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Mycoses in India—study in Madras
92 TRANSACTIONS OF THH ROYAL SOCIETY OF TROPICAL. MEDICINE
Mycoses
AND HYGIENE,
VOL.
in India-study
A. KAMALAM, A. S. THAMBIAH,
75, NO.
in
1, 1981
Madras*
M. BAGAVANDAS
AND S. GOVINDARAJU Dept. of Dermatology, Madras Medical College & Government General Hospital, Dept. qf Statistics, Madras Christian College, Madras, India.
Summary The incidence of mycoses is high in Madras accounting for over 13’z of dermatoses diagnosed in a three-year period. Dermatophytoses (tinea corporis and tinea cruris) and pityriasis versicolor were most common in May and October. A correlation was observed between these infections and environmental temperature, humidity and rainfall. Most cases of all dermatophytoses except tinea capitis were recorded between 10 and 30 years of age but the latter was most common between one and 10 years. Males were predominantly affected with all except tinea axillaris, candidiasis and piedra. The incidence of piedra and deep mycoses was low. Introduction From ancient times to the modern space era, dermatophytoses have been a major public health problem throughout the world, including India. The state of Tamil Nadu has a population of 41,199,168 and its capital, Madras, has a population of 27.88.000 (1975 census). Overcrowding is a , , common feat&e in all cities of the state and is worst in Madras. There are five major general hospitals in the city. Most patients attend the Government General Hospital (GGH), which is the oldest and largest hospital in Madras, serving some 5000 to 6000 patients daily. The mycoses diagnosed at the GGH during 1973 to 1976 were studied and the results are presented here. Materials and Methods Clinical material was collected on alternate days from the Out-Patient Department of Dermatology, GGH between November 1973 and October 1976. Laboratory investigations were done in the Mycology section of the same department. Following a thorough clinical examination, routine wet preparations were made of the diseased tissues in KOH when appropriate preparations were mounts, stained bv Gram and Ziehl Neelsen urocedures. Cultures &ere made in Sabouraud’s dextrose agar with and without cycloheximide and chloramphenicol (EMMONS et al., 1970). Biopsy sections were stained with haematoxylin and eosin and periodic Schiff reagent. Some isolates were sent to Prof. I,. N. Mohapatra, Delhi and Dr. L. Ajello, Atlanta, Georgia, USA for confirmation or identification.
-
~
* This formed part of the thesis submitted for Ph.D. of Madras University in 1977 by A. Kamalam.
and
Data regarding environmental temperature, humidity and rainfall during the period of study were obtained from the Metereological Centre, Nungambakkam, Madras. When quantitative data are arranged in the order of their occurrence, the resulting statistical series is called a time series. The components of a time series are the individual various elements which may be separated from the observed data. These are secular trend, seasonal variation, cyclical fluctuation and random fluctuations. Seasonal variations are those periodic movements which repeat themselves hourly, daily, monthly, quarterly or even annually. These variations can be measured in terms of relative seasonal indices in rates or in percentages. The seasonal indices are calculated as “Ratio to moving average” method. For monthly data, a 12-month moving average completely eliminates the seasonal movements if they are of constant pattern. So, 12-month moving averages were used to calculate the monthly trends. Seasonal indices and trend values were calculated making use of the IBM 370/l% computer at the Indian Institute of Technology Computer Centre, Madras. The relationship of climatic conditions to the various mycoses was studied for a total period of four years by including previous work (KAMALAM & THAMBIAH, 1976) in the present work in order to have a wider duration for correlation. The population census (1975) of Madras city was obtained from the Corporation of Madras for comparative study. Observations During the three-year period there were 104,797 new cases of dermatoses with an average of 34,932 cases yearly. This formed 50”;) of the total dermatoses seen in the department. Among this group 15,082 patients were investigated for evidence of mycoses. A total of 13,724 cases was confirmed by the methods employed in this study (Table I). This represented 13.1 o:, of all dermatoses diagnosed during-the study perio& For individual yea&, the annual incidence of mycoses was 9.96”;, 12.89:‘; and 16.45”. of the total dermatoses. The most common skin disorder was scabies followed by impetigo. Mycoses were the third most common. Fig. 1 illustrates the incidence of mycoses in relation to total dermatoses during the three years of study. Mycoses were diagnosed more frequently during the hot summer months although a rise was also observed during October.
