Dentistry , Management Strategies

Current Concepts in Periodontal Disease

Brook A. Niemiec DVM, DAVDC, DEVDC, FAVD

Dr. Niemiec is chief of staff of Veterinary Dental Specialties & Oral Surgery, with 14 offices throughout the United States. He is a regular speaker on local, national, and international levels and was elected Clinical Instructor of the Year for the 2016 Western Veterinary Conference. He has authored many articles, chapters, and books and founded the veterinary dental telemedicine website vetdentalrad.com. Finally, he coordinates the San Diego Vet Dental Training Center, with 3 to 4 meetings per year covering basic and intermediate veterinary dentistry.

Kymberley Stewart DVM

Dr. Stewart is a graduate of the Western College of Veterinary Medicine at the University of Saskatchewan. She was a member of the first Canadian graduating class in animal welfare at the University of British Columbia, and is passionate about furthering understanding of the veterinary applications of animal welfare. Dr. Stewart has authored several chapters on applied animal welfare, along with the welfare section of the WSAVA International Dental Guidelines. She is currently pursuing her board certification with the American College of Animal Welfare.

Current Concepts in Periodontal Disease
OPEN WIDE Infection from unchecked periodontal disease has several significant local and potentially systemic consequences. Igor Chus/Shutterstock.com
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Of the most common health problems of companion animals throughout their life, dental disease stands out as the number 1 concern. While studies from previous decades list the prevalence of periodontal disease in the 60% to 70% range,1-4 a 2018 study found that almost 90% of all canine patients had some degree of periodontal disease.5 Another 2018 study using more accurate diagnostics found evidence of periodontal disease in 100% of canine subjects and concluded that periodontal disease is underdiagnosed based on visual examination alone.6 In cats, the incidence is reported to be as high as 70% by 2 years old.7 Based on its chronicity, prevalence, and impact on overall health, dental disease was considered the number 1 health-related welfare concern in dogs in the United Kingdom in 2019.8

Sadly, many owners and veterinarians still misunderstand the significant effects of periodontal disease, believing them to be limited to bad breath and tooth loss. This lack of understanding, combined with improper or outdated diagnostic methods, can lead to delayed therapy at best and misdiagnosis at worst. Both of these situations are concerning, as significant pain and infection from unchecked periodontal disease have several local and potentially systemic consequences (Box 1). Intervention by veterinarians and educated owners is the only solution to improving health and alleviating distress in these patients.

BOX 1 Potential Consequences of Periodontal Disease
Local9
  • Oronasal fistulas
  • Class II periodontic-endodontic lesions
  • Pathologic fractures
  • Ocular problems
  • Osteomyelitis
  • Oral cancer

Systemic10

  • Renal, hepatic, and cardiac disease
  • Increased inflammatory markers
  • Anemia of chronic disease
  • Arthritis
  • Diabetes mellitus

PATHOGENESIS

There are two recognized stages to periodontal disease—gingivitis and periodontitis—but they often present concurrently. In the initial stage, gingivitis, the inflammation is confined to the gingiva. This is a reversible process. When gingivitis progresses due to lack of or inappropriate treatment, periodontitis typically ensues. Periodontitis is defined as an inflammatory disease of the deeper supporting structures of the tooth (the periodontal ligament and alveolar bone) that is caused by bacteria and their byproducts. Progressive destruction of the periodontal tissues leads to attachment loss. Periodontitis is considered an irreversible process, unless the patient is treated with advanced periodontal surgery techniques including guided tissue regeneration.

Periodontal disease begins with the formation of plaque.11 Plaque, one of many biofilms that naturally occur, is made up almost entirely of oral bacteria that adhere to the teeth and are held together by a matrix of extracellular polysaccharides and salivary glycoproteins. Plaque can be found on tooth surfaces within 24 hours of dental cleaning.

When plaque is visible on the surface of the tooth, it is known as supragingival plaque. Once it extends below the gumline, it is called subgingival plaque. While supragingival plaque is easier to see, the damaging effects of periodontal disease come from the presence of subgingival plaque within the gingival sulcus or periodontal pocket.12 Calculus, or tartar, is also relatively nonpathogenic. Therefore, control of supragingival plaque or tartar alone, as is found with non-anesthesia dentistry, is ineffective in controlling the progression of periodontal disease.5,13

When subgingival bacteria are able to proliferate, the combination of the inflammation produced by the bacteria themselves and the host’s own immune response begins the irreversible damage of periodontitis. Inflammation of the soft tissue weakens attachment, while osteoclastic activity decreases the bony support. Current studies suggest that there is a strong genetic component to periodontal disease, potentially related to the amount of damage attributed to the host response.2,13,14 Periodontal disease culminates in tooth loss; however, significant problems can precede tooth exfoliation.

