari
•
Received: 24 May 2014 / Accepted: 8 August 2014 / Published online: 20 August 2014 Ó Springer-Verlag Berlin Heidelberg 2014
Abstract Purpose To evaluate the effect of an exercise training program combining low-impact dance aerobic, resistance and stretching exercise on physical fitness, hormone and lipid levels of postpartum, primiparous, lactating women. Methods Thirty seven primiparous, lactating women were randomly assigned at 4-6 weeks postpartum to either follow an exercise training program of 50-60 min aerobic, strengthening and stretching exercise, 3 days a week, for 12 weeks (interventional group; n = 20) or no training program at all (control group; n = 17). The following parameters were measured at baseline and 12 weeks later: (1) for evaluation of physical fitness: VO2max, muscular endurance, joint mobility and body fat; (2) for evaluation of the lipidemic profile: triglyceride, total cholesterol, HDL and LDL levels, and (3) levels of hormones associated with lactation: prolactin, estradiol, cortisol, TSH, fT3 and fT4. Results After completion of the exercise training program, comparisons between the interventional and the control group showed statistically significant mean changes in VO2max (p = 0.003), muscular endurance of the upper
A. Zourladani B. Chatzigiannis C. Matziari School of Physical Education and Sport Science, Aristotle University of Thessaloniki, Thessaloniki, Greece M. Zafrakas School of Health and Medical Care, Alexander Technological Educational Institute of Thessaloniki, Thessaloniki, Greece M. Zafrakas (&) Ethnikis Antistatseos 81, 55134 Thessaloniki, Greece e-mail: [email protected] P. Papasozomenou D. Vavilis 1st Department of Obstetrics and Gynecology, Medical School, Aristotle University of Thessaloniki, Thessaloniki, Greece
extremities (p \ 0.001), and the abdomen (p \ 0.001), flexibility (p = 0.042), and body fat (p = 0.007). There were no significant differences between the two groups in mean changes of lipid and hormone levels. Conclusion Implementation of a low-impact exercise training program appears to improve physical fitness of postpartum women, while it does not seem to affect lipid levels and lactation-associated hormone levels. Hence, implementation of an exercise training program combining low-impact dance aerobic, resistance and stretching exercise is feasible in postpartum, primiparous, lactating women. Keywords VO2max Muscular endurance Joint mobility Body fat Lipidemic profile Hormone levels
Introduction A woman’s body undergoes remarkable changes after childbirth, regardless of the mode of delivery, and it may take up to 1 year for these changes to be completed [1]. Evidence suggests that, the aerobic capacity and strength of women decline in the early postpartum period [2]. Furthermore, physical complaints, such as backache, emotional problems, including increased anxiety, and functional limitations related to childcare, everyday household activities and work are common after birth, and all tend to increase over time [3]. Physical activity and exercise are well-established factors promoting lifelong physical health and enhancing wellness in the general population [4, 5]. Health-related components of physical fitness, including aerobic capacity, muscular endurance, flexibility, and body composition, are characterized by an ability to perform daily activities with
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526
vigor, and demonstrate the traits and capacities associated with low risk of premature development of hypokinetic disease [4]. It is noteworthy that women are less likely to participate in a physical exercise program than men [5]. Moreover, childbearing may further compromise a woman’s ability to participate in physical exercise programs [6]. Healthcare providers rarely incorporate exercise programs into postpartum care plans [7]. More research results are needed to create effective evidence-based exercise programs and fitness plans for postpartum women. Low-impact aerobics aim to provide cardiovascular and muscle-toning workout without risking injury to a person, due to intense stress on joints, tendons and muscles [8]. The relative importance of strengthening and flexibility to activities of daily living requires the inclusion of such exercises in an exercise routine [4]. In most studies, the effect of vigorous exercise programs on milk volume and composition has been evaluated [9, 10]. In few studies, the effect of a long-term exercise program on some of the parameters of postpartum physical fitness has been assessed [9, 11], while others have just recorded physical exercise of their subjects without the implementation of an exercise program [2, 12]. In some research projects, the effect of different types of aerobic exercise on postpartum health was evaluated [9, 10, 13], while others examined the effect of aerobic and resistance exercise on bone mineral density during lactation [14]. In addition, only few studies have examined the effects of exercise on the lipid profile of postpartum women [13], and on hormones associated with lactation [9, 13]. Given that women in western countries are increasingly asking for postpartum exercise programs, the purpose of this study was to investigate the effect of an exercise program combining low-impact dance aerobic, resistance and stretching exercises on the physical fitness of postpartum women. Additionally, given that abnormal plasma lipid and hormone concentrations are associated with increased risk of cardiovascular disease and the metabolic syndrome, their levels were compared between exercising and non-exercising women, to determine whether moderate exercise may affect the physical health of postpartum women.
