Ir J Med Sci (2016) 185:249–257 DOI 10.1007/s11845-015-1287-4
ORIGINAL ARTICLE
Microscopic studies on postmortem vermiform appendix of the adult males of Bangladesh S. M. A. Bakar1 • M. Shamim2 • A. Salam3 • S. A. Sultana4
Received: 26 June 2014 / Accepted: 29 March 2015 / Published online: 17 April 2015 Ó Royal Academy of Medicine in Ireland 2015
Abstract Background The anatomy of the vermiform appendix shows variations in its macroscopic dimensions and microscopic features, some of which have potentials of influencing the clinical aspects of the appendix. Aim The aim of this study was to find out some microscopic features of appendix and evaluate the correlation between the microscopic features of the appendix and the age of the subjects and to determine whether these findings should influence the clinical implications of appendix. Methods In this cross-sectional observational study, thirty adult males’ (age from 18 to 67 years) postmortem appendices and adnexa from Bangladeshi victims of road traffic accidents were sectioned at the base, midzone and tip stained with H?E stain and examined under microscope. Measurements were taken at the base, at the
midzone and at the tip of the appendix, and the mean of the three measurements was considered as the overall value. Results The overall number of mucosal glands in a section ranged from 42.33 to 130.00 and the number of the germinal centres varied between 2.33 and 10.00. The overall luminal diameter ranged between 1764.58 and 3208.33 lm. The overall luminal diameter in more than 52 % of cases was between 2700.00 and 3299.99 lm with a median value of 2750 lm. Conclusion The overall number of mucosal glands showed a tendency towards a positive correlation with age. The overall luminal diameter and the overall number of germinal centres showed a tendency towards a negative correlation with the age. However, none of the tendencies of correlation reached statistically any significant level. Keywords Vermiform appendix Luminal diameter Germinal centres Mucosal glands Appendicitis
& S. M. A. Bakar
[email protected];
[email protected] M. Shamim
[email protected]
Introduction
A. Salam
[email protected]
The vermiform appendix is an interesting organ, always raising questions and contradictions among researchers. It has long been regarded as an intestinal appendage, and hence the name. The adjective ‘‘vermiform’’ literally means ‘‘worm like’’ and reflects the narrow, elongated shape of this organ. In humans, the vermiform appendix is a small finger-sized structure, found at the end of our small caecum and located near the beginning of the large intestine. Its length varies from 2 to 20 cm with an average length of 9 cm [4]. It is longest in childhood and gradually shrinks throughout life. It arises as a diverticulum from the postero-medial wall of the caecum about 2 cm below the ileocaecal junction [34, 36].
S. A. Sultana
[email protected] 1
Department of Anatomy, Faculty of Medicine, University of Malaya, 50603 Kuala Lumpur, Malaysia
2
Department of Anatomy, Faculty of Basic Medical Science, Banghabandu Sheikh Mujib Medical University, Shahbag, Dhaka, Bangladesh
3
Department of Medical Education, University Kebangsaan Malaysia (UKM) Medical Centre, Kuala Lumpur, Malaysia
4
Department of Microbiology, University of Chittagong, Chittagong, Bangladesh
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Appendix shows variations in its microscopic features. For example, the number of lymphoid follicles in the mucosa/submucosa is supposed to vary according to the amount, time and duration of exposure to antigens. This would imply that different populations, being exposed to antigens differently may have difference in the number of lymphoid follicles and their germinal centres. The lymphoid structure of the appendix also varies with age [20], being well developed in the infants and children and atrophied at the old age. The decrease in size begins in the early adulthood [3]. It may be assumed that the structural components like the number of lymphoid follicles and glands may have implications on the luminal diameter and vice versa. Again, the wall thickness may be linked to the luminal diameter as well as to external diameter of the organ. From the clinical perspective, despite considerable advances in the management of appendix-related problems, ‘‘there is still a morbidity and mortality that cannot be considered insignificant’’ [9]. In current medical diagnosis and treatment [18], appendicitis (the inflammation of appendix) has been considered as ‘‘the most common abdominal surgical emergency, affecting approximately 10 % of the population’’. The lifetime risk of acute appendicitis is 7 % [32]. The higher incidence of appendicitis in the young adults than in the children or elderly has been attributed to the changes in its luminal diameter with age. Variables such as luminal diameter and lymphoid aggregations may be expected to have implications on the causes and consequences of the clinical conditions. The appendix is also the most frequent site of carcinoid tumours [30] that arise from the argentaffin cells of the