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Seasonality of births in horizontal strabismus: comparison with birth seasonality in schizophrenia and other disease conditions

Published online by Cambridge University Press:  22 March 2019

A. B. Agarwal ,
K. Cassinelli ,
L. A. Johnson ,
K. Matsuda ,
B. Kirkpatrick ,
W. Yang  and
C. S. von Bartheld Open the ORCID record for C. S. von Bartheld [Opens in a new window]
A. B. Agarwal
Affiliation:
Department of Physiology & Cell Biology, University of Nevada, Reno School of Medicine, Reno, NV, USA
K. Cassinelli
Affiliation:
Sierra Eye Associates, Reno, NV, USA
L. A. Johnson
Affiliation:
Department of Physiology & Cell Biology, University of Nevada, Reno School of Medicine, Reno, NV, USA Sierra Eye Associates, Reno, NV, USA
K. Matsuda
Affiliation:
Matsuda Eye Clinic, Sennan, Osaka, Japan
B. Kirkpatrick
Affiliation:
Department of Psychiatry & Behavioral Sciences, University of Nevada, Reno School of Medicine, Reno, NV, USA
W. Yang
Affiliation:
School of Community Health Sciences, Nevada Center for Health Statistics and Informatics, University of Nevada, Reno, NV, USA
C. S. von Bartheld*
Affiliation:
Department of Physiology & Cell Biology, University of Nevada, Reno School of Medicine, Reno, NV, USA
*
Address for correspondence: C. S. von Bartheld, Department of Physiology & Cell Biology, University of Nevada, Reno School of Medicine, Reno, NV, USA. E-mail: cvonbartheld@med.unr.edu
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Abstract

Recent work has implicated one type of horizontal strabismus (exotropia) as a risk factor for schizophrenia. This new insight raises questions about a potential common developmental origin of the two diseases. Seasonality of births is well established for schizophrenia. Seasonal factors such as light exposure affect eye growth and can cause vision abnormalities, but little is known about seasonality of births in strabismus. We examined birth seasonality in people with horizontal strabismus in a retrospective study in Washoe County, Nevada, and re-examined similar previously obtained data from Osaka, Japan. We then compared seasonal patterns of births between strabismus, refractive error, schizophrenia and congenital toxoplasmosis. Patients with esotropia had a significant seasonality of births, with a deficit in March, then increasing to an excess in September, while patients with exotropia had a distinctly different pattern, with an excess of births in July, gradually decreasing to a deficit in November. These seasonalities were statistically significant with either χ2 or Kolmogorov–Smirnov-type statistics. The birth seasonality of esotropia resembled that for hyperopia, with an increase in amplitude, while the seasonality for myopia involved a phase-shift. There was no correlation between seasonality of births between strabismus and congenital toxoplasmosis. The pattern of an excess of summer births for people with exotropia was remarkably similar to the well-established birth seasonality of one schizophrenia subtype, the deficit syndrome, but not schizophrenia as a whole. This suggests a testable hypothesis: that exotropia may be a risk factor primarily for the deficit type of schizophrenia.

Keywords

refractive errorschizophreniaseasonality of birthsstrabismustoxoplasmosis
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 10 , Issue 6 , December 2019 , pp. 636 - 644
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2019 

