Effect of inspiratory muscle training on respiratory muscle strength, post-operative pulmonary complications and pulmonary function in abdominal surgery- Evidence from systematic reviews.

Introduction

The early postoperative period following abdominal surgery is associated with fatigue and limited chest movements due to surgical pain, restricted diaphragmatic mobility, anesthetic effect, site, and length of the surgical incision, reduced physical activity, and positional dependence.¹ These factors alter the thoracoabdominal mechanism and length-tension relationship, reducing chest mobility and various post-surgical impairments such as inadequate air entry and impaired cough mechanism leading to postoperative pulmonary complications (PPCs).^2,3

Alteration in the breathing pattern due to the effect of general anesthesia and peri-operative drugs causes changes in neural drive, which further reduces functional residual capacity (FRC) post-operatively, leading to ventilation-perfusion mismatch and eventually leading to hypoxemia and increase in respiratory rate.^1,4

Additional factors such as surgical incision around the diaphragm and abdominal muscles, and length of incision influence the development of PPCs. The site of an incision limits the respiratory movement due to reflex inhibition of the phrenic nerve and response to pain stimulus from nerve innervating abdominal muscles. Also, as the length of the incision increases, the peritoneal area near the abdominal viscera is severely affected. As a result, open abdominal surgery has a higher chance of developing PPCs than laparoscopic surgery.^2,4,5

Postoperative pain, limited respiratory movements, and analgesics are believed to be important factors associated with cough impairment.⁶ Inadequate cough reflex post-surgery is commonly related to the pathophysiological basis of PPCs as it leads to excessive secretion accumulation, reduced vital capacity, and increases the risk of respiratory infection eventually causing PPCs.^6,7

Similarly, preoperative patient-related risk factor causes PPC. Risk factors such as age, pre-existing respiratory disease, obesity, and smoking history alter normal respiratory physiology.⁸ Thus, identification of preoperative risk factors and modification of modifiable risk factors is essential to reduce the occurrence of PPCs.^9,10

Diaphragmatic weakness pre-operatively and post-operatively are identified as potential modifiable contributors in developing PPCs.^11,12 The incidence of postoperative lung atelectasis and pneumonia is the main pathophysiological mechanism behind the development of PPCs. Hypoventilation due to altered consciousness, respiratory muscle weakness, decrease FRC with dependency in supine position causes reversible alveolar collapse resulting from obstruction of airways due to impaired mucociliary function and inadequate cough reflex, resulting in the retention of mucus and altering ventilation-perfusion ratio.¹³

Pre-rehabilitation and preoperative chest physiotherapy include deep breathing techniques, splinted active coughing, incentive spirometry (IS), inspiratory muscle training (IMT), and education regarding early mobilization helps in reducing the occurrence of PPCs. Effective training improves respiratory function pre-operatively and benefits in improving lung expansion postoperatively than no intervention.^8,14

However, recent literature suggests that the effectiveness of incentive spirometry post-abdominal surgery has no impact on reducing PPCs and that IMT with or without additional therapy, given as pre-rehabilitation has a beneficial effect of reducing PPCs and length of hospital stay.^8,11

Clinical trials of preoperative IMT have revealed fewer declines in inspiratory muscle strength postoperatively by promoting deep breathing and reducing the occurrence of PPCs.⁸ IMT aims to increase strength and endurance by applying a resistive load to inspiratory muscle to achieve a training effect.³ It helps to restore lung function rapidly thus assisting in improving lung expansion which facilitates forceful expiratory maneuver for secretion clearance and earlier recovery in the postoperative period.¹²

Despite the beneficial effect of IMT, there are few limitations such as improper experimental design depending on participants pre-surgical status, type of surgery, control of training intensity, and patient selection as its benefits changes according to training dose given, i.e., starting load, load increment, duration of intervention, frequency, duration of the training, number of sessions and degree of supervision.^11,15

Various outcome measures are used by researchers to observe the clinical course of IMT with its relationship with PPCs, most notable being such as length of hospital stay, respiratory muscle strength (RMS), lung volume, and capacities. It has been observed that RMS reduces following major abdominal surgery due to surgical pain, exertion while breathing, and maybe pre-cursor of PPCs affecting lung volume and capacities postoperatively.¹²

Thus, this review aims to synthesize findings from a systematic review that evaluates the effectiveness of IMT on abdominal surgery.

Methods

An evidence-based review, on IMT for participants undergoing abdominal surgery was undertaken. The review adheres to the PRISMA checklist for reporting the systematic review and the same has been deposited into the online repository. (OSF registry (DOI 10.17605/OSF.IO/K8NGV). This review was registered in PROSPERO (177876).

