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\def\RunningAuthor{Hulal Saleh Sahib }
\firstPage{669}
\articleType{Original Article}
\receivedDate{12.09.2019}
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\title{Adenoid hypertrophy among school-aged Iraqi children, the effect of severity and duration on its co-morbidities}
\author{Hulal~Saleh~Sahib\textsuperscript{*}~\\[5pt]{Department of Pediatrics, College of Dentistry, University of Al-Qadisiyah, Al Diwaniyah, Iraq}}

\begin{abstract}
Adenoid hypertrophy is a common pediatrics health problem that usually results in several morbidities such as sleep disorder, adenoid facies, impaired physical growth, cardiac complications, glue ear and nocturnal enuresis. Patients and methods:\textbf{\space }Forty-two school-aged children were enrolled in this study (6-12 years old), thirty were male and twelve were female, all are suffering from chronic snoring. All of them were subjected to standard history and physical examination to the most related health problems such as assessment of physical growth, craniofacial malformation, associated tonsillar enlargement. Investigations were performed in the form of lateral neck X-ray and ECG for all of them. The study period was 9 months from 1\ensuremath{^{st}} of March 2018 to the 1\ensuremath{^{st}} of December 2018. Results:\textbf{\space }There was a significant association between a higher grade of disease and speech disorders, tonsillar hypertrophy, adenoid facies, recurrent otitis media, nocturnal enuresis, impaired school performance, physical growth impairment, apnea at sleep, day time drowsiness, ECG abnormalities and deglutition problems (\textit{P} \textless\ 0.05). \textbf{\space }The associated co-morbidities, namely Speech disorders, tonsillar hypertrophy, adenoid facies, recurrent otitis media, nocturnal enuresis, impaired school performance, impaired school performance, physical growth impairment, apnea at sleep, day time drowsiness, ECG abnormalities and deglutition problems, were significantly correlated to the longer duration of disease. Conclusion:\textbf{\space }Longer duration of disease and higher grade of adenoid hypertrophy are strongly correlated with disease complications and morbidities, hence early diagnosis and properly timed management is important to prevent these complications.
\end{abstract}\def\keywordstitle{Keywords}

\begin{keywords}pediatrics,\newline Adenoid,\newline hypertrophy,\newline co-morbidities,\newline Iraq
\end{keywords}
\twocolumn[ \maketitle {\printKwdAbsBox}]
\makeatletter{\raggedright\textsuperscript{*}Corresponding Author\par Name:\ Hulal~Saleh~Sahib~\\ Phone:\ ~\\  Email:\ Hulal.sahib@qu.edu.iq
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\section{Introduction}
Adenoids are masses of lymphoid tissue sited at the posterior part of the nasopharynx. It performs a remarkable immunological function by a reaction to inhaled or ingested pathogens. The adenoidal size varies among children, and it also changes in the same person as he becomes older.

In general, increasing the size of adenoid is usually happens between 5-7 years, later it usually regresses until completely disappear by the age of 20 in most \unskip~\citep{664883:15668130}. 

When adenoid hypertrophy, it will result in obstruction to posterior choanae causing airflow impedance. Hence if left untreated it may result in many health problems such as otitis media, disordered sleep, impaired physical growth, pulmonary hypertension, nocturnal enuresis, poor school performance, dental and maxillofacial developmental problems \unskip~\citep{664883:15668131}. 

Middle ear disease secondary to adenoid hypertrophy are seen frequently as a result of Eustachian tube dysfunction. This may result in hearing loss if persistent middle ear disease.

Associated tonsillar hypertrophy is another problem that may worsen upper airway obstruction (both adenoid and tonsillar tissue are part of waldeyer ring, they can be enlarged secondary to both inflammatory and allergic factors) \unskip~\citep{664883:15668132,664883:15668134}.

Snoring is a common complaint among adenoidal patients as upper airway obstruction makes breathing harder on rest.  Chronic sinusitis can also be seen in those patients as hypertrophied lymphoid tissue will disrupt good drainage of sinus cavities \unskip~\citep{664883:15668133}.  

Deglutition problems may take place as the enlarged tissue hinder the ingestion of foods.  

