Changes in serum prealbumin as a marker for nitrogen balance in surgical oncology patients

doi:10.21203/rs.3.rs-1622649/v1

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Changes in serum prealbumin as a marker for nitrogen balance in surgical oncology patients

https://doi.org/10.21203/rs.3.rs-1622649/v1

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published 18 Oct, 2023

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Background

Serum prealbumin has long been used as a marker of nutritional status. However, prealbumin is a negative acute phase reactant influenced by several non-nutritional-related factors including surgery, infection, and cancer. An increasing prealbumin has been correlated with a positive nitrogen balance in general surgery patients receiving parenteral nutrition (PN) with 88% specificity and 70% sensitivity. To date, no trial has evaluated the effect of concurrent cancer and surgery on the value of prealbumin in predicting nitrogen balance.

Methods

This study is a concurrent retrospective design of post-operative patients (≥ 19 years of age) identified by the nutrition support service who received PN for ≥ 5 days, had a baseline and follow-up serum prealbumin and C-reactive Protein (CRP) measured, as well as a 24-hour urinary urea nitrogen (UUN) performed between days 5-10 of PN. Exclusion criteria include anuric renal failure, Child-Pugh Class C liver failure, pregnancy, and corticosteroid use. Prealbumin was correlated to nitrogen balance, measuring sensitivity, specificity, and negative and positive predictive values. Information was collected regarding patient demographics and presence or absence of metastatic cancer.

Results

Thirty patients were identified and evaluated for this study from December 1st, 2010 to July 15th, 2011. Patients included in the study had a mean age of 57 years old (range 20-82), 53% male, with a mean weight of 84 kg (range 42-140) and body mass index (BMI) of 29 kg/m² (range 14.9-56.8). The mean daily caloric dose of PN per actual body weight was 21 kcal/kg (range 10-34) and the mean daily protein dose was 1.4 g/kg (range 1-2). Forty seven percent of patients were obese (BMI > 30 kg/m²) and were prescribed high-protein hypocaloric PN. The most common indication for PN was post-operative ileus (23/30 patients). 24-hour urine collection for UUN was performed on average of day 8 after PN initiation (range 5-10 days). Nitrogen balance as calculated from 24-hour UUN was positive in 17/30 patients. A positive prealbumin change of greater than 2.8 mg/dL was found to have a statistically significant association with positive nitrogen balance (p = 0.02). At the cut off level of positive 2.8 mg/dL, the likelihood of a positive nitrogen balance had a sensitivity of 82% (95% confidence interval (CI) 64% - 100%); specificity of 62% (95% CI 35% - 88%); positive predictive value of 74% (95% CI 54%-93%); negative predictive value of 73% (95% CI 46% - 99%). No absolute value for prealbumin level (e.g., > 20 mg/dL) was found to be a significant predictor of positive nitrogen balance. CRP levels at initiation of PN were significantly elevated with a mean level of 147 mg/dL.

Conclusion

These results indicate a positive change in serum prealbumin (>2.8 mg/dL) has sufficient sensitivity (82%) to predict positive changes in nitrogen balance in the surgical oncology population. However, the low specificity (62%) makes it less useful in predicting a negative nitrogen balance. Absolute prealbumin levels were greatly affected by inflammation, as evidenced by CRP levels, and single values were not useful in predicting positive nitrogen balance.

Positive changes in serum prealbumin levels have previously been associated with a positive nitrogen balance (NB) in surgical patients receiving parenteral nutrition (PN); however, it is unclear if this is true in oncologic surgery patients. This study highlights how changing levels of serum prealbumin and C-reactive protein correlates to NB for cancer patients in the post-operative period requiring PN. Changes in prealbumin levels from baseline showed sufficient sensitivity, but not specificity to utilize routinely for predicting NB in this population.

