Acessibilidade / Reportar erro

INFLAMMATORY BOWEL DISEASE IN HISPANIC COMMUNITIES: a concerted South American approach could identify the aetiology of Crohn’s disease and ulcerative colitis

Doença inflamatória intestinal nas comunidades Hispânicas: uma orquestrada abordagem Sul-Americana poderia identificar a etiologia da doença de Crohn e da retocolite ulcerativa

Abstracts

Despite intensive research we remain ignorant of the cause of both Crohn’s disease and ulcerative colitis. The dramatic rise in incidence, particularly of Crohn’s disease, points towards environmental factors as playing a significant role. A major purpose of this review is to stimulate a co-ordinated international effort to establish an on-going data base in Central and South America in which new cases are registered and through which investigations into aetiology can be conducted. In both Brazil and Mexico there is evidence that the incidence of ulcerative colitis is increasing, as also is the case for Crohn’s disease in Brazil. The pattern of disease is, therefore, directly comparable to that reported from Europe and the USA during the 1970s and 1980s, but much lower than contemporary data from Spain. Although the incidence is similar to that reported from Portugal, the studies from Almada and Braga were conducted a decade before that from Sao Paulo. The situation in Brazil compares dramatically with Uruguay and Argentina where the reported incidence of inflammatory bowel disease is significantly less. However, with growing industrialisation it is likely that there will be an explosion of inflammatory bowel disease in some areas of Central and South America over the next 20 years. The creation of a network of researchers across South and Central America is a real possibility and through a Concerted Action there is the possibility that major strides could be made towards understanding the cause of inflammatory bowel disease and so develop preventive strategies.

Inflammatory bowel diseases; Crohn disease; Proctocolitis; Ulcerative colitis; Database


Apesar da pesquisa intensa, ainda permanecemos ignorantes quanto à causa da doença de Crohn e da retocolite ulcerativa. O aumento dramático da incidência, particularmente da doença de Crohn, aponta para fatores ambientais desempenhando um papel significativo. Um grande propósito desta revisão é estimular um esforço internacional coordenado para estabelecer uma base de dados em curso na América Central e do Sul, na qual novos casos são registrados e através dos quais investigações sobre a etiologia seriam realizadas. No Brasil e no México, há evidências de que a incidência da colite ulcerosa está aumentando, como também é o caso da doença de Crohn no Brasil. O padrão da doença é, portanto, diretamente comparável àquela relatada da Europa e dos Estados Unidos durante a década de 1970 e 1980, mas muito mais baixa do que dados contemporâneos da Espanha. Embora a incidência seja semelhante à relatada a partir de Portugal, os estudos de Almada e Braga ocorreram uma década antes do que em São Paulo. A situação no Brasil compara-se dramaticamente com Uruguai e Argentina, onde a incidência relatada de doença inflamatória intestinal é significativamente menor. No entanto, com a crescente industrialização é provável que haja uma explosão de doença inflamatória intestinal em algumas áreas da América Central e do Sul nos próximos 20 anos. A criação de uma rede de pesquisadores em toda a América Central e do Sul é uma possibilidade real e, através de uma ação articulada, há a possibilidade de que grandes avanços poderiam ser feitos no sentido de compreender a causa da doença inflamatória intestinal e então desenvolverem-se estratégias preventivas.

Doenças inflamatórias intestinais; Doença de Crohn; Proctocolite; Colite ulcerativa; Base de dados


INTRODUCTION

Interest in the epidemiology and aetiology of inflammatory bowel disease has been a central theme in gastroenterology for a long time. One hundred years ago Kennedy Dalziel was amongst the earliest clinicians to describe what later became known as Crohn’s disease. At the time he wrote: “I can only regret that the aetiology of the condition remains in obscurity, but I trust that ‘ere long further consideration will clear up the difficulty”(1616. Dalzeil TK. Chronic interstitial enteritis. Br Med J (Clin Res Ed). 1913;2:1068-70.).

However, despite intensive research on all fronts we remain ignorant of the cause of both conditions with many theories coming into fashion only to be later dismissed. The dramatic rise in incidence, particularly of Crohn’s disease, points towards environmental factors as playing a significant role. Further support for such a view comes from the spread of the disease into Southern and Eastern Europe and now India and China. In 1985 following reviews of the epidemiology of ulcerative colitis(3131. Mayberry JF. Some aspects of the epidemiology of ulcerative colitis. Gut. 1985;26:968-74.), Crohn’s disease(3333. Mayberry JF, Rhodes J. Epidemiological aspects of Crohn’s disease: a review of the literature. Gut. 1984;25:886-99.) and a study of mortality(1717. D’Oliveira R, Mayberry JF Newcombe RG, Rhodes J. International comparison of mortality from inflammatory bowel disease in the Latin-speaking countries Venezuela, Italy and France. Digestion 1984;29:106-11.) it was suggested that: “Particular attention in the future will focus on such countries as Spain and Portugal; Central and South America are of interest for similar reasons”(3131. Mayberry JF. Some aspects of the epidemiology of ulcerative colitis. Gut. 1985;26:968-74.).

