Seasonal Affective Disorders: Relevance of Icelandic and Icelandic-Canadian Evidence to Etiologic Hypotheses

Orig i nal Re search Seasonal Affective Disorders: Relevance of Icelandic and Icelandic-Canadian Evidence to Etiologic Hypotheses Jóhann Axelsson, PhD, DPhil 1, Jón G Stefánsson, MD 2, Andrés Magnússon, MD, PhD 3, Helgi Sigvaldason, PhD 4, Mikael M Karlsson, PhD 5 Ob jec tive: This study tests the sug ges tion of ear lier stud ies con cern ing the im por tance of ge netic fac tors in the eti ol ogy of win ter sea sonal af fec tive dis or ders (SADs) and sub syn - dro mal win ter SAD (S- SAD). Method: Two study popu la tions of Win ni peg, Mani toba resi dents were can vassed: 250 adults of wholly Ice landic de scent and 1000 adults of non- Icelandic de scent. We dis trib - uted the Sea sonal Pat tern As sess ment Ques tion naire by mail to these 2 popu la tions, yield - ing 204 and 449 valid re sponses, re spec tively. Results: Rates of SAD and S- SAD proved mark edly lower in the Ice landic popu la tion than those in the non- Icelandic popu la tion. Con clu sions: These dif fer ences seem un ex plained by dif fer ences in am bi ent light or cli - mate, thus in di cat ing that ge netic fac tors con trib ute to the ex pres sion of SADs. Com pared with ear lier find ings from a group of adults of wholly Ice landic de scent liv ing in nearby ru - ral Mani toba, the etio logic im por tance of as- yet- undetermined en vi ron mental fac tors un re - lated to lati tude or am bi ent light is also in di cated. (Can J Psy chia try 2002;47:153 158) Clini cal Im pli ca tions: This study points out the inade quacy of the etio logic com po nent of the lati tude hy pothe sis in ex plain ing win ter sea sonal af fec tive dis or ders (SADs). The study im plies that SADs are im por tantly de pendent upon ge netic fac tors. The study sug gests that SADs are also de pend ent upon non-light- related en vi ron mental fac tors. Limi ta tions The study relies upon genea logic and an thro pomet ric data in as sessing ge netic simi lar ity. The study leaves unexplained the simi lar ity in preva lences of SAD and SAD plus S- SAD in Ice landic popu la tions in Mani toba and in Ice land, de spite the large dif fer ence in lati tude be - tween the places of resi dence of these populations. The pres ent study does not iso late the non- light- related en vi ron mental fac tors which evi dently play a role in the ex pres sion of SADS Key Words : SAD, sea sonal af fec tive dis or der, sea sonal dis or der, af fec tive dis or der, mood dis or der, de pres sion, com par a tive study Seasonal Af fec tive Dis or der (SAD), in the sense dis cussed Most epidemiologic re search on SAD has made use of the here (some times called winter SAD), is a de pres sion Sea sonal Pat tern As sess ment Ques tion naire (SPAQ), an in - which oc curs reg u larly in fall and win ter, with re mis sion dur - strument de vel oped by Rosenthal and his col leagues (3), and ing spring and sum mer (1,2). of the SPAQ cri te ria for SAD, which Kasper and as so ci ates sub se quently de vel oped (4). Subsyndromal win ter SAD W Can J Psy chia try, Vol 47, No 2, March 2002 153

The Ca na dian Jour nal of Psy chia try Orig i nal Re search (S-SAD), a milder form of the dis or der, has also been de - scribed (4,5). In a well-known study, Rosen, Rosenthal, and co work ers used the SPAQ to de ter mine prevalences of SAD and S-SAD at 4 lo ca tions along the US east ern sea board: Sarasota, Florida (latitude 27 N); Mont gom ery County, Mary land (lat i tude 39 N); New York City (latitude 40 N); and Nashua, New Hamp shire (lat i tude 42.5 N) (6). They found that prevalences of SAD and S-SAD cor re lated pos i tively with lat i tude, and this ac corded with ear lier sur veys, not based upon the SPAQ (7,8). The idea that prevalences of SAD and S-SAD vary di rectly with lat i tude, due to the in verse vari a tion of win ter am bi ent light with lat i tude, may for con ve nience be styled the lat i tude hy poth e sis (9). This hy poth e sis has 2 sep a ra ble el e ments: a descriptive el e ment (di rect vari ance of prev a lence with lat i - tude) and an etiologic el e ment (light