Nutrition is an integral part of supporting patients with acute illness. Often the use of specialized nutrition support via enteral or parenteral routes is required. Tools exist to help estimate the nutritional needs of patients; however, determining the adequacy of nutritional interventions remains a challenge. The adequacy of protein provision in patients receiving parenteral nutrition (PN) has traditionally been assessed through measurement of 24-hour urinary urea nitrogen (UUN) excretion and subsequent estimation of nitrogen balance.¹ The 24-hour collection of urine can be technically challenging, time-consuming, costly, and easily prone to error. In an attempt to avoid some of the limitations associated with a 24-hour UUN, serum markers of visceral proteins (e.g., prealbumin) have been used as surrogate markers of achieving a positive nitrogen balance and improvement in nutrition status.

Prealbumin (also called transthyretin) is a visceral protein that has been studied in this manner. This short-lived transport protein is often used clinically as an indicator of adequate provision of nutrition. Church and Hill validated the use of serum prealbumin as an indicator of nitrogen balance.¹ In their study, prealbumin showed a sensitivity and specificity of 88% and 70%, respectively as a predictor of a positive nitrogen balance. However, these results have not been reliably replicated.^2-8 Prealbumin is known to be affected by several variables such as renal or hepatic failure, and medications (e.g., corticosteroids). Prealbumin is also a negative acute phase reactant sensitive to inflammation, malignancy, trauma, and surgery.^2,5,9-11 The most recent American Society for Parenteral and Enteral Nutrition guidelines for the provision of nutrition support in critically ill patients recommends against the use of prealbumin for determination of nutrition status for that same reason.¹² C-Reactive Protein (CRP) is a positive acute phase protein synthesized by the liver in response to inflammation. Moreover, the level of CRP has been shown to correlate with the degree of inflammation present.¹⁰ As such, CRP may be measured with prealbumin to evaluate the presence of an inflammatory state. Cancer is also known to cause elevations in acute phase inflammatory markers, such as CRP, which is often elevated in patients with metastatic cancer.¹³

Despite this, the use of prealbumin as a marker for nutritional status remains widespread. No study to date has evaluated the results of Church and Hill in a surgical oncology patient population with the current standards of practice for the provision of PN. The primary objective of this study was to evaluate the correlation (sensitivity, specificity, positive and negative predictive value) of prealbumin with nitrogen balance in a surgical oncology population.

This study is of concurrent retrospective design which included patients admitted to The University of Texas MD Anderson Cancer Center (MDACC) from December 1st, 2010 to July 15th, 2011. Surgical oncology patients were eligible for enrollment if they had elective or emergent surgery within the last thirty days and were receiving PN. Other inclusion criteria were adult patients (age > 18 years) with a 24-hour UUN, baseline and weekly serum prealbumin as well as CRP available, ordered as part of the nutrition support team protocol. Serum prealbumin, CRP and 24-hour UUN must have been obtained 5-10 days after initiation of PN, when PN was at goal as determined by the nutrition support team. Exclusion criteria included pregnancy, age ≤ 18 years, systemic corticosteroid prescription, acute or chronic renal failure (serum creatinine [SCr] increase > 0.5 mg/dL; increase > 50% baseline, or SCr > 3 mg/dL), Childs-Pugh class C liver failure.

Data collected on each patient included patient demographics (age, gender, weight, height, body mass index (BMI)), date and type of surgical intervention, presence or absence of metastatic disease, nutrition status (based on subjective global assessment), indication for PN, calorie and protein content of PN, and laboratory data (Prealbumin, 24-hr UUN, CRP). Nitrogen balance was calculated using the equation: (protein dose (g)/6.25) – [UUN (g) + 2 (correcting for non-urinary losses)].¹⁴ Hypocaloric feeding for the purpose of this study was defined when any patient received a daily caloric dose of < 20 kcal/kg based on actual body weight. Obesity was defined as any patient with BMI of ≥ 30 kg/m².

Study protocol was approved by IRB and waiver of informed consent granted.

