Indurometer vs. Tonometer: Is the Indurometer Currently Able to Replace and Improve Upon the Tonometer?

Abstract

Background:

The Indurometer is a tool designed by the Flinders Biomedical Engineering Department to replace the Tissue Tonometer. It measures the resistance to an applied force to quantify the amount of fibrosis present within the epifascial compartment of tissue. The aim of the study was to compare the current model of the Indurometer with the Tonometer to determine the level of variability and repeatability between the two devices and how the variability differs when compared to an individual's ISL stage.

Methods and Results:

Data were gathered on a total of 180 participants with unilateral arm lymphedema as part of an international multicenter trial. For each participant three repeat measurements were obtained with the Indurometer and Tonometer at the anterior mid forearm and anterior mid upper arm. The Indurometer gave lower measurement values than the Tonometer. The Tonometer was found to be less variable than the Indurometer when measurements were taken from the anterior mid upper arm and the anterior mid forearm site. The Tonometer values were significantly less variable than the Indurometer values in ISL stages 1 and 2. No significant variability was found in stage 3.

Conclusion:

The Indurometer is easier to use as compared to the Tonometer. Modification of the Indurometer needs to take place in order to improve its variability before it can be considered as a replacement for the Tonometer in the assessment of lymphedema. The lack of understanding of the ISL classification system is a significant issue.

Introduction

The Tonometer has been used for more than 30 years to measure changes within tissue affected by lymphedema.¹ It is a mechanical device that measures the resistance of the tissue to compression above the deep fascia. Research shows that tonometry can indicate the degree of fibrosis and the impact of treatment on tissue affected by lymphedema.^2–4 Despite these abilities, the Tonometer has a number of limitations: (i) a dial that is difficult to read;⁵ (ii) a dial that must be read while the device is held on the patient, which may be challenging at certain measurement sites;⁶ (iii) only functioning when used in a vertical position;⁶ (iv) being top heavy and thus forcing the operator to balance the tool on the measurement site; (v) requiring user training;⁷ (vi) requiring the user to record the reading at a fixed time after the 200 g mass is applied to ensure accuracy, especially when pitting is present.⁷

The Indurometer is under development by the Flinders Biomedical Engineering Department and is being designed to replace the Tonometer and overcome these limitations.⁵ The Indurometer uses a 200 g mass and a displacement gauge to objectively measure tissue induration.^5,8 The Indurometer is an electro-mechanical device that improves upon the Tonometer design by: (i) having 0.01 mm resolution; (ii) a digital screen that stores the results until cleared by the operator; (iii) recording the readings at the instant in time when 200 g mass is applied; (iv) using a constant force spring that allows it to be used in nonvertical positions; (v) having Bluetooth communication capability.⁵

Like the tonometer, the Indurometer does not provide an absolute measure, but rather provides a comparative measure of the limb's resistance to indentation. This allows for comparison between a patient's affected and unaffected limb or changes within a patient's limb over time.⁸ Tissue induration measurement is important in lymphedema because it is one factor that helps to determine the International Society of Lymphedema (ISL) stage of the individuals affected limb that is based on the firmness of the limb and the outcome after elevation.⁹ The criterion for each stage is presented in Table 1. Higher resistance to indentation indicates a higher amount of fibrosis within the tissue and thus more advanced lymphedema within the tissue. Determining the stage of lymphedema that a patient has is the most reliable and objective method for classifying patients for proper treatment and management.¹⁰

Table 1.

Criteria for ISL Stages ⁸

Stage	Criteria
0	Impaired lymph transport with no evident swelling or fluid accumulation
I	Swelling that subsides with 24 hour limb elevation with no evidence of dermal fibrosis and has pitting present
II	Dermal fibrosis which makes the limb firmer allowing for less pitting and cannot be resolved with 24 hour limb elevation
III	Absence of pitting and the presence of skin changes such as fat deposits and warty overgrowths

The study aims to compare the variability between the values obtained by the current model of the Indurometer with those of the Tonometer at the anterior mid forearm and the anterior mid upper arm. A comparison between the variability of the values was also conducted after grouping the participants into ISL stages to determine whether the device variability is affected.

Materials and Methods

Ethics approval for this study was granted by the Southern Adelaide Health Service (Flinders University) Human Research Ethics Committee (application number: 317/10).