de pri va tion as a prin ci pal causal fac tor). Aside from the sup port de rived from the em pir - ical find ings re viewed above, the lat i tude hy poth e sis gains cred i bil ity from the fact that both SAD and S-SAD re spond well to phototherapy (1,4, 5,10 14), as sum mer SAD does not (15,16). In 1993, Magnússon and Stefánsson pub lished the re sults of a study on SAD and S-SAD, which was con ducted in Ice land us ing Rosenthal s meth ods (11). Ice land is lo cated at 63.4º to 66.5ºN lat i tude. This study re vealed that the prev a lence rates for SAD and S-SAD were mark edly lower in Ice land than those found in 3 of the Amer i can lo ca tions stud ied by Rosenthal lo ca tions that lie 21º to 27.5º to the south of Ice - land. In ad di tion, Magnússon and Axelsson (9) found that the com bined prev a lence of SAD plus S-SAD in Manitobans of wholly Ice lan dic de scent (liv ing at ap prox i mately 50.5ºN lat i - tude) was only mar gin ally higher than that re ported by Rosenthal and co work ers from Sarasota, Florida, ly ing 23.5 to the south. These find ings con tra dicted the lat i tude hy poth e - sis in any simple form and sug gested that ge netic fac tors might play an im por tant causal role in SAD and S-SAD an idea sub se quently cor rob o rated by other re search ers (17 19). The pres ent study com pares prevalences of SAD and S-SAD in Win ni peg res i dents of 1) wholly Ice lan dic de scent and 2) non-icelandic de scent. A finding of sig nif i cantly dif fer ent prevalences of SAD and S-SAD in these 2 groups would pre - sum ably strengthen the case for the im por tance of ge netic fac - tors in the eti ol ogy of SADs. Methods Means of Mea sure ment Prevalence rates of SAD and S-SAD were mea sured in the 2 study pop u la tions us ing the SPAQ, an in stru ment for in ves ti - gat ing changes in mood and be hav iour with the sea sons (3). The SPAQ has sev eral com po nents, in clud ing 6 scales that mea sure sea sonal vari a tions in mood, ap pe tite, weight, sleep, en ergy, and so cial ac tiv ity. The sum of the scores on these 6 scales yields the sea son al ity score (SS), which can range from 0 to 24. Fur ther, the questionnaire evaluates the de gree to which seasonal changes are ex pe ri enced as a prob lem and iden ti fies the months of the year in which sub jects feel best and worst. The SPAQ-based cri te ria for SAD, and other psychometric prop er ties of the SPAQ, have re cently been re viewed (20,21). Fur ther, the SPAQ-based diagnoses were checked against clinical diagnoses, with which they agree rea son ably well (22 24). Un for tu nately, not all SPAQ-based stud ies use the same cri te ria for SAD and S-SAD. In the pres ent study, our cri te ria for SAD were an SS 11, feel ing worst in a pe riod in clud ing Jan u ary or Feb ru ary, and experiencing seasonal changes as a prob lem to at least a mod er ate de gree. Our cri - te ria for S-SAD were ei ther 1) SS 11 and ex pe ri enc ing sea - sonal changes as a prob lem mildly or not at all or 2) SS = 9 or 10 and ex pe ri enc ing sea sonal changes at least mildly. Again, the pe riod of feel ing worst had to in clude Jan u ary or Feb ru ary. Study Pop u la tions and Sur vey Methods Previous stud ies have iden ti fied a pop u la tion of wholly Ice - lan dic de scent liv ing in Man i toba (25,26). Like the pop u la tion of Ice land, from which it can not be dis tin guished anthropometrically (27), this population ex hib its a re mark - able de gree of ge netic ho mo ge ne ity (28). In the pres ent study, 250 adult Win ni peg res i dents of wholly Ice lan dic de scent were iden ti fied, and in Jan u ary 1993, we sent them the SPAQ, to gether with a cov er ing let ter. Of the 250, 210 re sponded (84%). In the fi nal sta tis ti cal anal y sis, 6 sets of answers were ex cluded be cause of missing values. Thus, the fi nal Ice lan dic study pop u la tion com prised 204 in di - vid u als, rang ing in age from 18 to 74 years. To con struct the non-icelandic pop u la tion, we pur chased a ran dom sam ple of 1000 res i den tial ad dresses from the Man i - toba Tele phone Sys tem da ta base. This da ta base, which is up - dated fre quently, con tains the