Association between acanthosis nigricans and overweight with hypertension in children and adolescents from low-income familiesSUMMARY
OBJECTIVE: This study aimed to describe the prevalence of acanthosis nigricans and high blood pressure in children and adolescents from low-income families, and to verify the association of elevated blood pressure with nutritional status and the presence of acanthosis nigricans.
METHODS: This is a cross-sectional and controlled study with 232 children and adolescents from an institution for low-income families. Pubertal stage, body mass index Z-score, waist-to-height circumference ratio (increased waist-to-height circumference ratio >0.5), the presence of acanthosis nigricans, and blood pressure were assessed.
RESULTS: The prevalence of excess weight and the change in waist-to-height circumference ratio was 37.9%. Acanthosis nigricans and increased blood pressure occurred in 20.3 and 34.8%, respectively. The prevalence of acanthosis nigricans and hypertension was higher in individuals with excess weight (p<0.001; p<0.001) and with an increased waist-to-height circumference ratio (p=0.009; p<0.001). Logistic regression showed a significant and independent association of body mass index Z-score (OR 2.35; 95%CI 1.52–3.65; p<0.001) and the presence of acanthosis nigricans (OR 2.43; 95%CI 1.12–5.23; p=0.023) with elevated blood pressure.
CONCLUSION: Acanthosis nigricans and elevated blood pressure occurred in one-fifth and one-third of the individuals in an institution for children from low-income families. Overweight and the presence of acanthosis nigricans increased the risk of high blood pressure more than twofold.
Keywords Acanthosis nigricans; Arterial pressure; Pediatric obesity; Cardiometabolic risk factors
INTRODUCTION
The prevalence of childhood obesity has increased tenfold in the last four decades worldwide1. In Brazil, excess weight (overweight and obesity) was observed in 30% of children aged between 5 and 9 years and in 19.4% of adolescents2.
Children and adolescents with obesity may present cardiometabolic risks, including arterial hypertension, which present insulin resistance as a central mechanism. Acanthosis nigricans (AN) occurs more frequently in conditions such as hyperinsulinism, insulin resistance, type 2 diabetes, and obesity at all ages, including pediatric age. The assessment of AN can be performed in a practical way and is part of the routine pediatric physical examination, assisting in the early diagnosis of these conditions3-5.
A meta-analysis including 47 cross-sectional studies with children and adolescents showed that overweight and obesity increased the risk of hypertension by 5 and 15 times, respectively6.
Studies evaluating the association between AN and arterial hypertension with excess weight in children and adolescents from low-income families in our country are rarely reported in the literature7.
The aims of this study were to describe the prevalence of AN and high blood pressure (BP) in children and adolescents from low-income families and to verify the association of elevated BP with nutritional status and the presence of AN.
METHODS
Since this is a cross-sectional study, 232 children and adolescents from an institution for children from low-income families in situations of social vulnerability in the city of Santo André, Brazil were included. The study was conducted from January to December 2019.
The exclusion criteria were as follows: patients with chronic diseases (except overweight, asthma, and rhinitis), such as genetic, cardiovascular, endocrine, and renal diseases, acute infections, and those using hormonal and non-hormonal anti-inflammatory drugs in 3 months prior to the clinical evaluation.
The anthropometric assessment was performed according to protocols standardized by the World Health Organization (WHO) and the Ministry of Health of Brazil8,9. Weight and height measurements were expressed as body mass index Z-score (zBMI), calculated using the WHO Anthro and WHO Anthro Plus 3.2.2 software. For the anthropometric classification, the cutoff points recommended by the WHO were adopted10. The children’s waist measurement was also obtained using an inextensible measuring tape, positioned at the midpoint between the superior border of the iliac crest and the last fixed rib cage, which was used to calculate the waist-to-height circumference ratio (WHtR). WHtR was classified as altered when the value was equal to or greater than 0.511.
The pubertal stage was defined by a single professional (pediatrician) and classified according to what was proposed by Marshall and Tanner12,13.
