Diagnostics , Endocrinology

Canine Pituitary Dependent Hyperadrenocorticism Series, Part 2: Diagnostic Approach

Canine Pituitary Dependent Hyperadrenocorticism Series, Part 2: Diagnostic Approach
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David Bruyette, DVM, Diplomate ACVIM
VCA West Los Angeles Animal Hospital, Los Angeles, California, and
Veterinary Diagnostic Investigation and Consultation, Woodland Hills, California

Canine pituitary dependent hyperadrenocorticism (PDH), also known as Cushing’s disease, is a common endocrine disorder in older dogs. This disorder is caused by a pituitary adenoma (PA) that secretes inappropriate amounts of adrenocorticotropic hormone (ACTH), which results in bilateral adrenal hyperplasia and disorderly and excessive production of cortisol by the adrenal gland.

Read Part 1 of this series—Comparative Epidemiology & Etiology in Dogs & Humans (November/December 2015)—at tvpjournal.com. This article briefly described the diagnosis of PDH, including clinical signs, common laboratory findings, and atypical presentations of canine PDH.

ACVIM Consensus Statement

In 2012, the American College of Veterinary Internal Medicine (acvim.org) issued a consensus statement, Diagnosis of Spontaneous Canine Hyperadrenocorticism, that provides a thorough review of the diagnostic approach to patients with PDH and addresses many common clinical concerns.1 Access this statement at onlinelibrary.wiley.com/doi/10.1111/jvim.12192/epdf.

BASELINE DIAGNOSTICS

In all patients being screened for PDH, the following initial diagnostics should be performed prior to endocrine diagnostics:

  • Thorough history, including prior treatment with systemic or topical glucocorticoids
  • Physical examination (Table 1)
  • Complete routine database, including complete blood count, serum biochemical profile, urinalysis, urine culture, and blood pressure (Table 2).

These diagnostics are important as the clinical signs of PDH are rarely pathognomonic, and patients are generally older and may have comorbidities that affect endocrine function tests (Table 3) and impact therapeutic options and prognosis.

T1601F03Table01

T1601F03Table02
T1601F03Table03

ENDOCRINE DIAGNOSTICS

Specific endocrine tests and imaging modalities are available to both diagnose PDH (Table 3) and distinguish between the various causes of hyperadrenocorticism (HAC). No single test is perfect and, if the initial screening test is negative and high clinical suspicion of PDH exists, additional tests should be performed to determine a definitive diagnosis.

Several endocrine screening tests are available to arrive at a diagnosis of HAC, including:

  • Low-dose dexamethasone suppression (LDDS)
  • ACTH stimulation
  • Urine cortisol to creatinine ratio (UCCR).

Additional tests may be required to differentiate PDH from other causes of hypercortisolemia, such as endogenous ACTH measurement and advanced imaging.

If a patient has a concurrent serious illness, postpone testing until the illness or injury has resolved or been controlled to minimize false positive test results.

INITIAL ENDOCRINE SCREENING

Low-Dose Dexamethasone Suppression

LDDS demonstrates decreased pituitary sensitivity to negative feedback from glucocorticoids, via mechanisms discussed in the first article in this series.

Indications. Most consider LDDS the screening test of choice for HAC unless the patient history suggests iatrogenic HAC, in which case ACTH stimulation is preferred.

Sensitivity/Specificity. In veterinary medicine, the reported sensitivity and specificity of the LDDS test range from 85% to 100% and from 44% to 73%, respectively.2-10

Test Results. Blood samples are obtained (1) before, (2) 4 hours after, and (3) 8 hours after dexamethasone administration (0.01 mg/kg IV). Diagnosis of HAC is based on lack of suppression of cortisol concentration 8 hours after dexamethasone administration.

ACTH Stimulation

ACTH stimulation assesses adrenocortical reserve. Due to greater purity and quality control, use of synthetic ACTH is recommended. Use of compounded ACTH is discouraged, especially when monitoring patients on adrenolytic agents or adrenal enzyme blockers (see Synthetic Versus Compounded ACTH).

Indications. ACTH stimulation is the gold standard for diagnosis of iatrogenic HAC and spontaneous Addison’s disease (hypoadrenocorticism). Diagnosis of HAC is based on finding an elevated cortisol concentration (post ACTH administration) based on the reference range established by the laboratory.