This review cites more than 20 studies that have subsequently come from Spain and Portugal (Table 1 and Figure 1). A major drive to this work was the Concerted Action funded by the European Union during the 1990s(1919. Europa. Biomedical & Health Research Series: Epidemiology. [Internet]. [cited 2014 April 16]. Available from: http://ec.europa.eu/research/biomed/biom-p13.html.
http://ec.europa.eu/research/biomed/biom...
). It was a descriptive study of the incidence of inflammatory bowel disease in Northern and Southern Europe. It achieved this through standardisation of definitions of disease(3232. Mayberry JF. The development of a standardised protocol for a prospective study of inflammatory bowel disease in Europe. Scand J Gastroenterol. 1989;24:83-5.) and of the methodologies used to identify candidate cases and separate them into confirmed cases and non-cases(77. Van Blankenstein M, Shivananda S. European Collaborative Study on Inflammatory Bowel Disease (EC-IBD; preliminary results). In Epidemiology edited by Vuylsteek K & Hallen M. IOS Press. 1994. p. 354-62.). Additional benefits that arose from the program included:

TABLE 1.
Incidence studies of inflammatory bowel disease from Spain and Portugal
FIGURE 1.
Distribution of inflammatory bowel disease in Hispanic Communities.

Incidence data is quoted for ulcerative colitis and then Crohn’s disease. In the case of Madrid the most recent figures are quoted first.


  • The creation of networks of research teams in Europe;

    Promotion of national financing of research projects relevant to European priorities in health research;

    Transfer of expertise from centres of excellence to less advanced research teams(1919. Europa. Biomedical & Health Research Series: Epidemiology. [Internet]. [cited 2014 April 16]. Available from: http://ec.europa.eu/research/biomed/biom-p13.html.
    http://ec.europa.eu/research/biomed/biom...
    ).

However, by the 1990s the incidence of ulcerative colitis had dramatically increased in Spain and this change was to be followed shortly by similar increases in the frequency of Crohn’s disease (Table 1)(1515. Cebolla J, López Zaborras J, Sopeña F, Nerín JM, Gomollón F, Sainz R. Aspectos epidemilógicos de la enfermedad de Crohn en Zaragoza. Rev Esp Enferm Dig. 1991;79:186-9.). A Concerted Action 10 years earlier would have allowed more direct observation and assessment of those factors which are responsible for the worldwide expansion of these conditions. Such changes have now been reported in China, India and many other communities. Central and South America are the last major regions where inflammatory bowel disease is still uncommon and in which there is hope that the aetiology of these conditions might be identified through basic epidemiological research. A major purpose of this review is to stimulate a co-ordinated international effort to establish an on-going data base in Central and South America in which new cases are registered and through which investigations into aetiology can be conducted. It also presents a unique opportunity to investigate cohorts and the subsequent occurrence of Crohn’s disease or ulcerative colitis. For example, young people who are recruited for military service are, in general, healthy and basic data on demography, social habits and family history can be recorded. Such a cohort can be followed long-term and this form of approach has been adopted in Korea, which is another low incidence area(2323. Kang J, Shin D, Lee J, Bang S, Kim D. Rapid increase in the prevalence of inflammatory bowel disease in candidates for the military service born after 1988 in Korea. Inflamm Bowel Dis. 2011;17:E22.). Retrospective studies using military cohorts have been used in the USA, but this lacks the rigour of a prospective approach(3737. Porter CK, Cash BD, Pimentel M, Akinseye A, Riddle MS. Risk of inflammatory bowel disease following a diagnosis of irritable bowel syndrome. BMC Gastroenterol. 2012;12:55.). The Millenium Cohort Study will address some of these issues(4141. Ryan MA, Smith TC, Smith B, Amoroso P, Boyko EJ, Gray GC, et al. Millenium Cohort: enrolment begins a 21-year contribution to understanding the impact of military service. Journal of Clinical Epidemiology. 2007;60:181-91.). It uses traditional and web based methods to follow almost 100,000 service personnel and such an approach could be adopted in Central and South America.

