The Roles of Lumbar load thresholds in lifetime cumulative lifting exposure to predict disk protrusion in Asian

Background: The purpose of this study was to determine whether if a specific threshold value exists in each lifting load, the accumulation above which best predicts lumbar disk protrusion, or on the other hand, all lifting load should be accumulated. Methods: This was a retrospective study. Subjects with various lifetime lifting exposures were recruited. Disk protrusion was determined by magnetic resonance imaging. Lifetime cumulative lifting load was the sum of time-weighed lumbar load for each job using a biomechanical software system. For accumulation above different thresholds, predictive capabilities for disk protrusion were compared using four statistical methods. Results: A total of 252 men and 301 women were included in the final analysis. For men, 3000 Newton for each lifting task was the optimal threshold value for predicting L4-S1 disk protrusion, whereas for women, 2800 Newton was optimal. Our findings suggested that when considering lifetime exposure, including all lifting loads without defining a minimal exposure limit might not be the optimal method for predicting disk protrusion. Conclusions: The NIOSH 3400 Newton recommended limits do not appear to be optimal threshold for preventing disk protrusion. Different lifting thresholds might be applied to men and women in the workplace for safety.


However, lifting objects with various weights is inevitable in everyday work and life.
A crucial question is whether a specific threshold value exists in each lifting load, the accumulation above which best predicts lumbar disk protrusion, or on the other hand, all lifting load should be accumulated.
A review of the literature revealed several recommended lifting thresholds, although most of them were used in the prevention of low back injury [9][10][11][12][13][14][15][16]. For example, the National Institute for Occupational Safety and Health (NIOSH) of the United States suggested that if spinal compression exceeds approximately 3400 N (Newton), workers would be at an increased risk of low back injury [17].
Nevertheless, those recommended lifting limits might not be practicable for calculating the cumulative effects for several reasons. First, they were examined for a single spontaneous lifting and the career-long effects of repeated lifting were not considered. Second, most of them were proposed for preventing LBP, not for to disk protrusion. Third, the safe manual lifting threshold value of 3400N recommended by NIOSH doesn't appear to be optimal as currently, more than 50% of work-related low back injuries are attributed to manual lifting tasks [18]. Fourth, uniform lifting limits are not generalizable across ethnicity and sex. Accordingly, this study was conducted to determine the optimal lifting threshold per lift for calculating the lifetime cumulative load in order to prevent disk protrusion in Asian, and to determine whether the threshold value differs between men and women.

Study Population
This was a retrospective study. The protocol and consent forms of the study were reviewed and approved by the National Taiwan University Hospital Research Ethics Committee (NTUH-REC No.:200805047R). Recruitment of the participants, measurements of the work exposure, and imaging studies of the lumbar spines were detailed elsewhere [8]. To obtain a broad spectrum of lifting exposures, the participants were recruited from 2 populations: (1) 263 walk-in clinic patients and (2) 452 workers who carry heavy loads. Patients visited the Internal Medicine Clinic of National Taiwan University Hospital and diagnosed with upper respiratory infections (URI), mostly the common cold, were recruited as the background population. The group that carried heavy loads were workers from one fruit and vegetable wholesale market. Lifting is a daily routine task for these workers. During recruitment, the market workers and the walk-in patients were not informed of the hypothesis of the study. They were invited to participate in an investigation regarding spine and bone disorders. The inclusion criteria were between 20 and 65 years old and at least 6 months of working experience. Participants diagnosed with several health conditions described previously were excluded [8]. We combined these 2 populations to examine the effects of lifting on disk protrusion. Before participating in the study, all workers and patients received written and oral information regarding the study procedures and potential adverse effects, and signed informed and published consent forms. Of these eligible 715 subjects, 162 were excluded from this study for the following reasons: 84 people experienced cancer, 27 people had major back trauma, 18 people had compression fractures, 16 people had psychiatric conditions, 13 people had spinal tumors, and 4 people had inflammatory spondylopathy.

Data Collection
Each participant was asked to complete a questionnaire and to obtain magnetic resonance imaging (MRI) of the lumbar spine. A detailed structured interview was implemented to the participants for assessing the relevant work tasks in each job held since they entered the workforce. The occupational history included job titles, tenures, body weights at each job, descriptions of tasks, carry load, lifting frequency and duration, working hours per day and working days per week. The participants were encouraged to recall their body weights during the period of each job. When the job period was longer than 5 years, the average body weight during this job period was used.

