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The Journal of Clinical Endocrinology & Metabolism Vol. 84, No. 8 2654-2658
Copyright © 1999 by The Endocrine Society

Original Studies

Hypocalcemia Induced during Major and Minor Abdominal Surgery in Humans

R. Lepage, G. Légaré, C. Racicot, J.-H. Brossard, R. Lapointe, M. Dagenais and P. D’Amour

Research Center, Campus Saint-Luc, and the Departments of Biochemistry (R.L.), Medicine, and Surgery (G.L., C.R., R.L., M.D.), Centre Hospitalier de l’Université de Montréal, Montreal, Canada

Address all correspondence and requests for reprint to: Pierre D’Amour, M.D., Centre de Recherche du Centre Hospitalier de l’Université de Montréal, Campus Saint-Luc, 264 René Lévesque boulevard East, Montreal, Quebec, Canada H2X 1P1


   Abstract
Top
 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
Hypocalcemia has only been rarely reported during surgical procedures not involving massive blood transfusions. The frequent observation in our hospital of a low serum ionized calcium level during surgery in nonacutely ill patients prompted us to investigate the calcium-PTH axis in three groups of subjects undergoing major (hepatectomy; n = 10), moderately severe, or minor surgery under general anesthesia (colectomy; n = 7, herniorrhaphy; n = 9) compared to that in one group of minor surgery cases under epidural anesthesia (herniorrhaphy; n = 15). Serum samples were obtained before anesthesia, after anesthesia but before surgery, and 40 and 120 min after the beginning of surgery in all groups of patients and for up to 3 days in major and moderately severe cases. Significant falls (P < 0.01), always proportional to the severity of the surgical/anesthesia procedure, were observed for ionized calcium (6–20%), total calcium (8–19%), and albumin (8–23%) accompanied by increases in intact PTH (105–635%). The decrease in ionized and total calcium correlated with a decrease in albumin (P < 0.001). Phosphorus, pH, and magnesium levels remained within the normal range. Adjustment of ionized calcium for variation in albumin revealed that 50–100% of the variation in ionized calcium could be attributed to a fall in albumin resulting from fluid administration to patients before admission to the surgery ward and between the onset of anesthesia and the end of surgery (1.2–5.6 L). Albumin- and pH-independent residual ionized calcium decreases of 12.2% in the hepatectomy group, 4.6% in the group of moderately severe and minor cases under general anesthesia, and 3.7% in the control group reflected the severity of the surgical/anesthesia procedure.


   Introduction
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 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
HYPOCALCEMIA is not an unusual finding in patients hospitalized for critical illnesses and has also been described during postsurgical procedures (1, 2, 3, 4, 5, 6, 7, 8). Numerous factors have been suggested as causing the hypocalcemia in these situations, such as changes in albumin affinity for calcium (9, 10, 11), chelation by citrate from blood transfusions (12, 13), or resistance to PTH or vitamin D action (14). In the absence of massive blood transfusion, only slight decreases in calcium levels within the normal range have been reported during surgical procedures, mostly attributed to pH variations (11, 15, 16).

Ionized calcium measurements are not routinely performed in our hospital during surgery, except during liver transplantation. Since the installation of a new blood gas analyzer giving simultaneous measurements of blood gas parameters and ionized calcium, we have, however, observed that low ionized calcium levels were frequent during surgery in anesthetized patients even in the absence of frank alkalosis or other obvious cause of hypocalcemia. We therefore decided to investigate possible changes in the calcium-PTH axis during major and minor abdominal surgery under general anesthesia in noncritically ill human subjects, comparing results to those obtained in subjects undergoing minor surgery under local anesthesia.