Statistical methods

Patient characteristics were tabulated using descriptive statistics. Univariate logistic regression models were used to evaluate the association between nitrogen balance and prealbumin, CRP, protein dose (per actual body weight), total caloric intake, hypocaloric feeding, or the presence of metastatic disease. An optimal cut point for prealbumin was computed to maximize the Youden’s Index¹⁵, that is, to maximize the sum of the sensitivity and specificity. To compare this optimal cut point with a pre-selected cut point of zero, the sensitivity, specificity, positive and negative predictive value, and the corresponding confidence intervals were computed. Fisher's exact tests were conducted to test the association between nitrogen balance and prealbumin difference defined by these cutpoints. The receiver characteristic curve (ROC curve) analysis was performed to evaluate the performance of the prediction of prealbumin difference on nitrogen balance, and the accuracy of prediction was measured by the area under the curve (AUC). Statistical analyses were performed using SAS 9.3 and R.

A total of 30 patients were evaluable for this study. Patient characteristics are reported in Table 1. Average age was 57 years (range 20–82), average weight was 84 kg (range 42–140) and average BMI was 29 kg/m² (range 14.9–56.8) with 47% of patients considered obese (BMI > 30 kg/m2). Approximately half of the patients were male (53%) and the majority of patients had metastatic disease present (67%). The most common indication for PN was post-operative ileus (77%). PN was provided for an average duration of 8 days prior to UUN, repeat prealbumin and repeat CRP levels (range 5–10 days). Time to PN initiation ranged from − 4 to 18 days post-op (negative number indicates pre-operative PN initiation). Table 2 summarizes the caloric and protein dosing of patients receiving PN. Table 3A summarizes the baseline, and repeat serum prealbumin and CRP levels as well as the mean difference between the baseline and repeat levels. Table 3B summarizes the number of patients with positive or negative changes in prealbumin, CRP and nitrogen balance.

Table 4 presents the association between nitrogen balance and baseline prealbumin, repeat prealbumin, prealbumin difference (in numbers and classified by zero), baseline CRP, repeat CRP, CRP changes (in numbers and classified by zero), hypocaloric feeding, the presence of metastatic disease, protein dose (per actual body weight), or total caloric intake (per actual body weight). It indicates that none of them were significantly associated with nitrogen balance.

Table 5 shows the relationship between the nitrogen balance and the prealbumin difference classified by zero. The sensitivity is 88% and its asymptotic 95% confidence interval is 73%-100%; The specificity is 38% and its asymptotic 95% confidence interval is 12%-65%; The positive predictive rate is 65% and its asymptotic 95% confidence interval is 46%-85%; The negative predictive rate is 71% and its asymptotic 95% confidence interval is 38%-100%. The p-value for Fisher’s exact test is 0.19, indicating that nitrogen balance was not significantly associated with the prealbumin difference classified by zero.

The optimal cut point for serum prealbumin change that maximized the sum of the sensitivity and specificity was 2.8 mg/dL (≥ 2.8 vs < 2.8). Table 6 shows the relationship between nitrogen balance and prealbumin difference classified by 2.8 mg/dL. The sensitivity is 82% and its asymptotic 95% confidence interval is 64%-100%; The specificity is 62% and its asymptotic 95% confidence interval is 35%-88%; The positive predictive rate is 74% and its asymptotic 95% confidence interval is 54%-93%; The negative predictive rate is 73% and its asymptotic 95% confidence interval is 46%-99%. The p-value for Fisher’s exact test was 0.02, implying that nitrogen balance was significantly associated with the prealbumin difference of 2.8 mg/dL.

The receiver operating characteristic curve shown in Fig. 1 shows that the serum prealbumin change of 2.8 mg/dL (AUC = 0.7195) had better discriminatory accuracy on the nitrogen balance than the serum prealbumin change of zero (AUC = 0.6335).

Repeat CRP levels showed the majority of patients maintained a level greater than 10 mg/dL indicative of ongoing inflammatory states (Fig. 2) with only 3 patients having a repeat CRP level of < 10mg/dL. Nearly all of these patients (25 out of 27) continued to have low prealbumin levels (< 20 mg/dL) as well.

As can be seen in Fig. 3, all but 1 patient had a decreased prealbumin at baseline, with only 3 patients showing resolution of inflammation (CRP < 10 mg/dL) between days 5–10 of PN.