Results

From the electronic database search, 1249 articles were identified; 40 were eligible for full-text review, and four systematic reviews and meta-analyses were included in the final review (Figure 1). Reviews were excluded because of unsuitable title and/or study design, primary intervention other than IMT, and report written other than the English language. Data for 276 participants were analyzed, 137 in the intervention group, and 139 in the control group.

Figure 1. PRISMA Flow chart.

Quality assessment

Quality assessment done by AMSTAR-2 has been summarized in Tables 4 and 5. Out of 4 systematic reviews, 3 systematic reviews were reported as high-quality reviews.

Table 4. Quality assessment using AMSTAR-2 for systematic reviews.

	PICO	Deviation from protocol	Explanation from study design	Comprehensive search strategy	Study selection in duplicate	Data extraction in duplicate	Justification from exclusion	Adequacy of detail	RoB assessment	funding	Meta-analysis: measures for statistics	Impact of RoB	Impact of RoB on results	Explanation for heterogeneity	Test for publication bias	Conflict of interest
Christina Mans et al.12 (2014)	Y	Y	Y	PY	Y	Y	Y	Y	Y	Y	Y	Y	Y	Y	N	Y
Katsura M. et al.8 (2015)	Y	Y	Y	Y	Y	Y	Y	Y	Y	Y	Y	Y	Y	Y	Y	Y
Filipa Kendall et al.11 (2017)	Y	PY	Y	PY	Y	Y	PY	Y	Y	Y	Y	Y	Y	Y	Y	Y
Xiaoqing Ge et al.16 (2018)	Y	N	Y	Y	Y	Y	PY	Y	Y	Y	Y	Y	N	N	Y	Y

Table 5. Level of evidence.

Sr no.	Author name	Level of evidence (AMSTAR 2)
1	Mans et al.12	High-quality review
2	Katsura M. et al.8	High-quality review
3	Filipa Kendall et al.11	High-quality review
4	Xiaoqing Ge et al.16	Low-quality review

This review involved meta-analyses of the following outcome measures:

• 1. Respiratory Muscle Strength

  • i. Maximum inspiratory pressure (MIP): Six studies were analyzed for MIP,^{1–3,7,14,17} observing 93 participants in the intervention group and 87 participants in the control group. Heterogeneity [I²] was 53% (P_{heterogeneity} = 0.06). The mean difference was 4.97 (95% CI -5.07 to 15.01) for the intervention group versus the control group (Figure 2).

  • ii. Maximum expiratory pressure (MEP): Two studies were analyzed for MEP,^7,14 observing 38 participants in the intervention group and 38 participants in the control group. Heterogeneity [I²] was 0% (P_{heterogeneity} = 0.49). The mean difference was 3.32(95% CI -9.10 to 15.74) for the intervention group versus the control group (Figure 3).

• 2. Postoperative pulmonary complications:

  • i. Atelectasis: Three studies were analyzed for the occurrence of an adverse event of PPC (atelectasis),^1,3,19 observing 35 participants in the intervention group and 37 participants in the control group. Heterogeneity [I²] was 0% (P_{heterogeneity} = 0.93). The risk ratio was 0.40 (95% CI 0.19 to 0.88) for the intervention group versus the control group. The test for overall effect (P = 0.02) was statistically significant, favoring intervention (Figure 4).

  • ii. Pneumonia: Five studies were analyzed for the occurrence of the adverse effect of PPC (pneumonia)^1,17–20 observing 74 participants in the intervention group and 76 participants in the control group. Heterogeneity [I²] was 0% (P_{heterogeneity} = 0.57). The risk ratio was 0.41 (95% CI 0.14 to 1.19) for the intervention group versus the control group. Out of the five studies analyzed, four studies favor intervention (Figure 5).

• 3. Pulmonary function test

  • i. Forced vital capacity: Two studies were analyzed for forced vital capacity (FVC),^2,7 observing 30 participants in the intervention group and 32 participants in the control group. Heterogeneity [I²] was 0% (P_{heterogeneity} = 0.93). The mean difference was 0.25 (95% CI -0.25 to 0.75) for the intervention group versus the control group (Figure 6).

  • ii. Forced Expiratory Volume (FEV1) in the first second: Two studies were analyzed for FEV1^2,7 observing 30 participants in the intervention group and 32 participants in the control group. Heterogeneity [I²] was 0% (P_{heterogeneity} = 0.61). The mean difference was 0.26 (95% CI -0.24 to 0.76) for the intervention group versus the control group (Figure 7).

