Hypocalcemia: Practice Essentials, Pathophysiology, Etiology (original) (raw)
The causes of hypocalcemia include the following:
- Hypoalbuminemia
- Hypomagnesemia
- Hyperphosphatemia
- Multifactorial enhanced protein binding and anion chelation
- Medication effects
- Surgical effects
- PTH deficiency or resistance
- Vitamin D deficiency or resistance
Hypoalbuminemia
Hypoalbuminemia is the most common cause of hypocalcemia. Causes include cirrhosis, nephrosis, malnutrition, burns, chronic illness, and sepsis. In patients who are critically ill, low calcium levels can be simply due to hypoalbuminemia, which has no clinical significance because the active fraction (ionized) is not affected. However, to prevent missing a second hypocalcemic disorder, measure the ionized calcium level whenever the albumin level is low.
In a patient with hypocalcemia, measurement of the serum albumin is essential to distinguish true hypocalcemia, which involves a reduction in ionized serum calcium, from factitious hypocalcemia, meaning decreased total, but not ionized, calcium. To correct for hypoalbuminemia, add 0.8 mg/dL to the total serum calcium for each 1.0 g/dL decrease in albumin below 4.0 g/dL.
Parathyroid hormone–related hypocalcemia
Hypoparathyroidism can be hereditary or acquired. The hereditary and acquired varieties share the same symptoms, although hereditary hypoparathyroidism tends to have a gradual onset. [11]
Acquired hypoparathyroidism may result from the following:
- Neck irradiation/radioiodine therapy [12]
- Postparathyroidectomy in dialysis patients [13]
- Inadvertent surgical removal (can be transient or permanent)
- Infiltrative disease (eg, hemochromatosis, granulomatous disease [sarcoidosis], thalassemia, amyloidosis, or metastatic malignant infiltration
Late-onset hypoparathyroidism can be seen as a part of a complex autoimmune disorder involving ovarian failure and adrenal failure. Mucocutaneous candidiasis, alopecia, vitiligo, and pernicious anemia are associated with this disorder, which is referred to as polyglandular autoimmune disease (PGA I).
Hereditary hypoparathyroidism may be familial or sporadic, and it can occur as an isolated entity or can be associated with other endocrine manifestations. The familial forms include autosomal dominant and autosomal recessive, as well as a sex-linked form of early onset, for which the gene has been located on the long arm of the X chromosome.
Sporadic, late-onset hypoparathyroidism is a feature of several hereditary syndromes. These syndromes, and their associated features, are as follows:
- DiGeorge syndrome: congenital heart disease, cleft palate/lip, and abnormal facies
- Kearns-Sayre syndrome: heart block, retinitis pigmentosa, and ophthalmoplegia
- Kenny-Caffey syndrome: medullary stenosis of the long bones and growth retardation
Pseudohypoparathyroidism
Pseudohypoparathyroidism is characterized by end-organ resistance to the effects of PTH. PTH binds to the PTH receptor, which, in turn, activates cAMP through guanine nucleotide regulatory proteins (Gs). These proteins consist of alpha, beta, and gamma subunits.
Pseudohypoparathyroidism is classified into types I and II. Type I is further subdivided into Ia, Ib, and Ic. [11]
Type Ia
Type Ia pseudohypoparathyroidism results from a decrease in the Gs-alpha protein. This disorder comprises the biochemical features of pseudohypoparathyroidism along with the following somatic features of Albright hereditary osteodystrophy (AHO):
- Short stature
- Intellectual disability
- Obesity
- Round-shaped face
- Brachymetacarpia
- Brachymetatarsia
- Subcutaneous bone formation
Laboratory findings in AHO include hypocalcemia, hyperphosphatemia (with normal or high PTH levels), and low calcitriol. Vitamin D levels may be decreased because of inhibition by elevated levels of phosphorus and by decreased PTH stimulation of 25-hydroxyvitamin D 1-alpha-hydroxylase. The low calcitriol levels, in turn, may cause the resistance to the hypercalcemic effects of PTH in the bone.