A. KAMALAM
Table I-Types 1973-1976
of mycoses
Diseases
diagnosed
between
No. of cases
Dermatophytoses Tinea versicolor Candidiasis Deep mycoses Piedra
10,122 2,252 1,324 20 6
73-75 16.41 9.65 o-15 o-044
Total
13,724
100
The statistical data of monthly mean value with standard deviation of the various entities have been given in Table II. The actual incidence and trend lines are given in Figs. 2a to 2g. Total
Mycoses
The monthly mean value with standard deviation of total mvcoses was 369 * 16 -t 148.63. The highest incidence2 was seen in October (151.77%)-and May(132.707’) and thelowest in January(52.56%). There was a downward trend from 1973 to 1974 with a gradual upward trend during 1975 and 1976 (Fig. 2a). Total mycoses correlated with all types of dermatophytoses, pityriasis versicolor, candidiasis, minimum and maximum temperature and rainfall. Tinea capitis
There were a total of 790 (5.23”:,)
cases of tinea
93
et al.
capitis with monthly mean value with standard deviation of 16-45 f 13.32. The highest incidence was found in August (136.39%) and the lowest in January. Between 1973 and 1976 there was an upward trend (Fig. 2b). The disease was highly correlated with total mycoses, tinea facei, tinea barbae, tinea corporis, tinea cruris, tinea manuum, tinea pedis, tinea unguium, pityriasis versicolor and candidiasis. Correlation with temperature, humidity and rainfall was not marked or was lacking. Tinea facei
There were 673 (4.87%,) cases of tinea facei. The monthly mean value and standard deviation was 17.95 i 6.29. The highest incidence was in October (157.37%) and the lowest in December (61.68’;4) and was highly correlated with total mycoses, tinea corporis, tinea cruris, tinea manuum, tinea pedis, pityriasis versicolor, candidiasis and humidity and rainfall but not with temperature. There was change in trend value from 1972 to 1975 but there was a slight rise in 1976. Tinea barbae
A total of 372 (2.69%) cases were of this type. The monthly mean value with standard deviation was 8.79 & 4.75. The highest incidence was in July (150.56). It was found to be highly correlated with total mycoses, tinea facei, tinea pedis, tinea cruris, tinea corporis, tinea manuum, tinea unguium and pityriasis versicolor but not with temperature, humidity or rainfall. There was a gradual rise in trend value from 1973 to 1976.
4000 I 35oc 1 -
\
DERMATOSES
A
3ooc )250CI2000 / 1500 1000 500 0
Fig. 1. Incidence of total dermatoses, scabies and mycoses from November
1973 to October 1976.
91.34 94.96 94.50 65.14 90.37 88.36 *47 77.28 60.11 64.96
108.10 88.83
mycoses capitis facei barbae corporis cruris axillaris manuum pedis unguium
Total Tinea Tinea Tinea Tinea Tinea Tinea Tinea Tinea Tinea
Tinea versicolor Candidiasis
50.60 84.44
72.57 110.35 61.68 57.97 64.20 64.13 28 74.85 68.13 83-73
Dec.
39.87 90.72
52.56 51.03 81.96 87.35 53.00 46.26 32 87.09 76.01 54.43
Jan.
79-78 87.52
74.21 87.90 85.69 69.46 57.20 65.36 27 105.68 101.02 74.75
Feb.
102.75 102.38
93.31 119.66 124.53 96.20 76.51 85.03 34 97.31 147.31 97.74
Mar.
and mean value with standard
117.88 107.49
111-11 114.88 98.87 125.03 104.92 107.90 35 121.70 148.39 127.22
Apr.
deviation
III-Monthly
Temp. Min. Temp. Max. Hum. 08.30 h Hum. 17.30 h Rainfall
Table
91.56 89.50 107.76 107.80 265 *37
Nov.
Dec.
82.76 86.16 105.70 96.24 12.16
Jan. 86.06 92.36 105.35 96.67 0.21
Feb. 95.55 99.82 105.28 100.68 0.52
Mar.
and mean value with standard
88.59 85.45 104.90 101.62 84.44
incidence
109.20 105.76 99.37 107.40 0.00
Apr.