Sensitivity/Specificity. Sensitivity of ACTH stimulation for all forms of spontaneous canine HAC ranges from 57% to 95%. In dogs with PDH, sensitivity is 80% to 83%. Specificity ranges from 59% to 93%.11-18

Due to its low sensitivity, it is inferior to LDDS as a screening test for spontaneous HAC. However, many clinicians still use ACTH stimulation because of its convenient study duration of 60 minutes and relative effectiveness in the clinical setting, especially when combined with abdominal ultrasound evaluation and interpreted in light of the history and physical examination.

Synthetic Versus Compounded ACTH

Synthetic polypeptides, such as Cortrosyn (cosyntropin) or Synacthen (tetracosactrin), contain the biologically active first 24 amino acids of ACTH; however, their potencies have not been compared.

In several studies, after administration of cosyntropin (5 mcg/kg or 250 mcg/dog IV or IM), peak cortisol concentrations occurred at 60 to 90 minutes. After administration of 5 mcg/kg IV, no difference was detected between 60- and 90-minute cortisol concentrations.13-16

Cosyntropin can be reconstituted, divided into aliquots in plastic syringes, and frozen at -20°C for 6 months.19 Whether tetracosactrin can be frozen has not been investigated; according to the manufacturer, store it at temperatures from 2°C to 8°C.

Compounded ACTH products have been evaluated in healthy dogs. Sixty minutes after administration, cortisol concentrations were similar among 4 compounded products (2.2 U/kg IM) and cosyntropin (5 mcg/kg IV). However, at later times, cortisol concentrations varied considerably with the compounded products.13

Urine Cortisol to Creatinine Ratio

UCCR provides an integrated reflection of cortisol production, adjusting for fluctuations in blood concentrations. Determination of basal UCCRs can be performed alone or in tandem with other endocrine testing.

Indications. UCCR can be used as a screening test for hypercortisolemia, although a single positive result should not be overinterpreted. Adding oral dexamethasone suppression to UCCR testing has the advantage of potentially demonstrating both increased cortisol production and decreased sensitivity to glucocorticoid feedback.

Sensitivity/Specificity. When a single, random urine sample is collected in veterinary hospitals, reported sensitivity and specificity of UCCR for diagnosis of HAC ranges from 75% to 100% and 20% to 25%, respectively.20,21 In some dogs, there is considerable day-to-day variation in UCCR results.22

However, in dogs with physical and biochemical changes consistent with HAC, when 2 basal UCCRs were above the cut-off level:22

  • Sensitivity was 99%; 95% confidence interval (94%–100%)
  • Specificity was 77%; 95% confidence interval (64%–87%).

DIFFERENTIATING PDH FROM ADH: LABORATORY ANALYSIS

Given that PDH and adrenal dependent hyperadrenocorticism (ADH) are the most common forms of HAC, and that their treatment options and prognoses differ, it is important to recommend additional testing to determine the exact etiology of HAC. Several diagnostic modalities are commonly used to differentiate between PDH and ADH (Table 4):

  • Endogenous ACTH
  • Dexamethasone suppression
  • Dexamethasone suppression with UCCR.

Endogenous ACTH

Canine ACTH is secreted from the pituitary gland in an episodic, pulsatile fashion in both healthy dogs and those with PDH.1 A circadian rhythm has not been convincingly demonstrated, although one study reported higher plasma concentrations of canine ACTH (cACTH) in late afternoon than in the morning.23
Indications. Concentrations of cACTH do not differ between healthy dogs and those with PDH, and its measurement is not useful to screen for HAC. However, measurement of cACTH is the most accurate stand-alone biochemical test for differentiating PDH from an adrenocortical tumor (AT), but the sensitivity of the assay differs with methodology. Normal or elevated concentrations of cACTH are consistent with PDH, while suppressed values are consistent with ADH.

Sensitivity/Specificity. The most common problem with the cACTH assay is poor sensitivity. The largest study of cACTH in dogs with HAC used a 2-site solid-phase chemiluminescent immunometric assay (Immulite 2000 Immunoassay System for ACTH; healthcare.siemens.com) and showed excellent discrimination between PDH and AT.

The likelihood of falsely low ACTH values in dogs with PDH is increased by:

  • Intra-assay and interassay variability (increased at lower cACTH concentrations)
  • Pulsatile ACTH secretion
  • Inappropriate sample handling allowing ACTH degradation.23-28

Dexamethasone Suppression

Dexamethasone administration in:

  • Normal dogs: Causes rapid and prolonged suppression of cortisol secretion
  • Patients with an AT: At any dosage does not suppress cortisol secretion
  • Dogs with PDH:2,29
  • Does not appropriately suppress ACTH secretion (therefore does not suppress cortisol) when a low dose (0.01 mg/kg) is administered
  • In 75% of dogs with PDH, ACTH and cortisol concentrations decrease when a high dose (0.1 mg/kg) is administered
  • In 25% of dogs with PDH, suppression of ACTH and cortisol does not occur even after administration of higher dosages; in these patients, a large pituitary tumor or a tumor developing from the pars intermedia is more likely.

