1. Surgical localisation

1.3. PICO table

For full details see the review protocol in appendix A.

Table 1

PICO characteristics of review question.

1.4. Clinical evidence

This review aimed to assess the clinical and cost effectiveness of various pre-operative and intra-operative tests to aid parathyroid surgery. These tests included both pre-operative/intra-operative localisation techniques to aid localisation of the affected gland(s), and intra-operative techniques to determine when all affected tissue has been excised and aid the decision to terminate surgery. Evidence for both of these is presented separately in the review. The latter intra-operative tests included intra-operative parathyroid hormone monitoring (IOPTH) and intra-operative frozen sections. All other index tests in the protocol were localisation techniques. Additionally, for both categories evidence was sought from both test-and-treat RCT studies and from diagnostic accuracy studies. Therefore, the clinical evidence in this review was organised as follows:

• Imaging localisation tests – evidence from test-and-treat RCTs
• Imaging localisation tests – evidence from diagnostic accuracy studies
• Intra-operative tests (IOPTH and frozen section) – evidence from test-and-treat RCTs
• Intra-operative tests (IOPTH and frozen section) – evidence from diagnostic accuracy studies

1.4.1. Localisation and intra-operative techniques

1.4.1.1. Imaging localisation tests – diagnostic accuracy methods

The following adapted methods were used to assess the accuracy of the localisation index tests. Localisation index tests included ultrasound (US), sestamibi scanning (including planar, subtraction, SPECT or SPECT/CT), MRI, CT, 4D-CT, venous sampling and methylene blue. All of these index tests are used pre-operatively with the exception of methylene blue which is used intra-operatively. An adapted diagnostic accuracy method was used for this part of the review, as described below.

A standard diagnostic accuracy 2×2 table could not be used for this review, as there is more than 1 possible outcome for each person (unlike a standard diagnostic accuracy study where each person either has the disease or not). As each person has more than 1 parathyroid gland, there is more than 1 possible outcome for both the index test and the reference standard (i.e. imaging could predict 1 or more possible affected glands, and the final outcome could be a single adenoma, more than 1 adenoma, or hyperplasia).

Therefore, to overcome this problem, the following 2×2 table was devised at protocol stage for this review. This method was chosen as it allows the accuracy of the tests to be determined according to whether the imaging test would have predicted the correct surgical approach in each person (focused surgery or exploratory surgery). It was agreed that this approach would give the most relevant information for determining the most clinically effective localisation test.

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		By the reference standard there was a single adenoma
		YES	NO
Index test –		True positive (correct application of focused surgery) - imaging identifies a single adenoma location correctly	False positive (either focused surgery would fail or would convert to exploratory) - Imaging shows a single adenoma but there is actually a double adenoma - Imaging shows a single adenoma but there is actually hyperplasia - single on imaging but nothing found
		False Negative - nothing on imaging so single adenoma missed (do another imaging or exploratory surgery) - Imaging incorrectly identifies the location of a single adenoma (either surgery would fail or would convert to exploratory) - multiple findings on imaging but only a single located	True Negative (correct application of exploratory surgery) - Imaging shows nothing and there are no adenomas found - Imaging correctly identifies hyperplasia - Imaging correctly identifies double adenoma - Imaging shows nothing but there is actually a double - Imaging shows nothing but there is hyperplasia - Imaging shows multiple glands but not all in hyperplasia
	TOTAL	Number of people with a single adenoma/should have focused	Number of people who should have exploratory surgery (either as no adenomas, hyperplasia or double adenomas).

If a study provided enough evidence to categorise each included participant according to the above 2×2 table (both as to the localisation of affected tissue according to the index test and the final localisation outcome from the reference standard) then it was included. For example, if a study stated that a participant had an imaging scan suggesting a single adenoma but the final outcome determined by the histology and post-operative normocalcaemia was a 4-gland hyperplasia, this person would be counted as a false positive. If it was not possible to categorise all the included participants for a given study into the above 2×2 table, then the study was excluded (for example, in people with persistent hypercalcaemia following surgery, unless the results of a further operation were provided in order to determine the final location according to the reference standard, then it would not be possible to determine whether the location of the affected tissue found on pre-operative imaging was correct or not).

