Accuracy of clinical indicators of the nursing diagnosis of dysfunctional gastrointestinal motility in infants

Abstract

This study aimed to analyze the accuracy of the clinical indicators of the nursing diagnosis of dysfunctional gastrointestinal motility in infants from neonatal units and identify their association with clinical variables. This is a study of the diagnostic accuracy of clinical indicators of the diagnosis of dysfunctional gastrointestinal motility, with a cross-sectional design, performed on 228 hospitalized infants in neonatal units. A high prevalence of dysfunctional gastrointestinal motility was identified in the studied population. Regarding accuracy measures, clinical indicators such as increased gastric residual, changes in bowel sounds, bile-colored gastric residual, regurgitation, absence of flatus, and hard and formed stool were useful to discriminate between infants with and without dysfunctional gastrointestinal motility. The findings can help nurses during the diagnostic process, as they identify which defining characteristics can be used to confirm or rule out the probability of occurrence of the diagnosis.

Keywords

Nursing diagnosis validation studies accuracy gastrointestinal motility newborn

Introduction

Gastrointestinal motility is a physiological phenomenon that favors the digestive process and involves the movement of food substances through the intestine and the absorption of nutrients, water and electrolytes and the elimination of waste (Faure et al., 2017). It is a complex function and depends on the integration of biochemical, anatomical, food, infectious and pharmacological factors (Viswanathan and Jadcherla, 2019). Thus, for the proper movement of ingested substances through the intestine, it is necessary that the reflexes of gastrointestinal motility develop, and this occurs from the 30th week of gestation and reaches maturation gradually in the first years of life (Macdonald et al., 2007).

Premature birth before 37 weeks of gestational age can cause developmental abnormalities in many of the components of the gastrointestinal system, thus causing gastrointestinal motility dysfunction (Neal-Kluever et al., 2019). Infants with this type of dysfunction have lower survival rates, as it directly interferes with the vital functions of nutrition and elimination, which are essential for maintaining life and can lead to irreversible damage in growth and development (Duggan and Jaksic, 2017).

In addition to the physiological immaturity of the development of the gastrointestinal tract that occurs due to premature birth, other clinical conditions may contribute to dysfunctional gastrointestinal motility in infants, such as nutritional disorders, increased intracranial pressure, use of mechanical ventilation, hemodynamic instability, use of vasoactive drugs, opioids and muscle relaxants that act on gastrointestinal receptors, that is, common conditions in hospitalized infants in a neonatal unit (Magalhães et al., 2009; Rang et al., 2012).

Data on the incidence of dysfunctional gastrointestinal motility are rare due to the varied clinical conditions that can lead to this morbidity and demonstrate a low incidence (Duggan and Jaksic, 2017). In a study carried out in Toronto, Canada, the incidence of 24.5 cases per 100,000 live births was estimated (Wales et al., 2004). Corroborating this evidence, a study carried out in 16 tertiary neonatal centers in the United States identified a frequency of 1.1% of very low birth weight newborns with dysfunctional gastrointestinal motility (Cole et al., 2008).

All clinical conditions reported above compromise the function of the gastrointestinal system and may influence the appearance of signs and symptoms characteristic of the nursing diagnosis dysfunctional gastrointestinal motility (DGM) (00,196), present in the NANDA-International Taxonomy (NANDA-I).

Background

The DGM diagnosis was included in this taxonomy in 2008 and was revised in 2017 and is defined as “increased, decreased, ineffective or absent peristaltic activity in the gastrointestinal system” (Herdman and Kamitsuru, 2018: p.243). It has 14 clinical indicators: increased gastric residual, bile-colored gastric residual, absence of flatus, accelerated gastric emptying, nausea, abdominal cramping, diarrhea, hard and formed stool, distended abdomen, difficulty defecating, abdominal pain, changes in bowel sounds, regurgitation, and vomiting (Herdman and Kamitsuru, 2018).

To make an accurate diagnosis, direct the planning of nursing actions and quickly reverse this condition to prevent other problems related to health care in the neonatal population, an accurate diagnostic inference is necessary (Paans et al., 2012). Therefore, it is necessary to define clinical indicators that more accurately predict the occurrence of this diagnosis (Paans et al., 2012). Thus, studies of diagnostic accuracy are useful because of their prediction ability, which involves judgment as to the degree of relevance, specificity and consistency of the existing indicators for a diagnosis (Lopes et al., 2012).