A description of how to perform dexamethasone suppression tests is outlined in Table 4. The largest study evaluating both suppression tests—LDDS and high-dose dexamethasone suppression (HDDS)—included dogs with PDH (n = 181) and ATs (n = 35).2 With LDDS, criteria for identifying dogs with PDH included:

  • 4-hour post LDDS cortisol concentrations below laboratory cutoff or < 50% of basal cortisol concentration
  • 8-hour post LDDS cortisol concentrations < 50% of the basal cortisol concentration and greater than the laboratory cutoff.

T1601F03Table04

With HDDS, criteria for cortisol suppression were a 4- and/or 8-hour cortisol concentration below the laboratory cutoff or < 50% of the basal cortisol concentration.

Approximately 75% of dogs with PDH met at least one criterion for suppression on either LDDS (88%) or HDDS (12%).2

Dexamethasone resistance (ie, no criteria were met) occurred in all dogs with AT and the remainder (25%) of the dogs with PDH.2 In another study of 41 dogs with ATs, 28 LDDS and 30 HDDS tests were performed, with no suppression seen on any test.2,30

In dogs demonstrating lack of suppression with LDDS, use of endogenous ACTH rather than HDDS is recommended to differentiate PDH from ADH. Since suppression in response to dexamethasone supports a diagnosis of PDH, a dog with dexamethasone resistance can have either AT or PDH.

Dexamethasone Suppression with UCCR

Decreased blood cortisol concentration after dexamethasone administration is reflected in decreased UCCR.

After the patient’s owner/handler collects a morning urine sample on 2 consecutive days, 3 doses of dexamethasone (0.1 mg/kg PO) are administered at 6 to 8 hour intervals, with a third urine sample collected the next morning.

Decrease in the third UCCR to < 50% of the mean cortisol basal values is consistent with PDH. Lack of suppression does not confirm AT.

In 160 dogs with HAC (49 with ATs, 111 with PDH), the UCCR in 72% of dogs with PDH suppressed to < 50% of the basal UCCR, while the other 28% of those with PDH were dexamethasone-resistant. In dogs with ATs, maximum suppression was 44% of the baseline sample.31

Evaluation of the Pituitary–Adrenal Axis

Evaluation of the pituitary-adrenal axis is indicated in the following circumstances:

  • Patients with clinical signs and laboratory findings consistent with PDH and in which nonadrenal illness has been ruled out or is well controlled.
  • Patients in which an adrenal/pituitary mass or bilateral adrenal hyperplasia has been discovered in conjunction with compatible clinical signs.
  • Patients with an incidentally discovered adrenal mass, with adrenalectomy being considered.
  • Diabetic dogs with insulin resistance.

DIFFERENTIATING PDH FROM ADH: IMAGING

While imaging can be very helpful in differentiating PDH from ADH, it cannot be used to establish a diagnosis of HAC. Moreover, finding normal adrenal glands on imaging studies does not rule out HAC.

Radiography

Imaging results may include:

  • Abdominal distension
  • Good contrast due to abdominal fat deposition
  • Hepatomegaly
  • Bladder distension
  • Mineralization of bronchi and pulmonary interstitium, and of dermal and subcutaneous tissues in areas predisposed to calcinosis cutis.

A small liver makes HAC unlikely. An AT may be visualized either due to mass effect or tumor calcification.32,33

Adrenal Gland Imaging

Adrenal gland width is the most informative parameter identified on ultrasonography (Figure 1). However, the following may affect correct measurement:

  • Long axis of adrenal gland often is misaligned with either the medial or dorsal plane of the body
  • Cross-sectional images may lead to oblique views and miscalculation of glandular dimensions
  • Breed and body size differences
  • Macronodular hyperplasia (a rare form of PDH) and some ATs can be difficult to differentiate.
T1601F03_Fig01

FIGURE 1. Ultrasound image of adrenal adenoma.

Test Results. In dogs with PDH, ultrasonography reveals normal sized or enlarged adrenal glands that are typically symmetrical; however, mild asymmetry may occur. In dogs with ATs, ultrasonography reveals moderate asymmetry, contralateral adrenocortical atrophy (adrenal width < 4–5 mm), destruction of normal tissue architecture, or some combination of these findings.34,35

Ultrasonography can also estimate AT size and possibly vascular or local soft tissue invasion. Although most ATs are unilateral, bilateral tumors may occur and in these patients, endogenous ACTH concentrations should be determined.