Incidence and prevalence in Central and South America

Almost without exception ulcerative colitis is commoner than Crohn’s disease and this is true in studies from Brazil, Uruguay and Puerto Rico (Table 2)(33. Appleyard CB, Hernández G, Rios-Bedoya CF. Basic epidemiology of inflammatory bowel disease in Puerto Rico. Inflamm Bowel Dis. 2004;10:106-11 , 1111. Buenavida G, Casañas A, Vásquez C, De Souza M, Martínez L, Gardil I, et al. Incidence of inflammatory bowel disease in five geographical areas of Uruguay in the biennial 2007 - 2008. Acta Gastroenterol Latinoam. 2011;41:281-7., 4949. Torres EA, Cruz A, Monagas M, Bernal M. Correa Y, Codero R, Carlo VL. Inflammatory bowel disease in Hispanics: The University of Puerto Rico IBD Registry. Int J Inflam. 2012;2012:574079., 5050. Victoria CR Sassak LY, Rubens de Carvalho Nunes H. Incidência e prevalência das doenças inflamatórias intestinais na região centro-oeste do Estado de São Paulo. Arq Gastroenterol. 2009;46:20-5.). In both Brazil(4747. Souza MH, Troncon LE, Rodrigues CM, Viana CF, Onofre PH, Monteiro RA, et al. Evolução da ocorrência (1980-1999) da doença de Crohn e da retocolite ulcerativa idiopática e análise das suas características clínicas em um hospital universitário do sudeste do Brasil. Arq Gastroenterol. 2002;39:98-105., 5050. Victoria CR Sassak LY, Rubens de Carvalho Nunes H. Incidência e prevalência das doenças inflamatórias intestinais na região centro-oeste do Estado de São Paulo. Arq Gastroenterol. 2009;46:20-5.) and Mexico(88. Bosques-Padilla FJ, Sandoval-Garcia ER, Martinez-Vázquez MA, Garza-González E, Maldonado-Garza HJ. Epidemiología y características clínicas de la colitis ulcerosa crónica idiopática en el noreste de México. Rev Gastroenterol Mex. 2011;76:34-8.) there is evidence that the incidence is increasing, as also is the case for Crohn’s disease in Brazil (Table 2)(5050. Victoria CR Sassak LY, Rubens de Carvalho Nunes H. Incidência e prevalência das doenças inflamatórias intestinais na região centro-oeste do Estado de São Paulo. Arq Gastroenterol. 2009;46:20-5.). The pattern of disease is, therefore, directly comparable to that reported from Europe and the USA during the 1970s and 1980s and more recently from Eastern Europe and China. However, the incidences are significantly lower than contemporary data from Spain. (Figure 1). In general, they are similar to those from Portugal but the studies from Almada and Braga were conducted a decade before that from Sao Paulo(4545. Shivananda S1, Lennard-Jones J, Logan R, Fear N, Price A, Carpenter L, van Blankenstein M. Incidence of inflammatory bowel disease across Europe: is there a difference between north and south? Results of the European Collaborative Study on Inflammatory Bowel Disease (EC-IBD). Gut 1996;39:690-7., 5050. Victoria CR Sassak LY, Rubens de Carvalho Nunes H. Incidência e prevalência das doenças inflamatórias intestinais na região centro-oeste do Estado de São Paulo. Arq Gastroenterol. 2009;46:20-5.).

TABLE 2.
Incidence studies on inflammatory bowel disease in Latin America

The situation in Brazil(4747. Souza MH, Troncon LE, Rodrigues CM, Viana CF, Onofre PH, Monteiro RA, et al. Evolução da ocorrência (1980-1999) da doença de Crohn e da retocolite ulcerativa idiopática e análise das suas características clínicas em um hospital universitário do sudeste do Brasil. Arq Gastroenterol. 2002;39:98-105., 5050. Victoria CR Sassak LY, Rubens de Carvalho Nunes H. Incidência e prevalência das doenças inflamatórias intestinais na região centro-oeste do Estado de São Paulo. Arq Gastroenterol. 2009;46:20-5.) compares dramatically with Uruguay and Argentina(1111. Buenavida G, Casañas A, Vásquez C, De Souza M, Martínez L, Gardil I, et al. Incidence of inflammatory bowel disease in five geographical areas of Uruguay in the biennial 2007 - 2008. Acta Gastroenterol Latinoam. 2011;41:281-7., 2424. Linares de la Cal JA, Cantȯn C, Hermida C, Pérez-Miranda M, Maté-Jiménez J. Estimated incidence of inflammatory bowel disease in Argentina and Panama (1987 - 1993). Rev Esp Enferm Dig. 1999;91:277-86.) where the reported incidence of inflammatory bowel disease is significantly less. Such variations between adjacent countries would give particular value to a continental study of inflammatory bowel disease, provided it adopted a more analytical style than the simple descriptive approach taken by the Concerted Action in Europe. Work in Uruguay would strongly support the view that such differences are real and not due to variations in the way cases were identified(1111. Buenavida G, Casañas A, Vásquez C, De Souza M, Martínez L, Gardil I, et al. Incidence of inflammatory bowel disease in five geographical areas of Uruguay in the biennial 2007 - 2008. Acta Gastroenterol Latinoam. 2011;41:281-7.). Clearly the very existence of such differences between countries should be a major stimulus to international co-operative studies in Central and South America.