names, ad dresses, and tele phone numbers of all tele phone-service sub scrib ers in Win ni peg. The SPAQ was sent, along with a cov er ing let ter, to all 1000 addresses during the first half of June 1993. One-half of the letters asked for a male re spon dent, and one-half asked for a fe male re spon dent. Of these mail ings, 949 were re ceived by ad dress ees, and 51 were re turned as un - de liv er able. Then, 3 weeks af ter the ini tial mail ing, a sec ond mail ing went out to those who had not re turned the ques tion - naire from the first mail ing. The Win ni peg Area Study ar - ranged and ad min is tered the pur chase of the ad dress list and the mail ings. We ultimately re ceived back 515 filled-out 154 W Can J Psy chia try, Vol 47, No 2, March 2002

Seasonal Affective Disorders: Relevance of Icelandic and Icelandic-Canadian Evidence to Etiologic Hypotheses ques tion naires (54.2%). In the fi nal sta tis ti cal anal y sis, 66 sets of an swers were excluded due to miss ing val ues. The fi nal non-icelandic study pop u la tion, there fore, com prised 449 in - di vid u als, rang ing in age from 18 to 74 years. Ice lan dic Ca na di ans in Man i toba form a cul tur ally co her ent group, which has tra di tion ally ex hib ited an en thu si as tic will - ing ness to par tic i pate in sci en tific stud ies with an Ice lan dic con nec tion. The high rate of re sponse to our mailed ques tion - naire was not un ex pected for this group. In contrast, our non-icelandic pop u la tion was drawn at ran dom from among the adult res i dents of Win ni peg, who form a more cul tur ally di verse group than the Ice lan dic Ca na di ans and have no tra di - tion-bound en thu si asm for pro jects con nected with Ice land. The Ice lan dic study population was significantly younger than those in the non-icelandic pop u la tion (P = 0.005). Women out num bered men in both pop u la tions, but there was no sta tis ti cally sig nif i cant dif fer ence in the dis tri bu tion of men and women in the 2 pop u la tions. Ta ble 1 pro vides an over view of the de mo graphic fea tures of both the Ice lan dic and the non-icelandic re spon dents. Sta tis ti cal Anal y sis Age stan dard iza tion was per formed us ing the world stan dard pop u la tion, trun cated to ages 15 to 74 years (29). We used mul ti ple lin ear re gres sion to find the de pend ence of SS on age, sex, and descent (non-icelandic or Ice lan dic). Age- and sex-standardized prev a lence rates with 95% con fi dence in ter - vals (CIs) were com puted us ing the pro gram pack age CIA (30). Be cause these CIs are ap prox i mate, they are not suited to the sta tis ti cal com par i son of prev a lence rates based upon small sam ples. Odds ra tios (ORs) be tween the 2 pop u la tion groups were cal - cu lated by lo gis tic re gres sion ad justed for age and sex for 1) SAD ver sus S-SAD plus No SAD; 2) S-SAD ver sus No SAD; and 3) SAD plus S-SAD ver sus No SAD. In ad di tion, polytomous lo gis tic re gres sion was ap plied to fit a model to the data, us ing the pro gram pack age SPIDA (31). Polytomous lo gis tic re gres sion is an ex ten sion of lo gis tic re - gres sion, al low ing the de pend ent vari able to take val ues in ad - di tion to 0 and 1; in this case, it al lows 3 val ues: 0 = No SAD, 1 = S-SAD, 2 = SAD. In this way, odds ra tios for each of SAD and S-SAD ver sus No SAD can be com puted si mul ta neously. Results Sea son al ity Scores The age-standardized SS proved markedly higher in the non-icelandic pop u la tion than in the Ice lan dic pop u la tion. In all age groups in the non-icelandic pop u la tion and in all but the youn gest and old est age groups in the Ice lan dic pop u la - tion, the SS was higher among women than among men. Mul - ti ple lin ear regression anal y sis showed that the mean SS de creased with in creas ing age by about 0.67 per 10 years (P < 0.001) in the com bined Ice lan dic and non-icelandic pop u la - tion. The re gres sion co ef fi cient for woman ver sus man was 1.09, P = 0.001; for non-icelandic ver sus Ice lan dic de scent, it was 1.51, P < 0.001. Sea sonal Af fec tive Dis or ders The age- and sex-standardized prevalences of SAD and of com