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E-ORIGINAL ARTICLE
Year : 2014  |  Volume : 59  |  Issue : 5  |  Page : 529
Mycetoma in Iran: Causative agents and geographic distribution


Department of Medical Mycology, Pasteur Institute of Iran, Iran

Date of Web Publication1-Sep-2014

Correspondence Address:
Shahindokht Bassiri-Jahromi
Department of Medical Mycology, Pasteur Institute of Iran, Pasteur Street, Number 69. P.O. Box: 1316943551
Iran
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Source of Support: This work was financial supported by Pasteur Institute of Iran., Conflict of Interest: None


DOI: 10.4103/0019-5154.139889

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   Abstract 

Background: Mycetoma is a chronic granulomatous disease caused by true fungi (eumycetoma) or filamentous bacteria (actinomycetoma). It usually involves the subcutaneous tissue after a traumatic inoculation of the causative organism. We reviewed retrospectively 13 patients with mycetoma. Materials and Methods: This study reports the etiologic agents and distribution of mycetoma in 35 cases from 1994 to2009 in Iran. The diagnostic of mycetoma were confirmed by histopathology and direct preparation, culture techniques, and histopathology of granules and surgical biopsies, radiological examination of the affected site. Results: Mycetoma was identified in 35 patients of 168 suspected patients (20.8%). They occurred in 22 male and 13 females. Their ages ranged from 14 to 80 years. The duration of the disease ranged from two months to 38 years. Sixteen patients had eumycetoma, and 19 patients had actinomycetoma, one of them had mix infections by eumycetoma and actinomycetoma. The majority of the patients were from central and states in south and north of Iran. The feet were most affected site (65.7%) of the cases, followed by hands (25.7%), face (2.8%), and trunk (2.8%), and buttock (2.8%). Most patients (68.5%) were more than 40 year-old. The male to female ratio was 5:3. The disease was abundant among housewife in urban and farmer in rural area of Iran. The most common prevalent mycetoma agents in this study were Actinomyces sp. There was a history of risk factors in 28.6% of patients in this study. Conclusion: Mycetoma occasionally occurs particularly in the South, Central, and North of Iran, and seen most often in persons, who live in hot, humid climates. If there are risk factors for invasive fungal infections traumatic inoculation with any fungus may result in rapid local spread and systemic disease, often with fatal outcome.


Keywords: Actinomycetoma, eumycetoma, fungal infections, mycetoma, subcutaneous fungal infection


How to cite this article:
Bassiri-Jahromi S. Mycetoma in Iran: Causative agents and geographic distribution. Indian J Dermatol 2014;59:529

How to cite this URL:
Bassiri-Jahromi S. Mycetoma in Iran: Causative agents and geographic distribution. Indian J Dermatol [serial online] 2014 [cited 2019 Jun 26];59:529. Available from: http://www.e-ijd.org/text.asp?2014/59/5/529/139889

What was known?
Mycetoma appear as inflammatory pseudo tumors, due to bacterial or fungal agent. Mycetoma is common in tropical and subtropical regions of the world. The morbidity caused by mycetoma is massive and enormous. It has many clinical and socio-economic impacts on patients, families and the community. In areas where mycetoma is endemic, local health care facilities and health education are usually insufficient and inadequate. Mycetoma is a hard-to-treat disease in many tropical and subtropical regions due to multifactorial reasons.
Although such infections rarely cause disseminated or invasive disease, they have an important impact on public health, and timely diagnosis and appropriate treatment remain important. Although some implantation mycoses are found in immunocompromised persons, the immunocompetent population is the principal target in Iran.