Estimation of Lumbar Disk Compression Load
The method of lumbar disk compression load estimation has been published previously [8]. Regarding the estimation of lifetime exposure, the participants recalled all of the jobs held after completing schooling, and the weight, frequency, and duration of each task. The participants performed a typical material handling task to simulate the positions and weights encountered at each job. Lifting activity was divided into a sequence of static postures, including the initial lift-up, transferring, and unloading postures, and each posture was analyzed. The initial position of the weight lifting task was defined as the lift-up posture, the final position was defined as the unloading posture, and the action of transferring material while walking was defined as the transferring posture. Although the initial and final positions of lifting may have varied during a typical day of materials handling on the job, the selected typical tasks, including the simulated positions and weights, were used to calculate the compression load to represent the job. The compression load on the disk during lifting was estimated using the 3D Static Strength Prediction Program (3DSSPP, University of Michigan, Michigan) software system [19,20]. Anthropometric data such as sex, height, body weight, carried weight, and working posture photograph of each participant were input into the system to predict lumbar load. To evaluate the intrarater and interrater reliability of lumbar load estimation by 3DSSPP, photographs of the simulated work conditions of the 60 study participants were repeatedly evaluated in 2 rounds, with the second round of evaluation was conducted 4 weeks after the first round.

Definition of Threshold in This Study
The threshold value in this study was defined as lumbar load per lift and above this proposed value was considered as contributed to disk protrusion over an entire career life, and was included in the lifetime cumulative calculation. In other words, the calculation neglected all exposures with a lumbar load below the threshold. The proposed threshold values were set at zero Newton (N), and at 100N increments from 2000 to 4000N.

Calculation of Lifetime Cumulative Lifting Exposures on the Lumbar Disk
The calculation method of lifetime cumulative lifting exposures on the lumbar disk was modified from the Mainz-Dortmund dose model (MDD), which is based on overproportional weighting of the lumbar disc compression force relative to the corresponding duration of lifting, and was applied by several studies [5,6,7,8]. where F represents the lifting load (Newton) on the lumbar disk and t represents time (seconds).
An example of the calculation of the sum of lifting exposures is given as below: One male worker with 170 cm body height and 75 kg body weight reported that he had carried object 1 (weighting 10kg, lift up for 1 second, walking for 30 seconds, and unload for 1 seconds), 100 times a day; and object 2 (weighting 20kg, lift up for 1.5 second, walking for 10 seconds, and unload for 1.5 seconds), 50 times a day, working 220 days a year. The total work tenure had been 20 years. zero. Therefore, the reliability of the transporting time and unloading time was not examined. In addition, we determined that pushing or pulling is not a common task for the majority of fruit market workers because they typically drive an electric pedicab to transfer fruit boxes. Therefore, the lumbar load of pushing and pulling was not assessed.
Each intervertebral disk at L4-L5 to L5-S1 was evaluated for disk bulging, protrusion, extrusion, and sequestration using MRI. All MRI examinations were conducted at the National Taiwan University Hospital. MRI equipment and protocol, definition of disk condition, the evaluation of intrarater reliability regarding the presence or absence of protrusion were described previously [8]. Two radiologist were responsible for the image interpretation and were blinded for the lifting exposure status of the participants.

Data Analysis
The reproducibility of the calculation of the lifting load and lifting measurements was analyzed using SPSS version 16.0 for Windows (SPSS Inc, Chicago, Illinois) to compute intraclass correlation coefficients (ICCs). Kappa was used to assess the intrarater reliability of disk protrusion on MRI. Logistic regression analysis using JMP 5.0 (SAS Institute Inc, Cary, North Carolina) was applied to identify the association between lifetime cumulative lifting load and disk protrusion at either of the lower disk levels, namely, L4-L5 and L5-S1 disk. Each variable was examined to determine the influence on the disk protrusion and was considered to be a potential confounder as having a statistically significant association (p<0.05). Thus, the logistic regression was adjusted for age, BMI, and history of smoking. Odds ratio (OR) and 95 % confidence intervals were calculated by logistic regression analysis.
To determine the best threshold of lifting load, four statistical values were used to compare outcome (L4-S1disk protrusion) to lifetime cumulative load while different threshold values was applied, namely, (1)  for L4-S1disk protrusion was good with 0.850. Figure 1 and Figure 2 showed the predictive abilities of lifetime liftload with different threshold to L4-S1 disk protrusion in male and female participants, respectively.
The detail information were shown in Supplemental Table 1 and Supplemental Table   2. With any of the threshold values, the lifetime cumulative lifting load was significantly associated with L4-S1 disk protrusion. Among the male participants, the maximal AUC (0.686) was found while lifting load of 3000N was used as threshold (Figure 1(a) and Supplemental Table 1). The R 2 statistic (0.0797), AIC (-390.3), and BIC (-387.8) were also optimal when 3000N ( Figure 1(b), (c), (d) and Supplemental Table 1). The ROC curves of 3400N, 3000N, and 0N models in male were showed in Figure 3. Among the female participants, the maximal AUC (0.615) was found while lifting load of both 2800N and 3000N were used as threshold (Figure 2(a) and Supplemental Table 2). The R 2 statistic (0.0321), AIC (-501.1), and BIC (-498.6) were also optimal when 2800N ( Figure 2(b), (c), (d) and Supplemental Table 2). The ROC curves of 3400N, 2800N, and 0N models in female were showed in Figure 4. as compared to those using 0 N, 3400 N, and 4000 N ( Table 3).