mucosa. Another aspect of the appendix is its questionable evolutionary background. Regarded by many as a vestigial organ [32] or as an organ of ‘‘obscure function’’ [14], it has also been viewed as a ‘‘highly specialized, well-differentiated organ apparently developed to the maximum in its specialisation in man’’ [9]. Studies on the anatomy of the human appendix in specific populations have clinical implications as well as usefulness in understanding the organ. However, while gross anatomical studies of the appendix are abundant since more than 100 years back, histological studies of the organ are still insufficient, especially in terms of various probable relationships among different dimensional and other numerical variables. Moreover, very few studies have been or are being done on the anatomy of the vermiform appendix of the Bangladeshi people, especially on the possible relationships among its various anatomical features. Objectives of the study Inflammation of the appendix is more common in males than in females [15]. The present study aimed at
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contributing to standardisation of different microscopic variables of the vermiform appendix in Bangladeshi adult males. The findings of this study are expected to help in understanding the prevalence and nature of appendicular pathologies in the population. For fulfilling the above aims, the following specific objectives were set for the study: 1.
Objective to be achieved through microscopic studies of histological sections of the appendix at three segmental levels (base, midzone and tip).
a.
To estimate the luminal diameter of the appendix at three segmental levels as well as the overall luminal diameter To estimate the number of mucosal glands at three segmental levels as well as the overall number To estimate the number of germinal centres at three segmental levels as well as the overall number
b. c. 2.
Objectives to be achieved through regression analysis: To assess the possible relationships with different microscopic variables of the appendix with age.
Materials and methods The study was observational and cross-sectional in nature. It was principally descriptive with some regression analyses done to assess relationships between variables and the age of the subject. The specimens (the vermiform appendix along with the caecum and adjacent parts of the ascending colon and terminal ileum) were collected from the morgue of the Department of Forensic Medicine of Dhaka Medical College (DMC). The study was carried out in the Department of Anatomy, Bangabandhu Sheikh Mujib Medical University (BSMMU), Dhaka, during the period of July 2006 to June 2007. Thirty unclaimed dead bodies of road traffic accident cases autopsied in the Department of Forensic Medicine of Dhaka Medical Collage morgue were used. Consent was taken from the authority of Dhaka Medical College Hospital to collect the appendices for study purposes. Inclusion criteria for the subjects (a) Adult by age 18 years and above, (b) Male by sex, (c) Bangladeshi by nationality (and Bengali by ethnic group as far as identifiable by name, physical features and records). Exclusion criteria for the specimens Any sign of decomposition, any injury to the appendix, caecum, proximal ascending colon or terminal ileum, inflammation of any of the above structures. Variables studied (a) Age of the subjects, (b) Microscopic variables of the appendix (measured at three segmental levels: base, midzone and tip): Luminal diameter, number of mucosal glands present in a section, number of germinal centres present in a section (the ‘overall’ value,
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i.e. the mean of the values at three segmental levels was also calculated for each of the above three variables).
Methods For the study, 30 specimens were chosen. The specimens were fixed in 10 % formol saline. Each of the 30 specimens was cut free from the caecum and was cut into three roughly equal segments at the three segmental levels: the base, the midzone and the tip. The three segments were processed for microscopic study and several 8-lm-thick transverse sections were made from each segmental level (base, midzone and tip) using a rotary microtome. The sections were stained with haematoxylin–eosin stain. For measurements and counting, one good section was selected for each segmental level. Method of estimating luminal diameter of the appendix At first, the section of the appendix was divided by drawing two lines on the cover slip at right angles to each other through the approximate centre of the lumen using a fine permanent marker pen (Fig. 1). Using an 94 objective and an 910 eyepiece, two diameter readings (reading 1 and reading 2) were taken from the lumen of a section at the base. The mean of the two readings was recognised as the actual luminal diameter at the base. Similar readings were taken for the midzone and for the tip. The diameters were expressed in centimetres. The mean value of the three diameters at the three segmental levels (base, midzone and tip) was regarded as the overall luminal diameter.