   Introduction Top


Mycetoma appear as inflammatory pseudotumors, and chronic granulomatous infection of the skin and subcutaneous tissue due to bacterial or fungal agent. Mycetoma is common in tropical and subtropical regions of the world. The morbidity caused by mycetoma is massive and enormous. It has many clinical and socio-economic impacts on patients, families and the community. In areas where mycetoma is endemic, local health care facilities and health education are usually insufficient and inadequate. Mycetoma is a hard-to-treat disease in many tropical and subtropical regions due to multifactorial reasons. Mycetoma is a common health problem in the tropical and subtropical regions of Asia, Africa, Sudan, Central and South America. [1]

Disease is unique from other cutaneous or subcutaneous diseases in its triad of localized swelling, underlying sinus tracts and production of grains or granules (comprised of aggregations of the causative organism) within the sinus tracts. [2] The infection caused by various genera of fungi or filamentous bacteria. The most common fungi which are responsible for eumycetoma include: Acremonium (Cephalosporium) falciforme, Exophiala (Phialophora) jeanselmei, Madurella grisea, and Pseudallescheria boydii, as well as others. Actinomycetoma are caused by filamentous bacteria such as: Actinomyces israelii, Streptomyces somaliensis, and Nocardia asteroides and brasiliensis.[3] Mycetoma is categorized according to etiology: Those caused by filamentous aerobic Actinomyces, such as Nocardia, Actinomadura, and Streptomyces, are referred to as actinomycetoma. Those caused by true fungi that named eumycetoma. Response to medical treatment is usually better in actinomycetoma than eumycetoma, which is difficult to treat with current therapies. [4]

The present report focuses on the etiologic agents and distribution of mycetoma infections in Iran from 1994 to 2009. The present report focuses the etiologic agents and distribution of mycetoma infections in Iran during 16 years and highlights the benefits of using observational studies as a form of research.


   Patients and Methods Top


This is a retrospective review of records selected from patients' records at the Medical Mycology Department, Pasteur Institute of Iran in Tehran, during a period 16 years from 1994 to 2009. All the cases were categorized depending upon the age, sex, duration of onset, site of involvement, radiological features, histopathology and culture. The material for investigations was collected from scrapings, crusts, pus from subcutaneous abscesses or exudation from sinus tracts, surgical debridement and biopsy specimens. Diagnosis was made by direct examination, culture, and histology. Specimens were cultured on Sabouraud's dextrose agar, blood agar and brain heart infusion agar (B.B.L), and fluid thioglycolate, anaerobic culture media, and biochemical properties. Duplicate cultures on each medium were incubated at 35 and 25°C regularly examined up to four weeks and identified using standard methods. Microscopic features of the isolates were studied by slide culture preparation. We also used of the Czapek's Agar for Aspergillus species identification. For diagnosis of Nocardia and Actinomyces the preparations were stained using Kynion, and Gram stain. Actinomyces and Nocardia were identified by culture, staining, and biochemical tests. Biochemical tests were performed at the Actinomyces Reference Laboratory of the Centers for Disease Control and Prevention (CDC) by the methods of Berd. [5]


   Results Top


Of 168 clinically suspected cases of mycetoma, 35 were confirmed by cultural and histopathological methods. They occurred in 22 (62.9%) male and 13 (37.1%) females with a male to female ratio of 5:3. Their ages ranged from 14 to 80 years. Most of the patients (68.5%) were more than 40 years. The duration of mycetoma ranged between two months and 38 years. Most (68.6%) had the disease for more than one year. The majority of the patients were from Central and States in South of Iran (Khuzestan, Bushehr and Bandar Abbas) (57.1%). Four patients (11.4%) were from North part of Iran. Most patients in urban area were housewives (28.6%), and in rural area were farmers (20%) [Table 1].
Table 1: Frequency of mycetoma respect to occupation


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Infections mainly occur among low socioeconomic groups, methods data were measured from socioeconomic position using education, household income, occupational class and area deprivation.

In this study, actinomycetoma (54.3%) were found more often than eumycetoma (45.7%).

There was a past history of reasons to caused the mycetoma in patients in this study included: Thistle accidental, hit the rocks, trauma after falling from the roof, cutting through by biting gums, accidental fish bone in the parotid, gum surgery, burn, tattoo removal, electric shock, knee surgery, war veteran, accidental glass palm, artificial joints, skin graft surgery for stumble, accidental needle, tooth infection, and contact with soil (constructor worker or farmer).