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References

Wadhwa, PD, Buss, C, Entringer, S, Swanson, JM. Developmental origins of health and disease: brief history of the approach and current focus on epigenetic mechanisms. Semin Reprod Med. 2009; 27, 358–368.CrossRefGoogle ScholarPubMed
Gluckman, PD, Hanson, MA, Buklijas, T. A conceptual framework for the developmental origins of health and disease. J Dev Orig Health Dis. 2010; 1, 6–18.CrossRefGoogle ScholarPubMed
Almond, D, Currie, J. Killing me softly: the fetal origins hypothesis. J Econ Perspect. 2011; 25, 153–172.CrossRefGoogle ScholarPubMed
Torrey, EF, Miller, J, Rawlings, R, Yolken, RH. Seasonality of births in schizophrenia and bipolar disorder: a review of the literature. Schizophr Res. 1997; 28, 1–38.CrossRefGoogle ScholarPubMed
Davies, G, Welham, J, Chant, D, Torrey, EF, McGrath, J. A systematic review and meta-analysis of Northern Hemisphere season of birth studies in schizophrenia. Schizophr Bull. 2003; 29, 587–593.CrossRefGoogle Scholar
Bembenek, A. Seasonality of birth in schizophrenia patients. Literature review. Psychiatr Pol. 2005; 39, 259–270.Google ScholarPubMed
Schiffman, J, Maeda, JA, Hayashi, K, et al. Premorbid childhood ocular alignment abnormalities and adult schizophrenia-spectrum disorder. Schizophr Res. 2006; 81, 253–260.CrossRefGoogle ScholarPubMed
Mohney, BG, McKenzie, JA, Capo, JA, et al. Mental illness in young adults who had strabismus as children. Pediatrics. 2008; 122, 1033–1038.CrossRefGoogle ScholarPubMed
Korn, H. Schizophrenia and eye movement – a new diagnostic and therapeutic concept. Med Hypotheses. 2004; 62, 29–34.CrossRefGoogle ScholarPubMed
Toyota, T, Yoshitsugu, K, Ebihara, M, et al. Association between schizophrenia with ocular misalignment and polyalanine length variation in PMX2B. Hum Mol Genet. 2004; 13, 551–561.CrossRefGoogle ScholarPubMed
Yoshitsugu, K, Yamada, K, Toyota, T, et al. A novel scale including strabismus and ‘cuspidal ear’ for distinguishing schizophrenia patients from controls using minor physical anomalies. Psychiatry Res. 2006; 145, 249–258.CrossRefGoogle ScholarPubMed
Ndlovu, D, Nhleko, S, Pillay, Y, et al. The prevalence of strabismus in schizophrenic patients in Durban, KwaZulu Natal. S Afr Optom. 2011; 70, 101–108.Google Scholar
Agarwal, AB, Christensen, AJ, Feng, CY, et al. Expression of schizophrenia biomarkers in extraocular muscles from patients with strabismus: an explanation for the link between exotropia and schizophrenia? PeerJ. 2017; 5, e4214.CrossRefGoogle Scholar
von Noorden, GK, Campos, EC. Binocular Vision and Ocular Motility, 6th edn, 2002. Mosby: St. Louis.Google Scholar
Matsuda, K, Yokoyama, T, Nakagawa, M, et al. Statistical analysis of the incidence of hyperopia by month of birth. Nippon Ganka Kiyo (Folia Ophthalmol Jpn). 1986; 37, 440–443.Google Scholar
Mandel, Y, Grotto, I, El-Yaniv, R, et al. Season of birth, natural light, and myopia. Ophthalmology. 2008; 115, 686–692.CrossRefGoogle ScholarPubMed
Matsuda, K, Yokoyama, T, Fukui, M, Morita, T, Kozaki, M. Inverse analysis of the relationship between ocular refraction and birth month using matrix equations. Nippon Ganka Gakkai Zasshi (J Jpn Ophthalmol Soc). 2016; 120, 533–539.Google ScholarPubMed
Matsuda, K, Nakagawa, M, Yokoyama, T, et al. Incidence of strabismus by season of birth. Ganka Rinsho Iho (Jpn Rev Clin Ophthalmol). 1985; 79, 2115–2118.Google Scholar
Chew, E, Remaley, NA, Tamboli, A, et al. Risk factors for esotropia and exotropia. Arch Ophthalmol. 1994; 112, 1349–1355.CrossRefGoogle ScholarPubMed
Saha, S, Chant, D, Welham, J, McGrath, J. A systematic review of the prevalence of schizophrenia. PLoS Med. 2005; 2, e141.CrossRefGoogle ScholarPubMed
Messias, E, Kirkpatrick, B, Bromet, E, et al. Summer birth and deficit schizophrenia: a pooled analysis from 6 countries. Arch Gen Psychiatry. 2004; 61, 985–989.CrossRefGoogle ScholarPubMed
Meenken, C, Rothova, A, Kijlstra, A, Oosting, J. Seasonal variation in congenital toxoplasmosis. Br J Ophthalmol. 1991; 75, 639.CrossRefGoogle ScholarPubMed
The Stanley Medical Research Institute. Epidemiological similarities and differences between toxoplasmosis and schizophrenia. Updated July, 2017. Retrieved from http://www.stanleyresearch.org/patient-and-provider-resources/toxoplasmosis-schizophrenia-research/epidemiological-similarities-and-differences-between-toxoplasmosis-and-schizophrenia/.Google Scholar