CLINICAL FEATURES

Healthy gingiva should look coral pink and have a thin edge. When gingivitis starts, the first clinically notable sign is erythema of the gums, followed by halitosis and gingival edema (Figure 1). While color change is a reliable sign of disease, bleeding on probing, chewing, or brushing is now recognized as the earliest clinical sign of gingivitis (Figure 2).15,16

Dental calculus is often present alongside gingivitis, but plaque bacteria are the true cause of gingivitis and periodontal disease. Therefore, gingivitis can occur in the absence of calculus. By the same logic, widespread supragingival calculus may be notable, with little to no gingivitis accompanying it.17

The hallmark clinical feature of periodontitis is attachment loss. This is considered to be periodontal pocket formation and/or gingival recession >3 mm in dogs or >1 mm in cats.18 Both presentations of attachment loss can occur in the same patient and, occasionally, on the same tooth.

LOCAL CONSEQUENCES

One of the most common of the severe local consequences of periodontal disease is oronasal fistulation (Figure 3).9,19 Oronasal fistulas can occur in cats as well as any breed of dog, but they are typically found in older small- and toy-breed dogs. An oronasal fistula forms when periodontal disease progresses apically from the palatal surface of a maxillary tooth, most commonly a canine. While it can be apparent during a conscious oral examination, definitive diagnosis typically requires periodontal probing under general anesthesia. A fistula can exist even when the gingiva looks relatively healthy and the tooth is well attached; therefore, probing every aspect of every tooth in the mouth is a vital part of an oral examination. Appropriate treatment of a fistula entails extraction of the tooth and closure of the defect with a mucogingival flap.19

When periodontal disease progresses toward the apex of the tooth and bacteria gain access to the endodontic system through the apical delta, the result is a class II periodontal-endodontic lesion.18,20,21 In these cases, the affected tooth dies and the infection can then spread via the common pulp chamber to other root(s) (Figure 4).

In some patients with apical progression of severe periodontal disease, especially brachycephalic patients, the proximity of the tooth root apices of the maxillary molars and distal root of the fourth premolars allow for infection transmission into the area behind the globe. This can lead to infection and abscessation of the periorbital tissue of the eye and may result in eye loss or blindness.22,23

When chronic periodontal loss weakens the bone, pathologic fracture of the jaw can occur (Figure 5).18,24 This condition is seen almost exclusively in small- and toy-breed dogs, in which the teeth are large in proportion to the jaws, and most frequently affects the mandible around the canines and first molars. It occasionally affects the mandibular canine area in cats.

Chronic osteomyelitis or osteonecrosis (Figure 6) are well-known sequelae of periodontal disease.25 Once periodontal bacteria gain access to them, deeper bony tissues become infected and die. Necrotic bone no longer has a functioning blood supply, so it can no longer respond to antibiotic therapy. In patients with suspected osteonecrosis, aggressive surgical debridement is necessary and may require partial or complete mandibulectomy. These animals can live long and comfortable lives after surgery, providing disease has been completely addressed.

In people, chronic periodontal disease has also been linked to an increased incidence of oral cancer.26,27 While the mechanism for this is currently unknown, the chronic inflammatory state that exists with periodontitis is the likely cause. Further studies in veterinary medicine are needed to establish this relationship in dogs and cats.

SYSTEMIC CONSEQUENCES

Systemic health consequences of periodontal disease have seen a strong uptick in research over the last few decades. While no causal relationship has been identified, and much of the research is in human medicine, the evidence that periodontal disease has negative consequences on systemic health is mounting, based on the ability of oral bacteria to gain access to the bloodstream through inflamed periodontal tissue. Once the bacteria have access to the rest of the body, multiple negative sequelae are possible (Table 1).

While further veterinary studies are needed to fully investigate the deleterious effects periodontal disease can have on companion animals, studies in people have correlated poor periodontal health with increased rates of gastrointestinal, kidney, pancreatic, and hematologic cancers,46-48 as well as a major contributor to complications of diabetes mellitus.44,45 Periodontal disease has been shown to be a significant predictor of early mortality in humans,49-51 with one study reporting that severe periodontal disease is linked to a higher risk factor of early death than smoking.52

HEALTH AND WELFARE BENEFITS OF PERIODONTAL THERAPY

Veterinary patients require both doctors and owners to provide frequent, clinically effective dental care to support good health and quality of life. Owners, therefore, must be educated about the impact of periodontal disease on an animal’s health-based welfare.  Additionally, while it may seem counterintuitive, patients rarely show obvious behavioral changes in response to oral pain, so waiting for these signs simply lengthens time to appropriate therapy and increases the severity of disease for the patient. Veterinarians are considered leaders in the assessment and improvement of animal welfare globally;53 however, incorporating animal welfare conversations into daily practice can be challenging, especially when an animal’s needs differ from the client’s desires.