Most patients in the Brazilian study were urban dwellers and of European descent(5050. Victoria CR Sassak LY, Rubens de Carvalho Nunes H. Incidência e prevalência das doenças inflamatórias intestinais na região centro-oeste do Estado de São Paulo. Arq Gastroenterol. 2009;46:20-5.). The urban predominance of inflammatory bowel disease has been described in a number of studies(1818. Ekbom A, Helmick C, Zack M, Adami HQ. The epidemiology of inflammatory bowel disease: a large, population-based study in Sweden. Gastroenterology. 1991;100:350-8., 2929. Maté-Jimenez J, Muñoz S, Vicent D, Pajares JM. Incidence and prevalence of ulcerative colitis and Crohn’s disease in urban and rural areas of Spain from 1981 to 1988. J Clin Gastroenteol. 1994;18:27-31., 3434. Mayberry JF, Rhodes, J, Newcombe RG. Crohn’s disease in Wales, 1967-1976; an epidemiological survey based on hospital admissions. Postgrad Med J. 1980;56:336-41., 4646. Soon IS, Molodecky NA, Rabi DM, Ghall WA, Barkema HW, Kaplan GC. The relationship between urban environment and the inflammatory bowel diseases: a systematic review and meta-analysis. BMC Gastroenterol. 2012;12:51.). It seems to be a particular feature early in the appearance of the condition in a community with the difference lessening and ultimately disappearing with time. It is of interest that the Brazilian study links the movement of people into urban areas with economic driving factors including the need for women to work in factories and other industries so exposing them to environmental factors which may play a part in the aetiology of inflammatory bowel disease.

The flow of immigrants into Argentina, Uruguay, Brazil and Venezuela also provides opportunity for further assessments(2222. International Organisation for Migration. 2014. [Cited 2014 April 17]. Available from: https://www.iom.int/cms/en/sites/iom/home/where-we-work/americas/south-america.html.
https://www.iom.int/cms/en/sites/iom/hom...
). Such work was done on the occurrence of cancer in migrants in the 1990s in Uruguay(4848. De Stefani E, Parkin DM, Khlat M, Vassallo A, Abella M. Cancer in migrants to Uruguay. Int J Cancer Suppl. 1990;46:233-7.), Brazil(99. Bouchardy C, Khlat M, Mirra AP, Parkin DM. Cancer risks among European migrants in São Paulo, Brazil. Eur J Cancer. 1993;29:1418-23.) and Argentina(3030. Matos EL, Khlat M, Loria DI, Vilensky M, Parkin DM. Cancer in migrants to Argentina. Int J Cancer Suppl. 1991;49:805-11.). An interesting recent Spanish study on emigration looked at 34 patients who had emigrated to other parts of Europe and 16 to South America(66. Barreiro-de AM, Alvarez Castro A, Souto R, Iglesias M, Lorenzo A, Dominguez-Muňoz JE. Emigration to western industrialised countries: A risk factor for developing inflammatory bowel disease. J Crohn’s Colitis. 2011;5:566-9.). The authors suggested that emigration was associated with ulcerative colitis and not with Crohn’s disease. It also linked emigration to industrialised European countries and not to Latin America during the first decade of the 21st Century. Work in the UK has demonstrated that the incidence of colitis can rise to that of the host population and even exceed it within one generation(1414. Carr I, Mayberry JF. The effects of migration on ulcerative colitis: a three-year prospective study among Europeans and first- and second-generation South Asians in Leicester (1991-1994). Am J Gastroenterol. 1999;94:2918-22.). With growing industrialisation it is likely that there will be an explosion of inflammatory bowel disease in some areas of Central and South America over the next 20 years.