Metastasis. When an AT has been confirmed, certain thoracic and ultrasonographic findings suggest malignancy, including:

  • Adrenal gland width > 4 cm
  • Invasion into the vena cava or adjacent tissues.

However, computed tomography (CT) (Figure 2) and magnetic resonance imaging (MRI) are more sensitive techniques to identify vascular invasion and detect metastases.36

FIGURE 2. CT image of large right adrenal adenoma between the right kidney and caudal vena cava.

FIGURE 2. CT image of large right adrenal adenoma between the right kidney and caudal vena cava.

Adrenalectomy should not be performed without confirming the presence of an AT (and atrophy of contralateral adrenal gland) by abdominal ultrasonography (Figure 3), CT, MRI, or some combination of these. Metastasis can be confirmed by ultrasound-guided biopsy, but differentiating benign from malignant AT often is difficult, even with histopathologic examination.

FIGURE 3. Ultrasound (A) and surgical view (B) of adrenal adenoma.

FIGURE 3. Ultrasound (A) and surgical view (B) of adrenal adenoma.

Pituitary Imaging

Pituitary imaging provides valuable information regarding treatment options and prognosis.37 Pituitary lesions range from microscopic nests of hyperplastic cells to large tumors. Absence of neurologic abnormalities does not exclude pituitary macrotumors (ie, tumors that are > 1 cm in diameter, extend above the sella turcica, or have a pituitary:brain ratio of > 0.31).

Indications. Pituitary imaging should be considered for all dogs at time of PDH diagnosis, especially if hypophysectomy or radiation therapy is being considered. If clinical features suggest a pituitary macrotumor, confirmation requires imaging; clinical signs include:

  • Disorientation and aimless wandering
  • Severe polyuria/polydipsia
  • Lethargy
  • Hyporexia to anorexia
  • Visual impairment
  • Seizures (in some patients).

Test Results. Because pituitary lesions may be quite small, contrast-enhanced CT and MRI (Figure 4–6) may identify normal sized pituitary glands in dogs with PDH. However, dynamic contrast-enhanced CT takes advantage of the pituitary gland’s blood supply:

  • The posterior pituitary gland’s blood supply is direct (arterial)
  • The anterior pituitary gland’s blood supply is mainly indirect via the pituitary portal system.
FIGURE 4. Axial (A) and sagittal (B) T1 post contrast MRI images from a dog with PDH and large pituitary macroadenoma.

FIGURE 4. Axial (A) and sagittal (B) T1 post contrast MRI images from a dog with PDH and large pituitary macroadenoma.

FIGURE 5. Axial (A) and sagittal (B) T1 post contrast MRI images from a dog with PDH prior to surgery. Note the pituitary (arrows).

FIGURE 5. Axial (A) and sagittal (B) T1 post contrast MRI images from a dog with PDH prior to surgery. Note the pituitary (arrows).

FIGURE 6. Axial (A) and sagittal (B) T1 post contrast MRI images from dog in Figure 5 after surgery.

FIGURE 6. Axial (A) and sagittal (B) T1 post contrast MRI images from dog in Figure 5 after surgery.

In dogs with normal pituitary glands, after IV administration of contrast medium, the posterior pituitary gland can be identified first—this phase is called the “pituitary flush.” Its absence indicates atrophy of the posterior pituitary gland due to compression by a pituitary tumor. Displacement or distortion of the flush can be used to identify and localize anterior pituitary microtumors.

Dorsal displacement and decreased signal intensity of the posterior lobe on T1-weighted MRI indicates the presence of a microtumor.38,39

IN SUMMARY

Diagnosis of PDH requires incorporating information from the history, physical examination, and routine laboratory tests. Specific endocrine tests and imaging modalities are available to diagnose HAC and distinguish between the various causes of hypercortisolism. No single test is perfect and, if the initial screening test is negative and high clinical suspicion of HAC exists, additional tests should be performed. Endocrine evaluation of patients with HAC and nonadrenal illness can be difficult, and it is important to eliminate or manage the concurrent illness before undertaking adrenal function tests.