The reference standard test must be the best available method to determine the actual location(s) of the affected tissue. It was agreed that the reference standard should include both histology and post-operative serum calcium levels. Histology alone was not sufficient as the reference standard, as although it can prove the presence of an adenoma, post-operative normocalcaemia is also required to prove that there was no further affected tissue remaining. Normocalcaemia in isolation is also not sufficient, unless the person was normocalcaemic after a single gland was removed. This is because, if more than 1 gland is removed, normocalcaemia could result if 1 or both of the glands were abnormal, and histology is required to determine if 1 or both were abnormal. Any studies not reporting both histology and post-operative normocalcaemia, in order to determine the actual location of abnormal tissue, were excluded.

By the above method, sensitivity and specificity would not have the same interpretation as in a standard diagnostic review. Sensitivity and specificity could be interpreted as follows:

• Sensitivity = % of people who have a single adenoma, who are correctly picked up by imaging tests (also the % of people who would get correctly applied focused surgery).
• Specificity = % of people who should get exploratory surgery (final diagnosis is >1 adenoma or hyperplasia), that do (imaging shows no adenoma, hyperplasia or double adenoma).

An index test with a low sensitivity (resulting from a high number of people in the bottom left cell) may mean that more people end up getting exploratory surgery who could have had focused surgery (if imaging shows more adenomas then there actually are), or it may mean that more people having failed surgery (if imaging shows the incorrect location of a single adenoma, although this may be picked up during the surgical procedure). An index test with a low specificity (resulting from a high number of people in the top right cell) may mean that more people would fail focused surgery and have persistent PHPT (as imaging would predict a single adenoma but they actually have >1).

Some diagnostic accuracy studies identified in the search provided accuracy data in different formats. These studies were only included in this review if it was possible to categorise all included participants in the study according to the above 2×2 table method. Some studies used a ‘per-gland’ method, assuming each person had 4 parathyroid glands and therefore determining 4 possible outcomes in the 2×2 table for each person. For example, if a person had 1 suspected adenoma located on imaging, and the reference standard confirmed a single adenoma at the same location, that person would have 1 true positive and 3 true negative results. Or, if a person had 1 suspected adenoma located on imaging but the final outcome according to the reference standard was 4-gland hyperplasia, then that person would be deemed to have 1 true positive and 3 false negative results. Another method adopted by some studies was an adapted ‘per-person’ method. If a person had all affected glands (either a single adenoma or more than 1 gland) correctly identified on imaging then they would be deemed a true positive. However, this causes problems of how to categorise people who have all their affected glands correctly identified on imaging, but the imaging also suggests further affected tissue in a location which is normal according to the reference standard. These people would be deemed to be true positives, even though relying on the imaging result alone would result in more glands being explored at surgery than was necessary.

Neither of the above methods (‘per-gland’ and ‘per-person’) were used for this review. The method used in this review was chosen as it allows the accuracy of the tests to be determined according to whether the imaging test would have predicted the correct surgical approach (focused surgery or exploratory surgery).

All clinical evidence was stratified according to whether the participants had undergone previous parathyroidectomy. Results were stratified into studies only including people having their first operation, studies only including people having re-operation, and studies with a mixed population of first operation or re-operation that could not be analysed separately. Data were available for the following tests for each population stratum:

-

1^st operation (or studies including ≤5% people with re-operation)

• US
• MIBI
• MIBI (subtraction)
• SPECT
• SPECT/CT
• MRI
• SPECT + US

-

Mixed 1^st operation and re-operation (>5% re-operation and not reported separately)

• US
• MIBI
• MRI
• CT

-

Reoperation only

• MIBI

For the localisation tests, sub selection of people based on the pre-operative imaging may introduce heterogeneity in the results, as studies using a pre-selection process will not be representative of the whole population. Therefore, sensitivity analysis was performed to stratify results into studies reporting all people (no pre-selection for the study based on imaging), studies only reporting people with a suspected single adenoma from imaging, and studies only reporting people with negative imaging. Results of this sensitivity analysis are reported in Table 13.

1.4.1.2. Intra-operative tests – diagnostic accuracy methods

The intra-operative tests of IOPTH and intra-operative frozen sections are not used to aid localisation of the affected tissue, but rather are used to determine whether all the affected tissue has been excised and whether surgery can be terminated. Therefore the method of assessing accuracy of these tests is different to the localisation tests.

