Resistance Training Does Not Decrease Placental Blood Flow During Valsalva Maneuver: A Novel Use of 3D Doppler Power Flow Ultrasonography

Abstract

Background:

The Valsalva maneuver may increase maternal blood pressure and intra-abdominal pressure, resulting in decreased blood flow to the fetus during resistance training.

Hypothesis:

There is no significant reduction in placental blood flow in pregnancy during resistance training in recreational athletes, as documented by a 3-dimensional power flow Doppler ultrasonography.

Study Design:

Cohort.

Level of Evidence:

Level 3.

Methods:

A cohort of healthy women who participated in recreational athletics was enrolled in a prospective study to assess placental blood flow during a resistance exercise. A 1 repetition maximum (1RM, up to 50 lb) was determined through a modified chest press as a marker of heavy resistance training. Three-dimensional volume measurements and power Doppler flow were determined at the rest phase and during the 1RM lift phase. The vascular flow index (VFI) was calculated to determine placental perfusion during each phase.

Results:

A total of 22 women participated. The mean age of participants was 31 years. Gestational age ranged from 13 to 28 weeks. Average 1RM weight lifted was 30 lb. Four women (18%) were able to lift 50 lb, the maximum weight that the study allowed. The remaining 18 women (82%) lifted their true 1RM. Mean VFI during lift phase was 2.185 compared with 2.071 at rest (P = 0.03). There was a slight mean increase in VFI during lift phase, 0.114 (95% CI 0.009-0.182) from 2.071 to 2.185 with lifting (P = 0.03). The 15 women who participated in structured exercise had a mean VFI at rest and during the lift phase of 2.031 and 2.203, respectively (P = 0.01).

Conclusion:

Three-dimensional power flow Doppler imaging can guide resistance training during pregnancy to prevent fetal injury due to hypoperfusion. Resistance training up to an RM1 of 50 lb did not result in a significant reduction of placental blood flow from resting state in the study population.

Clinical Relevance:

This technique may be used to guide training parameters among pregnant athletes.

Peak fertility coincides with peak athletic performance years for women, placing a subset of these women into exercise regimens guided largely by theoretical recommendations and unknown risks. Experts have advocated that both aerobic and anaerobic exercise could convey health benefits, including decreased pregnancy morbidity to the mother and improved neonatal neuromotor skills, to the offspring, and should be recommended for nearly every pregnant woman.^1,5,11 However, The American College of Obstetrics and Gynecology reports in their committee opinion on “Physical Activity and Exercise During Pregnancy and the Postpartum Period”¹ that certain conditions, such as vaginal bleeding, abdominal pain, and regular painful contractions, should preclude exercise during pregnancy. The lack of available data on these conditions leaves unanswered questions for what is considered “safe” in pregnancy. Despite the enthusiasm for global exercise participation in pregnancy, resistance training has not been as well studied in pregnancy.¹⁸ As fetal safety is directly related to placental perfusion, we aim to document stable placental blood flow during resistance training in women recreational athletes as assessed by a 3-dimensional (3D) power flow Doppler ultrasonography.

Background

The International Olympic Committee expert consensus panel concluded in their report on the subject of exercise in pregnancy that there is sparse knowledge on strength training.⁷ They specifically pointed out the largely theoretical risk that a Valsalva maneuver could increase maternal blood pressure and intra-abdominal pressure, resulting in decreased placental blood flow to the fetus during resistance training.⁷ Resistance training can theoretically decrease fetal blood flow due to possible shunting of blood away from the placenta as maternal intra-abdominal pressure rises and peripheral dilation increases to optimize maternal extremity blood flow. Despite this theoretical concern, media outlets have documented numerous women competing in the Olympic sports of curling (Kristie Moore) and beach volleyball (Anita Spring) during their second trimester of pregnancy.²¹ These sports require excellent core strength, the practice of which constitutes resistance training.