ACTH = adrenocorticotropic hormone; ADH = adrenal dependent hyperadrenocorticism; AT = adrenocortical tumor; cACTH = canine ACTH; CT = computed tomography; HAC = hyperadrenocorticism; HDDS = high-dose dexamethasone suppression; LDDS = low-dose dexamethasone suppression; MRI = magnetic resonance imaging; PA = pituitary adenoma; PDH = pituitary dependent hyperadrenocorticism; UCCR = urine cortisol to creatinine ratio

References

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  38. van der Vlugt-Meijer RH, Meij BP, van den Ingh TSGAM, et al. Dynamic computed tomography of the pituitary gland in dogs with pituitary-dependent hyperadrenocorticism. J Vet Intern Med 2003; 17:773-780.
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Author_D-BruyetteDavid Bruyette, DVM, Diplomate ACVIM, is the medical director at VCA West Los Angeles Animal Hospital and President and CEO of Veterinary Diagnostic Investigation and Consultation. He was an assistant professor and head of internal medicine at Kansas State University and director of its Analytical Chemistry Laboratory. Dr. Bruyette received his DVM from University of Missouri and completed an internship at Purdue University and residency in internal medicine at University of California–Davis. He then became a staff internist at West Los Angeles Veterinary Medical Group and member of the Department of Comparative Medicine at Stanford University.