Fig. 1 Method of measuring the luminal diameter of the appendix. Line a the longest diameter; line b the maximum diameter at right angles to line a (Modified from Eroschenko [8])
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Method of estimating the number of mucosal glands in a section For counting the number of mucosal glands, each section was divided into four quadrants by two thin lines drawn on the cover slip at right angles to each other through the approximate centre of the lumen using a fine marker pen (Fig. 2). The entire section was focused under an 920 objective and 910 eyepiece of a light microscope. For each quadrant, the number of mucosal glands was counted in a clockwise manner (Fig. 3). As the two marker lines that divided the section into four quadrants were broad enough to overlap a few glands, a quadrant was considered from the distal margin of a line to the distal margin of the other line while counting in a clockwise fashion. Thus, for a section of the ‘base’ segment of an appendix, four counts were made. The summated count of the four quadrants represented the number of the mucosal glands in a section at the segmental level concerned. The overall number of mucosal glands in a section was then calculated by averaging the values at the three segmental levels: base, midzone and tip. Method of estimating the number of germinal centres in a section The entire section was focused under an 910 objective and of 910 eyepiece of a light microscope. Then, the germinal centres were counted, for example, in a section at the base from the 12 o’clock position of the field clockwise to reach
Fig. 2 Method of counting the number of mucosal glands in a cross section of the vermiform appendix. The lines ab and cd have divided the section into four quadrants. The counting was done clockwise from the 12 o’clock position to get back to the same position. As the arrows show, the glands overlapped by the lines were counted once only, for example, from the distal edge of one line to the distal edge of the other (Modified from Eroschenko [8])
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Fig. 3 Diagrammatic representation of how each microscopic section of the appendix was divided into four quadrants by drawing fine continuous lines (ab and cd) at right angles to each other with a permanent marker pen on the cover slip. These quadrants were used for counting mucosal glands. Another two lines were also drawn (ef and gh) that divided each quadrant into two equal halves to make the measurement more accurate
the 12 o’clock position. Again (Fig. 4), the lines shown here are the same (‘ab’ and ‘cd’) that are shown to divide each section into four quadrants (Fig. 2). Similarly, counts were made for the midzone and tip. The mean of the three segmental counts represented the overall number of germinal centres in a section. Method of standardising ocular micrometre with stage micrometre The stage micrometre had such calibrations that the smallest divisions divided a 1 mm length into 100. Thus, 100 smallest divisions of the stage micrometre = 1 mm = 1000 lm. Therefore, one smallest division of the stage micrometre = 1000/100 lm = 10 lm For standardisation, the stage micrometre calibrations were focused under the objective to be used and the ocular micrometre calibrations were superimposed on them in such a way that a mark on the micrometre calibration matched exactly with a starting mark on the stage micrometre. Then, the marks on the stage and ocular micrometres that corresponded with each other most closely were noted. Thus, it was possible to determine how many of the smallest divisions of the ocular micrometre corresponded to how many smallest divisions of the stage micrometre for an objective and an eyepiece of particular magnifications.
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Fig. 4 Method of counting the number of germinal centres in a transverse section of the vermiform appendix. Although no separate counting was done for the quadrants, line ab was used to begin counting at the 12 o’clock position and counting was proceeded clockwise to get back to the 12 o’clock position (Modified from Ross et al. [29])
The following were noted for the 94 objective and 910 eyepiece. 18 smallest divisions of the ocular micrometre matched with 20 smallest divisions of the stage micrometre. So, 1 smallest division of the ocular micrometre matched with 20/18 = 1.11 smallest divisions of the stage micrometre. Because, one smallest division of the stage micrometre = 10 lm (as already shown) 1.11 smallest divisions of the stage micrometre = 1.11 9 10 lm = 11.1 lm. Therefore, 1 smallest division of the ocular micrometre represented 11.1 lm on the stage (11.1 lm of the section) under an 94 objective and an 910 eye piece. Statistical processing of data The ranges, means, medians and standard deviations were calculated for different quantitative variables and percentage values were calculated for the qualitative variables using the computer software Microsoft Excel 2000. The same software was also used for creating the frequency distributions of the quantitative data. The software SPSS version 11.5 was used for doing regression analyses and testing statistical significance and assessing relationships between pairs of variables. The p values less than 0.05 were regarded as significant.