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of their predicted maximal heart rate, strengthening and stretching for 50-60 min per day, 3 days a week for 12 weeks. The maximal number of women in each exercise session was 6-7 participants. In the second group (control group, n = 20), women did not undertake physical exercise during the study period. The method of randomization was alternating sequence. Two authors (ZA and CB) generated the random allocation sequence, enrolled participants, and assigned participants to interventions. Blinding of participants and care providers after assignment to interventions was not possible, due to the nature of the study. After randomization, five women, two from the experimental and three from the control group dropped out of the study, leaving 20 participants in the interventional and 17 in the control group. Women dropped out of the study for the following reasons: (a) two women from the experimental group failed to follow the exercise program, by missing the pre-scheduled appointments; (b) two women from the control group did not show up at the end of the study period, to repeat physical measurements and blood tests; (c) one woman from the control group was diagnosed with colon cancer during the study period. Power analysis was conducted (with one-way fixed effects analysis of covariance) and the sample size of the study was considered to be adequate (effect size f = 0.4, power = 0.693). The following inclusion criteria were used: healthy, primiparous, lactating women. The following exclusion criteria were used: obstetrical complications during pregnancy (i.e., preterm birth, bleeding in any trimester, intrauterine growth restriction, intrauterine infection, and fetal anatomic and chromosomal anomalies), multiple gestation, pregnancy-induced hypertension, severe heart disease, chronic renal disease, chronic pulmonary disease, drug abuse and alcoholism, and serious mental and psychiatric illness. All women were informed of risks involved (i.e., physical trauma during exercise and triggering of previously undiagnosed cardiovascular or respiratory disease by exercise) and signed a consent form prior to participation. All interventions were in accordance with the Helsinki declaration of 1975 for experimentation in humans and the study was approved by the Ethics Committee of the Medical School of the Aristotle University of Thessaloniki. Physical exercise protocol
Materials and methods Recruitment and randomization Initially, 42 healthy, primiparous, lactating women were recruited at 4-6 weeks postpartum, and randomly assigned in two groups. In the first group (interventional group, n = 22), participants were engaged in an exercise program, consisting of aerobic exercise at an intensity of 60-70 %
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As previously described [15], the exercise program was in accordance with the American Council on Exercise (ACE) guidelines, and consisted of four parts: (a) warm-up, (b) low-impact aerobics, (c) muscle strengthening and (d) relaxation. The first part was a 10-min warm-up, including low-impact dance aerobics and stretching of main muscle groups, followed by the second part of 2025 min of low-impact aerobics. The intensity of exercise
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was consistent with the guidelines issued in 2003 by the American College of Obstetricians and Gynecologists (ACOG) [16]. Exercise intensity was tailored according to each participant’s fitness level limited to up to approximately 70 % of her maximal heart rate. The intensity of exercise was 140.4 ± 14.1 pulses per minute according to a heart rate monitor, and 12.1 ± 1.1 according to Borg’s scale of fatigue [17]. The third part of the exercise program was 15-20 min of muscle strengthening, consisting of exercises for all major muscle groups. Emphasis was given to the upper and lower back muscles, the abdominal muscles, and the pelvic floor. Each exercise program initially consisted of 1-3 sets, with 8-12 repetitions per set, which gradually increased. The fourth part of the exercise program was 10 min of relaxation, often including yoga. Emphasis was given on stretching of the thoracic muscles to relieve stress caused by extra breast weight and/or constant muscle contraction from breastfeeding and infant cuddling. All stretches were performed both on an active and static basis, and lasted 10-20 s each. The same 35-year-old instructor, certified by the Aerobics and Fitness Association of America (AFAA), with extensive experience in this field, supervised all classes [1]. The following physical