BP was measured in the right arm relaxed, at heart height, with the palm facing up and supported on a rigid surface, with the individual seated and at rest. A sphygmomanometer was used with a cuff suitable for arm circumference. Three measurements were obtained with a minimum interval of 2 min between them, and the mean of the values was calculated. BP was classified according to the criteria of the Manual de orientação de hipertensão arterial na infância e adolescência da Sociedade Brasileira de Pediatria – 201914: altered blood pressure levels (elevated BP): ≥90th percentile (P90) for age, sex, and height (BP ≥P90 and <P95: elevated BP; PB ≥P95 and <P95+12 mmHg: hypertension stage 1; BP ≥P95+12 mmHg: hypertension stage 2).
The skin of the cervical and bilateral axillary regions was evaluated in search of AN, the regions where acanthosis occurs most frequently15. Each child was evaluated simultaneously by two pediatricians.
The data were entered, revised, and consolidated in an Excel spreadsheet (Office®). For statistical analysis, Epi InfoTM, version 7.2.2.6 was used. Qualitative variables were presented as absolute numbers and percentages and compared through the χ2 test: logistic regression (dependent variable: elevated BP (≥P90); independent variables: zBMI, WHtR) and the presence of acanthosis. The significance level adopted was 5%.
This study was approved by the Research Ethics Committee of the Centro Universitário FMABC, under opinion number: 3.058.583.
RESULTS
The study included 232 children and adolescents aged 4–14 years (mean 8.4±3.2 years). The general characteristics of the study population are presented in Table 1. Excess weight (overweight and obesity) and a change in WHtR occurred in 37.9% of the participants. Cervical and/or axillary AN and elevated blood pressure (≥P90) were observed in 20.3% and 34.8% of participants, respectively.
Table 2 shows the general characteristics stratified according to the presence of AN and BP. There was no difference between the overweight and non-overweight groups regarding sex, age, or pubertal stage. Individuals with AN had a higher prevalence of overweight (p<0.001) and altered WHtR (p=0.009).
Comparison of clinical variables in relation to acanthosis nigricans (absent or present) and blood pressure (normal or increased).
There was no difference between the groups of individuals with normal BP in relation to sex, age, and pubertal stage. The group of children with altered BP presented a higher prevalence of overweight (p<0.001), change in WHtR (p<0.001), and AN (p<0.001) (Table 2).
Logistic regression showed a significant and independent association of zBMI (OR 2.35; 95%CI 1.52–3.65; p<0.001) and the presence of AN (OR 2.43; 95%CI 1.12–5.23; p=0.023) with elevated BP. There was no association between WHtR and the risk of elevated BP (p=0.567) (Table 3).
DISCUSSION
Overweight and the presence of AN increased the risk of elevated BP in the study population by 2.3 and 2.4 times, respectively. The association between these risk factors (overweight, presence of AN, and elevated BP) increases the risk of future cardiovascular events16. More than one-third of the participants had overweight and/or altered WHtR. This study was conducted in an institution for children in situations of social vulnerability from low-income families. Food disorders may justify the higher prevalence of overweight and obesity in this population. Childhood obesity is increased by low socioeconomic status and place of residence17,18. A cross-sectional study conducted on 175 children and adolescents aged 6–17 years, from a low-income community in the city of Santa Rita do Sapucaí, Brazil, observed 37.2% of overweight, the levels similar to that observed in this study7.
The prevalence of AN in this study was one in five children. Sex, age, and pubertal stage did not influence the risk of AN. Children with AN had higher zBMI and WHtR levels. A study conducted in Turkey evaluated 160 overweight children and adolescents (10.4±3.3 years old), and also found no significant difference in the presence of AN in relation to these variables. Apparently, the only predictive factors for AN are hyperinsulinism and the severity of obesity19. A systematic review showed that AN is associated with insulin resistance and risk for type 2 diabetes mellitus20. A study on 8,371 children from territories belonging to the United States in the Pacific demonstrated that intervention measures addressing eating habits, lifestyle, and sleep and screen time control significantly reduced excess weight, waist circumference, and the presence of AN when compared to the control group (overweight [effect size] d= -3.95%; 95%CI -7.47 to -0.43); waist circumference (d= -0.71%; 95%CI -1.37 to -0.05), and AN prevalence (d= -2.28%; 95%CI -2.77 to -1.57)21.