The identification of a set of accurate indicators can differentiate individuals with and without a nursing diagnosis, establish greater reliability of the diagnostic choice and contribute to quick, safe and more effective decisions (Pereira et al., 2015). Therefore, the question is as follows: which clinical indicators best predict the nursing diagnosis of dysfunctional gastrointestinal motility in hospitalized infants in a neonatal unit?

Scientific evidence regarding this nursing diagnosis is still limited, and studies of diagnostic accuracy can help to accurately infer nursing diagnoses (Lunney, 2003), specifically in the care field of neonatology. In this specific population, nurses must recognize the early signs and symptoms of the diagnosis of dysfunctional gastrointestinal motility, considering the high vulnerability of this population to clinical conditions that can compromise their health status (Neal-Kluever et al., 2019).

Aims

To analyze the accuracy of the clinical indicators of the nursing diagnosis dysfunctional gastrointestinal motility in infants and to verify associations between the clinical indicators of this nursing diagnosis and other clinical variables of this population.

Methods

Design

Diagnostic accuracy study of clinical indicators of nursing diagnosis dysfunctional gastrointestinal motility, with cross-sectional design.

Setting

The study was developed in Conventional Neonatal Intermediate Care Units and Neonatal Intensive Care Units in two tertiary public hospitals, characterized by assistance, teaching and research, located in northeastern Brazil. The first hospital has up to 51 neonatal acute care beds for premature and high-risk infant care. The second hospital has up to 31 neonatal acute care beds and serves as a referral center for neonatal surgery.

All parents/guardians were informed about the purpose of the study and consented to the collection of data by signing the informed consent form. Concerning the research’s ethical aspects, this study was submitted and approved by the Research Ethics Committee (approval number: 1.292.620), on 1 October 2015. The study was conducted according to the Declaration of Helsinki.

Sample

The participants were selected using the consecutive sampling procedure; as such, newborns admitted to the study site were consecutively enrolled if they met the inclusion criteria (Hulley, et al., 2015). Newborns and infants hospitalized with a minimum stay of 24 h, with gestational age between 24 and 42 weeks, were included, confirmed by the New Ballard scale or by the somatic Capurro assessment technique. Exclusion criteria were newborns whose health status worsened with physical examination or children who had congenital abdominal malformations that prevented data collection, such as gastroschisis and omphalocele not corrected by surgical methods.

Of the 14 clinical indicators present in the NANDA-I taxonomy, three were not evaluated: accelerated gastric emptying, nausea and abdominal cramping. The lack of evaluation of these indicators was due to the specificity of the study population, because neonates and infants cannot verbally communicate and these assessment methods were not routinely performed in neonatal units where data were collected.

To determine the required sample size, a latent class model was used, as has been recommended: 15 to 30 individuals must be included for each clinical indicator (Swanson et al., 2012). For this study, 20 subjects were adopted for each indicator. The total number of clinical indicators evaluated was 11. Given the above, the sample included 228 children hospitalized in neonatal units.

Data collection

The data were collected by trained nurses with the aid of an instrument that directed the performance of the abdominal physical examination and consultation of the child’s medical record. For data collection, we developed an instrument that was subdivided into four parts: (1) sociodemographic data (name, date of assessment, date of birth, days of life, sex, diagnosis and length of stay), (2) data of birth (type of delivery, Apgar score, twinning, birth weight, height, history of cardiopulmonary resuscitation), (3) clinical data (type of diet, form of diet administration, drugs used, history of diseases of the gastrointestinal tract) and (4) evaluation of the clinical indicators of the diagnosis of dysfunctional gastrointestinal motility through abdominal physical examination and consultation of medical records.

The data collection instrument used was based on the operational definitions developed for each clinical indicator drawn from the literature and submitted to the evaluation of a group of professors and students experienced in diagnostic accuracy studies who are members of a research group that studies nursing diagnosis in children. After the discussion, concept texts were adjusted for better results.