The defect of the Gs-alpha protein is not confined to the effects of PTH but also affects other hormonal systems (eg, resistance to glucagon, thyroid-stimulating hormone, gonadotropins). The gene for the Gs-alpha protein is located on chromosome 20. Some family members carry the mutation and display the AHO phenotype but do not have pseudohypoparathyroidism. This is termed pseudo-pseudohypoparathyroidism.
Types Ib and Ic
In type Ib pseudohypoparathyroidism, patients do not present with the somatic features of AHO. These patients have normal Gs-alpha protein, with hormonal resistance to PTH—an impaired cAMP response to PTH, suggesting that the defect lies on the receptor. At what level the receptor is affected is not yet clear.
In type Ic pseudohypoparathyroidism, patients present with resistance to multiple hormonal receptors. However, Gs-alpha protein expression is normal.
Type II
In type II pseudohypoparathyroidism, PTH raises cAMP normally but fails to increase levels of serum calcium or urinary phosphate excretion, suggesting that the defect is located downstream of the generation of cAMP. These patients present with hypocalcemia, hypophosphaturia, and elevated immunoreactive PTH (iPTH) levels. These findings also occur in vitamin D deficiency, but in patients with a vitamin D deficiency, all parameters return to normal after vitamin D administration.
Hypomagnesemia
Severe hypomagnesemia can lead to hypocalcemia that is resistant to the administration of calcium and vitamin D. The usual cause of hypomagnesemia is loss via the kidneys (eg, osmotic diuresis, drugs) or the gastrointestinal tract (eg, chronic diarrhea, severe pancreatitis, bypass or resection of small bowel). Many drugs cause renal magnesium wasting, such as diuretics, aminoglycosides, amphotericin B, cisplatin, cyclosporine, and pentamidine These patients present with low or inappropriately normal PTH levels in the presence of hypocalcemia.
The mechanism of hypocalcemia includes resistance to PTH in the bone and kidneys, as well as a decrease in PTH secretion. Acute magnesium restoration rapidly corrects the PTH level, suggesting the hypomagnesemia affects the release of PTH rather than its synthesis.
Vitamin D deficiency
Vitamin D is a necessary cofactor for the normal response to PTH, and vitamin D deficiency renders PTH ineffective. Poor nutritional intake, chronic kidney disease, or reduced exposure to sunlight may cause vitamin D deficiency.
Current Recommended Dietary Allowances (RDAs) for vitamin D are 400 IU of vitamin D per day for infants, 600 IU of vitamin D per day for individuals from 1 to 70 years of age, and 800 IU per day for those over 70 years. [14] Studies have demonstrated that despite adequate intake, vitamin D insufficiency can still occur and lead to an increased PTH and subsequent bone turnover. Studies have also shown that dietary intake of vitamin D varies greatly by race and age. In a review of National Health and Nutrition Examination Survey (NHANES) III data from 2001-2006, 32% of African-American women were at risk for vitamin D deficiency—defined as serum 25-hydroxyvitamin D (24[OH]D) levels < 30 nmol/L—as compared with only 3% of White women. [15]
An observational study in elderly adults found that 74% of those studied were deficient in vitamin D, defined as 25(OH)D concentrations < 32 ng/mL, despite intake of more than 400-600 IU/d, which was the recommended RDA at the time. [16] The authors of this study suggested that elderly individuals may require as much as 1000 IU per day.
Mild hypovitaminosis D may not be trivial. In an elderly population with an increased PTH and osteoporosis, response to alendronate was attenuated. This attenuation was improved when vitamin D was administered. [17]
Impaired absorption
Numerous conditions can impair the absorption of vitamin D. Small bowel diseases, such as celiac disease, gastric bypass (particularly long limb Roux-en-Y gastric bypass), steatorrhea, and pancreatic diseases can all lead to low vitamin D levels. [18]
Pseudovitamin D deficiency rickets
This condition is secondary to an autosomal mutation of the 1-hydroxylase gene. Ultimately, calcidiol is not hydroxylated to calcitriol, and calcium is not absorbed appropriately. This condition is considered a pseudovitamin D deficiency because high doses of vitamin D can overcome the clinical and biochemical findings of this disease.