  • iii. Inspiratory vital capacity (IVC)/Vital Capacity (VC): Three studies were analyzed for IVC/VC^3,7,18 observing 39 participants in the intervention group and 39 participants in the control group. Heterogeneity [I²] was 31% (P_{heterogeneity} = 0.23). The mean difference was -0.11 (95% CI -0.59 to 0.38) for the intervention group versus the control group (Figure 8).

• 4. Length of hospital stay: Three studies were analyzed for the length of hospital stay^1,17,20 observing 44 participants in the intervention group and 45 participants in the control group. Heterogeneity [I²] was 0% (P_{heterogeneity} = 0.54). The mean difference was 0.15 (95% CI -3.43 to 3.74) for the intervention group versus the control group. The test for overall effect (P = 0.93), concludes data to be statistically insignificant (Figure 9).

• 5. Functional capacity: One study reported functional capacity using a six-minute walk test. The preoperative and postoperative six-minute walk distance value (median and range) in the intervention group was higher as compared to the control group (Table 6).

Figure 2. Meta-analysis of Maximum Inspiratory Pressure (MIP).

I² = heterogeneity/test for heterogeneity, CI = confidence interval.

Figure 3. Meta-analysis of Maximum Expiratory Pressure.

I² = heterogeneity/test for heterogeneity, CI = confidence interval.

Figure 4. Meta-analysis of PPC atelectasis.

I² = heterogeneity/test for heterogeneity, CI = confidence interval.

Figure 5. Meta-analysis of PPC Pneumonia.

I² = heterogeneity/test for heterogeneity, CI = confidence interval.

Figure 6. Meta-analysis of PFT parameter Forced vital capacity.

I² = heterogeneity/test for heterogeneity, CI = confidence interval.

Figure 7. Meta-analysis of PFT parameter forced expiratory volume in 1^st second.

I² = heterogeneity/test for heterogeneity, CI = confidence interval.

Figure 8. Meta-analysis of PFT parameter Vital Capacity.

I² = heterogeneity/test for heterogeneity, CI = confidence interval.

Figure 9. Meta-analysis of length of stay.

I² = heterogeneity/test for heterogeneity, CI = confidence interval.

Table 6. Functional capacity (6MWD).

6MWD in meters: Soares et al. 20131
Intervention group						Control group
Pre-operative median	Pre-operative range	Pre-operative (N)	Post-operative median	Post-operative range	Post-operative (N)	Pre-operative median	Pre-operative range	Pre-operative (N)	Post-operative median	Post-operative range	Post-operative (N)
514.4	460.8-557.5	12	486	392.3-562.3	12	441.5	412.3-505.9	8	447.3	373.7-465.8	8

Discussions

This review was summarized using 4 systematic reviews and meta-analyses. The included systematic reviews highlighted the effect of IMT not only on abdominal surgery but also included cardiac and thoracic surgeries. However, this review only focused on abdominal surgery. Abdominal, cardiac, or thoracic surgeries lead to PPCs but the incision close to the diaphragm or respiratory muscle may have a higher incidence of PPCs compared to others. The reason can be viable tissue damage during surgery, pain, and diaphragm dysfunction.²¹

In cardiac surgeries, the most common procedure sternotomy has reported less respiratory muscle dysfunction as compared to abdominal surgery and thoracic surgery where the respiratory muscles are directly affected.²² The inspiratory muscle diaphragm accounts for 60–70% change in lung volume and capacities and, also, the inspiratory tone in the diaphragm prevents abdominal viscera from compressing lungs.²³

Following abdominal or thoracic surgery, due to respiratory muscle dysfunction, a restrictive pattern develops in the immediate post-operative period. As per Laplace’s law, “curvature of the diaphragm is an important determinant of its ability to produce pressure.” Thus, in abdominal surgery, it is common to find a decrease in maximal inspiratory, transdiaphragmatic, and expiratory muscle pressure.²²

In addition, surgery-associated conditions such as peritonitis, abdominal trauma, and fluid shifts can cause respiratory failure by increasing intra-abdominal pressure. This increase in intra-abdominal pressure can decrease chest wall compliance and diaphragmatic excursion.²³

The meta-analysis was performed to compare various outcome measures for the participants undergoing abdominal surgery. The different outcome measures for quantitative analysis were respiratory muscle strength (MIP/MEP), PPCs (atelectasis and pneumonia), pulmonary functional capacity, and length of hospital stay, and qualitative analysis on functional capacity Six Minute Walk Distance (6MWD) The result suggests that IMT as preoperative or postoperative intervention plays a significant role in improving inspiratory capacity and then eventually reduces the incidence of PPC and health-related cost of care.