Faltering growth in the form of underweight and stunting are confirmed by many studies.\ensuremath{^{}} Mechanisms standing behind that are decreased intake, increased caloric consumption as a result of hard night breathing, hypoxia at night and abnormal night time growth hormone production.

Obstructive sleep apnea syndrome is a condition of night time hypoxia resulting from the severe situation of upper airway obstruction\ensuremath{^{. }} Its commonly caused by adenoid hypertrophy in children. 

If long-standing cases of chronic hypoxia, pulmonary hypertension, right ventricular hypertrophy and cor-pulmonale are a sequlae \unskip~\citep{664883:15668136}.

Obstructive sleep apnea may cause many day time and night time troubles. The child usually suffers from drowsiness and increasing sleeping tendencies during the day. At night there is usually increasing loudness and frequency of snoring with breathing difficulty, apnea, unsteady sleeping posture and nocturnal enuresis \unskip~\citep{664883:15668137,664883:15668138}. 

Nocturnal enuresis is not an uncommon problem in patients with sleep breathing disorder may be related to decreased arousal, increased intra-abdominal pressure causing increased bladder pressure, altered urodynamic, inappropriate vasopressin hormone level \unskip~\citep{664883:15668139}.

There are a number of complications related to obstructive sleep apnea, including cardiac complications, cognitive and behavioral problems \unskip~\citep{664883:15668140}. 

If adenoid hypertrophy was left untreated, all of the obstructive sleep apnea, failure to thrive, craniofacial malformation, ear problems and pulmonary hypertension will be reported. 

To determine whether adeno-tonsillar enlargement is sufficient to cause significant symptoms, the physician depend on a detailed history and physical finding (which is not usually much helpful in determining the degree of adenoidal enlargement). Hence imaging and endoscopic evaluation is prerequisite \unskip~\citep{664883:15668141}. 

The size of adenoid and space available in the nasopharynx are the main determinant of the severity of symptoms \unskip~\citep{664883:15668142}.

Lateral nasopharyngeal x-ray is still used as a diagnostic way to evaluate adenoidal size as it assesses the adenoid nasopharyngeal ratio (ANR); it's simple and valuable.  

Adenoidectomy with or without tonsillectomy are the usual approach for adenoid hypertrophy as they relieve all the obstructive symptom, but they may result in many serious complications like bleeding and postoperative respiratory compromise \unskip~\citep{664883:15668143}. 

Obstructive sleep apnea is an absolute indication to adenoidectomy, there are many other indications including growth failure, glue ear, chronic or recurrent sinusitis and craniofacial anomalies \unskip~\citep{664883:15668144}. 

Medical treatments are taken into account by numerous studies.\ensuremath{^{}} The use of intranasal corticosteroid was approved to be effective by their anti-inflammatory action \unskip~\citep{664883:15668145}.

Further studies support the use of antibiotics (antibacterial) azithromycin as it has a valid action against streptococcal pneumonia, H. influenza and B-lactamase bacteria.\ensuremath{^{}} Azithromycin and intranasal fluticasone are shown to be suitable for mild to moderate adenoidal hypertrophy. 

\textbf{Aim of The Study }
  
  \begin{enumerate}
  \item \relax To estimate the clinical issues and morbidities among school-aged Iraqi children with adenoid hypertrophy.
  \item \relax To assess the correlation between disease morbidities with the severity and duration of the disease.
  \end{enumerate}
  
    
\section{Patients and Methods}
Forty-two school-aged children were enrolled in our study (6-12 years old), thirty were male and twelve were female, all are suffering from chronic snoring. The study period was 9 months from 1\ensuremath{^{st}} of March 2018 to the 1\ensuremath{^{st}} of December 2018.

Those children were evaluated in the pediatric outpatient consultation clinic at maternity and pediatric teaching hospital at Al Diwaniyah province / Iraq. Oral consent was possessed from their parents or their caregiver.

All of them were subjected to a standard history regarding their gender, residency, socioeconomic status, duration of symptoms, their past history of recurrent or chronic otitis media, chronic sinusitis, nocturnal enuresis, disordered sleep, deglutition problems, speech troubles and their school performance. 

Physical examination was also done to the most related clinical signs such as assessment of physical growth (underweight, stunting), craniofacial changes (adenoid facies, open-mouthed patients with long and narrow face), throat examination for associated tonsillar enlargement and ear examination.