Discussion
This study found optimal threshold values of load per lift which allow for best prediction of disk protrusion by cumulating exposures. Cumulative lifting load provided best prediction for L4-S1 disk protrusion when the threshold value was set at 3000N for male, and 2800N for female participants. Furthermore, the study was conducted among Asian population and the results might be more applicable in Asia because uniform lifting limits might not be generalizable across ethnicity and sex.
One of the recommended lifting limits, the NIOSH 3400N, is widely used by ergonomists as well as health and safety practitioners [12,21]. It is based on the studies by Evans and Lisner [22] , and Sonoda [23]. These studies show that microfractures of the vertebral cartilage endplates started to happen among cadavers of subjects 60 or more years old, when applying average axial loads of 3400 N. The major limitations of NIOSH 3400 N are that the results are based on cadaver studies and immediate effects on the vertebral cartilage end plate, but not for cumulative effects. Our study is important complement to the NIOSH 3400 N criteria and provides recommendations to long-term lifting limits.
To our best knowledge, only few studies examined dose-effect relationship between lifetime cumulative lifting load and disk protrusion. Seilder [5] conducted a thorough investigation of all past lifting load for the participants. They showed that male workers who had been exposed to 5 -21.5 × 10 6 Nh lifetime lifting load exhibited a 1.7-fold risk of disk protrusion comparing to those exposed to 0 -<5 × 10 6 Nh, suggesting cumulative effects of all lifting loads, without threshold, on disk protrusion [5][6][7]. In a later study [8], participants who had been exposed to high lifting load (≥8.9 × 10 6 Nh) exhibited an OR of 2.2 for disk protrusion, as compared to those exposed to a low lifting load (<4.9 × 10 5 Nh). This latter study also assumed no per lift threshold for cumulated load. In this current study, a concept of threshold per lift load was tested, and the result showed that applying certain thresholds provided better prediction in calculating lifetime cumulative load than not. Our findings suggested that when calculating lifetime exposure, including all lifting loads without defining a minimal exposure limit might not be the optimal method for predicting disk protrusion. Besides, the investigation was carried out among Asian population, therefore, the findings of this study might be limited the generalizability to other population.
Considering disk protrusion as the health outcome, male participants seemed to tolerate higher lumbar load than females in a per lift load basis. It is possible that men generally had larger cross-sectional areas in lower lumbar disks than women [24]. The larger areas allowed men to endure higher compression load. Thus, the results of this investigation suggest that different lifting thresholds should be applied to men and women in the workplace for safety.
The strengths of our study were the detail investigation of the lifetime lifting exposure, outcome assessment by using MRI, and applying the concept of threshold per lift to lifetime cumulative lifting load calculation. However, there were several limitations in this study. First, the AUC, R 2 , AIC, and BIC statistics are the summary scores of prediction using each threshold value. They did not allow for statistical comparisons among the proposed threshold values. Second, we relied on the participants' memories regarding their occupational history and relevant work tasks from several decades ago. Although the repeatability of current job tasks was examined and found to be satisfactory, the reliability of the information pertaining to previous jobs was difficult to determine. In order to enhance reliability, a structured interview was executed to provide the participants with adequate time for recalling the work details of their previous jobs. The trained interviewers used life milestones to help the participants recollect the necessary details, and captured the working simulation photos by following a standard procedure. Studies have indicated that self-reported data did not provide satisfactory validity [25]. However, Pope showed the accuracy of self-reported manual material handling activities and presented satisfactorily accurate results regarding frequency, duration, and amplitude [26]. Direct measurements obtained using work or laboratory simulations yield the most accurate information; however, it is impractical by using such methods in retrospective studies involving relatively large sample sizes.
There is another limitation that we did not consider the lifting load in leisure and home activities. In Kelsey's study [27], it found that there was no association between acute herniation and participating in baseball, softball, jogging, golf, bowling, tennis, swimming or bicycling. Although the other study [28] showed that leisure activities involved gardening, snow clearing, or building of a summer cottage were associated with greater disc degeneration in the upper lumbar levels, in Taiwan snowing and building a summer cottage are rarely happened. Therefore, the risk factor of leisure and home activities were not thoroughly inquired in our study.