CONCLUSION

What is the way forward? The main impact of the Concerted Action on inflammatory bowel disease in Europe was to create an atmosphere in which multi-national studies became a real possibility. Clinicians with an interest in inflammatory bowel disease from a range of countries came together and worked out common agendas for research and shared their methods and pooled results. Into these groups they drew statisticians and patient representatives. Such activities helped stimulate the emergence of organisations such as the European Crohn’s and Colitis Organisation (ECCO) (1313. Caprilli R, D’Haens G, Gassull M. 10 year ECCO Anniversary Book. [Internet]. Feeding Science, digesting knowledge. 2012. [cited 2014 April 16]. Available from: https://www.ecco-ibd.eu/images/1_About_ECCO/ECCO_10yr_Anniversary_Book.pdf.
https://www.ecco-ibd.eu/images/1_About_E...
). The creation of a network of researchers across South and Central America is a real possibility. There already exist registers of patients with inflammatory bowel disease in a number of countries e.g. Brazil(4747. Souza MH, Troncon LE, Rodrigues CM, Viana CF, Onofre PH, Monteiro RA, et al. Evolução da ocorrência (1980-1999) da doença de Crohn e da retocolite ulcerativa idiopática e análise das suas características clínicas em um hospital universitário do sudeste do Brasil. Arq Gastroenterol. 2002;39:98-105., 5050. Victoria CR Sassak LY, Rubens de Carvalho Nunes H. Incidência e prevalência das doenças inflamatórias intestinais na região centro-oeste do Estado de São Paulo. Arq Gastroenterol. 2009;46:20-5.), Argentina(2424. Linares de la Cal JA, Cantȯn C, Hermida C, Pérez-Miranda M, Maté-Jiménez J. Estimated incidence of inflammatory bowel disease in Argentina and Panama (1987 - 1993). Rev Esp Enferm Dig. 1999;91:277-86.), Panama(2424. Linares de la Cal JA, Cantȯn C, Hermida C, Pérez-Miranda M, Maté-Jiménez J. Estimated incidence of inflammatory bowel disease in Argentina and Panama (1987 - 1993). Rev Esp Enferm Dig. 1999;91:277-86.), Uruguay(1111. Buenavida G, Casañas A, Vásquez C, De Souza M, Martínez L, Gardil I, et al. Incidence of inflammatory bowel disease in five geographical areas of Uruguay in the biennial 2007 - 2008. Acta Gastroenterol Latinoam. 2011;41:281-7.), and Puerto Rico(4949. Torres EA, Cruz A, Monagas M, Bernal M. Correa Y, Codero R, Carlo VL. Inflammatory bowel disease in Hispanics: The University of Puerto Rico IBD Registry. Int J Inflam. 2012;2012:574079.). The maintenance of such registers can be costly and requires dedicated staff. Registration on computer data bases and sharing of data can be restricted by legislation related to privacy and by concerns about the availability of such data outside national boundaries. However, such difficulties can be overcome and by pooling data the results become more robust and such studies may be the last opportunity to readily identify those environmental factors which are likely to be a significant factor in the emergence and spread of inflammatory bowel disease across the world.

Patient self help groups can provide useful support to any network of researchers through explanations to members and, at times, political lobbying. Such groups already exist in Brazil and Argentina. They tend to appeal to a certain sector of the population e.g in the UK membership is dominated by English women and a significant number of people do not join because they do not wish to “broadcast their illness”(3636. Moody GA, Bhakta P, Mayberry JF. Disinterest in local self-help groups amongst patients with inflammatory bowel disease. Int J Colorectal Dis. 1993;8:181-3.). Nevertheless the European Federation of Crohn’s and Ulcerative Colitis Associations (EFCCA) has emerged as a significant umbrella organisation which supports patients and clinicians. It recently welcomed Fundación Mas Vida de Crohn & Colitis Ulcerosa from Argentina as an associate member.

The development of these networks, the facilitation of meetings and support of a research program with common protocols and clearly defined endpoints, which will include measures of incidence and an investigation of potential aetiological factors, will require funding. In days when such funds are hard to achieve the role of pharma companies should not be dismissed. South America is likely to be a major market for 5ASA compounds and for biologic therapies. It is not unreasonable to expect them to provide seeding funds to, at least, initiate an international meeting of clinicians in Central and South America so that a “Concerted Action” on the epidemiology and aetiology of inflammatory bowel disease can happen.