Hereditary vitamin D resistance rickets
This condition is extremely rare and is caused by a mutation in the vitamin D receptor. Typically, this condition presents within the first 2 years of life.
Liver disease
Liver disease with decreased synthetic function can cause vitamin D deficiency from several sources, as follows:
- Impaired 25-hydroxylation of vitamin D
- Decreased bile salts with malabsorption of vitamin D
- Decreased synthesis of vitamin D–binding protein
- Other factors
Patients with cirrhosis and osteomalacia have low or normal levels of calcitriol, suggesting that other factors may interfere with vitamin D function or are synergistic with malabsorption or decreased sun exposure. These patients require administration of calcidiol or calcitriol for the treatment of hypocalcemia.
Kidney disease
Chronic kidney disease leads to a decrease in the conversion of 25-hydroxyvitamin D to its active form 1,25-dihydroxyvitamin D, particularly when the glomerular filtration rate (GFR) falls below 30 mL/min. This results in an increase in PTH. Ultimately, the increased absorption of phosphorus and calcium can lead to calcium-phosphorus mineral deposition in the soft tissues. In the early stages of chronic kidney disease, hypocalcemia can occur because of the decrease in calcitriol production and a subsequent decrease in the intestinal absorption of calcium.
Hungry bone syndrome
Surgical correction of primary or secondary hyperparathyroidism may be associated with severe hypocalcemia due to a rapid increase in bone remodeling. Hypocalcemia results if the rate of skeletal mineralization exceeds the rate of osteoclast-mediated bone resorption.
A less severe picture is also observed after correction of thyrotoxicosis, after institution of vitamin D therapy for osteomalacia, and with tumors associated with bone formation (eg, prostate, breast, leukemia). All of these disease states result in hypocalcemia due to mineralization of large amounts of unmineralized osteoid. [19]
Acute pancreatitis
Pancreatitis can be associated with tetany and hypocalcemia. It is caused primarily by precipitation of calcium soaps in the abdominal cavity, but glucagon-stimulated calcitonin release and decreased PTH secretion may play a role.
When the pancreas is damaged, free fatty acids are generated by the action of pancreatic lipase. Insoluble calcium salts are present in the pancreas, and the free fatty acids avidly chelate the salts, resulting in calcium deposition in the retroperitoneum. In addition, hypoalbuminemia may be a part of the clinical picture, resulting in a reduction in total serum calcium. In individuals with concomitant alcohol abuse, a poor nutritional intake of calcium and vitamin D, as well as accompanying hypomagnesemia, may predispose them to hypocalcemia. [20]
Hyperphosphatemia
Hyperphosphatemia may be seen in critical illness and in patients who have used phosphate-containing enemas. Phosphate binds calcium avidly, causing acute hypocalcemia. Acute hypocalcemia secondary to hyperphosphatemia may also result from kidney failure or excess tissue breakdown because of rhabdomyolysis or tumor lysis.
In acute hyperphosphatemia, calcium is deposited mostly in the bone but also in the extraskeletal tissue. In contrast, in chronic hyperphosphatemia, which is nearly always from chronic kidney disease, calcium efflux from the bone is inhibited and the calcium absorption is low, because of reduced renal synthesis of 1,25-dihydroxyvitamin D. However, other consequences of kidney failure, including a primary impairment in calcitriol synthesis, also contribute to hypocalcemia.