   Subjects and Methods
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 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
 References
 
A total of 41 subjects scheduled for elective surgery participated in this study. They were assigned to 1 of 3 study groups: group I comprised 10 subjects undergoing major surgery under general anesthesia (partial hepatectomy) for hepatic metastasis secondary to colon cancer (n = 5), hepatic focal necrosis (n = 3), giant hemangioma (n = 1), or hydatic cyst (n = 1); group II included 16 subjects scheduled for either moderately severe or light surgery under general anesthesia: colectomy for colon neoplasia (n = 4), polyposis (n = 3), or herniorrhaphy (inguinal: n = 5; other: n = 4); and group III comprised 15 subjects submitted to inguinal herniorrhaphy under epidural anesthesia. Nineteen of the 24 herniorrhaphy cases were admitted through the 1-day care unit. Exclusion criteria were: age less than 18 yr or more than 80 yr; emergency surgery, diabetes, alcoholism (>60 g/day), cirrhosis, malnutrition (albumin <30 g/L or recent loss of >10% of body weight), chronic renal disease (creatinine >150 µmol/L), septicemia, steroids in the last 3 months, or antacids or diuretics in the week preceding surgery or during the study phase. Patients with significant respiratory (pCO2, <30 mm Hg) or metabolic (HCO3-, >35 mmol/L) alkalosis (pH > 7.45) during the study phase were also excluded.

Experimental protocol

The study protocol was approved by a local ethics committee, and informed consent was obtained from all participants. Anesthesia protocols were standardized. For general anesthesia, only the following agents could be used: midazolam, propofol, fentanyl, sulfentanyl, enflurane, isoflurane, doxacurium, mivacurium, and succinylcholine. The regional anesthesia protocol consisted of intraspinal administration of xylocaine and fentanyl. If necessary, narcotics or anxiolytics could be used parenterally. Total fluid administration before and during surgery amounted to 5.6 ± 0.5 L (mean ± SE) in group I, 2.3 ± 0.4 L in group II; and 1.2 ± 0.08 L in group III. For subjects undergoing moderate and major surgery, blood samples were obtained on the day before surgery, after induction of anesthesia but before surgery (time zero), then every 20 min until the end of surgery and on days 1 and 3 postsurgery. For herniorrhaphy subjects (part of group II and group III), sampling was performed on the morning of the surgery, after anesthesia but before surgery, then at 20 and 40 min during surgery and before the subjects left the 1-day care unit.

Laboratory methods

Sodium, potassium, and ionized calcium (reported at pH 7.40) were measured within 30 min after sampling by direct ISE on a Corning 288 Blood Gas System (Ciba Corning Diagnostics, Medfield, MA). Serum creatinine, total calcium, phosphorus, albumin, and magnesium were measured on the day of sampling by automated colorimetry (Baxter Paramax, Irvine, CA). Serum was also aliquoted, kept at -20 to -70 C and thawed only once before batch measurement of intact PTH (Allegro, Nichols Institute Diagnostics, San Juan Capistrano, CA).

Mathematical and statistical analysis

Results are the mean ± SEM. Comparisons against time within each group of patients were made by ANOVA for repeated measurements followed by Dunnett’s test for multiple comparisons. Results in the three subject groups at various time points were compared by ANOVA followed by Bonferroni adjustment for multiple comparisons using Instat 2.03 software (GraphPad Software, Inc., San Diego, CA).


   Results
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 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
Except for age and male/female ratio, the baseline characteristics of the three groups of subjects, including weight and creatinine level, were similar. Patients in group II were older (53.4 ± 3.7 vs. 43.5 ± 3.1 and 40.8 ± 3.3 yr, respectively, for groups I and III). The proportion of male subjects was higher in group III (100% vs. 69% and 25% in groups I and II, respectively). As shown in Fig. 1Go, significant differences were also noted before surgery for phosphorus (group I) and total calcium and albumin levels (groups I and II).



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  		Figure 1. Variation (mean ± SE) in ionized calcium, total calcium, albumin, phosphorus, pH, and intact PTH during major surgery ({blacksquare}; group I; n = 10), moderately severe and minor surgery under general anesthesia ({blacktriangleup}; group II; n = 16), and minor surgery under epidural anesthesia (•; group III, n = 15). Anova followed by Bonferroni adjustment. *, **, and***, P < 0.05, P < 0.01, and P < 0.001 vs. group III. +, ++, and +++, P < 0.05, P < 0.01, and P < 0.001 vs. group II.