The results of this study in postoperative cancer patients show a significant relationship between a positive increase of 2.8 mg/dL in prealbumin levels and positive nitrogen balance. However, the change in prealbumin alone is a poor indicator of nitrogen balance because while it has a high sensitivity (82%), it lacks specificity (62%). While the change in prealbumin in predicting positive nitrogen balance has sensitivity close to that previously reported by Church and Hill (88% in both studies), the specificity was lower (62% versus 70%). This indicates that while a positive change in prealbumin may be predictive of a positive nitrogen balance, a negative change in prealbumin is not as predictive of a negative nitrogen balance. When the data were analyzed for serum prealbumin change classified by zero for sensitivity and specificity, it showed a higher sensitivity (88%), but specificity decreased to 38%.

Some of the limitations of this study are its concurrent retrospective design. However, one of the benefits of the concurrent design allowed us to better verify the accuracy of the 24-hour UUN by being able to monitor and verify the volumes of urine collected over 24 hours and making sure proper procedures were followed for collection of the samples. The small number of patients is also a limitation, but is consistent with previous studies. Another limitation of this study is the lack of control of the nutrition support provided as patients were given PN at doses determined by the individual clinician. Also nearly half of the patients enrolled were obese (BMI > 30 kg/m²) and received hypocaloric PN. This represents a pragmatic approach to cancer patients supported with PN postoperatively.

However, given these limitations, the majority of patients enrolled in this study did attain a positive nitrogen balance (Table 3B). It is also has been well described that after surgery, serum prealbumin decreases and then increases slowly over 1–2 weeks.¹⁶ As the cancer patients collected in our study had recent surgery, it is possible that the prealbumin would rise after the post-surgical nadir, regardless of nitrogen balance. This may explain why such a large number of patients had positive changes in prealbumin versus only 3 that had a decrease in prealbumin.

Another consideration is approximately 2/3rds of patients enrolled in our study had metastatic cancer present. Of the patients with metastatic disease, 90% of them had a repeat CRP level of > 10 mg/dL and 95% of them had a repeat prealbumin of < 20 mg/dL. In the case of these patients, the presence of underlying metastatic cancer and resulting inflammation may render prealbumin to be chronically low with an elevated CRP.

Given these preliminary results, we conclude that while the sensitivity of prealbumin is sufficient to utilize in predicting positive nitrogen balance, the test lacks the specificity to enable accurate analysis of negative changes. Our data support the fact that prealbumin is highly affected by inflammation and is not a reliable marker for the postoperative oncology patient population.