All children who have a history of chronic upper airway obstruction secondary to other causes (such as allergic rhinitis and septal deviation), facial anomaly and developmental and mental subnormality were excluded from the study.

Investigations were performed in the form of lateral nasopharyngeal X-ray to assess the grade of adenoidal enlargement, which is regarded as follow;

\textbf{Grade 1}

mild adenoidal enlargement (when the adenoid tissue occludes about less than 50\% of nasopharynx).

\textbf{Grade 2}

moderate adenoidal enlargement (when the adenoid tissue occludes 50-75\% of nasopharynx).

\textbf{Grade 3}

severe adenoidal enlargement (when the adenoid tissue occludes {\textgreater}75\% of nasopharynx).

As cardiac complication is a possibility facing a patient with adenoidal enlargement ECG was done for all the study groups. 
    
\section{Results and Discussion}
The current study includes 42 cases of adenoid hypertrophy with a mean age of 8.93 \ensuremath{\pm} 1.93 years and an age range of 6 {\textendash} 12 years. The sample included 30 (71.4 \%) males and 12 (28.6 \%) females with a male: female ratio of 2.5:1. According to residency, children were classified into 21 (50.0 \%) and 21 (50.0 \%) as urban and rural, respectively. With respect to socioeconomic status, the sample was categorized into 18 (42.9 \%), 20 (47.6 \%) and 4 (9.5 \%) as being poor, of moderate status and good, respectively. These demographic data are demonstrated at Table~\ref{tw-27e30170c5dc}.

The disease characteristics, namely duration of symptoms and severity grade, are shown in Table~\ref{tw-73b4c6f887de}. The mean duration was 2.21 \ensuremath{\pm} 1.02 years and it ranged from 1 to 4 years. According to grade, patients were grouped into 4 (9.5 \%), 15 (35.7 \%) and 23 (54.8 \%) as mild (grade I), moderate (grade II) and severe adenoid enlargement (grade III), respectively, Table~\ref{tw-73b4c6f887de}.

The association between disease grading and associated co-morbidities and complications is shown in Table~\ref{tw-326481aa0605}. From a statistical perspective, grade III was contrasted against grade I~and grade II (combined as a single group) because chi-square produced more than 20 \% of cells with an expected count of \textless\ 5 when grades were considered separately; Fischer exact test was used instead. There was a significant association between a higher grade of disease and speech disorders, tonsillar hypertrophy, adenoid facies, recurrent otitis media, nocturnal enuresis, impaired school performance, physical growth impairment, apnea at sleep, day time drowsiness, ECG abnormalities and deglutition problems (\textit{P} \textless\ 0.05), as shown in Table~\ref{tw-326481aa0605}.

The associated co-morbidities, namely speech disorders, tonsillar hypertrophy, adenoid facies, recurrent otitis media, nocturnal enuresis, impaired school performance, physical growth impairment, apnea at sleep, day time drowsiness, ECG abnormalities and deglutition problems, were significantly correlated to longer duration of disease, as shown in Table~\ref{tw-8c21e838cdc3}. 


\begin{table*}[!htbp]
\caption{\boldmath {Demographic characteristics of the study sample } }
\label{tw-27e30170c5dc}
\centering 
\begin{threeparttable}

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\tbltoprule \rowcolor{kwdboxcolor}Characteristic &  Value\\
\tblmidrule 
Number of cases &
  42\\
Age (years)  &
  \\
Range &
  6 {\textendash} 12\\
Mean \ensuremath{\pm}SD &
  8.93 \ensuremath{\pm} 1.93\\
Gender &
  \\
Male, n (\%) &
  30 (71.4 \%)\\
Female, n (\%) &
  12 (28.6 \%)\\
Residency &
  \\
Urban, n (\%) &
  21 (50.0 \%)\\
Rural, n (\%) &
  21 (50.0 \%)\\
Socioeconomic status  &
  \\
Poor, n (\%) &
  18 (42.9 \%)\\
Moderate, n (\%) &
  20 (47.6 \%)\\
Good, n (\%) &
  4 (9.5 \%)\\
\tblbottomrule 
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\begin{tablenotes}\footnotesize 
    