In this study, 10 patients (28.6%) had concomitant medical problems, including diabetes (1_2.9%), renal translation and antibacterial and immunotherapy after that (2_5. 7%), chronic granulomatosis diseases CGD (1_2.9%), Myasthenia Gravis (1_2.9%), and colon cancer (1_2.9%). [Table 2] shows the various reasons to initiate the mycetoma infections.
Table 2: Concomitant medical problem in patients with mycetoma


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The feet were found to be affected in 62.8% of the cases, followed by hands (25.7%) [Figure 1], [Figure 2], face (2.9%), and other affected sit were trunk (2.9%), neck (2.9%), and buttocks (2.9%).
Figure 1: Advanced mycetoma of the foot. Note the swelling, deformity and sinuses

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Figure 2: Mix mycetoma in palm and back of hand due to Nocardia asteroides and Pseudallescheria boydii in the brass worker woman, resident in North of Iran

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Figure 3: Mix mycetoma in palm and back of hand due to Nocardia asteroides and Pseudallescheria boydii in the brass worker woman, resident in North of Iran

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Out of 35 cases of mycetoma identified, fifteen were Actinomyces species [Figure 4] and [Figure 5], four Nocardia species (n = 4), and others included Aspergillus species (n = 3) [Figure 6], [Figure 7], [Figure 8], Pseudallescheria boydii (n = 3) [Figure 9], Fusarium species (n = 2), Acremonium species (n = 2), Paecilomyces species (n = 2) [Figure 10], [Figure 11], [Figure 12], and Fonsecaea pedrosoi (n = 1), and Candida species (n = 3) [Figure 13], show in [Table 3].
Figure 4: Actinomadura madurae revealing the numerous, delicate (1μm) gram positive filaments at the periphery of the granule

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Figure 5: Higher magnification of Actinomycetoma granule showing details of granule embedded in purulent exudates

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Figure 6: H and E stained tissue section of mycetoma showing branched, septate hyphae of Aspergillus fumigatus

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Figure 7: Microscopic morphology of Aspergillus fumigatus showing typical columnar, uniseriate conidial heads and conidia

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Figure 8: Histopathology of mycetoma showing branched, septate hyphae of Aspergillus flavus (H and E, stain)

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Figure 9: Microscopic morphology of Petriellidium boydii, in the imperfect state, ovoid or pyriform, is produced singly at the tip of conidiophores

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Figure 10: Macroscopic characteristic of Paecilomyces lilacinus showing colony pigmentation

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Figure 11: Microscopic morphology of Paecilomyces lilacinus showing divergent phialides and chains of ellipsoidal conidia

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Figure 12: Histopathology of Paecilomyces lilacinus stained by hematoxylin and eosin

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Figure 13: Colonies of C. albicans, Sabouraud glucose agar, 25C

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Table 3: Distribution of causative agents of mycetoma in Iranian patients


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This paper has highlighted that there is significant benefits of using observational studies in answering questions where large sample sizes of patient groups would be impossible to be accumulated in a reasonable length of time.


   Discussion Top


Mycetoma is a slowly progressive, local chronic, granulomatous, inflammatory cutaneous and subcutaneous tissue, fascia, muscle, and bone. Infection caused by various genera of fungi (eumycetoma) or filamentous bacteria (actinomycetoma) organism. Mycetoma has a worldwide but uneven distribution. The disease is endemic in tropical and subtropical regions. The disease predominates in rural workers between 20 and 40 years of age. [6]

Mycetoma usually affecting the lower extremities, and is found mostly in India, the Middle East, Africa and South America in tropical and subtropical climate zones. [7] The causative agents of mycetoma vary from region to region and with climate. [8] Mycetoma occasionally occurs in Iran, particularly in the South and North. [8] The majority of the patients reported from Iran, were from North and States in South of Iran (Khuzestan, Bushehr and Bandar Abbas) (57.1%), which has high temperature and humid climate. Four patients (11.4%) were from North part of Iran. It may be attributed to subtropical and humid climates in North of Iran, so hot and humid climates predispose to fungal, skin diseases.