fitness parameters were measured: (1) body weight and body fat. The body weight was evaluated electronically, using a special monitor (Tanita InnerScan body composition monitor BC-533, Sindelfingen, Germany). Body fat was evaluated by measuring the skinfold thickness with a skinfold caliper (Lange Skinfold Calliper, Beta Technology Incorporated, Cambridge, Maryland) at the following sites: the triceps, thigh, subscapular, chest, mid-axillary, supra-iliac, and abdominal area. Body density and body fat were calculated using the equation of Jackson & Pollock [18]. (2) VO2max: the Astrand-Rhyming cycle ergometer test was used to estimate VO2max from simple heart rate measurements [19]. The exercise protocol involved constant power output (50-100 W) for 6 min; the pedal rate was set at 50 rpm; the heart rate was measured during the 5th and 6th min of work. (3) Muscular endurance: muscular endurance of the upper extremities was assessed by the YMCA bench press endurance test [4]. Abdominal muscular endurance was assessed by the abdominal bent-knee curl up test [4]. (4) Flexibility: for low back and posterior thigh flexibility the modified sit and reach test [20] was used. Plasma lipid and hormone analyses Blood samples were collected from all women at 68 weeks postpartum (baseline), between 08:00 and 09:00 AM, at least 12 h after the last meal, 1.5 h after breastfeeding, and before exercise. Plasma concentrations
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Fig. 1 Investigational protocol
of total cholesterol, high-density lipoproteins (HDL), lowdensity lipoproteins (LDL), and total triglycerides were measured using a clinical chemistry analyzer (Instrumentation Laboratory ILab 600, Brussels, Belgium). Concentrations of T3, T4, TSH and prolactin were measured by chemiluminescence enzyme immunoassay (CLIA), using the ADVIA CentaurÒ CP Immunoassay System (Siemens, Germany). Estradiol and cortisol were measured by the Electrochemiluminescence (ECL) assay, using E170 Modular Analytics (Roche diagnostics, Greece). Samples were transported in a cooler to the laboratory for separation after centrifugation, and plasma was frozen immediately at –20 °C. Two days after the last exercise session, all physical fitness measurements and plasma lipid and hormone tests were repeated for both the interventional and the control group. An overview of the investigational protocol is presented as a flow chart in Fig. 1. Statistical analysis Descriptive data are presented as minimum and maximum values, means, standard deviations or standard error of the mean. The assumption of normality was tested by the Shapiro–Wilk test (N \ 50). The Pearson’s Correlation Coefficient r was calculated between baseline and followup for normally distributed measurements. When r \ 0.5, differences between groups at baseline were analyzed by the two independent samples t test; the one-way ANCOVA
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model (including baseline measurements as a covariate at each case) was used to compare mean changes between the two groups, while differences between baseline and followup for both groups were analyzed with the paired t test. When r C 0.5, a Linear Mixed model was used. The Mann–Whitney U test for two independent groups and the Wilcoxon test for paired data were used for not normally distributed measurements. Computation of p values was done by the Monte Carlo method. The SPSS 15.0 software was used (IBM Corp, New York, USA), and the level of statistical significance was set at p \ 0.05.
Results According to self-reported data about the course of pregnancy, 20 % of women in the interventional and 22 % in the control group were rarely engaged in low-intensity physical activity (walking) during pregnancy; 35 % in the interventional and 55 % in the control group had attended antenatal classes for 1-3 weeks; 35 % of women in the interventional and 45 % in the control group gave birth by cesarean section. The majority of participants were breastfeeding almost exclusively throughout the study period. By the beginning of the study, three women in each group combined breastfeeding with one or two meals with a milk formula, while by the end of the study five women in the interventional and six in the control group did so. Table 1 provides descriptive data for each group. At baseline, by the beginning of the study, there were no differences between the interventional and the control group in any of the parameters measured, i.e., physical fitness, lipid and hormone levels. After completion of the exercise training program, 12 weeks later, measurements were repeated, and the following statistically significant differences were found in the interventional group as compared with initial measurements: (1) VO2max (p \ 0.001), (2) muscular endurance of the upper extremities (p \ 0.001), (3) abdominal muscular endurance (p \ 0.001), (4) Table 1 Descriptive data of women participating in the study Interventional group (n = 20) (Mean ± SD)