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Results
Table 2 Number of mucosal glands and germinal centres present in a section of the appendix
Luminal diameter of the appendix The luminal diameter of the vermiform appendix ranged from 2406.25 to 4331.25 lm at the base, 1375.00 to 4193.75 lm at the midzone, 893.75 to 2956.25 lm at the tip (Table 1). The overall luminal diameter ranged between 1764.58 lm and 3208.33 lm. The overall luminal diameter in more than 52 % of measured cases was between 2700.00 and 3299.99 lm (Fig. 5) with a median value of 2750 lm (Table 1). Table 1 also shows that the mean and median values of the luminal diameter gradually decreased from the base to the tip. Number of the mucosal glands present in a section The number of mucosal glands present in a section varied greatly at every segmental level (Table 2). The lowest number (19) was found in a section at the tip, while the highest number (190) was found in a section at the midzone. The mean and median values also showed a tendency to be the highest at the midzone, intermediate at the base and the lowest at the tip. The overall number of mucosal glands present in a section varied between 42.33 and 130.00 (Table 2). However, in more than 43 % of cases, the count was between 60 and 79 (Fig. 6). Number of germinal centres present in a section The number of germinal centres present in a section was also very variable showing no germinal centres in a section at
Variable
Range
Mean ± SD
Median
Number of mucosal glands present in a section At the base
29–170
84.16 ± 37.79
71.50
At the midzone At the tip
24–190 19–114
92.40 ± 41.38 55.66 ± 21.62
84.00 48.00
42.33–130.00
77.41 ± 22.38
71.16
Overall
Number of the germinal centres present in a section At the base
2–13
6.76 ± 3.37
6.00
At the midzone
2–13
6.23 ± 2.90
6.00
At the tip Overall
0–9
5.16 ± 2.35
4.50
2.33–10.00
5.98 ± 1.88
5.99
Frequency (%)
No. of appendices in section = 30 for each variable at each segmental level and for the overall value
50 45 40 35 30 25 20 15 10 5 0
43.33%
20.00%
20.00% 6.66%
40
60
80
100
10.00%
120
140
Overall number of mucosal glands in a section
Fig. 6 Histogram showing the frequency distribution of the overall number of mucosal glands in a section of the appendix (n = 30)
Table 1 Luminal diameter of the appendix Luminal diameter (lm) Range
Mean ± SD
Median
At the base
2406.25–4331.25
3222.12 ± 638.29
3437.50
At the midzone
1375.00–4193.75
2616.79 ± 646.11
2543.75
893.75–2956.25
2148.18 ± 627.04
2371.56
1764.58–3208.33
2662.36 ± 397.99
2750.00
At the tip Overall
No. of transverse sections of appendices = 30 for each segmental level and for the overall value
Frequency (%)
Segmental level
Number
50 45 40 35 30 25 20 15 10 5 0
36.66%
33.33% 16.66%
13.33%
2
4
6
8
10
Overall number of germinal centres in a section
26.66% 26.66%
Frequency (%)
30 25 16.66%
20 15 10
20.00%
10.00%
5 0
1700
2100
2400
2700
3000
3300
Overall lum inal diam eter (µm )
Fig. 5 Histogram showing the frequency distribution of the overall luminal diameter of the appendix (n = 30). Note that the frequencies rose almost as the values of the luminal diameter rose
Fig. 7 Histogram showing the frequency distribution of the overall number of germinal centres in a section of the appendix (n = 30)
the tip to 13 germinal centres in a section at the base (Table 2). The mean and median values shown in Table 2 reveal a general tendency of decreasing numbers from the base towards the tip. The overall number of germinal centres present in a section varied from 2.33 to 10. In more than 65 % of the sections, the overall number was counted between 4.00 and 7.99 (Fig. 7). Relationships of the microscopic variables with the age of subject The overall number of mucosal glands (Fig. 9)
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Discussion on the luminal diameter of the appendix
Overall luminal diameter (µm)
R2 =0.003 3500 3000 2500 2000 1500 1000 500 0
0
20
40
60
80
Age (years) Fig. 8 Scatter diagram with regression analysis showing non-significant negative correlation between the age of the subject and the overall luminal diameter of the appendix (r = 0.057, p = 0.765)
showed a tendency towards a positive correlation with age. The overall luminal diameter (Fig. 8) and the overall number of germinal centres (Fig. 10) showed a tendency towards a negative correlation with the age of the subject. However, none of the tendencies of correlation reached statistically any significant level.