Medications
Cinacalcet, a calcimimetic agent used to help control secondary hyperparathyroidism in patients with chronic kidney disease who are on dialysis, may produce hypocalcemia as a result of acute inhibition of PTH release. Most cases resolve spontaneously within 14 days. Severe hypocalcemia occurs in approximately 18% of patients treated with cinacalcet. [21]
Hypocalcemia can also occur in patients treated with some chemotherapeutic drugs. For example, cisplatin can induce hypocalcemia by causing hypomagnesemia, and combination therapy with 5-fluorouracil and leucovorin can cause mild hypocalcemia (65% of patients in one series), possibly by decreasing calcitriol production. [22] In addition, acute kidney injury and hypocalcemia have been reported as adverse effects in patients receiving the programmed cell death protein 1 (PD-1) inhibitors nivolumab and pembrolizumab. [23]
Hypocalcemia may result from the treatment of hypercalcemia with bisphosphonates, particularly zoledronic acid, which is significantly more potent than other bisphosphonates in suppressing the formation and function of osteoclasts. Patients who are affected appear to lack an adequate PTH response to decreasing serum calcium levels. [24]
Hypocalcemia and osteomalacia have been described with prolonged therapy with anticonvulsants (eg, phenytoin, phenobarbital). [25] The mechanisms differ according to the class of anticonvulsants; for example, phenytoin induces cytochrome P450 enzymes and enhances vitamin D catabolism.
Foscarnet is an antiviral agent used to treat refractory cytomegalovirus and herpes infections in patients who are immunocompromised. It complexes ionized calcium and, therefore, lowers ionized calcium concentrations, potentially causing symptomatic hypocalcemia. Therefore, the ionized calcium concentration should be measured at the end of an infusion of foscarnet.
Denosumab is a fully human monoclonal antibody to the receptor activator of nuclear factor kappa B ligand (RANKL), an osteoclast differentiating factor. It inhibits osteoclast formation, decreases bone resorption, increases bone mineral density (BMD), and reduces the risk of fracture. See the Fracture Index WITH known Bone Mineral Density (BMD) calculator.
In the denosumab trials, all women were supplemented with daily calcium (1000 mg) and vitamin D (400-800 U). A small proportion of women in the denosumab trials had a decrease in the serum calcium level to less than 8.5 mg/dL. However, in patients with conditions that predispose to hypocalcemia, such as chronic kidney disease, malabsorption syndromes, or hypoparathyroidism, symptomatic hypocalcemia may occur. The nadir in serum calcium occurs approximately 10 days after administration. Thus, denosumab should not be given to patients with preexisting hypocalcemia until it is corrected. In addition, patients with conditions predisposing to hypocalcemia (eg, chronic kidney disease and creatinine clearance < 30 mL/min) should be monitored for hypocalcemia. [26]
Symptomatic hypocalcemia during transfusion of citrated blood or plasma is rare, because healthy patients rapidly metabolize citrate in the liver and kidney. However, a clinically important fall in serum ionized calcium concentration can occur if citrate metabolism is impaired due to liver or kidney failure or if large quantities of citrate are given rapidly—for example, during plasma exchange or massive blood transfusion.
Agents used to cleanse the bowel prior to GI procedures such as colonoscopy—especially sodium phosphate preparations, but also polyethylene glycol—can lead to acute hyperphosphatemia and subsequent hypocalcemia in certain populations. [27, 28] Risk factors include the following:
- Kidney failure
- Advanced age
- Chronic heart failure
- Hepatic insufficiency
- Volume depletion
- Use of angiotensin-converting enzyme (ACE) inhibitors or nonsteroidal anti-inflammatory drugs (NSAIDs)
Some radiographic contrast dyes may contain ethylenediaminetetraacetic acid (EDTA), which chelates calcium in serum, thereby reducing serum ionized calcium concentration, resulting in hypocalcemia. Gadolinium-based contrast material can falsely lower serum calcium levels and should be considered if levels are drawn shortly after magnetic resonance imaging.
Rarely, an excess intake of fluoride can cause hypocalcemia; this effect is presumably mediated by inhibition of bone resorption. Overfluorinated public water supplies and ingestion of fluoride-containing cleaning agents have been associated with low serum calcium levels. In this case, hypocalcemia is thought to be due to excessive rates of skeletal mineralization secondary to formation of calcium difluoride complex.