Given that the concerns on strength training in pregnancy are related to the theoretical risk of shunting blood away from the fetus, we sought to determine parameters of which to assess placental blood flow during strength training in gravid women. We did this by directly measuring placental blood flow during weight lifting utilizing 3D power Doppler ultrasound to quantify blood flow in the placental vascular network to assess any changes related to maternal resistance training. The vascular flow index (VFI) was selected as our parameter of interest as this technique has been well described, validated, and normative data have been developed.^14,15,22

Methods

Participants

This was an observational study that enrolled 22 healthy women with uncomplicated pregnancies (Table 1). Most of the women were recreational athletes. Recreational exercise was defined as structured cardiovascular, resistance, or a combination of both. The women were largely normal weight, with only 2 (9%) having a body mass index >30 kg/m² during their second trimester of pregnancy. The mean age of participants was 31 years with a range from 27 to 38 years. Gestational age ranged from 13 to 28 weeks. Participants were recruited via flyers that were posted in clinical offices and posted on social media. Participants determined their individual 1 repetition maximum (1RM) weight to demonstrate heavy resistance training. The participants received 3D images of their fetuses for their participation. As the study consisted of a single visit, no participants were lost to follow-up or excluded from analysis. The study was approved by the University of Alabama (UAB) Institutional Review Board and the UAB Center for Women’s Reproductive Health. Written, informed consent was obtained from each participant. A total of 22 women were needed for enrollment to have 90% power to detect a 0.5 SD change in placental blood flow as measured by the VFI.

Table 1.

Participant characteristics

Participant	Age, y	Regular Participation in Scheduled Exercise	Gestational Age
1	34	No	25 wk 5 d
2	28	No	19 wk 3 d
3	38	Yes	28 wk 5 d
4	33	No	28 wk 2 d
5	29	Yes	26 wk 1 d
6	30	Yes	18 wk 0 d
7	27	Yes	19 wk 5 d
8	37	Yes	21 wk 3 d
9	28	Yes	23 wk 1 d
10	28	No	15 wk 4 d
11	27	Yes	26 wk 3 d
12	30	Yes	21 wk 1 d
13	33	Yes	17 wk 4 d
14	27	Yes	22 wk 0 d
15	33	Yes	22 wk 4 d
16	34	Yes	19 wk 4 d
17	31	Yes	13 wk 3 d
18	31	Yes	17 wk 2 d
19	36	Yes	14 wk 3 d
20	34	No	17 wk 4 d
21	30	No	23 wk 6 d
22	30	No	28 wk 4 d

Ultrasound Examination

We defined moderate-to-heavy strength training as a 1RM as determined by the maximal weight each participate could lift, up to a maximum of 50 lb. Participants were advised to lift as much as they could while maintaining proper form, without eliciting pain. Weight increments started at 10 lb and increased in 10-lb increments, if the participant felt they could not lift any more weight. The maximum total weight was set at 50 lb, which has long been defined in occupational literature as the upper limit of weight that is considered safe for the general population to lift during the second trimester of pregnancy. Using dumbbells, the participants performed a modified bench press in a semisupine position, with approximately 30° elevation of the head. Historically, exercise in a supine position (as in a bench press) has been avoided because of concerns for venal caval obstruction by the gravid uterus and can decrease uterine blood flow up to 25%.¹⁹ A 30° inclination was selected, as there is no evidence to suggest a decrease in placental blood flow from this position.⁸ The study was supervised by a specialist in maternal-fetal medicine who has expertise in sonographic techniques and the diagnosis of fetal pathologic conditions, as well as a sports medicine specialist with expertise in musculoskeletal conditions during pregnancy.

Once the 1RM was determined for each participant, we performed a placental vascular sonobiopsy with 3D power flow Doppler ultrasound while the participant was at rest. A sonobiopsy technique was chosen as it allows for a single ultrasound measurement to be taken, which is representative of the blood flow through the entire placenta^14,15,22 (Figure 1).

Figure 1.

Placental sonobiopsy.

Ultrasonography was performed using a Logiq S7 Rev level 3.0.8 (GE Healthcare) and a broad-spectrum convex volume 3.1- to 8-MHz transducer, which was placed on the maternal abdomen. The placenta was then located and the power Doppler window was placed over the scan section to include the visualized portions of the placenta (settings: power, 95%; gain, 18 dB; frequency, 3.6 MHz; quality, mid1; wall filter, 157 (low); and pulse repetition frequency 1.5 MHz). The 3D volume box was then placed at a prefixed angle of 84° over the placenta and the 3D volume was acquired. This procedure was repeated while the patient performed a modified bench press using the predetermined 1RM weight. The duration of the sweep was approximately 10 seconds, as previously described²² and it was recorded simultaneously with the maximal lift. After the maximal lift, an ultrasound was performed to assess for fetal bradycardia.

The data were stored and analyzed later using the virtual organ computer-aided analysis program (VOCAL II, GE Healthcare). Calculations were performed with the sphere mode using a 30° rotation step. We selected placental sonobiopsy volumes of 4 cm for each participant, taking care to avoid spiral arteries, the chorionic and basal plates. Then VFI was calculated. It is determined using the other 3D vascular indices: vascularization index (VI) and flow index (FI). VFI is calculated by multiplying VI by FI and dividing the result by 2.² The VFI was chosen as it represents both a percentage of vascularized placental tissue as well as the mean velocity of flow into the sample tissue.^12,16 It also is a simple tool that is highly reproducible¹³ and calculated by the VOCAL software.