The Five Animal Welfare Needs (FAWN) framework (Box 2) provides veterinarians with a context in which patient welfare may be more easily evaluated and discussed with clients in language they can understand and embrace.54 The need to be protected from pain, suffering, injury, and disease is the most obvious FAWN element in the assessment of periodontal disease. Remembering the need for a suitable diet and the need to be able to exhibit normal behavior patterns may also lead to discussions that uncover potential improvements that can be realized through adequate dental care.

BOX 2 The Five Animal Welfare Needs54
1. Health: To be protected from suffering, injury, disease states, and pain, and to be treated if illness or injury occurs
2. Behavior: To behave in a normal species-specific manner (e.g., to dig, chew, scratch, play)
3. Companionship: To live with, or apart from, other animals as is appropriate to the species and individual animal’s preference
4. Diet: To be fed a biologically appropriate diet for the age, species, and activity level of the animal that provides adequate nourishment without obesity or poor body condition, and to have access to freely available fresh water
5. Environment: To live in a suitable, safe, comfortable environment that contains places to rest, hide, explore, and exercise

For a patient to truly benefit from dental care, both the veterinarian and owner must understand, accept, and incorporate the changes necessary to effectively control periodontal disease. Discussing ways that periodontal disease can negatively affect an animal’s daily welfare may help the pet owner understand how dental health affects their pet’s quantity and quality of life and increase compliance with treatment instructions.55

CONCLUSION

Patients with periodontal disease are exposed to oral bacteria in the systemic bloodstream daily, creating a state of chronic disease. Veterinarians and pet owners must learn to view periodontal disease as not merely a dental problem, but as an initiator of more severe local and systemic consequences. With this knowledge, both veterinary professionals and clients can feel confident they are making informed, welfare-centric decisions for the pet’s oral care.

Drs. Niemiec and Stewart are contributors to the WSAVA Global Dental Guidelines, which contain expanded information on periodontal disease. These guidelines are available at: wsava.org/global-guidelines/global-dental-guidelines.

References

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2. Marshall MD, Wallis CV, Milella L, et al. A longitudinal assessment of periodontal disease in 52 miniature schnauzers. BMC Vet Res
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3. Lund EM, Armstrong PJ, Kirk CA, et al. Health status and population characteristics of dogs and cats examined at private veterinary practices in the United States. JAVMA 1999;214(9):1336-1341.

4. Hoffmann T, Gaengler P. Clinical and pathomorphological investigation of spontaneously occurring periodontal disease in dogs. J Small Anim Pract 1996;37(10):471-479.

5. Stella JL, Bauer AE, Croney CC. A cross-sectional study to estimate prevalence of periodontal disease in a population of dogs (Canis familiaris) in commercial breeding facilities in Indiana and Illinois. PLoS One 2018;13(1):e0191395.

6. Queck KE, Chapman A, Herzog LJ, et al. Oral-fluid thiol-detection test identifies underlying active periodontal disease not detected by the visual awake examination. JAAHA 2018;54(3):132-137.

7. National Companion Animal Study. In: University of Minnesota Center for companion animal health. 1996:3.

8. Summers JF, O’Neill DG, Church D, et al. Health-related welfare prioritisation of canine disorders using electronic health records in primary care practice in the UK. BMC Vet Res 2019;15(1):163.

9. Niemiec BA. Local and regional consequences of periodontal disease. In: Niemiec BA, ed. Veterinary Periodontology. Ames, IA: Wiley Blackwell; 2013:69-80.

10. Niemiec BA. Systemic manifestations of periodontal disease. In: Niemiec BA, ed. Veterinary Periodontology. Ames, IA: Wiley Blackwell; 2013:81-90.

11. Lindhe J, Hamp S, Löe H. Plaque induced periodontal disease in beagle dogs: a 4-year clinical, roentgenographical and histometrical study. J Periodont Res 1975;10(5):243-255.

12. Quirynen M, Teughels W, Kinder Haake S, et al. Microbiology of periodontal diseases. In: Carranza FA, Numan MG, Takai HH, et al, eds. Carranza’s Clinical Periodontology. St. Louis, MO: WB Saunders; 2006:134-169.