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id='choice_6_15_2' /> <label for='choice_6_15_2' id='label_6_15_2'>Today's Veterinary Business eNewsletter<br><div style="font-size: 12px; color: #808080;">Covers topics relating to practice management, financial metrics, marketing, retailing and merchandising, and industry news.</div></label> </li><li class='gchoice_6_15_3'> <input name='input_15.3' type='checkbox' value='Today&#039;s Veterinary Nurse eNewsletter&lt;br&gt;&lt;div style=&quot;font-size: 12px;color: #808080&quot;&gt;Provides practical, peer-reviewed companion animal educational CE for veterinary nurses, technicians and assistants.&lt;/div&gt;' id='choice_6_15_3' /> <label for='choice_6_15_3' id='label_6_15_3'>Today's Veterinary Nurse eNewsletter<br><div style="font-size: 12px; color: #808080;">Provides practical, peer-reviewed companion animal educational CE for veterinary nurses, technicians and assistants.</div></label> </li><li class='gchoice_6_15_4'> <input name='input_15.4' type='checkbox' value='Today&#039;s Veterinary Practice eNewsletter&lt;br&gt;&lt;div style=&quot;font-size: 12px;color: #808080&quot;&gt;Provides practical, peer-reviewed articles focused on the latest diagnostic and treatment techniques to enhance your knowledge and confidence.&lt;/div&gt;' id='choice_6_15_4' /> <label for='choice_6_15_4' id='label_6_15_4'>Today's Veterinary Practice eNewsletter<br><div style="font-size: 12px; color: #808080;">Provides practical, peer-reviewed articles focused on the latest diagnostic and treatment techniques to enhance your knowledge and confidence.</div></label> </li><li class='gchoice_6_15_5'> <input name='input_15.5' type='checkbox' value='VetFolio eNewsletter&lt;br&gt;&lt;div style=&quot;font-size: 12px;color: #808080&quot;&gt;Discover online CE resources offered in a variety of formats including videos, podcasts, webinars and more.&lt;/div&gt;' id='choice_6_15_5' /> <label for='choice_6_15_5' id='label_6_15_5'>VetFolio eNewsletter<br><div style="font-size: 12px; color: #808080;">Discover online CE resources offered in a variety of formats including videos, podcasts, webinars and more.</div></label> </li><li class='gchoice_6_15_6'> <input name='input_15.6' type='checkbox' value='Partner Emails&lt;br&gt;&lt;div style=&quot;font-size: 12px;color: #808080&quot;&gt;Exclusive deals and information from our partners.&lt;/div&gt;' id='choice_6_15_6' /> <label for='choice_6_15_6' id='label_6_15_6'>Partner Emails<br><div style="font-size: 12px; color: #808080;">Exclusive deals and information from our partners.</div></label> </li></ul></div></li><li id='field_6_19' class='gfield gfield_html gfield_html_formatted field_sublabel_below field_description_below gfield_visibility_visible' ><br></li><li id='field_6_22' class='gfield field_sublabel_below field_description_below gfield_visibility_visible' ><label class='gfield_label' >Do you want to be added to our postal mailing list?</label><div class='ginput_container ginput_container_checkbox'><ul class='gfield_checkbox' id='input_6_22'><li class='gchoice_6_22_1'> <input name='input_22.1' type='checkbox' value='Yes, I love mail!' id='choice_6_22_1' /> <label for='choice_6_22_1' id='label_6_22_1'>Yes, I love mail!</label> </li><li class='gchoice_6_22_2'> <input name='input_22.2' type='checkbox' value='No thank you.' id='choice_6_22_2' /> <label for='choice_6_22_2' id='label_6_22_2'>No thank you.</label> </li></ul></div></li><li id='field_6_10' class='gfield gfield_contains_required field_sublabel_below field_description_below gfield_visibility_visible' ><label class='gfield_label gfield_label_before_complex' >Please provide your mailing address below.<span class='gfield_required'>*</span></label> <div class='ginput_complex ginput_container has_street has_street2 has_city has_state has_zip has_country ginput_container_address' id='input_6_10' > <span class='ginput_full address_line_1' id='input_6_10_1_container' > <input type='text' name='input_10.1' id='input_6_10_1' value='' aria-required="true"/> <label for='input_6_10_1' id='input_6_10_1_label' >Street Address</label> </span><span class='ginput_full address_line_2' id='input_6_10_2_container' > <input type='text' name='input_10.2' id='input_6_10_2' value='' /> <label for='input_6_10_2' id='input_6_10_2_label' >Address Line 2</label> </span><span class='ginput_left address_city' id='input_6_10_3_container' > <input type='text' name='input_10.3' id='input_6_10_3' value='' aria-required="true"/> <label for='input_6_10_3' id='input_6_10_3_label' >City</label> </span><span class='ginput_right address_state' id='input_6_10_4_container' > <input type='text' name='input_10.4' id='input_6_10_4' value='' aria-required="true"/> <label for='input_6_10_4' id='input_6_10_4_label' >State / Province / Region</label> </span><span class='ginput_left address_zip' id='input_6_10_5_container' > <input type='text' name='input_10.5' id='input_6_10_5' value='' aria-required="true"/> <label for='input_6_10_5' id='input_6_10_5_label' >ZIP / Postal Code</label> </span><span class='ginput_right address_country' id='input_6_10_6_container' > <select name='input_10.6' id='input_6_10_6' aria-required="true"><option value='' selected='selected'></option><option value='Afghanistan' >Afghanistan</option><option value='Åland Islands' >Åland Islands</option><option value='Albania' >Albania</option><option value='Algeria' >Algeria</option><option value='American Samoa' >American Samoa</option><option value='Andorra' >Andorra</option><option value='Angola' >Angola</option><option value='Anguilla' >Anguilla</option><option value='Antarctica' >Antarctica</option><option