\item{n: number of cases; SD: standard deviation}
\end{tablenotes}
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\end{table*}

\begin{table*}[!htbp]
\caption{\boldmath {Duration of disease and grading of severity} }
\label{tw-73b4c6f887de}
\centering 
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\tbltoprule \rowcolor{kwdboxcolor}Characteristic & Value\\
\tblmidrule 
Duration of symptoms  &
  \\
Range &
  1 {\textendash} 4\\
Mean \ensuremath{\pm}SD &
  2.21 \ensuremath{\pm} 1.02\\
Grade I~(mild), n (\%) &
  4 (9.5 \%)\\
Grade II (moderate), n (\%) &
  15 (35.7 \%)\\
Grade III (severe), n (\%) &
  23 (54.8 \%)\\
\tblbottomrule 
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\begin{tablenotes}\footnotesize 
    
\item{n: number of cases; SD: standard deviation}
\end{tablenotes}
\end{threeparttable}

\end{table*}

\begin{table*}[!htbp]
\caption{\boldmath {Associated co-morbidities and disease complications according to grade} }
\label{tw-326481aa0605}
\centering 
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\ignorespaces 
\centering 
\begin{tabulary}{\linewidth}{p{\dimexpr.17669999999999998\linewidth-2\tabcolsep}p{\dimexpr.08959999999999997\linewidth-2\tabcolsep}p{\dimexpr.10570000000000002\linewidth-2\tabcolsep}p{\dimexpr.10620000000000001\linewidth-2\tabcolsep}p{\dimexpr.0779\linewidth-2\tabcolsep}p{\dimexpr.07780000000000001\linewidth-2\tabcolsep}p{\dimexpr.10549999999999999\linewidth-2\tabcolsep}p{\dimexpr.0973\linewidth-2\tabcolsep}p{\dimexpr.0993\linewidth-2\tabcolsep}p{\dimexpr.064\linewidth-2\tabcolsep}}
\tbltoprule \rowcolor{kwdboxcolor}Characteristic & Total  \mbox{}\protect\newline  = 42 &  & \multicolumn{2}{p{\dimexpr(.1841\linewidth-2\tabcolsep)}}{Grade I~\mbox{}\protect\newline =4} & \multicolumn{2}{p{\dimexpr(.1833\linewidth-2\tabcolsep)}}{Grade II  \mbox{}\protect\newline   = 15} & \multicolumn{2}{p{\dimexpr(.1966\linewidth-2\tabcolsep)}}{Grade III  \mbox{}\protect\newline  = 23} & \\
\rowcolor{kwdboxcolor} &  & \% &  &  &  & \% &  & \% & \\
\tblmidrule 
Speech disorders &
  19 &
  45.2 &
  1 &
  25.0 &
  1 &
  6.7 &
  17 &
  73.9 &
  {\textless}0.001**\\
Tonsillar hypertrophy &
  9 &
  21.4 &
  0 &
  0.0 &
  1 &
  6.7 &
  8 &
  34.8 &
  0.027*\\
Adenoid facies &
  10 &
  23.8 &
  0 &
  0.0 &
  0 &
  0.0 &
  10 &
  43.5 &
  0.001**\\
Snoring  &
  42 &
  100.0 &
  4 &
  100.0 &
  15 &
  100.0 &
  23 &
  100.0 &
  ---\\
Recurrent otitis media  &
  6 &
  14.3 &
  0 &
  0.0 &
  0 &
  0.0 &
  6 &
  26.1 &
  0.024*\\
Chronic sinusitis &
  8 &
  19.0 &
  1 &
  25.0 &
  0 &
  0.0 &
  7 &
  30.4 &
  0.054\\
Nocturnal enuresis &
  15 &
  35.7 &
  1 &
  25.0 &
  2 &
  13.3 &
  12 &
  52.2 &
  0.023*\\
Impaired School performance &
  19 &
  45.2 &
  0 &
  0.0 &
  4 &
  26.7 &
  15 &
  65.2 &
  0.006**\\
Physical growth impairment &
  7 &
  16.7 &
  0 &
  0.0 &
  0 &
  0.0 &
  7 &
  30.4 &
  0.011*\\
Behavioral Changes &
  27 &
  64.3 &
  2 &
  50.0 &
  8 &
  53.3 &
  17 &
  73.9 &
  0.202\\
Apnea At sleep &
  23 &
  54.8 &
  0 &
  0.0 &
  0 &
  0.0 &
  23 &
  100.0 &
  {\textless}0.001**\\
Day time drowsiness &
  24 &
  57.1 &
  0 &
  0.0 &
  2 &
  13.3 &
  22 &
  95.7 &
  {\textless}0.001**\\
ECG Abnormalities &
  8 &
  19.0 &
  0 &
  0.0 &
  0 &
  0.0 &
  8 &
  34.8 &
  0.005**\\
Deglutition Problems &
  12 &
  28.6 &
  0 &
  0.0 &
  1 &
  6.7 &
  11 &
  47.8 &
  0.005**\\
\tblbottomrule 
\end{tabulary}\par 
\begin{tablenotes}\footnotesize 
    