bined SAD plus S-SAD were markedly higher in the non-icelandic pop u la tion than were in the Ice lan dic Table 1. Demographic features of Icelandic and non-icelandic respondents from Winnipeg Ice landic Non- Icelandic Mean age in years 45.2 SD 14.2 (%) 48.8 SD 16.6 (%) Sex Men 98 46.7 234 47.1 Women 112 53.3 263 52.9 Marital status Sin gle 43 20.7 101 20.6 Mar ried or wid owed 146 71.1 337 68.6 Sepa rated or di vorced 17 8.2 53 10.8 Mean years of edu ca tion Less than 4 years of high school 15 7.2 59 12.1 High school only 48 23.2 142 29.0 1 to 3 years post high school 56 27.1 162 25.8 4 or more years post high school 88 42.5 126 25.8 W Can J Psy chia try, Vol 47, No 2, March 2002 155

The Ca na dian Jour nal of Psy chia try Orig i nal Re search Table 2. Classification of respondents of Icelandic and non-icelandic descent Age groups 18 24 25 34 35 44 45 54 55 64 65 74 To tal % 95% CI P Total Ice landic 16 44 36 46 42 20 204 Non- Icelandic 33 88 110 75 75 80 449 SAD Ice landic 2 1 3 0 0 0 6 4.80 0.1 9.6 Non- Icelandic 3 12 8 11 3 3 40 9.10 5.9 12.2 < 0.01 S-SAD Ice landic 3 8 3 4 4 0 22 12.80 6.1 19.6 Non- Icelandic 7 11 21 11 12 5 67 15.90 11.3 20.5 > 0.10 SAD plus S-SAD Ice landic 5 9 6 4 4 0 28 17.70 9.4 25.9 Non- Icelandic 10 23 39 22 15 8 107 25.00 19.4 30.6 < 0.01 Table 3. Results of polytomous regression SAD S- SAD OR CI OR CI Age (per 10 years) 0.71 0.57 0.90 0.80 0.68 0.93 Sex (women vs men) 3.23 1.60 6.51 1.46 0.93 2.28 Descent (non-icelandic vs Icelandic) 3.35 1.38 8.10 1.40 0.85 2.30 population (Ta ble 2): 9.1% ver sus 4.8% for SAD (P < 0.01) and 25.0% ver sus 17.7% for SAD plus S-SAD (P < 0.01). The age- and sex-standardized prev a lence of S-SAD was higher in the non-icelandic pop u la tion than in the Ice lan dic pop u la tion (15.9% vs 12.8%), but this dif fer ence was not sta tis ti cally sig - nificant (P > 0.10). Sex- and age-adjusted ORs (non-icelandic vs Ice lan dic) for SAD, S-SAD, and SAD plus S-SAD were cal cu lated first by lo gis tic re gres sion. For SAD, the OR proved to be 3.3 (P < 0.008); for SAD plus S-SAD, it was 2.1 (P < 0.002). The ORs for SAD and S-SAD were then re cal cu lated us ing polytomous lo gis tic re gres sion, which yielded sim i lar re sults (Ta ble 3). Ta ble 3 also shows the de pend ence of SAD and S-SAD upon age and sex. For SAD, the cal cu lated OR for age per 10 years in the com bined Ice lan dic and non-icelandic pop u la tion was 0.71 (P = 0.004). In other words, if 2 in di vid u als of the same de scent and gen der are sep a rated in age by 10 years, the older individual is 29% less likely to suf fer from SAD than the youn ger. For S-SAD, the cal cu lated OR for age per 10 years was 0.80 (P = 0.005). In the com bined pop u la tion, the OR for women ver sus men were 3.23 for SAD (P = 0.001) and 1.46 for S-SAD (P = 0.10). The vari ables weight, ed u ca tion, and mar i tal sta tus were also tested but did not prove to have pre dic tive sig nif i cance for SAD or S-SAD. Discussion In the pres ent study, we found that prevalences of SAD and com bined SAD plus S-SAD in Win ni peg res i dents of wholly Ice lan dic de scent dif fered sig nif i cantly from the prevalences found in Winnipeg res i dents of non-icelandic de scent. For those not of Ice lan dic de scent, the OR for SAD was more than 3 times as high, and the OR for SAD plus S-SAD more than twice as high, as for those of Icelandic de scent. The prev a - lence of S-SAD dif fered no tice ably be tween the 2 groups, but this dif fer ence was not sta tis ti cally sig nif i cant. These re sults strongly sup port the sug ges tion of ear lier stud ies (9, 17 19) that ge netic fac tors play an im por tant role in the 156 W Can J Psy chia try, Vol 47, No 2, March 2002