Data analysis

The data were analyzed with the support of R version 2.12.1 software (R Development Core Team, Vienna, Austria). The descriptive analysis includes calculations of absolute frequencies, percentages, measures of central tendency and dispersion. The proportions of categorical variables were calculated, including 95% confidence intervals. The Kolmogorov-Smirnov test verified adherence to a normal distribution. The chi-square test or Fisher-Freeman-Halton exact probability test verified the association between clinical indicators and nursing diagnosis, according to the expected frequencies of each category. The magnitude of the relationship between clinical indicators and categorical variables of interest was measured by the prevalence ratio and 95% confidence intervals. The Mann-Whitney test verified the comparison of the average positions of the clinical variables between individuals with or without the diagnosis.

The measures of accuracy of sensitivity and specificity of each clinical indicator were based on the latent class analysis (LCA) method. To verify the models generated by the LCA, the likelihood ratio test (G2) and Pearson’s chi-square test (X₂) were applied. A clinical indicator was considered statistically significant if at least one of its confidence intervals (either for sensitivity or specificity) was higher and did not exceed 0.5.

Results

Sample characteristics

Of the 228 infants, 135 (59.2%) were male, 152 (66.3%) were born through abdominal delivery (cesarean section), and 85 (37.3%) received cardiopulmonary resuscitation at birth. The mean Apgar score at 1 min was 7 (±3), and at 5 min was 8 (±1). The infants had a mean of 15 (±27) days of life, 14 (±27) days of hospitalization, birth weight of 1470 (±1079) grams, height of 40 (±10) centimeters, weight loss of 0 (±0), and gestational age of 32 (±7) weeks. The weight loss variable was measured according to birth weight and the weight presented on the day of capture of these newborns for study sample.

The most frequent medical diagnosis in the sample was prematurity, corresponding to 221 (92.5%), followed by respiratory distress syndrome with 162 (71.1%), neonatal maternal infection with 73 (32%), and jaundice with 59 (25.9%). It is worth mentioning that, among the infants evaluated, 108 (46%) were diagnosed with changes during hospitalization; among them, the most frequent was food intolerance with 58 (25.4%) cases, followed by gastroesophageal reflux with 34 (14.5%) cases, and necrotizing enterocolitis with 7 (3.1%) cases.

Regarding the use of drugs, 182 (79.8%) of the sample received medications during the data collection period. Among the most used were multivitamins, which corresponded to 98 (46.1%), followed by antibiotics with 98 (43.0%) and gastrointestinal tract drugs with 56 (24.6%).

The type of milk that presented the highest frequency of supply was pasteurized human milk (PHM), corresponding to 83 (36.4%) infants, followed by expressed breast milk (69; 30.3%) and formula milk (FM) (46; 20.2%). The most frequently used routes of diet administration were orogastric tube (OGT) with 126 (55.3%), oral route (OR) with 57 (25%), and nasoenteral tube (NET) with 22 (9.6%). The diet administration modalities were gravity feeding (169; 73.2%) and pump administration (28; 11.2%).

Table 1 lists the clinical indicators of the nursing diagnosis. Clinical indicators of dysfunctional gastrointestinal motility were evaluated, and among them, the most frequent in the studied population was an increase in gastric residual (52.6%), followed by changes in bowel sounds (46.5%), regurgitation (39.5%) and distended abdomen (39.5%).

Table 1.

Distribution of clinical indicators of the nursing diagnosis of dysfunctional gastrointestinal motility in infants.

Clinical indicators	n	%	CI 95%
Increased in gastric residual	120	52.6	45.9–59.2
Changes in bowel sounds	106	46.5	39.9–53.2
Regurgitation	90	39.5	33.1–46.2
Distended abdomen	68	29.8	24.1–36.3
Difficulty defecation	65	28.4	22.8–34.9
Diarrhea	59	25.9	20.4–32.2
Absence of flatus	45	19.7	14.9–25.6
Bile-colored gastric residual	43	18.9	14.1–24.7
Hard, formed stool	42	18.4	13.7–24.2
Abdominal pain	40	17.5	13–23.2
Vomiting	22	9.6	6.3–14.4

n = absolute frequency; % = percentage; CI 95%: 95% confidence interval.

Diagnostic inferences

The final model, shown in Table 2, included six clinical indicators, of which increased gastric residual showed high values for sensitivity and specificity (100% for both measurements). Changes in bowel sounds (sens. = 60%; spec. = 70%) and regurgitation (sens. = 59%; spec. = 83%) were also important indicators for the inference of the diagnosis. The bile-colored gastric residual (spec. = 100%), absence of flatus (spec. = 86%) and hard, formed stool (spec. = 79%) stood out as indicators that help confirm the diagnosis under study. Finally, the prevalence of the dysfunctional gastrointestinal motility nursing diagnosis was estimated using the latent class model with random effects in 52.6%.