This might have potentially caused misclassification and error in the cumulative lifting load estimates. The R 2 values in male were ranged from 0.0546 to 0.0797, in female were ranged from 0.0143 to 0.0321, those were very low in the study. The result was consistent with Battie's finding [28]. In the L4-5 and L5S1 region of this study, physical loading only explained 2 % of the variance in disc degeneration.
With the addition of age to the model increased the explained variability in disc from 2 % to 9 %, and to 43% with the addition of familial aggregation. Thus, the genetic factors had great amount influence in disc degeneration. It might be the reasons that explanatory power of lifting loading on disc protrusion was small.
Disk protrusion has been reported to be associated with manual handling activity [1][2][3][4][5][6][7][8], which may lead to low back pain. There are also many other potential risk factors may cause disk herniation. However, in Jensen's study [29], they found that 64% of asymptomatic individuals had lumbar disk abnormalities (disk bulge, protrusion, or extrusion). Meanwhile, the cause of low back pain is also multifactorial such as disk degeneration, disk herniation, ligament/tendon damage, muscle strains, manual handling activities, vibration, smoking, and psychological factors. Above these reasons, this is a limitation that we used lifting load as the only measurement to determine the development of disk protrusion even we had adjusted other potential risk factors including age, BMI, smoking status. Although disk herniation is often seen in asymptomatic population, setting a lifting threshold in workplace is important to prevent worker from low back pain. It could be a useful tool for risk assessment and for prevention purpose to reduce the injuries and medical cost.
In the previous study [8], Therefore, liftloads below the threshold were neglected in the cumulative calculation and lead to an zero N-hr as the lifetime cumulative exposure. Thus, those participants were finally enrolled into the low lifting exposure group with zero N-hr. Even they were not really experienced zero N-hr at work. In the establishment of the thresholds, this approach has to eliminate some extent amount of cumulative loading, and it may cause underestimation when interpreting the results.
The intervertebral disk degeneration has a complex multifactorial etiology, and also results in a multitude of disk conditions such as disk herniation. Various risk factors have been reported to be associated with disk protrusion, including ageing, physical loading, vibration, genetic factor and even the interaction of factors above [30].
Kumar [31] reported cumulative load or lifetime exposure to biomechanical loads as an important risk factor for low back pain. In order to determine the lifetime cumulative exposure, we investigated the lumbar compression force the workers exposed to(force), time of exposure (duration), and the repetitive task exposure (frequency). The lifetime cumulative exposure calculation method utilized in this study by multiplying Newtons by time has been used previously by other studies [5][6][7][8]. One question was raised that the injury accrued by short duration with high loading might be equivalent to longer duration with low loading by using multiplying Newton by time approach. However, it appears to be the truth that exposure to high magnitude loads causes greater damage to tissues than low magnitude loads. That is one reason we utilized threshold into the multiplying Newton by time approach to confront the long duration with low magnitude loads cases. It is the limitation that this approach may not be the most optimal method of assessing the effects of cumulative loading for musculoskeletal tissues. When exposed to repetitive stresses, musculoskeletal tissues were experienced fatigue failure process of cumulative damage development. The theory of fatigue failure in musculoskeletal tissues may be an important etiological mechanism in the development of disk degeneration and should be considered. In Gallagher's study [32]

Consent for Publication
All subjects signed consent forms for publication before participating in the study.

Availability of data and material
The dataset used for analysis during the current study are available from the corresponding author on reasonable request.

Competing interests
The authors declare that they have no competing interests.

Funding
This study was supported by a grant from the Taiwan National Health Research Institute (NHRI-98~100A1-PDCO-0108111). The funding agency did not have any involvement in data collection, data analysis, and data interpretation. BMI, body mass index; SD, standard deviation *Yes means ever having regular exercise for 30 minutes or longer each session, at least one session per week, minimum duration of 3 months, from age of 12 years to the present time.  Figure 1 (a). The AUC statistic distrubution of L4-S1 disc protrusion with proposed threshold values in Figure 2 (a). The AUC statistic distrubution of L4-S1 disc protrusion with proposed threshold values in Figure 3 Receiver-operating characteristic curves for the prediction of L4-S1 disc protrusion in male p