\item{* Significant at P \ensuremath{\leq } 0.05; **Highly significant at P \ensuremath{\leq } 0.01}
\end{tablenotes}
\end{threeparttable}

\end{table*}

\begin{table*}[!htbp]
\caption{\boldmath {Correlation of Associated co-morbidities and disease complications according to the duration of disease } }
\label{tw-8c21e838cdc3}
\centering 
\begin{threeparttable}

\def\arraystretch{1.1}
\ignorespaces 
\centering 
\begin{tabulary}{\linewidth}{p{\dimexpr.6749000000000001\linewidth-2\tabcolsep}p{\dimexpr.1722\linewidth-2\tabcolsep}p{\dimexpr.15290000000000003\linewidth-2\tabcolsep}}
\tbltoprule \rowcolor{kwdboxcolor}Characteristic & \textit{r} & \textit{p}\\
\tblmidrule 
Speech disorders &
  0.443 &
  0.003 **\\
Tonsillar hypertrophy &
  0.327 &
  0.035 *\\
Adenoid facies &
  0.538 &
  {\textless}0.001**\\
Snoring &
  --- &
  ---\\
Recurrent otitis media &
  0.197 &
  0.210\\
Chronic sinusitis &
  0.196 &
  0.213\\
Nocturnal enuresis &
  0.353 &
  0.022 *\\
impaired School performance &
  0.358 &
  0.020 *\\
Physical growth impairment &
  0.411 &
  0.007 **\\
Behavioral Changes &
  0.092 &
  0.563\\
Apnea At sleep &
  0.726 &
  {\textless}0.001**\\
Day time drowsiness &
  0.672 &
  {\textless}0.001**\\
ECG Abnormalities &
  0.535 &
  {\textless}0.001**\\
Deglutition Problems &
  0.390 &
  0.011*\\
\tblbottomrule 
\end{tabulary}\par 
\begin{tablenotes}\footnotesize 
    
\item{* Significant at P \ensuremath{\leq } 0.05; **Highly significant at P \ensuremath{\leq } 0.01}
\end{tablenotes}
\end{threeparttable}

\end{table*}
Regarding ECG changes, five patients presented with isolated right axis deviation while three patients had right axis deviation with (tall R wave in the right sided leads V1, V2, AVR and deep S in left-sided leads V5, V6, I), all of them were of obstructive adenoid grade III on nasopharyngeal X-ray.

\textbf{Statistical analysis}

Data were analyzed using statistical package for social sciences (SPSS version 23) and Microsoft Office Excel 2010. Numeric data were presented as mean, standard deviation and range, whereas categorical data were presented as number and percentage. Fischer exact test was used to study the association between a grade of disease and associated co-morbidities, while Spearman correlation test was used to study the correlation of associated co-morbidities to disease duration. The level of significance was considered at \textit{P} \ensuremath{\leq } 0.05 and of high significance at \textit{P} \ensuremath{\leq } 0.01. 

In this study 42 school-aged children (6-12 years old) were involved, 30 boys (71.4\%) and 12 girls (28.6\%), with a female to male ratio 2.5:1.

This result was approximate to that reported by ES KOLO et al., as they found that 64.7\% were males and 35.3\% were females \unskip~\citep{664883:15668146}. 

While another study showed that 54\% of children involved were males and 46\% were female, with a male to female preponderance 1.1:1 \ensuremath{^{}}

Metin et al. study was performed on 38 patients, and they found that 63.15\% males and 36.84\% females \unskip~\citep{664883:15668147}.