Control group (n = 17) (Mean ± SD)
Age (years)
30.9 ± 2.5
31.7 ± 2.5
Height (cm)
166.7 ± 5.3
168.3 ± 6.0
Body weight before pregnancy (kg)
61.0 ± 10.52
60.8 ± 9.1
Body weight at baseline (kg)
65.1 ± 9.6
65.7 ± 10.8
Body weight at follow-up (kg)
61.8 ± 10.0
64.4 ± 10.7
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flexibility (p \ 0.001), and (5) body fat (p \ 0.001). Likewise, statistically significant changes in the interventional group were found regarding blood levels of cholesterol (p = 0.022), LDL (p = 0.032), prolactin (p = 0.006) and estradiol (p = 0.045). Similar comparisons between baseline and 12 weeks later in the control group showed statistically significant changes in the following parameters: body fat (p = 0.006), flexibility (p = 0.001), cholesterol (p = 0.029), T4 (p = 0.035), and estradiol (p = 0.030). Comparisons between the two groups at follow-up showed differences in VO2max (p = 0.012), muscular endurance of the upper extremities (p \ 0.001) and muscular endurance of the abdominal muscles (p = 0.001). Furthermore, comparisons between the interventional and the control group showed statistically significant mean changes in the following parameters: (1) VO2max (p = 0.003), (2) muscular endurance of the upper extremities (p \ 0.001), (3) abdominal muscle endurance (p \ 0.001), (4) flexibility (p = 0.042), and (5) body fat (p = 0.007). There were no significant differences between the two groups in mean changes of lipid and hormone levels. An overview of results regarding physical fitness, lipid and hormone levels between and within the two groups of women is presented in Table 2.
Discussion This study was prompted by the lack of detailed practice guidelines regarding physical exercise in postpartum women; in general, gradual resumption of activity as tolerated is advised, however, more evidence about the type, frequency and duration of exercise is needed. In the present study, a physical exercise program was planned specifically for postpartum, lactating women and proved to be effective in improving physical fitness, without any adverse effects on lactation. In particular, in respect to cardio-pulmonary function, the VO2max increased significantly in women participating in the exercise program, as compared with the control group. Consistently, similar increases of the VO2max between 13 [21] and 25 % [9] have been previously reported. This finding is particularly important, given that women appear to have physiologically decreased aerobic capacity after childbirth as compared with that before pregnancy [2, 22]. In the present study, muscular endurance of the upper extremities and the abdomen increased significantly after physical exercise, whereas no changes were found in the control group. These findings are consistent with those previously published in a small study, including ten postpartum women engaged in exercise and ten controls [14]. Interestingly, muscular endurance is known to decrease physiologically after childbirth [2, 23, 24].
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Table 2 Overview of comparisons (p values) regarding physical fitness, lipid and hormone levels between and within the two groups of women
Ns not statistically significant a
Results from Linear Mixed Model
b
Results from one-way ANCOVA and t test
c
Results from Mann–Whitney and Wilcoxon tests
Interventional (n = 20) vs. control group at baseline (n = 17)
Interventional (n = 20) vs. control group at follow-up (n = 17)
Comparison of means
Body weighta
Ns
Ns
Ns
Ns
Ns
Body fata
Ns
Ns
0.007
\0.001
0.006
Upper extremity endurancea
Ns
\0.001
\0.001
\0.001
Ns
Flexibilitya
Ns
Ns
0.042
\0.001
0.001
VO2maxc
Ns
0.012
0.003
\0.001
Ns
Abdominal muscle endurancea
Ns
0.001
\0.001
\0.001
Ns
Cholesterolb
Ns
Ns
Ns
0.022
0.029
Triglyceridesc
Ns
Ns
Ns
Ns
Ns
LDLb
Ns
Ns
Ns
0.032
Ns
HDLa
Ns
Ns
Ns
Ns
Ns
Ns
Ns
Ns
Ns
Ns
Prolactin
Ns
Ns
Ns
0.006
Ns
TSHc T3c
Ns Ns
Ns Ns
Ns Ns
Ns Ns
Ns Ns
T4c
Ns
Ns
Ns
Ns
0.035
Estradiolc
Ns
Ns
Ns
0.045
0.030
Cortisolb c