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14. O’Neill DG, Butcher C, Church DB, et al. Miniature schnauzers under primary veterinary care in the UK in 2013: demography, mortality and disorders. Canine Genet Epidemiol 2019;6:1.

15. Meitner SW, Zander HA, Iker HP, et al. Identification of inflamed gingival surfaces. J Clin Periodontol 1979;6:93-97.

16. Niemiec BA. Etiology and pathogenesis of periodontal disease. In: Niemiec BA, ed. Veterinary Periodontology. Ames, IA: John Wiley and Sons; 2012:18-34.

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19. Marretta SM, Smith MM. Single mucoperiosteal flap for oronasal fistula repair. J Vet Dent 2005;22(3):200-205.

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22. Ramsey DT, Marretta SM, Hamor RE, et al. Ophthalmic manifestations and complications of dental disease in dogs and cats. JAAHA 1996;32(3):215-224.

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25. Peralta S, Arzi B, Nemec A, et al. Non-radiation-related osteonecrosis of the jaws in dogs: 14 cases (1996-2014). Front Vet Sci 2015;2:7.

26. Zheng TZ, Boyle P, Hu HF, et al. Dentition, oral hygiene, and risk of oral cancer: a case-control study in Beijing, People’s Republic of China. Cancer Causes Control 1990;1:235-1241.

27. Wen BW, Tsai CS, Lin CL, et al. Cancer risk among gingivitis and periodontitis patients: a nationwide cohort study. QJM 2014;107(4):283-290.

28. Taboada J, Meyer DJ. Cholestasis in associated with extrahepatic bacterial infection in five dogs. J Vet Intern Med 1989;3(4):216-220.

29. Pavlica Z, Petelin M, Juntes P, et al. Periodontal disease burden and pathological changes in organs of dogs. J Vet Dent 2008;25(2):97-105.

30. MacDougal DF, Cook T, Steward AP, Cattell V. Canine chronic renal disease: prevalence and types of glomerulonephritis in the dog. Kidney Int 1986;29(6):1144-1151.

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33. Trevejo RT, Lefebvre SL, Yang M, et al. Survival analysis to evaluate associations between periodontal disease and the risk of development of chronic azotemic kidney disease in cats evaluated at primary care veterinary hospitals. JAVMA 2018;252(6):710-720.

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36. Franek E, Klamczynska E, Ganowicz E, et al. Association of chronic periodontitis with left ventricular mass and central blood pressure in treated patients with essential hypertension. Am J Hypertens 2009;22(2):203-207.

37. Geerts SO, Legrand V, Charpentier J, et al. Further evidence of the association between periodontal conditions and coronary artery disease. J Periodontol 2004;75(9):1274-1280.

38. Kouki MI, Papadimitriou SA, Kazakos GM, et al. Periodontal disease as a potential factor for systemic inflammatory response in the dog. J Vet Dent 2013;30(1):26-29.

39. McFadden T, Marretta SM. Consequences of untreated periodontal disease in dogs and cats. J Vet Dent 2013;30:266-275.

40. Rawlinson JE, Goldstein RE, Reiter AM, et al. Association of periodontal disease with systemic health indices in dogs and the systemic response to treatment of periodontal disease. JAVMA 2011;238(5):601-609.

41. Nemec A, Verstraete FJ, Jerin A, et al. Periodontal disease, periodontal treatment and systemic nitric oxide in dogs. Res Vet Sci
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42. Cotič J, Ferran M, Karišik J, et al. Oral health and systemic inflammatory, cardiac and nitroxid biomarkers in hemodialysis patients. Med Oral Patol Oral Cir Bucal 2017;22(4):e432-e439.

43. Noack B, Genco RJ, Trevisan M, et al. Periodontal infections contribute to elevated systemic C-reactive protein level. J Periodontol 2001;72(9):1221-1227.

44. Benguigui C, Bongard V, Ruidavets JB, et al. Metabolic syndrome, insulin resistance, and periodontitis: a cross-sectional study in a middle-aged French population. J Clin Periodontol 2010;37(7):601-608.

45. Wang TF, Jen IA, Chou C, Lei YP. Effects of periodontal therapy on metabolic control in patients with type 2 diabetes mellitus and periodontal disease: a meta-analysis. Medicine 2014;93(28):e292.

46. Abnet CC, Qiao YL, Mark SD, et al. Prospective study of tooth loss and incident esophageal and gastric cancers in China. Cancer Causes Control 2001;12(9):847-854.

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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' >Zimbabwe</option></select> <label for='input_6_10_6' id='input_6_10_6_label' 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