value='Antigua and Barbuda' >Antigua and Barbuda</option><option value='Argentina' >Argentina</option><option value='Armenia' >Armenia</option><option value='Aruba' >Aruba</option><option value='Australia' >Australia</option><option value='Austria' >Austria</option><option value='Azerbaijan' >Azerbaijan</option><option value='Bahamas' >Bahamas</option><option value='Bahrain' >Bahrain</option><option value='Bangladesh' >Bangladesh</option><option value='Barbados' >Barbados</option><option value='Belarus' >Belarus</option><option value='Belgium' >Belgium</option><option value='Belize' >Belize</option><option value='Benin' >Benin</option><option value='Bermuda' >Bermuda</option><option value='Bhutan' >Bhutan</option><option value='Bolivia' >Bolivia</option><option value='Bonaire, Sint Eustatius and Saba' >Bonaire, Sint Eustatius and Saba</option><option value='Bosnia and Herzegovina' >Bosnia and Herzegovina</option><option value='Botswana' >Botswana</option><option value='Bouvet Island' >Bouvet Island</option><option value='Brazil' >Brazil</option><option value='British Indian Ocean Territory' >British Indian Ocean Territory</option><option value='Brunei Darussalam' >Brunei Darussalam</option><option value='Bulgaria' >Bulgaria</option><option value='Burkina Faso' >Burkina Faso</option><option value='Burundi' >Burundi</option><option value='Cambodia' >Cambodia</option><option value='Cameroon' >Cameroon</option><option value='Canada' >Canada</option><option value='Cape Verde' >Cape Verde</option><option value='Cayman Islands' >Cayman Islands</option><option value='Central African Republic' >Central African Republic</option><option value='Chad' >Chad</option><option value='Chile' >Chile</option><option value='China' >China</option><option value='Christmas Island' >Christmas Island</option><option value='Cocos Islands' >Cocos Islands</option><option value='Colombia' >Colombia</option><option value='Comoros' >Comoros</option><option value='Congo, Democratic Republic of the' >Congo, Democratic Republic of the</option><option value='Congo, Republic of the' >Congo, Republic of the</option><option value='Cook Islands' >Cook Islands</option><option value='Costa Rica' >Costa Rica</option><option value='Côte d&#039;Ivoire' >Côte d&#039;Ivoire</option><option value='Croatia' >Croatia</option><option value='Cuba' >Cuba</option><option value='Curaçao' >Curaçao</option><option value='Cyprus' >Cyprus</option><option value='Czech Republic' >Czech Republic</option><option value='Denmark' >Denmark</option><option value='Djibouti' >Djibouti</option><option value='Dominica' >Dominica</option><option value='Dominican Republic' >Dominican Republic</option><option value='Ecuador' >Ecuador</option><option value='Egypt' >Egypt</option><option value='El Salvador' >El Salvador</option><option value='Equatorial Guinea' >Equatorial Guinea</option><option value='Eritrea' >Eritrea</option><option value='Estonia' >Estonia</option><option value='Eswatini (Swaziland)' >Eswatini (Swaziland)</option><option value='Ethiopia' >Ethiopia</option><option value='Falkland Islands' >Falkland Islands</option><option value='Faroe Islands' >Faroe Islands</option><option value='Fiji' >Fiji</option><option value='Finland' >Finland</option><option value='France' >France</option><option value='French Guiana' >French Guiana</option><option value='French Polynesia' >French Polynesia</option><option value='French Southern Territories' >French Southern Territories</option><option value='Gabon' >Gabon</option><option value='Gambia' >Gambia</option><option value='Georgia' >Georgia</option><option value='Germany' >Germany</option><option value='Ghana' >Ghana</option><option value='Gibraltar' >Gibraltar</option><option value='Greece' >Greece</option><option value='Greenland' >Greenland</option><option value='Grenada' >Grenada</option><option value='Guadeloupe' >Guadeloupe</option><option value='Guam' >Guam</option><option value='Guatemala' >Guatemala</option><option value='Guernsey' >Guernsey</option><option value='Guinea' >Guinea</option><option value='Guinea-Bissau' >Guinea-Bissau</option><option value='Guyana' >Guyana</option><option value='Haiti' >Haiti</option><option value='Heard and McDonald Islands' >Heard and McDonald Islands</option><option value='Holy See' >Holy See</option><option value='Honduras' >Honduras</option><option value='Hong Kong' >Hong Kong</option><option value='Hungary' >Hungary</option><option value='Iceland' >Iceland</option><option value='India' >India</option><option value='Indonesia' >Indonesia</option><option value='Iran' >Iran</option><option value='Iraq' >Iraq</option><option value='Ireland' >Ireland</option><option value='Isle of Man' >Isle of Man</option><option value='Israel' >Israel</option><option value='Italy' >Italy</option><option value='Jamaica' >Jamaica</option><option value='Japan' >Japan</option><option value='Jersey' >Jersey</option><option value='Jordan' >Jordan</option><option value='Kazakhstan' >Kazakhstan</option><option value='Kenya' >Kenya</option><option value='Kiribati' >Kiribati</option><option value='Kuwait' >Kuwait</option><option value='Kyrgyzstan' >Kyrgyzstan</option><option value='Lao People&#039;s Democratic Republic' >Lao People&#039;s Democratic Republic</option><option value='Latvia' >Latvia</option><option value='Lebanon' >Lebanon</option><option value='Lesotho' >Lesotho</option><option value='Liberia' >Liberia</option><option value='Libya' >Libya</option><option value='Liechtenstein' >Liechtenstein</option><option value='Lithuania' >Lithuania</option><option value='Luxembourg' >Luxembourg</option><option value='Macau' >Macau</option><option