In a meta-analysis of MIP, the studies Barbalho-Moulim et al., Llorens et al., Soares et al. found a significant difference in pre-intervention and Casali et al. in post-intervention MIP level in the intervention group vs. control group, whereas Dronkers et al. (2008) and Dronkers et al. (2010) could not find any significant difference. Meta-analysis showed moderate heterogeneity between studies I² = 53% and found a combined positive effect of IMT on MIP.^{1–3,7,14,17}

Studies have shown that better MIP values among intervention groups are acknowledged due to the recruitment of motor units of respiratory muscle that promote increased muscle strength. Respiratory muscle, like any skeletal muscle, responds to the increasing load imposed by IMT and follows the physiological principle of muscle training. Threshold IMT offers a flow-independent one-way valve to ensure constant resistance. Thus, increment in frequency, duration, and intensity of IMT provides more load/resistance, improving muscle function and observing morphological changes in the diaphragm.^24,25

Post-surgery, participants show restrictive ventilator defects due to reducing chest movement and modified breathing patterns. Threshold IMT is characterized by active recruitment of diaphragm and abdominal muscles by providing constant specific pressure for strength and endurance training of inspiratory muscles. Post IMT training, it has been observed that by increasing the inspiratory muscle function, there is an improvement in lung volume and capacities and improving physical capacity.

The result of the incidence of PPC atelectasis was found clinically and statistically significant. PPC pneumonia was found clinically significant, favoring the intervention group. IMT helps to achieve higher MIP pre-operatively and helps to retain higher MIP, as compared to control, postoperatively as well, by restoring pulmonary function rapidly. Filipa Kendall et al. suggest that IMT provides a better result as it helps to maintain strength and endurance postoperatively and prevents the decline of MIP in the early postoperative period and may reduce the occurrence of PPC.¹¹

Postoperative respiratory muscle dysfunction reduces vital capacity, tidal volume, and total lung capacity, eventually leading to a reduction in FRC and causing atelectasis. According to Kulkarni et al., post IMT training participants’ ability to overcome elastic load to inhalation improved and helped in maintaining baseline level vital capacity. The author suggests that the maintenance of vital capacity improves cough efficacy and reduces changes to PPC. Similarly, Casali et al. reported that IMT was associated with early and faster recovery of FEV1, Peak Expiratory Force (PEF), and forced expiratory flow 25-75 (FEF25-75). Improved respiratory muscle strength permits larger lung volumes and provides an improvement in expiratory flow volumes.¹⁸

The length of hospital stay was neither clinically nor statistically significant. The incidence of PPC may increase the length of hospital stay. However, there are other reasons than PPCs such as pain, systemic complications, or wound dehiscence, which further affects the course of postoperative management effectively.

Functional capacity was measured using a 6MWD, which showed results favoring the intervention group, pre-operatively as well as postoperatively. A recent study done by Keeratichananont W. et al. reported that pre-operative 6MWD less than 325 m had a sensitivity of 77% and specificity of 100% to predict a high risk of PPC. However, only one study reported the use of 6MWD as an assessment of functional capacity. Similarly, a study done by Cargnin et al. showed that post-IMT there is a positive linear association between lung function and functional capacity due to increase inspiratory capacity which eventually leads to higher tolerance to fatigability and improve functional capacity.^26,27 This concludes that 6MWD can be used as an alternative predictor of PPCs.

Most of the systematic review and primary RCTs focused on preoperative IMT training, only one study (Casali et al.) Focused on postoperative IMT training from post-operative day (POD)-2 to POD-30. Studies on preoperative IMT training show a positive effect on the reduction of PPC and prevent significant changes in MIP postoperatively. However, preoperative IMT training suggests elective abdominal surgery. Thus, more studies are required, which concentrate on postoperative IMT to provide better information regarding its effect on emergency surgeries. The primary RCTs included in the systematic review had a smaller sample size, thus providing a larger confidence interval among studies affecting pooled data analysis.