REFERENCES

  • 1
    Alonso P, Ulla M, Soriano M, Aquise M & Del Villar V. Enfermedad inflammatoria crȯnica intestinal en la provincial de Soria. Studio clinic y epidmiolȯgico retrospective del periodo 1981 to 1990. Rev Esp Enferm Dig. 1992;82:87-91.
  • 2
    Antón Martínez J, Ortega Gómez A, Arranz Carrero, Molina Sánchez A, Alvarez García JF, Moreiras Jiménez JL, et al. Incidencia de enfermedad inflamatoria intestinal en el área de salud de Navalmoral de la Mata (Cáceres, España) entre 2000 y 2009. Gastroenterol Hepatol. 2010;33:694-9.
  • 3
    Appleyard CB, Hernández G, Rios-Bedoya CF. Basic epidemiology of inflammatory bowel disease in Puerto Rico. Inflamm Bowel Dis. 2004;10:106-11
  • 4
    Arin Letamendia A, Burusco Paternain MJ, Borda Celaya F, Pueyo Royo A, Martínez Echeverría A, Jiménez Pérez FJ. Epidemiological aspects of inflammatory bowel disease in the Pamplona area. Rev Esp Enferm Dig.1999;99:323-8.
  • 5
    Arin Letamendia A, Borda Celaya F, Burusco Paternain MJ, Prieto Martínez C, Martínez Echeverría A, Elizalde Apestegui I, et al. Altas tasas de incidencia de enfermedad inflamatoria intestinal en Navarra. Resultados de un estudio prospectivo y poblacional. Gastroenterol Hepatol. 2008;31:111-6.
  • 6
    Barreiro-de AM, Alvarez Castro A, Souto R, Iglesias M, Lorenzo A, Dominguez-Muňoz JE. Emigration to western industrialised countries: A risk factor for developing inflammatory bowel disease. J Crohn’s Colitis. 2011;5:566-9.
  • 7
    Van Blankenstein M, Shivananda S. European Collaborative Study on Inflammatory Bowel Disease (EC-IBD; preliminary results). In Epidemiology edited by Vuylsteek K & Hallen M. IOS Press. 1994. p. 354-62.
  • 8
    Bosques-Padilla FJ, Sandoval-Garcia ER, Martinez-Vázquez MA, Garza-González E, Maldonado-Garza HJ. Epidemiología y características clínicas de la colitis ulcerosa crónica idiopática en el noreste de México. Rev Gastroenterol Mex. 2011;76:34-8.
  • 9
    Bouchardy C, Khlat M, Mirra AP, Parkin DM. Cancer risks among European migrants in São Paulo, Brazil. Eur J Cancer. 1993;29:1418-23.
  • 10
    Brullet E, Bonfill X, Urrútia G, Ruiz Ochoa V, Cueto M, Clofent J, et al. Estudio epidemiológico sobre la incidencia de enfermedad inflamatoria intestinal en cuatro áreas españolas. Med Clin (Barc). 1998;110:651-6.
  • 11
    Buenavida G, Casañas A, Vásquez C, De Souza M, Martínez L, Gardil I, et al. Incidence of inflammatory bowel disease in five geographical areas of Uruguay in the biennial 2007 - 2008. Acta Gastroenterol Latinoam. 2011;41:281-7.
  • 12
    Calderȯn AV, Velarde OF, Yoshidaira MY, Barahona ER. Perfil clínico y epidemio­lógico de la colitis ulcerativa en un Hospital de Lima. Rev Gastroenterol Peru. 2004;24:135-42.
  • 13
    Caprilli R, D’Haens G, Gassull M. 10 year ECCO Anniversary Book. [Internet]. Feeding Science, digesting knowledge. 2012. [cited 2014 April 16]. Available from: https://www.ecco-ibd.eu/images/1_About_ECCO/ECCO_10yr_Anniversary_Book.pdf.
    » https://www.ecco-ibd.eu/images/1_About_ECCO/ECCO_10yr_Anniversary_Book.pdf
  • 14
    Carr I, Mayberry JF. The effects of migration on ulcerative colitis: a three-year prospective study among Europeans and first- and second-generation South Asians in Leicester (1991-1994). Am J Gastroenterol. 1999;94:2918-22.
  • 15
    Cebolla J, López Zaborras J, Sopeña F, Nerín JM, Gomollón F, Sainz R. Aspectos epidemilógicos de la enfermedad de Crohn en Zaragoza. Rev Esp Enferm Dig. 1991;79:186-9.
  • 16
    Dalzeil TK. Chronic interstitial enteritis. Br Med J (Clin Res Ed). 1913;2:1068-70.
  • 17
    D’Oliveira R, Mayberry JF Newcombe RG, Rhodes J. International comparison of mortality from inflammatory bowel disease in the Latin-speaking countries Venezuela, Italy and France. Digestion 1984;29:106-11.