It is similar to survey by Zarei et al. [9] In tropical countries, where local health care facilities and health education are usually insufficient and inadequate, and mycetoma is a real public health problem. Disease occurs sporadically throughout most areas of the world, and some postulate that the increased numbers in tropical regions may also be in part the result of decreased use of protective clothing, chiefly shoes, in the warmer, poorer endemic regions. [8]

The infection occurs by inoculation as a result of minor injury to the skin, usually on the foot [Figure 1]. In this study, the longest duration of disease was 38 years. It is a slowly progressing disease affecting the deep dermis and subcutaneous tissues that can extent to the underlying bones. However, actinomycetoma has a rapid progressive course compared to eumycetoma.

The incidence of mycetoma is highest in men, farmers, animal herders, field workers, nomads, those who walk barefoot, and in the third and fourth decades of life. [10]

In current study, mycetoma was found to be abundant among housewives, in urban areas and farmers in rural areas of Iran [Table 1]. However, the disease has also been found in individuals who work in the city in various occupations [Table 1]. Mycetoma occurs most commonly in people who work in rural areas where they are exposed to soil and plants.

In this study male to female ratio were 5:3. The male predominance in mycetoma was attributed to the greater risk of exposure to organisms in the soil during outdoor activities of men. [11],[12],[13] On the other hand, sex hormones have shown to have a direct influence on the development of the fungus. [14],[15]

Mycetoma is an infrequent disease in Iran and is infrequently reported in the literature. In mycetoma, deformity and disability are common complications and it is difficult to know from this retrospective study whether they were due to disease. Most of reported patients had painless discharges sinuses. Furthermore, only a few of the patients recall history of local trauma at the mycetoma site in this series.

In one of our patient observed mix infection due to Pseudallescheria boydii [Figure 9] and Nocardia asteroides in palm of hand. She was a 58-year-old women, brass work, and resident in North of Iran [Figure 2] and [Figure 3]. In North of Iran, women even take a more active part in agricultural activities and still there is a local male predominance in mycetoma. [8],[16] Therefore, the chance of contacting mycetoma is similar for both males and females.

The foot was the most common affected location involvement in the present study (62.8%); however Zarei et al. [8] reported 66.8% in Iran. The most common anatomical site affected by this disease is the upper and lower limbs, particularly the feet and the lower legs. [13] In this study, the next most commonly affected sites were hands (25.7%), face (2.9%), neck (2.9%), trunk (2.9%) and buttock (2.9%) areas, but this varies from country to country. Rarely, mycetoma can be observed on the buttocks, the groin area the head, and the neck. [17]

In current study, 10 patients (28.6%) had concomitant medical problems, it may attributed that among immunocompromised persons, post-traumatic fungal infections are frequent. In the presence of severe underlying immunodeficiency, traumatic inoculation with any fungus may result in rapid local spread and systemic disease, often with fatal outcome.

In current study a 78-year-old woman residing in Damghan, central of Iran, diagnosed with chronic renal failure and diabetes mellitus for a long time. Organisms had inoculated in the left hand in the insulin induction site [Figure 14]. The patient had spiking fever and multiple subcutaneous abscesses in the left forearm. She had chronic renal failure over a period of 25 years and diabetes mellitus for over 14 years. [18]
Figure 14: Clinical appearance view of irregular, draining subcutaneous nodules of hand mycetoma due to Paecilomyces in the insulin induction site

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A large variety of microorganisms are capable of producing mycetoma. [Table 3] shows the causative agents of mycetoma in patients in this study.