Table 2.

Measures of diagnostic accuracy of clinical indicators of the diagnosis of dysfunctional gastrointestinal motility in infants, obtained from latent class analysis with random effects.

Clinical indicators	Se	CI 95%	Sp	CI 95%	PPV	CI 95%	NPV	CI 95%
Increased in gastric residual	1.0000	1.0000	1.0000	1.0000	0.9998	1.0000	1.0000	0.9998	1.0000	1.0000	1.0000	1.0000
Changes in bowel sounds	0.6163	0.4818	0.6978	0.7043	0.6061	0.7939	0.6984	0.5761	0.7900	0.6229	0.5128	0.7028
Regurgitation	0.5997	0.4616	0.6767	0.8341	0.7456	0.8934	0.8006	0.6684	0.8758	0.6522	0.5548	0.7132
Bile-colored gastric residual	0.3588	0.2475	0.4300	1.0000	1.0000	1.0000	1.000	1.000	1.000	0.5840	0.5446	0.6123
Absence of flatus	0.2506	0.1752	0.3328	0.8618	0.7833	0.9153	0.6683	0.4732	0.8136	0.5086	0.4608	0.5525
Prevalence: 52.63%		G² = 61.32	df = 50	p = 0.131

Notes: CI: 95% confidence interval; Se: sensitivity; Sp: specificity; NPV: negative predictive value; PPV: positive predictive value.

Statistical association between clinical variables and clinical indicators

Among the variables that showed a statistically significant association with the occurrence of the increased gastric residual indicator, these clinical variables stand out: use of cardiovascular drugs (OR = 8.68, 95% CI = 1.08–69.65), gastroesophageal reflux, cardiovascular resuscitation (OR = 1.74, 95% CI = 1.01–3.00), enterocolitis (OR = 1.92, 95% CI = 1.07–3.44) and type of milk offered.

Infants who had the bile-colored gastric residue indicator had a statistically significant association with the following clinical variables: perinatal anoxia (OR = 0.24, 95% CI = 0.06–1.05), use of drugs (OR = 6.40, 95% CI = 1.49–27.52), antibiotics (OR = 4.55, 95% CI = 2.19–9.45), enterocolitis (OR = 2.41, 95% CI = 1.22–4.78) and use of formula milk. It is noteworthy that it was not possible to calculate the OR and 95% CI for some variables of the clinical indicators, such as increase in gastric residue and gastric residue in bile color, due to the presence of null values.

It was observed that the neonates that had the clinical indicator regurgitation had hyperglycemia (OR = 11.55, 95% CI = 1.40–95.58), hypoglycemia (OR = 5.00, 95% CI = 1.31–19.01) and use of diuretics (OR = 4.66, 95% CI = 1.44–15.14). Neonates who had jaundice (OR = 0.48, 95% CI = 0.25–0.91), neonatal sepsis (OR = 0.36, 95% CI = 0.14–0.92) and who were using multivitamins (OR = 0.53, 95% CI = 0.31–0.91) had a 52% reduction in the chance of manifesting the regurgitation indicator, at 64% and 47%, respectively.

Only one clinical variable was associated with the indicator changes in bowel sounds: perinatal anoxia (OR = 3.67, 95% CI = 1.62–8.32). Infants with neonatal sepsis (OR = 0.26, 95% CI = 0.10–0.66) had a 74% reduction in the chance of exhibiting changes in bowel sounds.

Infants who had the distended abdomen indicator had perinatal anoxia (OR = 4.71, 95% CI = 2.18–10.18), neonatal maternal infection (OR = 7.98, 95% CI = 2, 09–30.50), use of drugs (OR = 7.96, 95% CI = 2.38–26.68), intestinal obstruction (OR = 9.90, CI 95% = 1.09–90.90), and enterocolitis (OR = 4.33, 95% CI = 2.35–8.00).

Among the associations with the abdominal pain indicator, the following were significant: perinatal anoxia (OR = 2.39, 95% CI = 1.03–5.53), gastrointestinal tract diseases (OR = 3.23, 95% CI = 1.58–6.62) and gastroesophageal reflux (OR = 4.15, 95% CI = 1.69–10.20).