One-third of the participants had increased blood pressure (≥P90). Sex, age, and pubertal stage did not influence the risk of altered BP. Children with elevated BP had a higher prevalence of increased zBMI, WHtR, and the presence of AN. A meta-analysis of 41 studies on hypertension in Africa, involving 52,918 participants aged 3–19 years from 10 countries, described a total prevalence of 18.8% of elevated BP and hypertension, with a significant predominance in overweight children (p<0.001)22. Another meta-analysis of 64 studies conducted in India, with 187,990 participants aged 4–19 years, described a similar prevalence of 17% of elevated BP and hypertension, also with significant predominance in overweight children (p<0.001)23. Song et al. conducted a meta-analysis on the worldwide prevalence of childhood hypertension with 186,630 participants under 19 years of age and described that overweight (OR 4.99; 95%CI 2.18–8.81, p<0.001) and obesity (OR 15.27; 95%CI 7.31–25.38, p<0.001) significantly increase the risk of elevated BP6. A systematic review and meta-analysis study with 18,925 children showed that an intervention combining diet and physical activity significantly reduced children’s blood pressure [effect size d= -1.64 mmHg (95%CI -2.56 to -0.71; p=0.001) for systolic BP and d= -1.44 mmHg (95%CI -2.28 to -0.60; p=0.001) for diastolic BP]24.
The high prevalence of elevated blood pressure in this study can be attributed to low socioeconomic status. Martinovic et al. evaluated 434 children aged 6–13 years from two schools in Montenegro and found that the worst socioeconomic level is a risk factor for increased blood pressure (p=0.021)25. In addition, although BP was verified three times in each child, measurements were obtained on the same day. The measurements were performed at the institution, with the presence of teachers and caregivers, but without the family members. Some children may have felt uncomfortable with transient elevated BP, not allowing us to affirm that this alteration represents a definitive diagnosis.
CONCLUSIONS
This study demonstrated that AN and BP increased in one-fifth and one-third of the individuals in an institution for children in situations of social vulnerability with low family income. Overweight and the presence of AN increased the risk of high blood pressure more than twofold.
BP measurement and skin assessment for AN add less time to a pediatric consultation and may help in the early diagnosis of comorbidities associated with childhood obesity, anticipating measures to control overweight and reduce future cardiometabolic risks.
REFERENCES
-
1. World Health Organization. Obesity and overweight. [cited on May 2022]. Available from: http://www.who.int/en/news-room/fact-sheets/detail/obesity-and-overweight
» http://www.who.int/en/news-room/fact-sheets/detail/obesity-and-overweight - 2. Brasil, Instituto Brasileiro de Geografia e Estatísticas, Pesquisa Nacional de Saúde. Atenção Primária à Saúde e Informações Antropométricas. Rio de Janeiro: IBGE; 2020.