Candida sp. was the causative agents of 8.6% of all cases, and all of them had underlying diseases. Underlying diseases for mycetoma due to Candida sp. were insulin dependent diabetes, in finger ulcer after electric shock, foot mycetoma in a patient under immunosuppressive therapy for colon cancer and burn, and foot mycetoma following leave mortar wound in a war veteran.

Mycetoma due to Candida is a rare condition. Only few cases have been reported. [19],[20] The primary pathogen of such infections is Candida sp.[21]

Although such infections rarely cause disseminated or invasive disease, they have an important impact on public health, and timely diagnosis and appropriate treatment remain important. [22]

Infections primarily occur among low socioeconomic groups and those living in rural areas or involved in farming, housewife, or other outdoor activities, and particularly among adult men.


   Conclusion Top


Mycetoma is seen most often in persons, who live in hot, humid climates, therefore it is important for physicians everywhere to be familiar with the mucocutaneous signs and symptoms of tropical mycoses and to be able to perform the proper diagnosis and initiate the appropriate therapy. Diseases were abundant among farmers in rural areas of Iran, housewives in urban area, northern and southern provinces. The most common prevalent mycetoma agents in this study were Actinomyces sp. If mycetoma is not diagnosed early on, it can cause functional and esthetical impairment. If left untreated, mycetoma can affect the underlying bones, joints, or adjacent organs. The infection occurs by inoculation as a result of minor injury to the skin, usually on the foot. In the patients with severe immunosuppression, CGD, high-dose corticosteroids, and diabetes, if there are risk factors for invasive fungal infections traumatic inoculation with any fungus may result in rapid local spread and systemic disease, with fatal outcome.

This article reported selected emerging less common agents of mycetoma (e.g. Candida species and Paecilomyces lilacinus). Paecilomyces lilacinus, a new etiologic agent agent was demonstrated in two cases of eumycotic mycetoma. The global frequency of P.lilacinus infections appears to be increasing, and it is considered as an emerging pathogen, not only in patients with a compromised immune system, but also in apparently healthy people.

This study highlights the benefits of using observational studies as a valuable tool in answering questions where large sample size of patient groups would be impossible to be accumulated in a reasonable length of time.


   Acknowledgment Top


The author is grateful to all the staffs in Medical Mycology Department, Pasteur Institute of Iran.

 
   References Top

1.Fahal AH. Review Mycetoma. Khartoum Med J 2011;4:514-23.  Back to cited text no. 1
    
2.Kwon-Chung KJ, Bennett JE. Mycetoma. In: Medical Mycology. Philadelphia: Lea and Febiger; 1992. p. 560-93.  Back to cited text no. 2
    
3.Burgoon CF, Johnson WC, Grappel SF. Mycetoma formation in Trichophyton rubrum infections. Br J Dermatol 1974;90:155-62.  Back to cited text no. 3
    
4.Geyer AS, Fox LP, Husain S, Della-Latta P, Grossman ME. Acremonium mycetoma in a heart transplant recipient. J Am Acad Dermatol 2006;55:1095-100.  Back to cited text no. 4
    
5.Berd D. Laboratory identification of clinically important aerobic actinomycetes. Appl Microbiol 1973;25:665-81.  Back to cited text no. 5
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6.Hajdu, Alexandra Obradovic, Elisabeth Presterl, V. Vécsei. Invasive mycoses following trauma. Injury 2009;40:548-54.  Back to cited text no. 6
    
7.Fahal AH, Sabaa AH. Mycetoma in children in Sudan. Trans R Soc Trop Med Hyg 2010;104:117-21.  Back to cited text no. 7
    
8.Duane R. Hospenthal. Agents of Mycetoma. Part III Infectious Diseases and Their Etiologic Agents. Chapter 262. Available from: http://www.elsevierjapan.com. [Last accessed on 2010]. [http://dx.doi.org/10.1016/j.physletb.2010.09.059].  Back to cited text no. 8
    