68.96 65.19
90.19 93.22 80.22 92-33 97.67 105.51 67 90.98 89.00 106.68
June
May
113.20 114.25 77.93 81.18 15.78
June
107.12 106.96 93.23 92.14 122.80
July
Aug.
101.44 110.29
105.76 78.28 96.67 102.10 118.33 112.30 89 86.73 77.06 109.35
Sept.
105.40 104.09 98.66 97.83 261.64
Aug.
104.39 102.64 105.60 107.63 90.74
Sept.
and rainfall
98.21 108.16
Ill-49 136.39 114.58 140.83 119.35 120.36 88 113.33 102.80 136.77
humidity
84.43 103.45
108.99 109.63 99.02 150.56 120.98 121.56 77 97.02 98.71 112.90
July
mycoses
of temperature,
165.63 128.91
132.70 110.38 103.97 93.57 131.85 134.00 67 137.30 109.98 127.02
May
of various
115.12 .115.31 85.35 96.60 16.02
deviation
* Values given for tinea axillaris denotes actual incidence. Mean value in all excepting in tinea axillaris is given with standard deviation.
Nov.
incidence
II-Monthly
Table
101.05 97.70 110.85 113.21 290.30
Oct.
182.35 122.62
151*77 93.32 157.37 119.46 165.67 149.17 82 110.67 121.48 104.35
Oct.
30.66 11.40 -
24.17 32.34 77.27 70.62 101.12
& 2.52 + 3.20 zt 7.21 zt 6.54 + 126.61
Mean value
61.10 i. 37.64 &
f 148.63 xt 13.32 zk 6.29 zt 4.75 + 61.19 i 81*21 56 18.00 + 6.22 16-77 * 7.45 24.04 f 17.05
369.16 16.45 17.95 8-79 148.75 171.81
Mean value
5 8 ’ 2 2 5
.,_^...,‘, ,.‘.
J 1975
N .I
I.
I
Fig. 2b
100
200
I\1J 1973
300
NJ 400 7 197_3Fig. 2d
60
N J’ 1973
J
.
0
J 1974
J 1974
.I
J 1975
v
J 1975
J
J 1976
19:s
0
80
Fig. 2e
-
rij 1973
NJ
I.
3
Trend Actual 2 incidence of Incidence of Incidence of Incidence of In’cidence of Incidence of tinea g. Incidence of
Figure a. b. c. d. e. f.
0
1
versicolor candidiasis
J
J 1975
19J75
total mycoses tinea capitis tinea corporis tinea cruris tinea unguium
incidence
Line
j 1974
J
t. _ J NJ 1201 1873 Fig. 2f 1974
20
200 .
J’ 1974
40’
400 ’
80 60,
Fig. 2s
600
800 ’
j 1976
J
J A 1976
0
0
x ?c
96
MYCOSES
Tinea corporis
This was detected in 5,209 (37.6574) cases. The monthly mean value and standard deviation was 148.75 i 61.19. The highest incidence was in October (165*67oj,) and May (131.85%) and the lowest in January (53%). It was highly correlated with total mycoses, tinea cruris, tinea manuum, tinea pedis, tinea unguium, pityriasis versicolor, candidiasis and temperature and rainfall but not with humidity. There was a downward trend from 1973 to 1974 and an upward trend in 1975 and 1976 (Fig. 2~). Tinea cruris
This was the most common expression of dermatophytosis, accounting for 6,388 (46.17%) of the cases diagnosed during the three-year period. This formed 6.10% of all dermatoses seen during this time. The monthly mean value and standard deviation was 171.81 f 81.21. The highest incidence was in October (149.17%) and May (13476) and the lowest in January (46.27”). The disease correlated highly with total mycoses, tinea manuum tinea pedis, tinea corporis, tinea unguium, pityriasis versicolor, candidiasis and temperature and rainfall but not with humidity. The trend line showed a
IN
INDIA
gradual fall in the middle of 1974 with a gradual rise thereafter as in tinea corporis (Fig. 2d). Tinea axillaris
This was detected in 673 (4.87%) cases. The highest incidence was observed during May to October. Incidence was lower during the cooler months from November to March. Tinea manuum
A total of 635 (4.59%) cases were recorded. The monthly mean value with standard deviation was 10.00 + 6.22. The highest incidence was observed in May (137 -30%) and the lowest in December (74.65%). It was highly correlated with tinea pedis, total mycoses, tinea unguium, candidiasis and pityriasis versicolor but not with temperature, humidity or rainfall. A downward trend in 1974 followed by an upward trend in 1975-76 was observed. Tinea pedis
This type was found in 630 (4.55%) cases. The monthly mean value with standard deviation was 16.77 & 7.45. The highest incidence was observed in April (148.390/,) and March (147.31%) and the
6500 6000 5500 5000 4500 44000 3500 3000 2500 2000 I
-
15oc I
-
1000 I
-
500 I
-
Fig. 3. Shows the consolidated incidence of various mycoses in males and females of 13,724 cases of mycoses during November 1976.