An international multicenter cross-sectional study was conducted with participates from six centers, resulting in data collection on a total of 180 participants with secondary unilateral arm lymphedema. Seven operators were involved in obtaining measurements on the participants. The following inclusion and exclusion criteria were set to recruit the participants:

Inclusion criteria

i) Have clinical defined unilateral lymphedema

ii) Report their general health as being satisfactory

iii) Give informed written consent

Exclusion criteria

i. Currently on diuretics

ii. Consumption of alcohol or caffeinated beverages within the 6 hours prior to the measurements

iii. Undertaken excessive exercise within 2 hours prior to the measurements

iv. Reported a fever of more than 38 degrees Celsius

v. Were currently in the fourth week of the menstrual cycle

vi. Were pregnant or breastfeeding

Participants with compression garments were instructed to remove the garment only during the measurements in the clinic, and all of the measurements were taken within 30 min of garment removal. For each subject three repeat measures were obtained with the Indurometer and the Tonometer on the anterior mid forearm and anterior mid upper arm on both the left and right sides of the body. For the measurements, the participants were required to lie on their back and relax their muscles for 5 min prior to the first measurement. The measurements were not taken consecutively at each site. Instead, they were taken sequentially around the sites until all three measurements were completed. This strategy was invoked to allow the tissue to recover from the prior measurement. Each site was marked with a water-based marker to ensure that the same location on the arm was measured for each of the three readings. The Indurometer measurements were taken first, followed by the Tonometer measurements. Each operator was provided with specific instructions on how to use the two devices. In addition to the compression measurements, the operator recorded the following information for each participant:

i. Age

ii. Gender

iii. Height

iv. Weight

v. Arm dominance

vi. Affected arm

vii. ISL stage

Using this data the BMI of each participant was calculated and they were categorised according to the World Health Organization classification system.¹¹

Examination of the results showed some inconsistencies within the Tonometer values. These were reported for two of the measurement sites. These were linked to the design of the Tonometer that only allows a measure up to 10 (equivalent to 1 cm depression) before rotating back to the start position (0 reading) on the dial. If the indenter continues to extend beyond that point, the dial beings to rotate around the face of the measurement panel once again. In some cases the operators would record a value of 10+, recognizing that the measurement was greater than 10. In some cases the operator did not recognize the measurement was greater than 10 and would record values as 0.8 when the true value was 10.8. The presence of values such as these would significantly skew the statistical analyses. In the collected data, 69/180 of the participants anterior chest measurements and 16/180 anterior mid upper arm measurements were found to have at least one of these inconsistencies. Examples of the two types of inconsistencies that were observed and an illustration of how these values were adjusted to remove such error from the results can be seen in Table 2.

Table 2.

Inconsistencies Adjusted for Within the Tonometer Results

	Inconsistencies
Scenario	Measurement 1		Measurement 2		Measurement 3
	Recorded Value	Value Used In Analysis	Recorded Value	Actual Value	Recorded Value	Actual Value
Scenario 1	9.31	9.31	0.8	10.8	9.9	9.9
Scenario 2	10+	removed	10+	removed	10+	removed

The data from each center were collected, checked, and edited before being analyzed in STATA version 12.0¹² and R software version 3.0.2.¹³ Descriptive statistics were expressed as mean and standard deviation for discrete and continuous measures, whereas percentages were reported for categorical variables. Median and Interquartile range (IQR) were also reported for skewed data. The normality assumption was visually checked by frequency histogram normal and Q-Q plot for continuous measurements and a Shapiro test was conducted to test the normality assumption.

To determine the repeatability measurements of both tonometer and Indurometer, the coefficient of variation (COV) for each device, for each location of control and affected arms was calculated using \documentclass{aastex}\usepackage{amsbsy}\usepackage{amsfonts}\usepackage{amssymb}\usepackage{bm}\usepackage{mathrsfs}\usepackage{pifont}\usepackage{stmaryrd}\usepackage{textcomp}\usepackage{portland, xspace}\usepackage{amsmath, amsxtra}\pagestyle{empty}\DeclareMathSizes{10}{9}{7}{6}\begin{document} \begin{align*} & COV = ({within \ subject \ standard \ deviation / Total \ mean}) \\ & \qquad \quad \times 100 .\end{align*} \end{document}

The modified Levene's test was used to test the differences of coefficient of variation (COV) between indurometer and tonometer devices for each location of affected and control arms.¹⁴ A 95% CI was also constructed for COV.¹⁵ The modified Levene's test was performed in R platform 3.0.2 with ci.cv command from MBESS package.^16,17

Results

The median age of the participants was 61 years (IQR=52–69 years) and 128 (71%) of the participants were found to have a BMI in the overweight or obese category. Of the 180 participants, 178 (99%) were female due to the high amount of unilateral arm lymphedema development after breast cancer treatment. The demographics of the participants can be seen in Table 3.