The study was powered to detect a change in placental blood flow, as measured by VFI, of 0.5 SD from normative data. A paired t test was used to compare VFI at rest and during the lift phase. P values of ≤0.05 (2-sided) were considered statistically significant.

Results

In this cohort of 22 women, a majority, 15 (68%), reported routine participation in a structured exercise program.

The mean 1RM weight lifted was 30 lb with 4 women (18%) lifting 50 lb, the maximum weight the study allowed. The remaining 18 women (82%) lifted their true 1RM. Z scores from previously established normative data¹⁵ provided benchmarks for the VFI (Table 2). For the entire cohort, the mean VFI at rest and during the lift phase were 2.071 and 2.185, respectively (P = 0.03, Table 3). There was a significant mean increase in placental blood flow of 0.114 (95% CI 0.009-0.182) during the lift phase.

Table 2.

Vascular flow index (VFI) at rest and during resistance exercise

Participant	VFI Rest	VFI Lift	Change	1RM (lb)	Scheduled Exercise	Predicted Value VFI8 for GA	Reference Range VFI for GA
1	2.775	2.636	−0.139	50	No	2.4	0.75-4.05
2	2.544	2.279	−0.265	30	No	1.99	0.34-3.64
3	4.583	4.448	−0.135	20	Yes	2.61	0.96-4.26
4	2.651	2.773	0.122	30	No	2.61	0.96-4.26
5	1.46	2.274	0.814	50	Yes	2.47	0.82-4.12
6	1.585	1.383	−0.202	20	Yes	1.92	0.27-3.57
7	1.509	1.662	0.153	30	Yes	1.99	0.34-3.64
8	1.76	2.012	0.252	30	Yes	2.12	0.47-3.77
9	1.518	1.732	0.214	30	Yes	2.26	0.61-3.91
10	1.558	1.454	−0.104	40	No	1.71	0.06-3.36
11	2.106	2.295	0.189	50	Yes	2.47	0.82-4.12
12	2.754	2.829	−0.075	50	Yes	2.12	0.82-4.12
13	1.471	1.69	−0.219	10	Yes	1.85	0.20-3.50
14	1.119	1.369	0.25	40	Yes	2.19	0.54-3.84
15	1.687	1.934	0.247	30	Yes	2.19	0.54-3.84
16	1.872	2.025	0.153	30	Yes	1.99	0.34-3.64
17	1.712	1.96	0.248	30	Yes	1.57	—
18	4.158	4.324	0.166	40	Yes	1.85	0.20-3.50
19	1.175	1.11	−0.065	20	Yes	1.67	—
20	1.717	1.548	−0.169	40	No	1.85	0.20-3.50
21	1.431	1.584	0.153	30	No	2.26	0.61-3.91
22	2.418	2.756	0.338	40	No	2.61	0.96-4.27

1RM, 1 repetition maximum; GA, gestational age.

Table 3.

Vascular flow index (VFI) of rest and lift based on participation in routine exercise

Participant	Number	VFI Rest	VFI Lift	P
Entire cohort	22	2.071	2.185	0.03
Participated in routine exercise	15	2.031	2.203	0.01
Nonexercisers	7	2.156	2.147	0.92

A predetermined subanalysis was performed on women who reported participation in structured exercise versus those who did not exercise outside of their regular daily routine. Of these 15 women who reported participation in a structured exercise program, the mean VFI at rest and during the lift phase were 2.031 and 2.203, respectively (P = 0.01). There was a significant mean increase in placental blood flow of 0.172 (95% CI 0.044-0.168) during the lift phase (Table 3). Of the 7 women who did not, the mean VFI at rest and during the lift phase were 2.156 and 2.147, respectively (P = 0.91, Table 3). There was no difference in placental blood flow of 0.172 (95% CI −0.209 to 0.139) during the lift phase.

Discussion

Our study demonstrated that placental perfusion, as measured by VFI, was not decreased during a moderate-to-heavy resistance exercise intervention as determined by a 1RM. Moreover, women who participate in structured exercise programs during pregnancy demonstrated a statistically significant increase in placental blood flow as measured by VFI.