1973 to October
0
E-
0
cn s
2l>
0”
8’
2.
T. CORPORIS
T. CAPITIS
op Ei H ul Ei
AGE IN YEARS . 0 m fs 10” s
z
g
g,
g-
2
T. VERSICOLOR
T. MANUUM
%
0” _
98
MYCOSES
lowest in November (60.11%). It was correlated with total mycoses, tinea unguium, pityriasis versicolor and candidiasis but there was no correlation with temperature, humidity and rainfall. The trend value showed a stable line from 1973 to 1975 with a gradual rise in 1976. Tinea unguium
This was detected in 906 (6.56%) cases. The monthly mean value with standard deviation was 24.04 & 17.05. The highest incidence was observed in April (127.22%) and the lowest in January (54.43%). There was significant correlation with total mycoses, candidiasis and pityriasis versicolor but no correlation with temperature, humidity and rainfall. There was a gradual downward trend from 1973 to 1974 and an upward trend from July 1974 to July 1975 followed by a second fall thereafter (Fig. 2~). Pityriasis
versicolor
This was detected in 2,252 (16.29%) cases. The monthly mean value with standard deviation was 61.10 + 30.66. The highest incidence was found in October (182.35%) &-id May (165.63%) and the lowest in January (39.87%). There was a downward trend from 1973 to July 1974 with an upward trend thereafter (Fig. 2f). The diseasewas highly correlated with total mycoses, tinea corporis, tinea cruris, tinea manuum, tinea pedis, tinea unguium, candidiasis, temperature and rainfall. Candidiasis
Candidiasis of the skin, mucous membranes and nails was detected in 1.324 (9 *57%) cases. The monthly mean value with standard’ “deviation was 37.64 -+ 11.40. The highest incidence was in May (128.91%) and October (122.62%) and the lowest in June (65.19%). There was a downward trend value from 1973 to 1974 and an upward trend thereafter (Fig. 2g). The disease was highly correlated with total mycoses, tinea unguium and tinea versicolor, and moderately correlated with all other types of dermatophytoses except tinea barbae. There was no correlation with temperature, humidity and rainfall. Pie&a
The incidence of piedra was the lowest of all mycoses and was found in only six (0.043%) cases. There were four cases of white piedra and two of black piedra. They were all recorded in the cooler months of October (three), November (two) and December (one). Deep Mycoses
A total of 20 (0.14%) cases was diagnosed, 18 with mycetoma and two with entomophthoramycosis. Most were recorded in July. Sex incidence of various mycoses
There were 9254 (66.89%) adult males, 3,963 (28.65%) adult females and 617 (4.46%) children less than 10 years old. Of these children, 326 (52.83%) were male and 291 (47.17%) were female. Fig. 3 shows the consolidated incidence of various mycoses seen in males and females among
IN INDIA
13,834 recorded cases from November 1973 to October 1976. Males were found to be predominantly affected by all but tinea axillaris, candidiasis and piedra. Age incidence of various mycoses
Fig. 4 shows the age incidence. In general, the majority affected were between 10 and 50 years of age. In tinea capitis, maximum cases were seen in the age group of five to 10 years. In all other diseases the incidence was maximum between 10 and 30 years of age. Climatic
conditions
Table III shows the monthly incidence and mean value with standard deviation of temperature, humidity and rainfall. Temperature minimum
The mean value with standard deviation of minimum temperature recorded was 24.17 & 2*52”C. The lowest minimum temperature was recorded in January (82.76%) and the highest in May (115 * 12%) with a straight trend line. The calculated values correlated with the incidence of tinea corporis, tinea cruris, pityriasis versicolor, total mycoses, maximum temperature and humidity. Temperature maximum
The mean value and standard deviation for maximum temperature was 32 a34 It 3.20%. The lowest maximum temperature was in December (85.45%) and the highest in May (115.31%) with a straight trend line. The calculated values correlated with tinea corporis, tinea cruris, pityriasis versicolor, total mycoses, minimum temperature and humidity. Humidity