9.Zarei Mahmoudabadi A, Zarrin M. Mycetomas in Iran: A review article. Mycopathologia 2008;165:135-41.  Back to cited text no. 9
    
10.George MA, Turiansky W, Benson PM, Sperling LC, Sau P, Salkin IF, et al. Phialophora verrucosa: A new cause of mycetoma. J Am Acad Dermatol 1995;32:311-5.  Back to cited text no. 10
    
11.Fahal AH. Mycetoma: Clinicopathological Monograph. Sudan: University of Khartoum Press; 2006. p. 7-18.  Back to cited text no. 11
    
12.Hassan MA, Fahal AH. Mycetoma. Mycetoma. In: Kamil R, Lumby J, editors, Textbook of Tropical Surgery. London: Westminster Publishing; 2004. p. 786-90.  Back to cited text no. 12
    
13.Fahal AH. Mycetoma thorn on the flesh. Trans R Soc Trop Med Hyg 2004;98:3-11.  Back to cited text no. 13
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14.Drutz DJ, Huppert M, Sun SH, McGuire WL. Human sex hormones stimulate the growth and maturation of Coccidioides immitis. Infect Immun 1981;32:897-907.  Back to cited text no. 14
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15.Restrepo A, Salazar ME, Cano LE, Stover EP, Feldman D, Stevens DA. Estrogens inhibit mycelium-to-yeast transformation in the fungus Paracoccidioides brasiliensis: Implications for resistance of females to paracoccidioidomycosis. Infect Immun 1984;46:346-53.  Back to cited text no. 15
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16.Griffiths WA, Kohout E, Vessal K. Mycetoma in Iran. Int J Dermatol 1975;14:209-13.  Back to cited text no. 16
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17.Liu A, Maender JL, Coleman N, Hsu S, Rosen T. Actinomycetoma with negative culture: A therapeutic challenge. Dermatol Online Journal 2008;15;14:5.  Back to cited text no. 17
    
18.Bassiri Jahromi S. Khaksar AA. Peacilomyces infection in an immunocompromised patient. Med J Islam Repub Iran 2004;18:181-4.  Back to cited text no. 18
    
19.Prats E, Sans J, Valldeperas J, Ferrer JE, Manresa F. Pulmonary mycetoma-like lesion caused by Candida tropicalis. Respir Med 1995;89:303-4.  Back to cited text no. 19
    
20.Shelly MA, Poe RH, Kapner LB. Pulmonary mycetoma due to Candida albicans: Case report and review. Clin Infect Dis 1996;22:133-5.  Back to cited text no. 20
    
21.Eggimann P, Calandra T, Fluckiger U, Bille J, Garbino J, Glauser MP, et al. Invasive candidiasis: Comparison of management choices by infectious disease and critical care specialists. Intensive Care Med 2005;31:1514-21.  Back to cited text no. 21
    
22.Queiroz-Telles F, Nucci M, Colombo AL, Tobón A, Restrepo A. Mycoses of implantation in Latin America: An overview of epidemiology, clinical manifestations, diagnosis and treatment. Med Mycol 2011;49:225-36.  Back to cited text no. 22
    

hat is new?
Infections primarily occur (1) among low socioeconomic groups, (2) among those living in rural areas or involved in farming, or other outdoor activities, and (3) particularly among adult men. This article focuses on microbiology and clinical feature of the most clinically significant implantation mycoses in Iran. In this article reported selected emerging less common agents of mycetoma (e.g., Candida species and Paecilomyces lilacinus). Paecilomyces lilacinus, a new mycetoma agent was demonstrated to be the etiologic agent in two cases of eumycotic mycetoma. This study highlights the benefits of using observational studies as a valuable tool in answering questions where large sample sizes of patient groups would be impossible to be accumulated in a reasonable length of time.


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8], [Figure 9], [Figure 10], [Figure 11], [Figure 12], [Figure 13], [Figure 14]
 
 
    Tables

  [Table 1], [Table 2], [Table 3]



 

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