Another finding in the present study was that flexibility of the posterior muscles of the thigh and the lower back were increased significantly in the interventional and the control group, and this difference between the two groups was statistically significant. The improvement of flexibility in the control group could be one of the physiological changes after childbirth. To the best of our knowledge, there are no published data regarding flexibility in postpartum women. A further finding in the present study was that body fat decreased significantly in the interventional and the control group. This decrease could be attributed to the fact that women in both groups were breastfeeding, since lactation is well known to reduce body fat [25], while physical exercise appears to have an additional effect. Similar findings have been previously reported in one study [11], whereas other studies reported in part contradictory results [9, 26]. Interestingly, despite its effect on body fat, exercise did not appear to have an effect on body weight reduction, in the present study. This could be due to the combination of aerobic and muscle-strengthening exercises, which both tend to increase non-fatty body mass and metabolic rate [15] without affecting body weight [27, 28]. Among its other positive effects on physiological functions and metabolism, physical exercise seems to have a favorable effect on the lipidemic profile of individuals [29] with further positive effects in the prevention of
Interventional group (n = 20): baseline vs. follow-up
Control group (n = 17): baseline vs. follow-up
cardiovascular disease [30]. It is also well known that the lipidemic profile of women changes in parallel with other physiological changes during pregnancy and postpartum [31]. In the present study, exercise did not appear to have any significant effect on total cholesterol, LDL, HDL and triglyceride levels, despite postpartum physiological reductions in these parameters. Similar results have been previously reported [16, 17], with one exception of increasing HDL levels following a program of aerobic exercise [13], which could be possibly explained by a reduction of other daily activities [13]. The lipidemic profile seems to change during the postpartum period by a combination of exercise with a special diet [17] or by diet only [16]. It is well established that during lactation and the postpartum period, a series of hormonal changes take place [32]. In the present study, such changes were found within the two groups, between baseline and after the 12-week period of either exercise or no intervention, and these findings could be attributed to physiological changes of the postpartum period. In contrast, no such changes were found between the interventional and the control group, and thus exercise did not seem to have any effect on prolactin, estradiol, cortisol, TSH, fT3, and fS4 levels. These findings are in line with those of previous studies, which did not show any effect of moderate [13] or intensive [10] exercise on hormone levels of postpartum women.
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The main strengths of the present study are prospective, randomized control study design, and use of strict inclusion and exclusion criteria. On the other hand, the main limitation is that only primiparous, breastfeeding, and healthy women were included. Future studies should include multiparous women and gradually more intensive exercise programs. In conclusion, implementation of a low-impact exercise training program appears to improve the overall physical fitness of postpartum women, including improvements of cardio-respiratory function (VO2max), muscle strength and endurance of the upper extremities and the abdomen, musculoskeletal stretching of the back and thighs, and reduction of total body fat. On the other hand, a low-impact exercise training program does not seem to be enough to improve the lipid profile of postpartum, lactating women beyond the physiological changes after childbirth.
Conflict of interest interest.
The authors declare no relevant conflict of
References 1. Zourladani A, Tsaloglidou A, Tzetzis G, Tsorbatzoudis CH, Matziari CH (2012) The effect of a low impact exercise training programme on the well-being of Greek postpartum women: a randomised controlled trial. Int Sport Med J 12:30–38 2. Treuth M, Butte N, Puyau M (2005) Pregnancy-related changes n physical activity, fitness, and strength. Med Sci Sports Exerc 37:832–837 3. Web DA, Bloch JR, Coyne JC, Chung EK, Benett IM, Culhane JF (2008) Postpartum physical symptoms in new mothers: their relationship to functional limitations and emotional well-being. Birth 35:179–187 4. American College of Sports Medicine (2006) ACSM’s guidelines for exercise testing and prescription, 7th edn. Lippincott Williams & Wilkins, USA 5. Trost SG, Owen N, Bauman AE, Sallis