The following 2×2 table was used to assess the accuracy of IOPTH and intra-operative frozen sections for predicting whether all abnormal tissue has been removed or not:

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		Reference standard
		+ve	−ve
Index test	+ve	True positive (>50%fall in PTH and all adenomas removed)	False positive (>50% fall in PTH but not all adenomas removed – person remains hypercalcaemic (up to 6 months) or requires re-op or subsequent glands resected in the same op)
	−ve	False Negative (no fall in PTH but all adenomas removed)	True Negative (no fall in PTH and not all adenomas removed – person remains hypercalcaemic (up to 6 months) or requires re-op or subsequent glands resected in the same op)
	TOTAL	Reference standard positive	Reference standard negative

Again, the reference standard was histology and post-operative serum calcium. Studies only stating the accuracy for prediction of post-operative normocalcaemia, without mention of histology, were excluded (unless all participants had normocalcaemia after removal of a single gland only). This is because, if >1 gland is removed, normocalcaemia is insufficient to determine whether 1 or both were abnormal. For example, IOPTH may not have fallen after removal of the first gland, so surgery continued and IOPTH fell after removal of the second gland. Without histology, it is not possible to classify the IOPTH result after removal of the first gland as a false negative or a true negative.

In this context:

• Sensitivity = the ability to identify people who have had all adenomas removed
• Specificity = the ability to identify people who have remaining abnormal tissue

An index test with a low sensitivity may result from a high proportion of people not having a drop in the IOPTH even when all abnormal tissue has been removed and therefore, may result in continuing to explore other glands unnecessarily if the decision to terminate surgery is based on the IOPTH alone. An index test with a low specificity may result from a high proportion of people having a drop in the IOPTH even though there is still abnormal tissue remaining and therefore, if the decision to terminate surgery is based on the IOPTH alone, the surgery would be terminated and the person would remain hypercalcaemic and require further surgery.

For IOPTH, it is possible to calculate the 2×2 table values in different ways for people who had >1 gland removed (i.e. for people with multigland disease). As there will be an IOPTH results after excision of the first gland (if this is negative in people who have remaining abnormal tissue and go on to have further glands excised, then people with MGD will be counted as true negatives) and an IOPTH result after excision of all abnormal glands (if this is positive in people with MGD once all their glands have been removed then people with MGD will be counted as true positives). In some studies, both methods can be calculated as they may report (in people with MGD) a negative IOPTH after excision of their first gland (a true negative due to remaining abnormal tissue), but a positive IOPTH after excision of all the abnormal glands (a true positive if all glands are removed and the person is rendered normocalcaemic). The preferred method for this review is to find the IOPTH accuracy after excision of a single gland or excision of the first gland (in people with MGD). This is because the predominant use of IOPTH is likely to be in focused surgery and the accuracy for predicting whether further abnormal tissue remains. Therefore, if it was possible to calculate both methods from a study, the result after excision of the first gland was preferred. The protocol stated a sensitivity analysis would be performed if there was heterogeneity to only include studies which give IOPTH results after excision of the first gland (or in studies where all included participants had single gland disease). Results from the sensitivity analysis are reported in table 14.

There are various criteria for the IOPTH test to indicate a positive result. The criterion specified in this review was the Miami criteria (a drop in parathyroid hormone at 10 minutes post-excision of at least 50% of the highest baseline value (either pre-incision or pre-excision). However, studies were also included if they used a 50% drop in PTH from either baseline value. Studies using the criteria of a 50% drop and into the normal/reference range for PTH were excluded (unless a drop of 50% alone (regardless of whether it went into the normal range) could be calculated).

The protocol also specified PTH values taken at 5 or 20 minutes post-excision.

Studies were stratified according to the time point at which IOPTH was measured; studies reporting up to 10 minutes (sample taken at ≤10 minutes) and studies reporting at >10 minutes (7 studies analysed in this stratum: 4 studies^{85, 94, 183, 537} took samples at 5, 10 and 15 minutes and the drop could be at any time point within 15 minutes, 1 study²⁰⁷ only reported the median sample time of 13 minutes, 1 study³²¹ the sample was taken at 12 minutes and 1 study³¹⁴ the sample was taken at 20 minutes). Twenty-six studies were analysed in the stratum up to 10 minutes.