The population among studies varied according to their age, gender, and body mass index (BMI). Studies on elderly participants,^3,17 obese participants,^2,14 and obese female participants⁷ provide a broader spectrum to focus, and its effect on pooled data. Llorens et al. and Barbalho-Moulim et al. suggested that obese participants develop an increased risk of hypoxemia postoperatively because of altered body mechanics such as fat deposition over the abdominal region, abdominal viscera affecting descent of the diaphragm, and compression over the chest wall. This compression results in excessive strain to the diaphragm and causes mechanical disadvantage to the muscle and affects effective training.^7,14 Dronkers et al. (2008) had a study population with age group younger in the control group (CG) as compared to the intervention group (IG) (mean (SD) of CG VS IG 59 (6) vs. 70 (6), respectively). The physiological changes that occur with age and the effect of surgery, cumulatively, might affect data analysis.³

Abdominal surgery involves a large variety of surgical procedures. Different types of surgery, based on the type of incision, i.e., open abdominal or laparoscopic surgery, area of the incision, length of incision, and the number of organs affected, helps to acknowledge the level of severity on the diaphragm and intercostal muscles and eventually to affect the biomechanics of respiration. The review had a heterogeneous group of upper and lower abdominal surgical procedures producing different levels of impairment on muscles of respiration. Kulkarni et al. focused on colorectal, gastrointestinal, vascular, and urological surgery, Llorens et al., on laparoscopic bariatric surgery, Barbalho-Moulim et al. and Casali et al. on bariatric surgery, Dronkers et al. (2008) on abdominal aortic aneurysm surgery, Dronkers et al. (2010) on elective abdominal oncological colon surgery and Soares et al. on surgery of esophagus, stomach, and biliary tract.^{1–3,7,14,17,18} Thus, variation in the type of surgery may have a varied effect on lung function and capacity.

The review involved a different type of surgical procedure, varied type of population, and lack of proper guidelines on IMT for upper and lower abdominal surgery. The starting load, maximal load, and dosage were different among studies. However, the maximum number of studies had starting load in the range of 20-30% of their MIP, pre-operatively,^1,3,7,14,18 and Dronkers et al. (2010) had 10-60% of MIP as their starting load. The increment of the load depends upon participants' tolerance subjectively on Borg rating of perceived exertion (RPE). In most of the preoperative IMT studies, the duration of training is 15 minutes per day,^1,3,7,17 Kulkarni et al.¹⁸ had two sessions of 15 minutes per day, and Llorens et al.¹⁴ had two sessions of 10 minutes.

In the only study on postoperative IMT, Casali et al. had two sessions of 20 minutes and 40% of MIP as their starting load from discharge to POD-30 for 30 minutes a day.² Although the studies provided information regarding the starting load and duration of the training, authors of primary RCT failed to report on the number of breathing cycles, respiratory flow and pattern, and rest interval between or within each set. Subjective increment based on RPE was adopted by most of the therapists. However, the chances of participants achieving a maximal level of load according to their capacity are debatable. Fear of eliciting pain, fatigue, and low quality of adherence are some of the factors affecting proper increment.

The ideal respiratory maneuver should include alveolar inflating pressure, time for alveolar inflation, and inflating volume.²⁸ Thus, the lack of knowledge on parameters such as inspiratory breathing pattern, volume near vital capacity or tidal volume, number of breaths per set, required flow, perioperative use, and progression of the procedure i.e., increment in frequency or dosage or both hinder various ideas about the methodological aspects of training and its effect on results and identify best effective IMT protocol.²⁹ Also, supervision played a significant role. Studies with increment strictly imposed by the therapist and supervised had a longer duration of the training, higher progressive loading, and adhered to the given protocol, which indicates that such groups had a higher final maximal load and greater chance to produce better results.

Conclusion

Inspiratory muscle training proves to be a beneficial intervention in improving MIP in patients undergoing abdominal surgery. Improvement in MIP has a positive association in reducing PPCs and improving lung function and capacity. Most of the systematic review included in this review agreed on the intervention of 2 weeks before surgery for 15 minutes can bring effective and positive outcomes in a wide range of the high-risk population. However, factors concerning breathing cycles, respiratory flow, and rest interval should be observed for better management post-operatively.

Author contributions

Conceptualization: Sampath Kumar Amaravadi, Khyati Shah, Stephen Samuel.

Data curation: Sampath Kumar Amaravadi, Khyati Shah.

Methodology: Sampath Kumar Amaravadi, Khyati Shah, Stephen Samuel, Ravi Shankar.

Resources: Sampath Kumar Amaravadi, Khyati Shah.

Writing – original draft: Sampath Kumar Amaravadi, Khyati Shah, Stephen Samuel, Ravi Shankar.

Writing – review & editing: Sampath Kumar Amaravadi, Khyati Shah, Stephen Samuel.

Formal analysis: Ravi Shankar

Data availability