-
3. Lopez-Alvarenga JC, Chittoor G, Paul SFD, Puppala S, Farook VS, Fowler SP, et al. Acanthosis nigricans as a composite marker of cardiometabolic risk and its complex association with obesity and insulin resistance in Mexican American children. PLoS One. 2020;15(10):e0240467. https://doi.org/10.1371/journal.pone.0240467
» https://doi.org/10.1371/journal.pone.0240467 -
4. Skinner AC, Perrin EM, Moss LA, Skelton JA. Cardiometabolic risks and severity of obesity in children and young adults. N Engl J Med. 2015;373(14):1307-17. https://doi.org/10.1056/NEJMoa1502821
» https://doi.org/10.1056/NEJMoa1502821 -
5. Spurr S, Bally J, Hill P, Gray K, Newman P, Hutton A. Exploring the prevalence of undiagnosed prediabetes, type 2 Diabetes Mellitus, and risk factors in adolescents: a systematic review. J Pediatr Nurs. 2020;50:94-104. https://doi.org/10.1016/j.pedn.2019.09.025
» https://doi.org/10.1016/j.pedn.2019.09.025 -
6. Song P, Zhang Y, Yu J, Zha M, Zhu Y, Rahimi K, et al. Global prevalence of hypertension in children: a systematic review and meta-analysis. JAMA Pediatr. 2019;173(12):1154-63. https://doi.org/10.1001/jamapediatrics.2019.3310
» https://doi.org/10.1001/jamapediatrics.2019.3310 -
7. Lima MC, Romaldini CC, Romaldini JH. Frequency of obesity and related risk factors among school children and adolescents in a low-income community. A cross-sectional study. Sao Paulo Med J. 2015;133(2):125-30. https://doi.org/10.1590/1516-3180.2014.8960412
» https://doi.org/10.1590/1516-3180.2014.8960412 -
8. World Health Organization. The WHO Child Growth Standards. Genebra: WHO; 2020 [cited on May, 2022]. Available from: https://www.who.int/growthref/en/
» https://www.who.int/growthref/en/ - 9. Brasil, Ministério da Saúde, Secretaria de Atenção à Saúde, Departamento de Atenção Básica. Orientações para a coleta e análise de dados antropométricos em serviços de saúde: Norma Técnica do Sistema de Vigilância Alimentar e Nutricional – SISVAN/Ministério da Saúde, Secretaria de Atenção à Saúde, Departamento de Atenção Básica. Brasília: Ministério da Saúde; 2011. 76 p.
-
10. Onis M. The use of anthropometry in the prevention of childhood overweight and obesity. Int J Obes Relat Metab Disord. 2004;28(Suppl 3):S81-5. https://doi.org/10.1038/sj.ijo.0802810
» https://doi.org/10.1038/sj.ijo.0802810 -
11. Haun DR, Pitanga FJ, Lessa I. Razão cintura/estatura comparado a outros indicadores antropométricos de obesidade como preditor de risco coronariano elevado. Rev Assoc Med Bras (1992). 2009;55(6):705-11. https://doi.org/10.1590/s0104-42302009000600015
» https://doi.org/10.1590/s0104-42302009000600015 -
12. Marshall WA, Tanner JM. Variations in pattern of pubertal changes in girls. Arch Dis Child. 1969; 44(235):291-303. https://doi.org/10.1136/adc.44.235.291
» https://doi.org/10.1136/adc.44.235.291 -
13. Marshall WA, Tanner JM. Variations in pattern of pubertal changes in boys. Arch Dis Child. 1970;45:13-23. https://doi.org/10.1136/adc.44.235.291
» https://doi.org/10.1136/adc.44.235.291 -
14. Sociedade Brasileira de Pediatria. Manual de orientação: hipertensão arterial na infância de adolescência da Sociedade. [cited on May, 2022]. Available from: https://www.sbp.com.br/fileadmin/user_upload/21635c-MO_-_Hipertensao_Arterial_Infanc_e_Adolesc.pdf
» https://www.sbp.com.br/fileadmin/user_upload/21635c-MO_-_Hipertensao_Arterial_Infanc_e_Adolesc.pdf -