Proton pump inhibitors (PPIs) and histamine-2 receptor blockers (eg, cimetidine) reduce gastric acid production; this slows fat breakdown, which is necessary to complex calcium for gut absorption. An association with these medicines and an increased risk for hip fractures in elderly patients has been made because of decreased calcium absorption.
Other medication effects that may lead to hypocalcemia are as follows:
- Calcitonin and bisphosphonates cause chelation and end-organ inhibition
- Ethylene glycol complexes with calcium
- Estrogen inhibits bone resorption
- Aluminum and alcohol suppress PTH
Enhanced protein binding and anion chelation
Protein binding is enhanced by elevated pH and free fatty acid release in high catecholamine states. Anion chelation is seen in high phosphate states (eg, kidney failure, rhabdomyolysis, mesenteric ischemia, oral administration of phosphate-containing enemas); high citrate states (eg, massive blood transfusion, radiocontrast dyes); and high bicarbonate, lactate, and oxalate levels.
Hypocalcemia in the emergency department
Multifactorial causes are probably the most clinically relevant in hypocalcemic emergencies in the emergency department (ED). These include the following:
- Rhabdomyolysis: increased phosphates from creatine phosphokinase (CPK) and other anions (ie, lactate, bicarbonate) chelate calcium
- Toxic shock syndrome can cause hypocalcemia
- High calcitonin levels cause low calcium
- Malignancy: osteoblastic metastases (eg, breast cancer, prostate cancer) and tumor lysis syndrome may cause hypocalcemia (by differing mechanisms)
- Infiltrative disease: sarcoidosis, tuberculosis, and hemochromatosis may infiltrate the parathyroids, causing dysfunction
- Toxicologic causes include hydrofluoric acid burn or ingestion
- Trauma patients with severe hemorrhage can present with hypocalcemia, which can be worsened by transfusion and resuscitation, and which can contribute to the potentially lethal triad of acidosis, coagulopathy, and hypothermia. [29, 30]
Critical illness and severe sepsis
Acute illness may lead to hypocalcemia for multiple reasons. In one study, the 3 most common factors identified in patients with hypocalcemia associated with acute illness were hypomagnesemia, acute kidney injury, and transfusions.
In gram-negative sepsis, there is a reduction in total and ionized serum calcium. The mechanism for this remains unknown, but it appears to be associated with multiple factors, including elevated levels of cytokines (eg, interleukin-6, interleukin-1, TNF-alpha), hypoparathyroidism, and vitamin D deficiency or resistance.
Mortality rates are increased in patients with sepsis and hypocalcemia, compared with patients who are normocalcemic. [31, 32] However, there is no clear evidence that treating critically ill patients with supplemental calcium alters outcomes. [33]
Low levels of both ionized and total calcium have been reported in COVID-19 patients. Lower calcium levels correlate with increased COVID-19 severity, and hypocalcemia may serve as an independent risk factor for worse clinical outcome. di Filippo et al found a higher rate of hypocalcemia with lower calcium levels in hospitalized patients with COVID-19 than in patients with non–COVID-19 acute respiratory infections, suggesting that hypocalcemia in COVID-19 is a distinctive feature of the disease rather than simply a marker of respiratory disease severity. [34]
Postsurgical effects
The following surgical procedures may result in hypocalcemia:
- Parathyroidectomy causes a transient hypocalcemia due to end-organ PTH resistance in the first postoperative day; in addition, vascular/parathyroid injury may occur as an operative mishap. Postoperative oral calcium supplementation, with dosing based on a protocol that considers patient variables affecting risk, can prevent postoperative hypocalcemia in almost all cases. [35]
- Pancreatectomy prevents calcium absorption in the duodenum and the jejunum by eliminating necessary enzymes
- Bowel resection may cause hypocalcemia by reducing the surface available to absorb fatty acids and calcium