 
Figure 1Go shows that ionized and total calcium, albumin, and intact PTH levels varied during surgery. Compared to presurgical levels, the changes were statistically significant (not shown) for all parameters at all sampling times from time zero (immediately at the onset of anesthesia but before surgery) up to 12 h postsurgery in the three groups of subjects with the exception of intact PTH in group III, which did not differ significantly from presurgical levels. Levels of ionized calcium dropped from normal in each group to minimal values of 0.99, 1.11, and 1.16 mmol/L at 2 h in groups I–III, respectively. Total calcium showed similar changes with nadirs at 2 h of 1.84, 2.05, and 2.22 mmol/L. Changes in albumin levels paralleled those affecting either total or ionized calcium with minimum levels varying from 29 (group I at 0 h), 28 (group 2 at 60 h) to 38 g/L (group III at 40 min). The relative change in each of these three parameters during surgery was systematically greater in group I (major surgery), with intermediate results in group II. Finally, intact PTH levels, although increasing in each of the three groups, reached abnormal levels only in groups I and II (23.5 and 7.3 pmol/L). Again, the order of change was the same: major surgery > minor to moderately severe surgery under general anesthesia > minor surgery under epidural anesthesia.

Phosphorus levels fell significantly in all groups of subjects, but remained within the normal range except for group I at 60 h, when the fall was significantly greater in group I (-48.6%) than in group II (-27.8%). The mean pH remained within the normal range in each subject (7.36–7.45), and no patient had to be excluded from this study because of alkalosis. There was, however, a small, but expected, rise in pH in the two groups of subjects under general anesthesia; this was significant only in group I. As also expected, pH showed no tendency to increase in subjects that were not mechanically ventilated (group III). Magnesium, sodium, and potassium levels were stable during the different surgical procedures (results not shown).

As the changes in ionized and total calcium were very similar to the fall in albumin, a regression analysis was conducted to evaluate the influence of albumin on both parameters, analyzing separately all pairs of results obtained within each group during the complete surgical procedure and, when available, postsurgery samples. The regression parameters are shown in Table 1Go. All correlations were statistically significant, with r2 > 0.33 for ionized calcium in groups I and II. The lower correlation coefficient observed in group III for ionized calcium reflected the modest span of values in this group of subjects.


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  		Table 1. Regression analysis of ionized and total calcium vs. albumin during surgical procedures/anesthesia of different severity in humans

 
Ionized and total calcium levels were adjusted for albumin variation according to the respective regression parameters. Albumin- and pH-independent residual variations in ionized and total calcium are shown in Table 2Go. A residual variation in ionized calcium that was significantly greater in groups I and II than in group III can still be noted. In the first 2 h, this difference averaged, respectively, -8.0%, -4.6%, and -0.5%. The greatest change was observed at 2 h in group I (-12.2%), compared to -4.6% and -3.7% in groups II and III, respectively.


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  		Table 2. Variation in albumin-independent ionized and total calcium during surgical/anesthesia procedures of varying severity in humans

 

   Discussion
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 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
In the absence of massive blood transfusions (12, 13), only minor falls in ionized calcium have been reported during standard surgical procedures and have been mostly attributed to changes in pH due to mechanical respiration (15, 16, 18). We are not aware of studies indicating falls in ionized calcium as important as those reported in this study. The observed fall in ionized calcium was systematic in all groups of patients, very rapid (already apparent before surgery), major (fell below the lower limit of the normal range), and varied according to the severity of the surgical intervention (20% to 6%). This decrease in ionized calcium was confirmed by similar changes in total calcium levels, before and after correction for the accompanying hypoalbuminemia.

Even though the increase in circulating intact PTH levels indicated true acute in vivo lowering of ionized calcium levels, sampling of some patients through a heparin lock (group I and colectomy patients from group II) could have resulted in underestimation of measured ionized calcium levels (19). Heparin interferes, however, only with ionized and not with total calcium measurements (20). A significant heparin interference would have manifested itself as a disproportionate decrease in the ionized calcium fraction, a situation that we did not observe. Similar falls of both total and ionized calcium also eliminated any potential interference from an unmeasured in vitro or in vivo chelator (such as globulins or citrate).