Some studies reported in a narrative in the results that some people had a delayed drop in IOPTH at 20 or 30 minutes. These studies did not specify in the methods that the 20-minute time point would be taken for all people without a drop in IOPTH at 10 minutes. Therefore it is unclear whether the 20-minute time point was assessed for everyone with an IOPTH negative at 10 minutes. Only the 10-minute time point was analysed for these studies^{153, 224, 464, 504}. In addition, some studies reporting that some people had a delayed drop, the delayed drop was at 30 minutes^{290, 291, 459} only the 10-minute data were analysed as 30 minutes is not included in the review protocol. Four studies actually reported in the methods that if the IOPTH did not fall at 10 minutes, a 20-minute sample would be taken before exploration continued^{34, 69, 96, 486}. These studies have been analysed separately, as this is not the same criterion as everyone having the sample taken at 20 minutes. Three of these studies are also included in the up to 10 minute stratum as it was possible to calculate the results at 10 minutes only.

All clinical evidence was also stratified according to whether the participants had undergone previous parathyroidectomy. Results were stratified into studies only including people having their first operation, studies only including people having re-operation, and studies with a mixed population of first operation or re-operation that could not be analysed separately. For the IOPTH test, data were available for all time points for studies looking at first operation. For re-operation or mixed studies, only the ≤10 minute time point was available as summarised below:

-

1^st operation (or studies including ≤5% people with re-operation)

• >50% drop at ≤10 minutes
• >50% drop at >10 minutes
• >50% drop at 10 minutes (but in people without a drop at 10 minutes, a 20 minute time point sample was taken before continuing exploration).

-

Mixed 1^st operation and re-operation (>5% re-operation and not reported separately)

• >50% drop at ≤10 minutes
  Data not available for any other time points

-

Reoperation only

• >50% drop at ≤10 minutes (data only available from a study subgroup analyses)
  Data not available for any other time points

The protocol stated a sensitivity analysis would be performed if there was heterogeneity to only include studies which give IOPTH results after excision of the first gland (or in studies where all included participants had single gland disease). Results of this sensitivity analysis are reported in Table 13.

1.4.2. Included studies

Fifty six studies were included in the clinical evidence review, (Aarum 2007¹, Agarwal 2012⁴, Agha 2007⁷, Barczynski 2007³⁴, Bobanga 2017⁵⁵, Bonjer 1997⁵⁷, Bradley 2016⁶⁰, Calo 2013⁶⁹, Casas 1994⁷⁹, Cayo 2009⁸⁵, Chen 2005⁹⁴, Chick 2017⁹⁶, Garner 1999¹⁵³, Hamilton 1988¹⁸¹, Hanif 2006¹⁸³, Harris 2008¹⁸⁶, Hathaway 2013¹⁸⁹, Hindie 1998¹⁹⁷, Hughes 2011²⁰⁷, Hwang 2010²⁰⁹, Iacobone 2005²¹⁰, Jaskowiak 2002²²⁴, Kairaluoma 1994²³⁴, Kim 2015²⁵⁰, Krausz 2006²⁶⁴, Kumar 2000²⁶⁸, Lee 2014²⁷⁶, Lo 2003²⁹⁰, Lo 2007²⁹¹, Lombardi 2008²⁹², Michel 2013³¹⁴, Miccoli 2008³¹³ Miura 2002³¹⁷, Morks 2001³²¹, Mozzon 2004³²⁵, Nilsen 2006³⁴³, Nordin 2001³⁴⁷, Orloff 2001³⁵⁵, Ozkul 2015³⁵⁸, Patel 1998³⁶⁵, Richards 2011³⁹¹, Rossi 2000³⁹⁷, Rubello 2006⁴⁰¹, Saaristo 2002⁴⁰⁹, Sagan 2010⁴¹², Sprouse 2001⁴⁵⁷, Stalberg 2006⁴⁵⁹, Stenner 2009⁴⁶⁴, Tampi 2014⁴⁷⁶, Timm 2004⁴⁸⁶, van Ginhoven 2011⁵⁰², Vignali 2002⁵⁰⁴, Wade 2012⁵⁰⁸, Wei 1997⁵¹⁵, Witteveen 2011⁵²⁴, Ypsilantis 2010⁵³⁷)

Three studies were RCT test-and-treat studies assessing the use of pre-operative imaging (2 studies) or IOPTH (1 study). Fifty-three studies assessed the accuracy of pre-operative imaging or intra-operative tests. All the included studies are summarised in table 2 and table 3 below.

1.4.3. Excluded studies

See the excluded studies list in appendix J.

1.4.4. Summary of clinical studies included in the evidence review

Table 2

Summary of test-and-treat studies included in the evidence review.

Table 3

Summary of diagnostic accuracy studies included in the evidence review.