#	Age (years)	Sex	Wt (kg)	BMI (kg/m²)	Primary Cancer	Mets	Surgical intervention	PN Indication
1	25	M	70.9	23.68	Germ Cell	Y	Small bowel resection	Post-op Ileus
2	77	M	103.6	32.33	Rectal	N	Resection of tumor	Post-op Ileus
3	55	F	139.9	56.75	Endometrial	Y	Total pelvic exenteration	Post-op Ileus
4	42	M	98.5	28.65	Pancreatic	Y	Small bowel resection, hepatic wedge resection, distal pancreatic resection	Post-op Ileus
5	50	F	59.2	23.41	Small bowel	Y	Resection of tumor	Post-op Ileus
6	62	F	82	28.71	Primary peritoneal	N	Repair of small bowel perforation	Bowel perforation
7	68	F	54.5	22.71	Liposarcoma	N	Resection of tumor, hemi-colectomy	Post-op Ileus
8	47	F	65.1	22.52	Liposarcoma	Y	Resection of tumor	Post-op Ileus
9	66	F	92.3	36.05	Appendiceal	Y	Tumor reductive surgery; HIPEC	Post-op Ileus
10	54	F	88.8	31.46	Neuroendocrine	Y	Repair of pancreatic leak	Pancreatic leak
11	69	M	58.8	19.2	Urothelial	Y	Resection of periaortic mass	Post-op Ileus
12	61	M	113	34.87	Prostate	N	Prostatectomy	Post-op Ileus
13	36	M	122.7	34.34	Schwannoma	N	Resection of tumor	Post-op Ileus
14	57	F	41.5	14.88	Anal	Y	Small bowel resection	Severe malnutrition
15	68	M	93.7	32.61	Bladder	Y	Resection of tumor, radical cystectomy, ileal conduit creation	Post-op ileus
16	51	F	68.5	28.14	Appendiceal	Y	Tumor reductive surgery; HIPEC	Post-op Ileus
17	63	M	113.7	34.32	Melanoma	Y	Small bowel resection x 6	Post-op ileus
18	82	M	83.6	30.7	Bladder	N	Cystectomy; ileal conduit creation	Post-op ileus
19	76	M	79.8	25.76	Rectal	N	APR with creation of end colostomy	Post-op ileus
20	58	M	84.9	27.88	Appendiceal	Y	Hemicolectomy, omentectomy, peritonectomy, abdominal washout, diverting loop ileostomy	Post-op ileus
21	42	M	50.8	18.21	Gastric lymphoma	N	Revision of gastrectomy	Expected prolonged NPO
22	57	F	131	48.11	Endometrial	N	TAH-BSO, extensive LND, partial omentectomy	Small bowel obstruction
23	45	F	67.9	21.79	Appendiceal	Y	Tumor reductive surgery; HIPEC	Post-op Ileus
24	20	F	72.6	26.03	Ewing sarcoma	Y	Internal hemipelvectomy, thrombectomy, reconstruction	Post-op ileus
25	65	M	53.8	18.39	Appendiceal	Y	Small Bowel resection	Expected prolonged NPO
26	52	F	78.1	29.39	Colon	Y	Ex-lap for bowel perf, abdominal washout, diverting loop ileostomy	Post-op ileus
27	77	F	109.1	45.11	Endometrial	Y	Small bowel resection, abdominal wall debridement	Expected prolonged NPO
28	66	M	88	27.16	Appendiceal	Y	Tumor reductive surgery; HIPEC	Post-op ileus
29	62	M	67	20.45	Lymphoma s/p SCT	N	Small Bowel resection	Post-op ileus
30	38	M	91	27.17	Peritoneal mesothelioma	Y	Tumor reductive surgery; HIPEC	Post-op Ileus
Mean	56		84	29
Wt = Actual body weight (kg); BMI = Body mass index (kg/m2); Mets = Metastatic cancer (Yes or No); M = male; F = female; PN = parenteral nutrition

Table 2

Summary of Nutrition Support on day 5–10
Characteristics	Mean	Std Dev	Median	Minimum	Maximum
Caloric intake on day 5–10
Total kcal/day	1689.7	266.6	1623	1296	2316
Kcal/kg/day (ABW)	21.6	6.0	21.2	9.9	34.2
Protein intake on day 5–10
Total grams/day	112.8	23.7	109	55	160
Grams/kg/day (ABW)	1.4	0.3	1.4	1	2
Duration of PN prior to UUN collection (days)	8	1	8	5	10
Time from post-op to PN initiation (days)	5	4.5	4	-4^†	18
Number of patients hypocalorically fed due to BMI > 30 kg/m2: 14/30 (47%)

ABW = actual body weight; PN = parenteral nutrition; UUN = urinary urea nitrogen

^† Negative number denotes pre-operative PN initiation.

Table 3

A Summary Table of Prealbumin, CRP and Nitrogen Balance (N = 30)
Characteristics	N	Mean	Std Dev	Median	Minimum	Maximum
Baseline Prealbumin (mg/dL)	30	8.75	4.37	7.40	2.90	21.80
Repeat Prealbumin (mg/dL)	30	13.52	6.62	11.85	4.80	32.50
Prealbumin Difference (repeat – baseline) (mg/dL)	30	4.76	6.80	4.05	-5.70	26.90
Baseline CRP (mg/dL)	30	144.17	88.91	133	2.49	347
Repeat CRP (mg/dL)	30	86.40	69.11	73.50	2.31	258
CRP Change (repeat – baseline) (mg/dL)	30	-57.77	86.19	-38.70	-278.40	84.60
24-hour UUN (g/day)	30	15.53	5.78	14	6	26
Time between baseline and repeat prealbumin and CRP (days)	30	7	1.1	7	9	7