For the absence of flatus indicator, the clinical variables that stood out were cardiopulmonary resuscitation (OR = 2.04, 95% CI = 1.05–3.95), cardiovascular drugs (OR = 4.45, 95% CI = 1.23–16.10) and diseases of the gastrointestinal tract (OR = 2.24, 95% CI = 1.11–4.51). Only two clinical variables were associated with the diarrhea indicator: hypovolemic shock (OR = 7.73, 95% CI = 1.46–41.0) and gastrointestinal tract diseases (OR = 0.39, 95 CI % = 0.17–0.89).

Clinical variables associated with the hard, formed stool indicator were cardiopulmonary resuscitation (OR = 2.15, 95% CI = 1.09–4.22) and use of nervous system drugs (OR = 4.16, 95% CI = 1.68–10.3).

Only the clinical variable intestinal obstruction (OR = 10.64, 95% CI = 1.16–100.00) was associated with the indicator of difficult defecation. Clinical variables respiratory distress syndrome (OR = 0.36, 95% CI = 0.20–0.67) and multivitamins (OR = 0.49, 95% CI = 0.27–0, 90) were presented as protective factors for the indicator of difficult defecation.

Discussion

Dysfunctional gastrointestinal motility was present in 52.6% of the infants. When analyzing the defining characteristics, increased gastric residual achieved high sensitivity and specificity values. Besides, bile-colored gastric residual, absence of flatus, and hard formed stool achieved high specificity values.

Studies that approach the accuracy of the indicator can help nurses identify a set of clinical characteristics that can better predict a particular nursing diagnosis. Thus, the precision of the measurements indicates the predictability of each defining characteristic, allowing us to distinguish individuals with a diagnosis of interest from individuals without a diagnosis (Lopes et al., 2012). Thus, the contribution of this type of study becomes even more significant for nursing diagnoses with little research and those that are poorly understood in specific populations, such as children with gastrointestinal motility disorders.

Among these problems, gastrointestinal motility disorders stand out and may be related to several etiologies, ranging from clinical conditions identified after delivery as well as clinical conditions acquired during the hospitalization period (Magalhães et al., 2009; Rang et al., 2012).

Gastrointestinal motility disorders can be commonly identified in hospitalized infants in neonatal units for multiple causes, which may compromise digestion and adequate absorption preventing satisfaction of the nutritional system, thus generating changes in nutritional patterns, growth and development (Duggan and Jaksic, 2017). Thus, the confluence of clinical conditions identified after delivery, as well as clinical conditions acquired during the hospitalization period, may justify the occurrence of clinical indicators increased in gastric residual, changes in bowel sounds, regurgitation, bile-colored gastric residual, absence of flatus and hard and formed stool because these signs and symptoms are related to gastrointestinal disorders.

The present study showed a lower frequency of the nursing diagnosis of dysfunctional gastrointestinal motility in infants when compared with another scientific finding found in a neonatal unit in northeastern Brazil, which had a prevalence of 70% in the newborns analyzed (Santos et al., 2014). The higher prevalence of this diagnosis in the cited literature is explained by the fact that the infants evaluated had sepsis, that is, a severe clinical condition when compared to this study, where not all infants had this condition (Medeiros et al., 2016).

Regarding the diagnostic accuracy measures, the indicator increased in gastric residual showed high values of sensitivity (100%) and specificity (100%). This suggests that, in the presence of dysfunctional gastrointestinal motility, patients had a high probability of increased gastric waste, whereas in the absence of dysfunctional gastrointestinal motility, this indicator will probably be absent; thus, it presented with good predictive capacity for this diagnosis. Similar findings have been reported in other studies that proved that the volume of gastric waste was higher among children with some type of gastrointestinal dysfunction than those without this condition (Bertino et al., 2009; Cobb et al., 2004).

In this study, the increase in gastric residual was associated with gastroesophageal reflux, cardiovascular resuscitation, use of cardiovascular drugs, necrotizing enterocolitis, and formula milk. These findings were consistent with other studies that showed a correlation between this indicator and these clinical variables (den Braber-Ymker, et al., 2017; López-Herce et al., 2008; Surmeli-Onay et al., 2013).