Discussions The correlation of the clinical, macroscopical and microscopical findings in acute appendicitis is important to formulate a sound surgical decision [12]. The discussion on the results of the present study has been prepared by comparing the results of several studies and descriptions by several authors. In this study, adult males were selected on the basis of the fact of correlation of appendicitis with age and sex found in the following mentioned studies. There was a statistically significant correlation between the diameter of the appendix and increasing age, the appendix becoming narrower with age [1]. It was also found that there was a negative correlation between the age and the length of the human vermiform appendix [2]. In another study, it was found that complications in acute appendicitis were higher in males and in those aged 45 years and above [28]. Appendicitis is more common in males, in those aged 20–29 years [22]. Inflammation of the appendix is more common in males than in females [15], appendicitis is twice as common in males as in females and that it occurs predominantly in young people (median age 20 years) [16]. The disease is common in men in their third decade [6]. The peak incidence of acute appendicitis is between 10 and 30 years of age [13]. The present study provides a microscopic feature of the appendix and tries to establish a correlation between the age of the subjects and some microscopic variables of the appendix.
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Many cases of acute appendicitis result from obstruction of the lumen of the appendix by lymphoid hyperplasia and the lymphoid follicles of the vermiform appendix vary with respect to their number, diameter and location in different ages [25]. Malas et al. [17] observed that luminal diameter of the appendix increased with gestational age in microscopic cross section of the vermiform appendix. Shugaba et al. [31] found that luminal diameter does not show uniformity along the length of the appendix. Shugaba et al. [31] also believed that factors such as thickness and amount of lymphoid follicles and age of the subject must play rules in determining the luminal diameter. Shugaba et al. [31] believed that the lumen decreases when either the mucosal thickness or the lymphoid follicle diameter increases in size. The average luminal diameter of appendix follows the normal trend in which there is decrease in luminal diameter from normal to appendicitis but the difference was not statistically significant [11]. Other factors such as the thickness of wall, amount of lymphoid follicles in the submucosa, the age of the subject or indeed the normality of the processed organ must be playing role in determining the luminal diameter [11]. Malas et al. [17] did not find significant differences in luminal diameter at the three segmental levels. The importance of luminal diameter of the appendix has clinical implication. The diameter is wide in children and the lumen is almost obliterated in the elderly. Therefore, the chances of feacal contents getting into the appendix and being stuck are less in these two age groups. Historically, obstruction of the appendiceal lumen, with subsequent secondary infection, has been the most popular theory regarding the pathogenesis of acute nonspecific appendicitis [5, 35]. The mean luminal diameter of vermiform appendix was more in female (60.71 lm) than the mean luminal diameter of vermiform appendix in male (60.11 lm) [27]. Although the difference is not significant, the present study targeted only the male subjects as in different studies it was found that appendicitis is more common in males than in females [15, 16, 28]. In the present study, we tried to find out if there is any correlation between the age of the subjects and the luminal diameter of appendix. In the present study, the luminal diameter of the appendix was measured at three segmental levels (base, midzone and tip) and it was found that the luminal diameter was gradually decreased from the base to the tip. In another study, it was found that there is a negative correlation between the age of the subjects and length of the appendix [2]. It was found that the normal diameter of the lymphoid follicles of the vermiform appendix reduced significantly with advancing age [25]. From these facts,
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Discussion on the number of mucosal glands in a section The number of mucosal glands present in a section varied greatly at every segmental level (Table 2). The lowest number (19) was found in a section at the tip, while the highest number (190) was found in a section at the midzone. The mean and median values also showed a tendency to be the highest at the midzone, intermediate at the base and the lowest at the tip. The overall number of mucosal glands (Fig. 9) showed a tendency towards a positive correlation with age. But the tendency of correlation did not reach statistically any significant level. Our findings suggest that the number of mucosal glands may not be a parameter of causing appendicitis in adults. Discussion on the number of germinal centres present in a section