Torrey, EF, Bartko, JJ, Yolken, RH. Toxoplasma gondii and other risk factors for schizophrenia: an update. Schizophr Bull. 2012; 38, 642–647.CrossRefGoogle ScholarPubMed
Carpenter, WT Jr, Heinrichs, DW, Wagman, AM. Deficit and nondeficit forms of schizophrenia: the concept. Am J Psychiatr. 1988; 145, 578–583.Google Scholar
Kirkpatrick, B, Buchanan, RW, Ross, DE, Carpenter, WT Jr. A separate disease within the syndrome of schizophrenia. Arch Gen Psychiatry. 2001; 58, 165–171.CrossRefGoogle ScholarPubMed
Kirkpatrick, B, Galderisi, S. Deficit schizophrenia: an update. World Psychiatry. 2008; 7, 143–147.CrossRefGoogle ScholarPubMed
Ross, DE, Thaker, GK, Buchanan, RW, et al. Eye tracking disorder in schizophrenia is characterized by specific ocular motor defects and is associated with the deficit syndrome. Biol Psychiatry. 1997; 42, 781–796.CrossRefGoogle ScholarPubMed
Ross, DE. The deficit syndrome and eye tracking disorder may reflect a distinct subtype within the syndrome of schizophrenia. Schizophr Bull. 2000; 26, 855–866.CrossRefGoogle ScholarPubMed
Nkam, I, Thibaut, F, Denise, P, et al. Saccadic and smooth-pursuit eye movements in deficit and non-deficit schizophrenia. Schizophr Res. 2001; 48, 145–153.CrossRefGoogle ScholarPubMed
von Bartheld CS, Agarwal AB, Feng CY, et al. Why is exotropia (one specific type of strabismus) a significant risk factor for schizophrenia? 5th Biennial Schizophrenia International Research Society Conference, Florence, Italy, April 2–6, 2016. npj Schizophrenia. 2016; 2, 78, Abstract T212.Google Scholar
Choi, TB, Lee, DA, Oelrich, FO, et al. A retrospective study of eye disease among first grade children in Los Angeles. J Am Optom Assoc. 1995; 66, 484–488.Google ScholarPubMed
Martinez-Bakker, M, Bakker, KM, King, AA, Rohani, P. Human birth seasonality: latitudinal gradient and interplay with childhood disease dynamics. Proc Biol Sci. 2014; 281, 20132438.CrossRefGoogle ScholarPubMed
Maruo, T, Kubota, N, Arimoto, H. The results of examinations for strabismus and amblyopia in elementary and secondary school pupils (in Japanese). Ganka Rinsho Iho (Jpn Rev Clin Ophthalmol). 1977; 71, 712–714.Google Scholar
Matsuda, S, Kahyo, H. Geographical differences and time trends in the seasonality of birth in Japan. Int J Epidemiol. 1994; 23, 107–118.CrossRefGoogle Scholar
Bradbury, TN, Miller, GA. Season of birth in schizophrenia: a review of evidence, methodology, and etiology. Psychol Bull. 1985; 98, 569–594.CrossRefGoogle ScholarPubMed
Verdoux, H, Takei, N, Cassou de Saint-Mathurin, R, Bourgeois, M. Analysis of the seasonal variation of schizophrenic births using a Kolmogorov-Smirnov type statistic. Eur Psychiatry. 1997; 12, 111–116.CrossRefGoogle ScholarPubMed
Nwogu, EC, Iwueze, IS, Nlebedim, VU. Some tests for seasonality in time series data. J Mod Appl Stat Meth. 2016; 15, 382–399.CrossRefGoogle Scholar
Freedman, LS. The use of a Kolmogorov–Smirnov type statistic in testing hypotheses about seasonal variation. J Epidemiol Community Health. 1979; 33, 223–228.CrossRefGoogle ScholarPubMed
Walter, SD. The power of a test for seasonality. Br J Prev Soc Med. 1977; 31, 137–140.Google ScholarPubMed
Logar, J, Soba, B, Premru-Srsen, T, Novak-Antolic, Z. Seasonal variations in acute toxoplasmosis in pregnant women in Slovenia. Clin Microbiol Infect. 2005; 11, 852–855.CrossRefGoogle ScholarPubMed
Sagel, U, Mikolajczyk, RT, Krämer, A. Seasonal trends in acute toxoplasmosis in pregnancy in the federal state of Upper Austria. Clin Microbiol Infect. 2010; 16, 515–517.CrossRefGoogle ScholarPubMed
Dollfus, S, Brazo, P, Langlois, S, et al. Month of birth in deficit and non-deficit schizophrenic patients. Eur Psychiatry. 1999; 14, 349–351.CrossRefGoogle ScholarPubMed
Lam, DA, Miron, JA. Global patterns of seasonal variation in human fertility. Ann N Y Acad Sci. 1994; 709, 9–28.CrossRefGoogle ScholarPubMed
Friger, M, Shoham-Vardi, I, Abu-Saad, K. Trends and seasonality in birth frequency: a comparison of Muslim and Jewish populations in southern Israel: daily time series analysis of 200 009 births, 1988-2005. Hum Reprod. 2009; 24, 1492–1500.CrossRefGoogle ScholarPubMed