Table 3.

Characteristics of 180 Participants

Characteristics	Value
Age, median (interquartile range)	61.0 (52.5–69.0)
Gender, number (%)
Male	2 (1.1)
Female	178 (98.9)
BMI, median (interquartile range)	28.1 (24.3–33.4)
BMI, number (%)
Underweight (<18.5 kg/m2)	3 (1.7)
Normal weight (≥18.5 to 24.9 kg/m2)	49 (27.2)
Overweight (≥25.0 to 29.9 kg/m2)	57 (31.7)
Obesity (BMI ≥30 kg/m2)	71 (39.4)
Dominant arm, number (%)
Left	20 (11.1)
Right	148 (82.2)
Unknown	12 (6.7)
Lymphedema arm, number (%)
Left	95 (52.8)
Right	79 (43.9)
Left/Right	6 (3.4)

Figure 1 shows a comparison between the Tonometer and Indurometer values. The Tonometer values were found to be higher than those from the Indurometer at both measurement sites. Past studies have shown that the longer the Tonometer weight is applied to the surface of the limb, the further the plunger will sink into the tissue because fluid shifts away from the applied mass.⁷ The Indurometer measurement is taken the instant the 200 g of force is applied to the tissue, whereas the Tonometer requires the operator to read the value, hence the value from the Tonometer is not read the instant the force is applied, but rather after a variable amount of time after the application. As a result, the smaller number obtained using the Indurometer is likely due to the shorter amount of time that passes before the value is recorded which allows for less fluid shift to occur.

FIG. 1.

Box plots of the Indurometer and Tonometer values obtained at each of the two sites for the control and affected arms. Three measurements were obtained at each site and each of these measurements is represented by its own bar.

The variability based on the standard deviation of the values obtained from each device at both sites can be seen in Figure 2. In the anterior mid forearm, the Indurometer values from both the affected and control arms appear to have a lower variability then the values from the Tonometer. In the anterior mid upper arm, the Indurometer values appear to have a higher variability than the Tonometer values.

FIG. 2.

Box plots of the variability between the three readings obtained using the Indurometer and the Tonometer at each site for both the control and the affected arms using standard deviation.

However, the results in Table 4 reveal that the COV was significantly lower in the Tonometer values compared to the Indurometer at both sites on the lymphedema affected arms and at the anterior mid upper arm site on the control arms of the participants. There was no significant variation between the two devices at the anterior mid forearm site in the control arms of the participants. This suggests that the values obtained from the Tonometer were less variable then those obtained from the Indurometer. These results are different from the results found in the study by Pallotta, et al., which suggested that there was a similar variability between the two devices when looking at these two sites.⁵

Table 4.

Coefficient of Variation (95% CI) Between the Three Measurements Obtained Using the Indurometer and the Tonometer at Each Site for Both Control and Affected Arms

	Indurometer	Tonometer
Arms and location	COV (95% CI)	COV (95% CI)	P value
Affected arm
Mid forearm	26.7 (24.1–30.1)	19.3 (17.5–21.7)	<0.01
Mid upper arm	32.0 (28.7–36.1)	23.0 (20.8–25.8)	<0.001
Control arm
Mid forearm	22.4 (20.3–25.2)	21.5 (19.4–24.1)	0.23
Mid upper arm	28.9 (26.0–32.6)	22.8 (20.6–25.6)	0.04

COV, coefficient of variation (%); CI, confidence interval; p values of less than 0.05 were considered statistically significant.

The variance between the induration values obtained from each device was then analysed after dividing participants into groups based on the ISL stage they were assigned. The results of this analysis can be seen in Table 5. In the stage 1 participants, the Indurometer measurements were significantly more variable then those of the Tonometer at both sites (p<0.01). In the stage 2 participants, the Indurometer measurements were also found to be significantly more variable then those of the Tonometer at the anterior mid forearm (p=0.04). All other differences in the variability were found to be insignificant. This may indicate that the Indurometer is not as reliable at measuring tissue with a greater fluid content compared to the Tonometer. It should be noted that only 9 participates were allocated as having ISL stage 0 lymphedema. As a result, little information can be gathered from this stage group.