Hypoalbuminemia has been reported as causing a negative interference in the measurement of ionized calcium (21, 22, 23, 24, 25, 26, 27, 28, 29). This interference is approximately 0.0027 mmol/L ionized calcium per g/L albumin when saturated KCl is used in the reference electrode as was the case in this study (24). Partial correction of ionized calcium for this interference represented maximally 0.02 mmol/L in our subjects, still leaving a significant fall of ionized calcium in each group of patients that appeared related to the diminished albumin concentration. This residual fall could not be further modified by adjusting for the small variations of pH observed in mechanically ventilated subjects. The average rise of 0.024–0.038 units of pH corresponded to an insignificant decrease in ionized calcium of 0.001–0.002 mmol/L according to the equation used by the Corning ionized calcium analyzer: Ca2+ at pH 7.40 = Ca2+ actual x [1 - 0.41 x (7.4 - pH)].

The in vivo fall in ionized calcium triggered an immediate increase in circulating intact PTH proportional to the severity of the surgical/anesthesia procedure (105–635%). The increase in intact PTH remained within the physiological range observed during acutely induced hypocalcemia (30, 31) except for a few points in group I that were well over this range. These points were observed at 120 min in three subjects subjected to 25–30 min of hylar clamping of the liver. Clamping of both the portal vein and hepatic artery during bouts of 15 min separated by 10 min of unclamping possibly reduced the major catabolic pathway for intact PTH (32), resulting in excessively high intact PTH levels for the prevailing hypocalcemia.

The fall in albumin already apparent at time zero was probably the result of the impressive amount of physiological saline administered to patients during surgery, particularly in group I (5.6 ± 0.5 L) and group II (2.3 ± 0.4 L) compared to that in group III (1.2 ± 0.08 L). An important fraction of this fluid proportional to the expected length of the surgery had already been administered upon arrival in the surgical ward and between the onset of anesthesia and the beginning of surgery (time zero). This could also explain why most of the changes in albumin level (and calcium fractions) were already apparent at time zero, then tended to stabilize.

At least half of the fall in ionized calcium during the first 40 min of surgery could be attributed to a combined dilutional/measurement effect of albumin. We are not aware of reported cases of hemodilutional ionized calcemia during surgery, except through the absorption of hypotonic irrigating fluids (33, 34). This was not the case here, as normal saline was used in all cases, with only minimal amounts of albumin or starch in two patients only. Furthermore, with hypotonic fluid absorption, hyponatremia accompanied ionized hypocalcemia (33, 34). This is not the case here, with completely stable sodium levels during surgery. It has already been proposed that dilutional ionized hypocalcemia could result from acute changes in extracellular water volume considering that the half-time for calcium equilibration from loosely bound bone salts is around 70 min (35). The exact cause of the nonalbumin-associated residual decrease in ionized calcium remains to be established, as all of the other major causes of hypocalcemia (1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16, 36, 37, 38) were not present in our subjects.

Part of the hypophosphatemia reported in this study may also have resulted from renal losses of phosphorus due to extracellular volume expansion (39). The decrease in phosphorus at 60 h after surgery in group I has been observed in patients undergoing major liver surgery. In addition to all other known causes of hypophosphatemia in major surgery patients, posthepatectomy hypophosphatemia has been attributed to a massive intracellular shift of phosphorous in the already regenerating liver (40, 41).

In conclusion, ionized hypocalcemia accompanied by significant elevation of intact PTH was present during surgical procedures of varying severity. An important part of this fall in ionized calcium was apparently associated with falls in albumin resulting from acute hemodilution by physiological saline. If one considers that the symptomatic level of hypocalcemia is quite variable and depends largely on its speed of onset (42), the relatively modest, but very rapid, fall in ionized calcium observed at the beginning of surgery may have clinical consequences; however, these remain to be established.

Received January 12, 1999.

Revised April 28, 1999.

Accepted May 4, 1999.


   References
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

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