The justification to corroborate these associations is the deficiency or inadequacy of esophageal sphincters causing a delay in emptying the stomach of the administered diet, in the case of gastroesophageal reflux (Magalhães et al., 2009), circulatory decrease in the mesenterial area after cardiovascular resuscitation (Mally et al., 2010), and use of drugs with effects on the smooth muscles of the gastrointestinal tract that can affect the hormonal release of gastric motility modulators, as in the case of cardiovascular drugs and opioid analgesics (Rang et al., 2012), the inflammatory response in the intestinal mucosa caused by necrotizing enterocolitis, supply of liquid foods with low temperature that cause relaxation of the gastric muscles (Duggan and Jaksic,2017) and formula milk due to its different chemical composition from human origin (Macdonald et al., 2007).

The clinical indicators that showed high specificity values, that is, those indicators that are useful for discriminating between infants with and without the nursing diagnosis dysfunctional gastrointestinal motility, were bile-colored gastric residual (100%), absence of flatus (86%), regurgitation (83%), hard and formed stool (79%) changes in bowel sounds (70%). Thus, infants who did not present this diagnosis also have a greater chance of not having these indicators.

All indicators that showed high specificity, except hard and formed stool, showed an important association with the clinical condition of perinatal anoxia. Perinatal anoxia is a disorder of impaired gas exchange that results in fetal hypoxemia and hypercapnia and thus compromises intestinal blood flow, causing a decrease in this flow, increasing the risk of tissue ischemia, and thus influencing the appearance of signs and clinical symptoms of dysfunctional gastric motility (Abrahamsson, 2017; Eaton et al., 2017).

Neonatal sepsis was another clinical condition that showed an important association with the indicators of this highly specific study, except for the indicators absence of flatus and hard and formed stool. This condition is defined as a systemic response to infection characterized by a clinical syndrome with several systemic manifestations, and among the signs and symptoms of this condition are gastrointestinal manifestations (Medeiros et al., 2016).

The use of formula milk showed an important association with clinical indicators of high specificity: bile-colored gastric residual, regurgitation, and changes in bowel sounds. Corroborating these data, a meta-analysis comparing the effect of formula milk versus human milk in newborns found that those fed formula milk had a higher risk of developing signs and symptoms of gastrointestinal dysfunction (Quigley and McGuire, 2014). Other studies have identified higher proportions in the fecal microbiota of bacteria of the genera Escherichia and Clostridium, the main bacteria associated with gastroenteritis, in newborns using formula milk than in those using exclusive human milk (Subramanian et al., 2014; Zanella et al., 2019).

Limitations

The cross-sectional approach, which is concentrated at a single timepoint, limited the monitoring of some clinical indicators that would be best represented longitudinally. In view of the specificity mentioned in the population, the registration of professionals had been used as a source of information, making it a limitation of the study, since subjectivity may have interfered with the results obtained. Thus, further research is suggested for this nursing diagnosis in the infant population to make comparisons. The lack of studies was identified in the literature using methods of measurement and analysis similar to this study, which may have limited the comparison of results.

Relevance to clinical practice

Despite the study’s limitations, identifying sensitive and specific defining characteristics of this nursing diagnosis allows the nurse to intervene early, favoring gastrointestinal motility maintenance. This early intervention reduces the gastrointestinal and nutritional complications increasing the survival of these infants. The evidence obtained from the gastrointestinal motility assessments and the accuracy analysis can guide pediatric nurses in their diagnostic decision-making. High sensitive indicators should be used as warning signs for dysfunctional gastrointestinal motility, and high specific indicators should be used as a confirmatory sign of this condition.

Conclusion

A high prevalence of the nursing diagnosis of dysfunctional gastrointestinal motility was identified in the population studied. Among the clinical indicators useful in discriminating between infants with and without dysfunctional gastrointestinal motility are increased gastric residual, changes in bowel sounds, bile-colored gastric residual, regurgitation, absence of flatus and hard and formed stools. Related to the clinical indicators were the conditions of birth, diseases registered from the moment of delivery until the evaluation period of infants, and the treatment performed during hospitalization.

Footnotes

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

Ethical approval

Concerning the research’s ethical aspects, this study was submitted and approved (approval number: 1.292.620) by the Research Ethics Committee, on 1 October 2015. The study was conducted according to the Declaration of Helsinki.

ORCID iDs

Viviane M. da Silva

Marcos Venícios de Oliveira Lopes

Nayana Maria Gomes de Souza

Nirla Gomes Guedes

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