Overall no. of mucosal glands
Presence of germinal centres reflects state of activity of the immune system of the body [33]. Mrozik, Hecker, Wiebecise et al [21] concluded, by planimetric study of lymphatic tissue, that lymphoid follicles and germinal centres become longer with appendicitis as compared to normal although the difference was not found to be statistically significant [10]. R2 =0.053
140 120 100 80 60 40 20 0 0
20
40
60
80
Age (years) Fig. 9 Scatter diagram with regression analysis showing non-significant positive correlation between age of the subject and the overall no. of mucosal glands in a section of the appendix (r = 0.053, p = 0.0783)
The present study showed that the number of germinal centres present in a section was very variable showing no germinal centres in a section at the tip to 13 germinal centres in a section at the base. This study reveals a general tendency of decreasing numbers of germinal centres from the base towards the tip. Rahman et al. [23] found that the numbers of germinal centre in vermiform appendix were highest (2.20 ± 0.45) in 21–35 years of age and lowest (0.00 ± 0.00) in 56–70 years of age. In another study, it was shown that the average number of germinal centres of the lymphoid follicle per histological section of vermiform appendix reduced with advancing age and showed a significant negative correlation with age (p \ 0.001) [24]. Rahman and Parash [24] divided the collected vermiform appendices into five groups according to age; Group A (0–20 years), Group B (21–30 years), Group C (31–40 years), Group D (41–50 years) and Group E ([50 years) and showed that the mean value was highest in group A (2.11 ± 0.72) and lowest in group E (0.11 ± 0.17) [24]. However, in the above-mentioned studies [23, 24], sex of the subject was not considered. Unlike the studies [23, 24], in the present study the subjects aged between 0 and 17 years are excluded. On the other hand, the present study has targeted only the adult age groups (18 years and above) that were male in sex as in different studies it was found that appendicitis is more common in males than in females [15, 16, 28] and appendicitis is more common in males in their third decade [6] and also the mean number of germinal centres in male (1.05) was more than in female (0.8) [26]. The present study revealed that the overall number of germinal centres (Fig. 10) showed a tendency towards a negative correlation with the age of the subject. However, the tendency of correlation did not reach statistically any significant level. So further study is recommended to find out the correlation between the number of germinal centres and the age and
Overall no. of germinal centres
it was assumed that the decreasing of luminal diameter of appendix from base to tip in adults might be correlated with the age of the subjects. To establish the fact of correlation between the age and the luminal diameter of the human vermiform appendix, a regression analysis was done. Regression analysis showed non-significant negative correlation between the age of the subject and the overall luminal diameter of the appendix. From this fact, it might be suggested that although there is a relatively higher frequency of appendicitis in the young adults, this higher frequency of appendicitis is not related with the luminal diameter of the appendix.
R2 =0.104
12 10 8 6 4 2 0 0
20
40
60
80
Age (years)
Fig. 10 Scatter diagram with regression analysis showing nonsignificant negative correlation between age of the subject and the overall number of germinal centres in a section (r = 0.322, p = 0.083)
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sex of the person. A comparative study is also recommended to find out a correlation between the number of germinal centres and the sex of the persons in different age groups.
Conclusion Studies on the anatomy of the human appendix in specific populations have clinical implications as well as usefulness in understanding the organ. An appropriate anatomical knowledge about vermiform appendix is important for surgeons, pathologists and other physicians for proper diagnosis and management of appendicitis and carcinoma [7, 19]. In this study, it was found that there is no significant correlation between the age of the subject and the luminal diameter, number of germinal centre, and number of mucosal glands. This microscopic anatomy of the appendix may be used to study appendicular features in different age groups to establish the age changes in the appendix. Acknowledgments We are indebted to the personnel of the Banghabandu Sheikh Mujib Medical University, Dhaka, Bangladesh and to the personnel of Department of forensic medicine, Dhaka Medical college, Bangladesh for their cordial cooperation to collect the human vermiform appendix. We are also thankful to Dr. Ishtiak Mannan, Gender and Reproductive Health Specialist, ICDDR, B., Dhaka for the statistical contribution.
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