The male preponderance among all these studies may be related to their higher outdoor activities hence more exposure to allergen and inflammation.

All the involved study group were complaining from chronic snoring at sleep. They consult a pediatrician searching for management of their co-morbid symptoms such as (faltering growth, nocturnal enuresis, sleep disorders and poor school performance).

In respect to socioeconomic status, the majority of children were poor (42.9\%) and moderate (47.6\%), while only (9.5\%) were of high status.

In respect to lateral nasopharyngeal X-ray, 52.8\% had severe adenoid enlargement, 35.7\% had moderate enlargement and only 9.5\% has mild one. This result may be reflective of late presentation among low and mid socioeconomic class families, which may be related to limited educational levels among them \unskip~\citep{664883:15668151,664883:15668152}.

The result was scarificial to what seen by yogita et al., as they found that 16\% were of mild enlargement,34\% were moderate and 50 \% were severe. 

Furthermore, in  Babak et al. reported that 10.1\% were with mild enlargement, 35.9\% were moderate, 53.9\% were severe \unskip~\citep{664883:15668153,664883:15668150}.

Many disease complications were found to be strongly correlated to the severity of adenoid hypertrophy on radiological grading (highly significant p value\textless\ 0.01) with speech disorder, adenoid facies, impaired school performance, impaired physical growth, apnea at sleep, day time drowsiness, ECG changes and deglutition problems \unskip~\citep{664883:15668158}.

There was also a significant correlation (p-value {\textless}0.05) with most co-morbid symptoms like associated tonsillar hypertrophy, recurrent or chronic otitis media, nocturnal enuresis.

But there was no correlation with associated chronic sinusitis and behavioral abnormalities.  

Yogita Dixit and Prem Siddharth notified that there was a good correlation between symptoms and X-ray finding \unskip~\citep{664883:15668148,664883:15668157}.

Shervin sharif Kashan did not notify any correlation between clinical scoring and radiological grading; he reports the correlation to endoscopic grading more. 

An opposite result was seen by Babak Saedi, as he found that symptoms was significantly correlated to radiological grading rather than to endoscopic grading. 

This results show that a lateral neck radiograph is still of an important diagnostic point.

The duration of symptoms prior to clinical presentation ranging from 1-4 years with a mean of 2.21 \ensuremath{\pm} 1.02 SD, which is considered a long duration \unskip~\citep{664883:15668154}.

Longer duration of the disease is statistically highly significant (p value{\textless}0.01) to speech issues, facial changes, affected physical growth, sleep disorders (night time apnea, day time drowsiness), ECG changes. It is also seen to be significantly correlated (p-value{\textless}0.05) with tonsillar hypertrophy, impaired school performance, deglutition problems. 

There is no correlation between disease duration and recurrent otitis media, chronic sinusitis and behavioral changes \unskip~\citep{664883:15668149,664883:15668135}. 

Mohammed Waheed El Anwar et al. in his study concluded that long term upper airway obstruction in those patients results in a negative impact on pulmonary function\ensuremath{^{. }}

Long-standing adenoiditis with subsequent adenoidal hypertrophy can lead to the development of what is known as adenoid facies and other consequences \unskip~\citep{664883:15668155,664883:15668156}.

The consequences of large adenoids depend on how it can result in narrower airways and in this study, it's confirmed that it's also related to how long the child was complaining.\ensuremath{^{}}

This is important to be considered to educate the parents and caregiver about the seriousness of this health problem and the importance of properly planned and properly timed management.
    
\section{Conclusions}
Clinically severe symptoms and most of the complications had a statistically significant correlation with radiological grading and disease duration.

Increasing education among families about many facts is crucial, these are;

Adenoid is a lymphoid tissue that has a considerable immune role, but when it hypertrophied its can lead to many serious morbidities.

There are many management options, and medical treatment with intranasal steroids and antibiotics is valuable for most mild to moderate cases. Hence early management is important to avoid surgical intervention.

Adenoidectomy is the treatment option for severely symptomatic and complicated cases, it has many possible postoperative complications, but most of the symptoms and complications will be reversed post adenoidectomy.

Electrocardiography (ECG) is not routinely required. It should be limited to a high-risk group. 
    

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