Table 5.

Coefficient of Variation (95% CI) Between the Three Measurements Obtained Using the Indurometer and the Tonometer at Each Site for Affected Arms Across Three Stages

		Indurometer	Tonometer
Stage	Affected arms location	COV (95% CI)	COV (95% CI)	P value
Stage 0	Mid forearm	29.9 (22.9–43.1)	30.1 (23.1–43.3)	0.78
	Mid upper arm	31.2 (23.9–45.2)	28.6 (22.0–41.1)	0.72
Stage 1	Mid forearm	28.7 (24.0–35.9)	13.0 (10.9–16.1)	<0.001
	Mid upper arm	33.6 (28.0–42.3)	20.2 (17.1–25.1)	<0.01
Stage 2	Mid forearm	21.8 (18.8–26.0)	15.5 (13.4–18.5)	0.04
	Mid upper arm	31.1 (26.7–37.5)	23.3 (20.1–27.8)	0.08
Stage 3	Mid forearm	26.0 (19.1–41.0)	16.9 (12.5–26.1)	0.21
	Mid upper arm	26.1 (19.1–41.2)	19.7 (14.6–30.6)	0.29

COV, coefficient of variation (%); CI, confidence interval; p values of less than 0.05 were considered statistically significant.

These results suggest that modification of the Indurometer is required in order to improve its variability before it can replace the Tonometer in clinical practice. However, feedback from the operators suggests that the Indurometer's design is a great improvement compared to that of the Tonometer. It was reported that the Indurometer's display, buttons, size, and shape make it comfortable and easy to use. Some minor suggestions for alteration of the size and opacity of the base plate were made by one operator; however the majority stated that no changes were required. It was reported that two participants were pinched by the device upon use, thus raising an issue with its design. The Operator's Manual was reported as easy to follow and the device itself was found to be easy and intuitive to use by all of the operators.

A lack of understanding of the classification system by the healthcare professionals and the subjective nature of the method of assigning these stages to participants should also be mentioned. Many of the operators suggested that they found it difficult to determine the ISL stage of their participants. One operator indicated that they used volume measurements to assign ISL staging values to their 30 participants instead of ISL staging definitions. As a result, this operator's data, based on 30 participants, was removed from the analysis. However, it is possible that some of the other operators also allowed variables unrelated to ISL stage classification, such as limb volume, to influence their decision of what ISL stage they assigned. This raises an important issue in regards to the ability of healthcare professionals working with lymphedema patients to utilize the ISL staging system within their practice. Although determining an individual's ISL stage helps to determine the best treatment for that individual, there are no simple, clear tools available to health professionals to determine an individual's ISL stage.¹⁰

An analysis of how the biological characteristics of a subject affected the Indurometer and Tonometer values was also conducted. The results suggested that the effect of these characteristics depended on the site of measurement. For instance, on the anterior mid forearm, BMI and age significantly affected the values obtained by both devices (p<0.05), while for the anterior mid upper arm, only BMI significantly affected the results (p<0.05). Arm dominance had no significant effect on the measurements. For this reason we belief that interpreting the induration values obtained with respect to the individual's characteristics should be conducted in practice by measuring the induration of a patient's unaffected arm as well as their affected arm. This would allow the extent to which the dysfunctional lymphatic drainage is affecting their lymphedema affected arm can be established against a reasonable baseline.

Conclusion

The Indurometer was designed to increase the ease with which the operator can obtain reliable and objective measurements on tissue induration and these results show that this has been accomplished. However, further modification of the Indurometer needs to take place in order to improve its variability before it can be considered as a replacement for the Tonometer in the assessment of lymphedema. This study has highlighted the subjective nature and lack of understanding and interpretation of the ISL classification system and this is a significant issue that needs to be addressed if ISL staging is going to be used in practice to help determine the treatment plan for individual patients.

Footnotes

Acknowledgments

We would like to thank Lyndelle Barry, Joyce Bosman, Sue Gordon, Nina Renkema, Carmelita Rifkin, Sharon Tilley, Michael Waters, and Tim Wonders for helping us with the data collecting for this study.

Author Disclosure Statement

No competing financial interests exist.

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