There is a growing body of evidence documenting that endurance exercise in pregnancy conveys health benefits to the mother and fetus. A meta-analysis of 9 randomized controlled trials demonstrated lower incidences of gestational diabetes mellitus, lower incidences of gestational hypertensive disorders, and a lower rate of cesarean delivery in the exercising group.⁴ Participation in aerobic exercise, such as running, throughout pregnancy has further been associated with an increase in villous vascular volume and cell proliferation of the placenta. This was most notable in women who ran at least 4 times a week for 40 to 60 minutes a session at an intensity 55% to 65% of their maximal aerobic capacity.⁶

It should be noted, however, that these studies were conducted in women who participated in aerobic exercise activity at a moderate intensity. Not all studies that have explored placental blood flow have demonstrated beneficial effects. Salvesen et al²⁰ documented fetal bradycardia and a high umbilical artery pulsatility index during exercise intensities greater than 90% of maximal maternal heart rate. They also documented a simultaneous reduction in uterine volume blood flow to less than 50% of the initial value. Thus, they concluded that exercise at intensities above 90% of maximal maternal heart rate could have negative effects on fetal health.¹⁸ These studies have been limited to effects of aerobic exercise in pregnancy. There is much more limited data on the effects of strength training, especially moderate-to-heavy intensities during pregnancy.

Maternal echocardiograms performed during Valsalva maneuver on women with uncomplicated pregnancies in the third trimester have demonstrated significantly higher left ventricular end-diastolic stroke volumes than nonpregnant controls.⁹ This is likely attributed to increased blood volume status during pregnancy. Interestingly, less than 50% of study participants had a normal blood pressure and heart rate response to the Valsalva maneuver. Another study¹⁷ documented no correlation between the maternal heart rate and ratings of perceive exercise intensity. These results suggest that the relationship between maternal-fetal hemodynamics and exercise is complicated and may not be accurately studied by traditional means of hemodynamic monitoring. Thus, the need for novel techniques to measure placental blood flow are necessary.

Although a limited number of studies^3,7 have been performed, it is reassuring that strength training has not been shown to elicit hypertensive responses in women; nor has it been shown to compromise fetal heart rate variability. Additionally, some women may experience fewer unpleasant symptoms of pregnancy, including headache, nausea, fatigue, and back pain, with strength training during pregnancy.¹⁰

Three-dimensional power flow Doppler ultrasonography using a sonobiopsy technique has been well documented and validated to assess placenta blood flow. Our study is unique in that we describe a novel application of this technique to measure placental perfusion during resistance training. Other studies that used ultrasonography to measure placental perfusion, measured uterine artery blood flow. These measurements were performed during pauses in the exercise, and not during peak exertion.²⁰ In contrast, our technique allowed blood flow measurements to be obtained at the peak of exertion, thereby documenting the conditions the fetus experiences at maximal exercise intensity in real time. This technique can be used to help guide resistance training during pregnancy for women who wish to engage in a structured exercise program, by establishing adequate placental perfusion during training.

No study is without limitations. Although we realized a statistically significant increase in placental blood flow as, measured by VFI, between rest and lift phases, the clinical significance of this change is unclear. The fluctuations of VFI that remain within a standard deviation of the expected VFI is of unclear clinical significance. We hypothesize that such change is not likely to have a clinical impact, particularly when compared with situations of pathologically reduced VFI, as occurs in fetal growth restriction.¹⁵ However, this does not conflict with our finding that adequate placental blood flow is maintained during moderate-to-heavy resistance training. Another limitation includes the change in placental blood flow based on placental location. Prior studies included only women with an anterior placental location because of the potential for Doppler signal attenuation. As distance between the placental vasculature and transducer increases, the quality of the technique can be degraded because of ultrasound signal scatter.^15,22 This is unlikely to be an issue for our study as all our results were within 1.5 SD of the expected VFI, regardless of placental location. Additionally, our participants were mostly ideal body weight, with a body mass index <30 kg/m², which improved image quality. Finally, all the participants may not have experienced a true 1RM. We did not assess if the 4 participants who lifted 50 lb would have been able to lift more weight. It is likely that for at least some of these participants, 50 lb did not represent a true maximal weight. Regardless, the exercise performance at a minimum still required moderate intensity effort.

Conclusion

Our results demonstrate that moderate-to-heavy resistance training, as defined by a single chest press at 1RM, did not reduce placental blood flow from a resting state as measured by 3D power flow Doppler imaging. Three-dimensional power flow Doppler imaging can be used to guide resistance training during pregnancy. Future studies should address the effects of conditioned versus nonconditioned participants, as well as the effect of repeated contraction cycles.