  • 18
    Ekbom A, Helmick C, Zack M, Adami HQ. The epidemiology of inflammatory bowel disease: a large, population-based study in Sweden. Gastroenterology. 1991;100:350-8.
  • 19
    Europa. Biomedical & Health Research Series: Epidemiology. [Internet]. [cited 2014 April 16]. Available from: http://ec.europa.eu/research/biomed/biom-p13.html.
    » http://ec.europa.eu/research/biomed/biom-p13.html
  • 20
    Garrido A, Martínez MJ, Ortega JA, Lobato A, Rodríguez MJ, Guerrero FJ. Epidemiology of chronic inflammatory bowel disease in the Northern area of Huelva. Rev Esp Enferm Dig. 2004;96:691-4.
  • 21
    Hinojosa J, Primo J, Lledó S, López A, Roig JV, Fernández J. Incidencia de enfermedad inflamatoria intestinal en Sagunto. Rev Esp Enferm Dig. 1990;78:283-7.
  • 22
    International Organisation for Migration. 2014. [Cited 2014 April 17]. Available from: https://www.iom.int/cms/en/sites/iom/home/where-we-work/americas/south-america.html.
    » https://www.iom.int/cms/en/sites/iom/home/where-we-work/americas/south-america.html
  • 23
    Kang J, Shin D, Lee J, Bang S, Kim D. Rapid increase in the prevalence of inflammatory bowel disease in candidates for the military service born after 1988 in Korea. Inflamm Bowel Dis. 2011;17:E22.
  • 24
    Linares de la Cal JA, Cantȯn C, Hermida C, Pérez-Miranda M, Maté-Jiménez J. Estimated incidence of inflammatory bowel disease in Argentina and Panama (1987 - 1993). Rev Esp Enferm Dig. 1999;91:277-86.
  • 25
    Lopez Miguel C, Sicilia B, Sierra E, Lopez Zaborras J, Arribas F, Gomollon F. Incidecia de la enfermedad inflamatoria intestinal en Aragon: resultados de un studio prospective y poblacional. Gastroenterol Hepatol. 1999;22:323-8.
  • 26
    López-Serrano P, Pérez-Calle JL, Carrera-Alonso E, Pérez-Fernández T, Rodríguez-Caravaca G, Boixeda-de-Miguel D, Fernández-Rodríguez CM. Epidemiologic study on the current incidence of inflammatory bowel disease in Madrid. Rev Esp Enferm Dig. 2009;101:768-72.
  • 27
    Martínez G, Fernández Y, Rodrigo Sáez L, Martínez E. Estudio epidemiológico de la enfermedad de Crohn en la región asturiana. Rev Esp Enferm Dig. 1983;63:534-41.
  • 28
    Martínez-Salmeron JF, Rodrigo M, de Teresa J, Nogueras F, García-Montero M, de Sola C, et al. Epidemiology of inflammatory bowel disease in the Province of Granada, Spain: a retrospective study from 1979 to 1988. Gut. 1993;34:1207-9.
  • 29
    Maté-Jimenez J, Muñoz S, Vicent D, Pajares JM. Incidence and prevalence of ulcerative colitis and Crohn’s disease in urban and rural areas of Spain from 1981 to 1988. J Clin Gastroenteol. 1994;18:27-31.
  • 30
    Matos EL, Khlat M, Loria DI, Vilensky M, Parkin DM. Cancer in migrants to Argentina. Int J Cancer Suppl. 1991;49:805-11.
  • 31
    Mayberry JF. Some aspects of the epidemiology of ulcerative colitis. Gut. 1985;26:968-74.
  • 32
    Mayberry JF. The development of a standardised protocol for a prospective study of inflammatory bowel disease in Europe. Scand J Gastroenterol. 1989;24:83-5.
  • 33
    Mayberry JF, Rhodes J. Epidemiological aspects of Crohn’s disease: a review of the literature. Gut. 1984;25:886-99.
  • 34
    Mayberry JF, Rhodes, J, Newcombe RG. Crohn’s disease in Wales, 1967-1976; an epidemiological survey based on hospital admissions. Postgrad Med J. 1980;56:336-41.
  • 35
    Monferrer Guardiola R, Marín Jiménez JA, Pedraza Sanz RG, Moreno Sánchez I, Soler Bahilo E, Hinojosa del Val J. Incidence of inflammatory bowel disease in the 02 health area of Castellón (1992-1996). Rev Esp Enferm Dig. 1999;91:40-6.
  • 36