15. Kluczynik CE, Mariz LS, Souza LC, Solano GB, Albuquerque FC, Medeiros CC. Acanthosis nigricans and insulin resistance in overweight children and adolescents. An Bras Dermatol. 2012;87(4):531-7. https://doi.org/10.1590/s0365-05962012000400002
» https://doi.org/10.1590/s0365-05962012000400002 -
16. Pool LR, Aguayo L, Brzezinski M, Perak AM, Davis MM, Greenland P, Hou L, Marino BS, Van Horn L, Wakschlag L, Labarthe D, Lloyd-Jones D, Allen NB. Childhood risk factors and adulthood cardiovascular disease: a systematic review. J Pediatr. 2021;232:118-26.e23. https://doi.org/10.1016/j.jpeds.2021.01.053
» https://doi.org/10.1016/j.jpeds.2021.01.053 -
17. Johnson KA, Showell NN, Flessa S, Janssen M, Reid N, Cheskin LJ, et al. Do neighborhoods matter? A systematic review of modifiable risk factors for obesity among low socio-economic status black and hispanic children. Child Obes. 2019;15(2):71-86. https://doi.org/10.1089/chi.2018.0044
» https://doi.org/10.1089/chi.2018.0044 -
18. Hails KA, Zhou Y, Shaw DS. The mediating effect of self-regulation in the association between poverty and child weight: a systematic review. Clin Child Fam Psychol Rev. 2019;22(3):290-315. https://doi.org/10.1007/s10567-019-00279-z
» https://doi.org/10.1007/s10567-019-00279-z -
19. Guran T, Turan S, Akcay T, Bereket A. Significance of acanthosis nigricans in childhood obesity. J Paediatr Child Health. 2008;44(6):338-41. https://doi.org/10.1111/j.1440-1754.2007.01272.x
» https://doi.org/10.1111/j.1440-1754.2007.01272.x -
20. Abraham C, Rozmus CL. Is acanthosis nigricans a reliable indicator for risk of type 2 diabetes in obese children and adolescents? A systematic review. J Sch Nurs. 2012;28(3):195-205. https://doi.org/10.1177/1059840511430952
» https://doi.org/10.1177/1059840511430952 -
21. Novotny R, Davis J, Butel J, Boushey CJ, Fialkowski MK, Nigg CR, et al. Effect of the children’s healthy living program on young child overweight, obesity, and acanthosis nigricans in the US-affiliated pacific region: a randomized clinical trial. JAMA Netw Open. 2018;1(6):e183896. https://doi.org/10.1001/jamanetworkopen.2018.3896
» https://doi.org/10.1001/jamanetworkopen.2018.3896 -
22. Crouch SH, Soepnel LM, Kolkenbeck-Ruh A, Maposa I, Naidoo S, Davies J, et al. Paediatric hypertension in Africa: a systematic review and meta-analysis. EClinicalMedicine. 2021;43:101229. https://doi.org/10.1016/j.eclinm.2021.101229
» https://doi.org/10.1016/j.eclinm.2021.101229 -
23. Meena J, Singh M, Agarwal A, Chauhan A, Jaiswal N. Prevalência de hipertensão entre crianças e adolescentes na Índia: uma revisão sistemática e meta-análise. Indian J Pediatr. 2021;88(11):1107-14. https://doi.org/10.1007/s12098-021-03686-9
» https://doi.org/10.1007/s12098-021-03686-9 -
24. Cai L, Wu Y, Wilson RF, Segal JB, Kim MT, Wang Y. Effect of childhood obesity prevention programs on blood pressure: a systematic review and meta-analysis. Circulation. 2014;129(18):1832-9. https://doi.org/10.1161/CIRCULATIONAHA.113.005666
» https://doi.org/10.1161/CIRCULATIONAHA.113.005666 -
25. Martinovic M, Belojevic G, Evans GW, Asanin B, Lausevic D, Kovacevic ND, Samardzic M, Jaksic M, Pantovic S. Blood pressure among rural Montenegrin children in relation to poverty and gender. Eur J Public Health. 2014;24(3):385-9. https://doi.org/10.1093/eurpub/ckt181
» https://doi.org/10.1093/eurpub/ckt181
Publication Dates
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Publication in this collection
25 Nov 2022 -
Date of issue
2022
History
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Received
15 June 2022 -
Accepted
03 Sept 2022