JF, Brown W (2002) Correlates of adults’ participation in physical activity: review and update. Med Sci Sports Exerc 34:1996–2001 6. Miller YD, Trost SG, Brown WJ (2002) Mediators of physical activity behavior change among women with young children. Am J Prev Med 23:98–103 7. Mottola MF (2002) Exercise in the postpartum period: practical applications. Curr Sports Med Rep 1:362–368 8. Ryan AS, Nicklas BJ, Dennis KE (1998) Aerobics exercise maintains regional bone mineral density during weight loss in postmenopausal women. J Appl Physiol 84:1305–1310 9. Dewey KG, Lovelady CA, Nommsen-Rivers LA, McCrory MA, Lonnerdal B (1994) A randomized study of the effects of aerobic exercise by lactating women on breast-milk volume and composition. N Engl J Med 330:449–454 10. Quin T, Carey GB (1999) Does exercise intensity or diet influence lactic acid accumulation in breast milk? Med Sci Sports Exerc 31:105–110 11. Lovelady CA, Lonnerdahl B, Dewey KG (1990) Lactation performance of exercising women. Am J Cl Nutr 52:103–109
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12. Sampselle CM, Seng J, Yeo S, Killion C, Oakley D (1999) Physical activity and postpartum well-being. J Obstet Gynecol Neonatal Nurs 28:41–49 13. Lovelady CA, Nommsen-Rivers LA, Mc-Grory MA, Dewey KG (1995) Effects of exercise on plasma lipids and metabolism of lactating women. Med Sci Sports Exerc 27:22–28 14. Lovelady CA, Bopp MJ, Colleran HL, Mackie HK, Wideman L (2009) Effect of exercise training on loss of bone mineral density during lactation. Med Sci Sports Exerc 41:1902–1907 15. Callaway C (1997) Low impact aerobics. In: Peg J (ed) Aerobics instructor manual, the resource for group fitness instructors. American Council on Exercise, San Diego, CA, pp 357–381 16. Artal R, O’Toole M (2003) Exercise in pregnancy: guidelines of the American College of Obstetricians and Gynaecologists for exercise during pregnancy and the postpartum period. Br J Sports Med 37:6–12 17. Edvardsen E, Hem E, Anderssen SA (2014) End criteria for reaching maximal oxygen uptake must be strict and adjusted to sex and age: a cross—sectional study. PLoS One 14:9e85276 18. Jackson AS, Pollock ML (1985) Practical assessment of body composition. Physician Sport Med 13:76–90 ˚ strand PO, Rhyming IA (1954) A nomogram for calculation of 19. A aerobic capacity (physical fitness) from pulse rate during submaximal work. J Appl Physiol 7:218–221 20. Hoeger WWK, Hopkins DR (1992) A comparison of the sit and reach and the modified sit and reach in the measurement of flexibility in women. Res Q Exerc Sport 63:191–195 21. Lovelady CA, Garner KE, Moreno KL, Williams JP (2000) The effect of weight loss in overweight, lactating women on the growth of their infants. N Engl J Med 342:449–453 22. Clapp JF 3rd, Capeless E (1997) Cardiovascular function before, during, and after the first and subsequent pregnancies. Am J Cardiol 80:1469–1473 23. McCrory M (2000) Aerobic exercise during lactation: safe, healthful, and compatible. J Hum Lact 16:95–98 24. Larson-Mayer DE (2002) Effect of postpartum exercise on mothers and their offspring, a review of the literature. Obes Res 10:841–853 25. Kramer FM, Stunkard AJ, Marshall KA, McKinney S, Liebschutz J (1993) Breast-feeding reduces maternal lower-body fat. J Am Diet Assoc 93:429–433 26. Little KD, Clapp JF (1998) Self-selected recreational exercise has no impact on early postpartum lactation—induced bone loss. Med Sci Sports Exerc 30:831–836 27. Schmitz KH, Jensen MD, Kugler KC, Jeffery RW, Leon AS (2003) Strength training for obesity prevention in midlife women. Int J Obes Relat Metab Disord 27:326–333 28. Velthuis MJ, Schuit AJ, Peeters PH, Twisk JW, Schuit AJ (2009) Exercise program affects body composition but not weight in postmenopausal women. Menopause 16:777–784 29. Leon AS, Sanchez OA (2001) Response of blood lipids to exercise training alone or combined with dietary intervention. Med Sci Sports Exerc 33:S502–S515 30. American Heart Association (2003) Exercise and physical activity in the prevention and treatment of atherosclerotic cardiovascular disease. A statement from the Council on Clinical Cardiology (subcommittee on exercise, rehabilitation, and prevention) and the Council on Nutrition, Physical Activity, and Metabolism (subcommittee on physical activity). Circulation 107:3109–3116 31. Quresi IA, Xi XR, Limbu YR, Bin HY, Chen MI (1999) Hyperlipidaemia during normal pregnancy, parturition and lactation. Ann Acad Med Singapore 28:217–221 32. Altemus M, Deuster P, Galliven E, Carter CS, Gold PW (1995) Suppression of hypothalamic—pituitary—adrenal axis. J Clin Endocrinol Metab 80:2954–2959