CRP = C-reactive protein

UUN = Urinary urea nitrogen

Table 3

B Summary Table of Prealbumin, CRP and Nitrogen Balance Changes in PN patients (N = 30)
Characteristics	N (%)
Prealbumin Change
+	23 (77%)
-	7 (23%)
CRP Change
+	9 (30%)
-	21 (70%)
Nitrogen Balance
+	17 (57%)
-	13 (43%)

CRP = C-reactive protein; PN = parenteral nutrition

Table 4

Univariate Logistic Regression for Nitrogen Balance
Characteristics	Level	N	Odds Ratio	95% CI	P-value
Baseline Prealbumin*		30	1.01	( 0.86, 1.20 )	0.90
Repeat Prealbumin*		30	0.97	( 0.87, 1.09 )	0.66
Prealbumin Difference*		30	0.97	( 0.87, 1.09 )	0.61
Prealbumin Difference	+ vs. -	30	0.21	( 0.03, 1.36 )	0.10
Baseline CRP*		30	1	( 1.00, 1.01 )	0.30
Repeat CRP*		30	1.01	( 1.00, 1.02 )	0.08
CRP Change*		30	1	( 0.99, 1.01 )	0.71
CRP Change	+ vs. -	30	2.03	( 0.42, 9.89 )	0.38
Hypocaloric Feeding	Yes vs. No	30	0.31	( 0.07, 1.43 )	0.13
Metastatic Disease	Yes vs. No	30	0.67	( 0.14, 3.07 )	0.60
Protein Actual Body Weight		30	2.37	( 0.13, 42.37 )	0.56
Kcal Actual Body Weight		30	1.05	( 0.93, 1.19 )	0.46

* based on per unit change; CRP = C-reactive protein

Table 5

Nitrogen Balance Distribution by Prealbumin Difference
	Nitrogen balance based on 24-hour UUN = positive	Nitrogen balance based on 24-hour UUN = negative
Prealbumin goes up between baseline and day 7 (positive)	15	8
Prealbumin goes down or remains the same between baseline and day 7 (negative)	2	5

UUN = urinary urea nitrogen

* The sensitivity is 88% and its asymptotic confidence interval is 73–100%; The specificity is 38% and its asymptotic confidence interval is 12–65%; The positive predictive value is 65% and its asymptotic confidence interval is 46–85%; The negative predictive rate is 71% and its asymptotic confidence interval is 38–100%.

Table 6

Nitrogen Balance Distribution by Prealbumin Difference (optimal cutoff : 2.8 mg/dL)
	Nitrogen balance based on 24-hour UUN = positive	Nitrogen balance based on 24-hour UUN = negative
Prealbumin difference between baseline and day 7 ≥ 2.8 mg/dL	14	5
Prealbumin difference between baseline and day 7 <2.8 mg/dL	3	8

UUN = urinary urea nitrogen

* The sensitivity is 82% and its asymptotic confidence interval is 64–100%; The specificity is 62% and its asymptotic confidence interval is 35–88%; The positive predictive rate is 74% and its asymptotic confidence interval is 54–93%; The negative predictive rate is 73% and its asymptotic confidence interval is 46–99%.

No relative conflicts of interest or financial disclosures.

Funding: The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.

Competing Interests: The authors have no relevant financial or non-financial interests to disclose.

Author Contributions: All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Jacob Hall. The first draft of the manuscript was written by Jacob Hall and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Ethics approval: Study protocol was approved by IRB and waiver of informed consent granted.

Consent to participate: Study protocol was approved by IRB and waiver of informed consent granted.

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No competing interests reported.

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Changes in serum prealbumin as a marker for nitrogen balance in surgical oncology patients

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