Seasonal Affective Disorders: Relevance of Icelandic and Icelandic-Canadian Evidence to Etiologic Hypotheses eti ol ogy of SADs, for the above-mentioned dif fer ences are ev i dently not ex plained by such en vi ron men tal fac tors as am - bi ent light or cli mate, which ap pear to be iden ti cal for both pop u la tions. Taken to gether with ear lier find ings, the pres ent re sults hint fur ther at the etiologic im por tance of en vi ron men tal fac tors un re lated to lat i tude or am bi ent light. Magnússon and Axelsson (9) found the prev a lence of SAD in Manitobans of wholly Ice lan dic de scent who live in the Interlake District (50.5 N lat i tude) to be 1.3%. The pres ent study finds the prev - a lence of SAD in Win ni peg res i dents (50 N) of wholly Ice lan - dic de scent to be 4.8%. Ac cord ing to all avail able in di ca tions, the Ice lan dic pop u la tion in Win ni peg is not ge net i cally dis tin - guish able from the Interlake study pop u la tion; the 2 pop u la - tions re side at an ef fec tively iden ti cal lat i tude, be ing sep a rated by only 90 km. That the ge netic sim i lar ity of these pop u la tions has not been ver i fied by the anal y sis of ge netic ma te rial but re - lies instead upon an thro po mor phic data (27,28) is a lim i ta tion of the pres ent study. DNA anal y sis was not possible at the time when the se ries of stud ies upon which the cur rent find - ings are built was ini ti ated (9,11,17,25,26). How ever, it may soon be come prac ti cal to as sess the ge netic sim i lar ity of the study pop u la tions by this means. Prior to the pres ent study, the di rect vari a tion with lat i tude in the prev a lence of SADs ap peared to hold for ge net i cally com - parable populations. The dif fer ences in the prevalences of SAD now found in the ge net i cally sim i lar Interlake and Win - ni peg pop u la tions do not fit com fort ably with this rule, but be - cause the differences are not sta tis ti cally sig nif i cant (P = 0.20), the point is still in con clu sive. Fur ther, it must be noted that the prev a lence of SAD in the combined Win ni peg and Interlake Ice lan dic pop u la tions (3.0%) is rather close to the prev a lence found in Ice land as a whole (3.6%), de spite the very large dif fer ence in lat i tude be - tween the Man i toba lo ca tions (50 to 50.5 N) and Ice land (63.4 to 66.5 N). For com bined SAD plus S-SAD, the com - pa ra ble fig ures are 10.4% and 11.6%. The de scrip tive el e ment of the lat i tude hy poth e sis would lead us to ex pect much larger dif fer ences, and only fur ther in ves ti ga tion can re veal why this ex pec ta tion is not fullfilled. The etiologic el e ment of the lat i tude hy poth e sis, ac cord ing to which light de pri va tion is a prin ci pal causal fac tor in the de - velopment of SADs, is still persuasive on the basis of the light-related, sea sonal on set, the re mis sion of symp toms, and the efficacy of phototherapy. Nonetheless, it is becoming clear that the ex pres sion of these dis or ders is also heavily de - pend ent upon ge netic fac tors, and there are at least some in di - ca tions that en vi ron men tal fac tors un re lated to lat i tude or am bi ent light may also be im por tant. This study does not in di - cate what these ad di tional fac tors might be; hence, this topic re quires fur ther in ves ti ga tion. Dis cerning these fac tors would pre sum ably help us to sup ple ment drug and phototherapy re - gimes in SAD treat ment. References 1. Rosenthal NE, Sack DA, Gillin JC, Lewy AJ, Goodwin FK, Dav en port Y. Sea - sonal af fec tive dis or der. A de scrip tion of the syn drome and pre lim i nary find ings with light ther apy. Arch Gen Psy chi a try 1984;41(1):72 80. 2. Amer i can Psy chi at ric As so ci a tion. Di ag nos tic and sta tis ti cal man ual of men tal dis or ders. 4th ed. Wash ing ton (DC): Amer i can Psy chi at ric As so ci a tion; 1994. 3. Rosenthal NE, Genhart M, Sack DA, Skwerer RG, Wehr TA. Sea sonal af fec tive dis or der: rel e vance for treat ment and re search of bulimia. In: Hud son JI, Pope HG. Psychobiology of bulimia. Wash ing ton (DC): Amer i can Psy chi at ric Press; 1987. p 205 28. 4. Kasper S, Wehr TA, Bartko JJ, Gaist PA, Rosenthal NE. Ep i de mi o log i cal find - ings of sea sonal changes in mood and be hav iour. A tele phone sur vey of Mont - gom ery County, Mary land. Arch Gen Psy chi a try 1989;46:823 33. 5. Kasper S, Rog ers SL, Yancy A, Schultz PM, Skwerer RG, Rosenthal NE. Phototherapy in in di vid u als with and with out subsyndromal sea sonal af fec tive dis or der. 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