at 08.30 hours
Humidity
at 17.30 hours
The mean value and standard deviation was 77.27 & 7.21. The lowest was in June (77.93%) and the highest in October (110*85?L) with a straight trend line. The calculated -v&es correlated with minimum and maximum temperature, humidity at 17.30 hours and rainfall. The mean value and standard deviation was 70.62 f 6.54. The lowest was in June (81.18%) and the highest in October (113 -21%). The trend line was straight. The calculated values correlated with tinea facei, pityriasis versicolor, maximum temperature, humidity at 08.30 hours and rainfall. Rainfall
The monthly mean value and standard deviation was 101.12 f 126.61. The lowest was in April (0.00%) and highest in October (290.30%). The trend line showed a tendency to rise during 1975 to 1976. The calculated values showed correlation with tinea facei, tinea corporis, tinea cruris, pityriasis versicolor, total mycoses and humidity at 08.30 hours and at 17.30 hours. Comment
The incidence of mycoses was 13.2%. They were the third most common disease diagnosed in skin
A. KAMALAMet al. clinics in Madras. Such a high incidence of mvcoses has also been found in Hvderabad (NAGABHUSHANAMet al., 1969) and -Bombay (DESAI & BJSAT, 1961). Higher incidences of mycoses, particularly dermatophytoses, pityriasis versicolor and candidiasis have been reported in areas which are situated at sea level where hot humid weather prevails (CANIZARES,1973). This climate prevails in Madras and when combined with a high population density these infections are likely to be prevalent. Such high incidences have also been found in Nigeria (SHRANK. 1965) \ -, and Japan (SIGEL, 1948). Mycoses, particularly dermatophytoses and pityriases versicolor were most common during May when the temperature is highest and in October the temperature is lower but when humidity and rainfall are highest. Such seasonal incidence has been similar over the preceding 12 years. Regions such as Mexico, Puerto Rico, certain Latin American countries, Nigeria and Philippines have a high incidence of mycoses (RIPPON, 1974; SHRANK, 1965; REVES& JACALNE,1962) as does India, suggesting that latitude and climatic conditions play a role in these infections. Temoerature. rainfall and humiditv recorded during-the present work have shown* a definite correlation with mycoses, particularly the major portions of dermatophytoses like tinea corporis, tinea cruris and pityriasis versicolor which were found collectively in 83.82% of patients. Humidity and rainfall were highly correlated to tinea facei. These tropical environmental conditions are comparable with the known favourable temperature of 25°C to 30°C and high humidity of 95% to 100% (COCHRANE, 1958; STOCKDALE, 1953) that are necessary for optimal growth of dermatophytes. Another contributory factor to high prevalence is the increased sweating in tropical environments which, in turn, would raise the pH of sweat from 4.5-5.5 to 7 (PILLSBURYet al., 1956) which is a known optimum pH for the growth of many dermatophytes. The incidence of other dermatophytoses such as tinea barbae, tinea manuum, tinea pedis and tinea unguium was found to be low. Correlation with temperature and humidity and rainfall were less striking in these types and there was no correlation between climatic conditions and tinea capitis. The incidence of piedra was very low, but its occurrence in cooler months with heavy rainfall and high humidity suggested that the disease might be associated with cooler and wet conditions. The incidence of deep mycoses was low (0.14%) and it would be erroneous to infer from this number any seasonal incidence since all reported caseswere either from outside Madras city or from the southern districts of Tamil Nadu such as Ramanathapuram, Tirunelveli and Madurai and had reported for treatment months or years after the onset of the disease. However, the incidence of deep mycoses in southern districts is known to be high and 266 cases had been previously recorded during 1959 to 1966 (Asirvatham, personal communication). These districts are in the same latitude as countries such as Sudan, Nigeria, Puerto Rico and certain Latin American countries