    Moody GA, Bhakta P, Mayberry JF. Disinterest in local self-help groups amongst patients with inflammatory bowel disease. Int J Colorectal Dis. 1993;8:181-3.
  • 37
    Porter CK, Cash BD, Pimentel M, Akinseye A, Riddle MS. Risk of inflammatory bowel disease following a diagnosis of irritable bowel syndrome. BMC Gastroenterol. 2012;12:55.
  • 38
    Pozzati L, Cabanillas A. Estudio hospitalario de incidencia de la enfermedad inflamatoria intestinal en el Área Sanitaria de Mérida. Gastroenterol Hepatol. 2002;25:541-4.
  • 39
    Rivera Irigoin R, de Sola Earle C, Ubiña Aznar E, Perea-Milla E, Fernández Pérez F, Navarro Tarabo JM, Fernández G. Incidencia y aspectos clinicoepidemiolȯgicos de la colitis ulcerosa en el area de influencia del Hospital Costa del Sol. Gastroenterol Hepatol. 2007;30:7-10.
  • 40
    Ruiz Ochoa V. Estudio epidemiológico de la Enfermedad de Crohn en Galicia en el periodo 1976 a 1983. Rev Esp Enferm Dig. 1984;66:273-9.
  • 41
    Ryan MA, Smith TC, Smith B, Amoroso P, Boyko EJ, Gray GC, et al. Millenium Cohort: enrolment begins a 21-year contribution to understanding the impact of military service. Journal of Clinical Epidemiology. 2007;60:181-91.
  • 42
    Saro Gismera C, Lacort Fernández M, Argüelles Fernández G, Antón Magarzo J, Navascues CA, Garcia López R, et al. Epidemiología de la enfermedad inflamatoria intestinal crónica en Gijón. Asturias. Gastroenterol Hepatol. 2001;24:228-35.
  • 43
    Saro Gismera C, Riestra Menéndez S, Sánchez Fernández R, Milla Crespo A, Lacort Fernández M, Argüelles Fernández G, et al. Epidemiología de la enfermedad inflamatoria intestinal crónica en cinco áreas de Asturias: España. An Med Interna. 2003;20:232-8.
  • 44
    Sebastián Domingo JJ, Bañares Cañizares R, Velo Bellver JL, Clemente Ricote G & Cos Arregui E. Aspectos epidemiologicos de la enfermedad inflamatoria intestinal cronica en un area asistencal de la Comunidad Autonoma de Madrid. An Med Interna. 1989;6:519-22.
  • 45
    Shivananda S1, Lennard-Jones J, Logan R, Fear N, Price A, Carpenter L, van Blankenstein M. Incidence of inflammatory bowel disease across Europe: is there a difference between north and south? Results of the European Collaborative Study on Inflammatory Bowel Disease (EC-IBD). Gut 1996;39:690-7.
  • 46
    Soon IS, Molodecky NA, Rabi DM, Ghall WA, Barkema HW, Kaplan GC. The relationship between urban environment and the inflammatory bowel diseases: a systematic review and meta-analysis. BMC Gastroenterol. 2012;12:51.
  • 47
    Souza MH, Troncon LE, Rodrigues CM, Viana CF, Onofre PH, Monteiro RA, et al. Evolução da ocorrência (1980-1999) da doença de Crohn e da retocolite ulcerativa idiopática e análise das suas características clínicas em um hospital universitário do sudeste do Brasil. Arq Gastroenterol. 2002;39:98-105.
  • 48
    De Stefani E, Parkin DM, Khlat M, Vassallo A, Abella M. Cancer in migrants to Uruguay. Int J Cancer Suppl. 1990;46:233-7.
  • 49
    Torres EA, Cruz A, Monagas M, Bernal M. Correa Y, Codero R, Carlo VL. Inflammatory bowel disease in Hispanics: The University of Puerto Rico IBD Registry. Int J Inflam. 2012;2012:574079.
  • 50
    Victoria CR Sassak LY, Rubens de Carvalho Nunes H. Incidência e prevalência das doenças inflamatórias intestinais na região centro-oeste do Estado de São Paulo. Arq Gastroenterol. 2009;46:20-5.
  • Disclosure of funding: no funding received

Publication Dates

  • Publication in this collection
    Oct-Dec 2014

History

  • Received
    20 Apr 2014
  • Accepted
    20 June 2014
Instituto Brasileiro de Estudos e Pesquisas de Gastroenterologia e Outras Especialidades - IBEPEGE. Rua Dr. Seng, 320, 01331-020 São Paulo - SP Brasil, Tel./Fax: +55 11 3147-6227 - São Paulo - SP - Brazil
E-mail: secretariaarqgastr@hospitaligesp.com.br