Kallel, L, Brunelin, J, Zghal, A, et al. Summer birth and deficit schizophrenia in Tunisia. Psychiatry Res. 2007; 152, 273–275.CrossRefGoogle ScholarPubMed
Kirkpatrick, B, Ram, R, Amador, XF, et al. Summer birth and the deficit syndrome of schizophrenia. Am J Psychiatry. 1998; 155, 1221–1226.CrossRefGoogle ScholarPubMed
Kirkpatrick, B, Castle, D, Murray, RM, Carpenter, WT Jr. Risk factors for the deficit syndrome of schizophrenia. Schizophr Bull. 2000; 26, 233–242.CrossRefGoogle ScholarPubMed
Messias, E, Kirkpatrick, B. Summer birth and deficit schizophrenia in the epidemiological catchment area study. J Nerv Ment Dis. 2001; 189, 608–612.CrossRefGoogle ScholarPubMed
Tek, C, Kirkpatrick, B, Kelly, C, McCreadie, RG. Summer birth and deficit schizophrenia in Nithsdale, Scotland. J Nerv Ment Dis. 2001; 189, 613–617.CrossRefGoogle ScholarPubMed
Kirkpatrick, B, Tek, C, Allardyce, J, Morrison, G, McCreadie, RG. Summer birth and deficit schizophrenia in Dumfries and Galloway, southwestern Scotland. Am J Psychiatry. 2002; 159, 1382–1387.CrossRefGoogle ScholarPubMed
Kirkpatrick, B, Herrera Castanedo, S, Vazquez-Barquero, JL. Summer birth and deficit schizophrenia: Cantabria, Spain. J Nerv Ment Dis. 2002; 190, 526–532.CrossRefGoogle ScholarPubMed
Mete, L, Sarıkaya, Ö, Erol, A. The relationship of deficit syndrome with clinical symptoms, summer births and heritability in patients with schizophrenia. Turk Psikiyatri Derg. 2015; 26, 229–235.Google ScholarPubMed
Brown, AS, Patterson, PH. Maternal infection and schizophrenia: implications for prevention. Schizophr Bull. 2011; 37, 284–290.CrossRefGoogle Scholar
McGrath, J, Selten, JP, Chant, D. Long-term trends in sunshine duration and its association with schizophrenia birth rates and age at first registration—data from Australia and the Netherlands. Schizophr Res. 2002; 54, 199–212.CrossRefGoogle ScholarPubMed
Messias, E, Mourao, C, Maia, J, et al. Season of birth and schizophrenia in Northeast Brazil: relationship to rainfall. J Nerv Ment Dis. 2006; 194, 870–873.CrossRefGoogle ScholarPubMed
Häfner, H, Haas, S, Pfeifer-Kurda, M, Eichhorn, S, Michitsuji, S. Abnormal seasonality of schizophrenic births. A specific finding? Eur Arch Psychiatry Neurol Sci. 1987; 236, 333–342.CrossRefGoogle ScholarPubMed
Tochigi, M, Okazaki, Y, Kato, N, Sasaki, T. What causes seasonality of birth in schizophrenia? Neurosci Res. 2004; 48, 1–11.CrossRefGoogle Scholar
Odegård, O. Season of birth in the population of Norway, with particular reference to the September birth maximum. Br J Psychiatry. 1977; 131, 339–344.CrossRefGoogle ScholarPubMed
McMahon, G, Zayats, T, Chen, YP, et al. Season of birth, daylight hours at birth, and high myopia. Ophthalmology. 2009; 116, 468–473.CrossRefGoogle ScholarPubMed
Nickla, DL. Ocular diurnal rhythms and eye growth regulation: where we are 50 years after Lauber. Exp Eye Res. 2013; 114, 25–34.CrossRefGoogle ScholarPubMed
Welham, J, Chant, D, Saha, S, et al. No association between the deficit syndrome in psychosis and summer birth in a Southern hemisphere country. Aust N Z J Psychiatry. 2006; 40, 935–936.CrossRefGoogle Scholar
Franzek, E, Beckmann, H. Gene-environment interaction in schizophrenia: season-of-birth effect reveals etiologically different subgroups. Psychopathology. 1996; 29, 14–26.CrossRefGoogle ScholarPubMed
Silverstein, SM, Wang, Y, Keane, BP. Cognitive and neuroplasticity mechanisms by which congenital or early blindness may confer a protective effect against schizophrenia. Frontiers Psychol. 2013; 3, Article 624.CrossRefGoogle ScholarPubMed
Landgraf, S, Osterheider, M. “To see or not to see: that is the question.” The “Protection-Against-Schizophrenia” (PaSZ) model: evidence from congenital blindness and visuo-cognitive aberrations. Frontiers Psychol. 2013; 4, Article 352.CrossRefGoogle ScholarPubMed
Kilgore, KP, Barraza, RA, Hodge, DO, McKenzie, JA, Mohney, BG. Surgical correction of childhood intermittent exotropia and the risk of developing mental illness. Am J Ophthalmol. 2014; 158, 788–792.CrossRefGoogle ScholarPubMed
Ochoa, S, Usall, J, Cobo, J, Labad, X, Kulkarni, J. Gender differences in schizophrenia and first-episode psychosis: a comprehensive literature review. Schizophr Res Treatment. 2012; 916198.Google ScholarPubMed