value='Macedonia' >Macedonia</option><option value='Madagascar' >Madagascar</option><option value='Malawi' >Malawi</option><option value='Malaysia' >Malaysia</option><option value='Maldives' >Maldives</option><option value='Mali' >Mali</option><option value='Malta' >Malta</option><option value='Marshall Islands' >Marshall Islands</option><option value='Martinique' >Martinique</option><option value='Mauritania' >Mauritania</option><option value='Mauritius' >Mauritius</option><option value='Mayotte' >Mayotte</option><option value='Mexico' >Mexico</option><option value='Micronesia' >Micronesia</option><option value='Moldova' >Moldova</option><option value='Monaco' >Monaco</option><option value='Mongolia' >Mongolia</option><option value='Montenegro' >Montenegro</option><option value='Montserrat' >Montserrat</option><option value='Morocco' >Morocco</option><option value='Mozambique' >Mozambique</option><option value='Myanmar' >Myanmar</option><option value='Namibia' >Namibia</option><option value='Nauru' >Nauru</option><option value='Nepal' >Nepal</option><option value='Netherlands' >Netherlands</option><option value='New Caledonia' >New Caledonia</option><option value='New Zealand' >New Zealand</option><option value='Nicaragua' >Nicaragua</option><option value='Niger' >Niger</option><option value='Nigeria' >Nigeria</option><option value='Niue' >Niue</option><option value='Norfolk Island' >Norfolk Island</option><option value='North Korea' >North Korea</option><option value='Northern Mariana Islands' >Northern Mariana Islands</option><option value='Norway' >Norway</option><option value='Oman' >Oman</option><option value='Pakistan' >Pakistan</option><option value='Palau' >Palau</option><option value='Palestine, State of' >Palestine, State of</option><option value='Panama' >Panama</option><option value='Papua New Guinea' >Papua New Guinea</option><option value='Paraguay' >Paraguay</option><option value='Peru' >Peru</option><option value='Philippines' >Philippines</option><option value='Pitcairn' >Pitcairn</option><option value='Poland' >Poland</option><option value='Portugal' >Portugal</option><option value='Puerto Rico' >Puerto Rico</option><option value='Qatar' >Qatar</option><option value='Réunion' >Réunion</option><option value='Romania' >Romania</option><option value='Russia' >Russia</option><option value='Rwanda' >Rwanda</option><option value='Saint Barthélemy' >Saint Barthélemy</option><option value='Saint Helena' >Saint Helena</option><option value='Saint Kitts and Nevis' >Saint Kitts and Nevis</option><option value='Saint Lucia' >Saint Lucia</option><option value='Saint Martin' >Saint Martin</option><option value='Saint Pierre and Miquelon' >Saint Pierre and Miquelon</option><option value='Saint Vincent and the Grenadines' >Saint Vincent and the Grenadines</option><option value='Samoa' >Samoa</option><option value='San Marino' >San Marino</option><option value='Sao Tome and Principe' >Sao Tome and Principe</option><option value='Saudi Arabia' >Saudi Arabia</option><option value='Senegal' >Senegal</option><option value='Serbia' >Serbia</option><option value='Seychelles' >Seychelles</option><option value='Sierra Leone' >Sierra Leone</option><option value='Singapore' >Singapore</option><option value='Sint Maarten' >Sint Maarten</option><option value='Slovakia' >Slovakia</option><option value='Slovenia' >Slovenia</option><option value='Solomon Islands' >Solomon Islands</option><option value='Somalia' >Somalia</option><option value='South Africa' >South Africa</option><option value='South Georgia' >South Georgia</option><option value='South Korea' >South Korea</option><option value='South Sudan' >South Sudan</option><option value='Spain' >Spain</option><option value='Sri Lanka' >Sri Lanka</option><option value='Sudan' >Sudan</option><option value='Suriname' >Suriname</option><option value='Svalbard and Jan Mayen Islands' >Svalbard and Jan Mayen Islands</option><option value='Sweden' >Sweden</option><option value='Switzerland' >Switzerland</option><option value='Syria' >Syria</option><option value='Taiwan' >Taiwan</option><option value='Tajikistan' >Tajikistan</option><option value='Tanzania' >Tanzania</option><option value='Thailand' >Thailand</option><option value='Timor-Leste' >Timor-Leste</option><option value='Togo' >Togo</option><option value='Tokelau' >Tokelau</option><option value='Tonga' >Tonga</option><option value='Trinidad and Tobago' >Trinidad and Tobago</option><option value='Tunisia' >Tunisia</option><option value='Turkey' >Turkey</option><option value='Turkmenistan' >Turkmenistan</option><option value='Turks and Caicos Islands' >Turks and Caicos Islands</option><option value='Tuvalu' >Tuvalu</option><option value='Uganda' >Uganda</option><option value='Ukraine' >Ukraine</option><option value='United Arab Emirates' >United Arab Emirates</option><option value='United Kingdom' >United Kingdom</option><option value='United States' >United States</option><option value='Uruguay' >Uruguay</option><option value='US Minor Outlying Islands' >US Minor Outlying Islands</option><option value='Uzbekistan' >Uzbekistan</option><option value='Vanuatu' >Vanuatu</option><option value='Venezuela' >Venezuela</option><option value='Vietnam' >Vietnam</option><option value='Virgin Islands, British' >Virgin Islands, British</option><option value='Virgin Islands, U.S.' >Virgin Islands, U.S.</option><option value='Wallis and Futuna' >Wallis and Futuna</option><option value='Western Sahara' >Western Sahara</option><option value='Yemen' >Yemen</option><option value='Zambia' >Zambia</option><option value='Zimbabwe' 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