See appendix D for full evidence tables.

1.4.5. Clinical Evidence Summaries

1.4.5.1. Imaging localisation tests – test and treat studies

Table 4

Clinical evidence summary (first operation stratum): MIBI+US pre-operative localisation versus no pre-operative localisation.

Table 5

Clinical evidence summary (first operation stratum): US pre-operative localisation versus no pre-operative localisation.

1.4.5.2. Imaging localisation tests – diagnostic accuracy studies

Table 6

Clinical evidence summary: 1^st operation stratum.

Table 7

Clinical evidence summary: Mixed 1^st and re-operation stratum.

Table 8

Clinical evidence summary: Re-operation stratum.

1.4.5.3. Intra-operative tests – test and treat studies

Table 9

Clinical evidence summary (first operation stratum): IOPTH versus no IOPTH.

1.4.5.4. Intra-operative tests – diagnostic accuracy studies

Table 10

Clinical evidence summary: 1^st operation stratum.

Table 11

Clinical evidence summary: Mixed 1^st and re-operation stratum.

Table 12

Clinical evidence summary: Re-operation stratum.

Table 13

Summary of sensitivity analyses for Imaging results. Sensitivity analysis (if heterogeneity) to subgroup into only those studies recruiting people with a single positive adenoma on imaging, those studies recruiting people with negative imaging and those (more...)

Table 14

Summary of sensitivity analyses for IOPTH results. Sensitivity analysis (if heterogeneity) to subgroup into those studies reporting IOPTH results after excision of the first gland only.

1.5. Economic evidence

1.5.1. Included studies

Two health economic studies were identified with the relevant comparison and have been included in this review.^{29, 363} These are summarised in the health economic evidence profiles below (Table 15 and Table 16) and the health economic evidence tables in appendix H.

1.5.2. Excluded studies

No health economic studies that were relevant to this question were excluded due to assessment of limited applicability or methodological limitations.

See also the health economic study selection flow chart in appendix G.

1.5.3. Summary of studies included in the economic evidence review

Table 15

Health economic evidence profile: Non-invasive imaging.

Table 16

Health economic evidence profile: Intra-operative techniques.

1.5.4. Unit costs of pre-operative imaging

Table 17

UK costs of non-invasive imaging techniques.

Table 18

UK costs of invasive imaging techniques.

1.5.5. Health economic analysis for intra-operative imaging

An exploratory analysis was conducted to consider whether the use of a rapid intra-operative parathyroid hormone (IOPTH) test during parathyroidectomy could be justified on an economic basis. This analysis sought to answer two questions:

1. What is the improvement in probability of successful surgery required to make IOPTH testing during a parathyroidectomy cost neutral?
2. What is the improvement in quality of life required following successful surgery to make IOPTH testing during a parathyroidectomy cost effective?

A detailed write up of this analysis is available in appendix I.

The results of the exploratory analysis indicate that including IOPTH testing during parathyroidectomy is highly unlikely to be cost-neutral, as the required improvement in probability of surgical cure attributable to IOPTH testing is too large to be realistic. Results also show that the required improvement in quality of life following successful surgery is higher than can be realistically expected for successful cure of PHPT, therefore IOPTH testing during a parathyroidectomy is highly unlikely to be cost effective.

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Appendices

Final

Diagnostic evidence review

This evidence review was developed by the National Guideline Centre

Disclaimer: The recommendations in this guideline represent the view of NICE, arrived at after careful consideration of the evidence available. When exercising their judgement, professionals are expected to take this guideline fully into account, alongside the individual needs, preferences and values of their patients or service users. The recommendations in this guideline are not mandatory and the guideline does not override the responsibility of healthcare professionals to make decisions appropriate to the circumstances of the individual patient, in consultation with the patient and/or their carer or guardian.

Local commissioners and/or providers have a responsibility to enable the guideline to be applied when individual health professionals and their patients or service users wish to use it. They should do so in the context of local and national priorities for funding and developing services, and in light of their duties to have due regard to the need to eliminate unlawful discrimination, to advance equality of opportunity and to reduce health inequalities. Nothing in this guideline should be interpreted in a way that would be inconsistent with compliance with those duties.

NICE guidelines cover health and care in England. Decisions on how they apply in other UK countries are made by ministers in the Welsh Government, Scottish Government, and Northern Ireland Executive. All NICE guidance is subject to regular review and may be updated or withdrawn.