99
where the prevailing temperature and rainfall is similar, namely, between 25 and 50 mm per year. In these areas the incidence of dermatophytoses is also high, relative humidity, temperature and rainfall being the main factors contributing to the epidemiological incidence of mycoses. Sex
A preponderance of males has been observed. This could be internreted in two wavs. One is the larger male populatibn of the city. Secondly not all the affected females report for treatment since they are commonly confined to the house by social practice. However, the difference in sex ratio of the affected subjects is too great to ignore the male preponderance, and the difference in the sex ratio of the population is not marked. A definite female preponderance has been observed in tinea capitis, iinea axillaris, candidiasis and niedra. The clothing: habit of close fitting blouse in females gives a local&ed tropical environment in the axillae which would explain this higher incidence for tinea axillaris. Occupational factors and the wet long hair in females could explain the higher incidences of candidiasis and piedra. Children below 10 years have shown a predominance of tinea capitis and candidiasis. For the former disease 47.03% of cases occurred in children. However, when the study population is compared, the ratio of children to adults is approximately 6 : 19 suggesting a definite age proneness. In general all other dermatophytoses showed a sudden increase after 10 years of age. This raises questions on the fungistatic activity of sebum secreted more during summer and after puberty, and suggests that further evaluation of the-role of skin li$ds in dermatoohvtoses is reauired. The higher incidence of &yriasis versicblor, a lipid dependent disease, between 10 and 30 years and in summer correlates with increased sebaceousactivity in this age group and during the summer months. A second peak incidence in October with lower temperature and highest rainfall and humidity may denote a species difference in causal agent of these diseases. Acknowledgement
We gratefully acknowledge the help given by the authorities, Meteorological Centre, Nungambakkam, Madras, Indian Institute of Technology Computer Centre, Madras and Corporation of Madras. We are also grateful to Prof. L. N. Mohapatra, Delhi and Dr. L. Ajello, Atlanta, USA, for help in culture work. References
Canizares, 0. (1973). Epidemiology of the dermatoses of Latin America. In: Essays of Tropical Dermatology. Marshall, J. (Editor). Amsterdam: Excerpta Medica, pp. 427-431. Cochrane, V. W. (1958). Cultivation and growth. In: Physiology of Fungi. New York: John Wiley & Sons, p. l-34. Desai, S. C. & Bhat, M. L. A. (1961). Dermatomycoses in Bombay. Indian Journal of Medical Research, 49, 662-671.
100
MYCOSES
Emmons, C. W., Binford, C. H. & Utz, J. P. (1970). Culture Media. In: Medical Mycology. Philadelphia: Lea & Febiger, pp. 464-468. Kamalam, A. & Thambiah, A. S. (1976). A study of 3891 cases of mycoses in the tropics. Sabouraudia, 14, 129-148. Nagabhushanam, P., Thirumala Rao, R. & Patnaik, R. (1969). Dermatomycoses in Hyderabad Area. Indian Journal of Dermatology and Venereology, 35, 120-123. Pillsbury, D. M., Shelley, W. B. & Kligman, A. M. (1956). The glands of the skin. In: Dermatology. Philadelphia: W. B. Saunders, pp. 52-66. Reyes, A. C. & Jacalne, A. V. (1962). As quoted by Kalique, A. et al., (1974). Incidence and types of Dermatomycoses in Aurangabad. Indian Journal of Dermatology and Venereology, 40,66-72.
IN
INDIA
Rippon, J. W. (1974). Dermatophytosis and Dermatomycosis. In: Medical Mycology. Philadelnhia. London & Toronto: W. B. Saunders, pp.- 96-174. Shrank, A. B. (1974). A field survey in Nigeria. Transactions of the St. Yohn’s HosPital Dermatological Society; 451, 85.” * Sigel, H. (1948). Cutaneous diseases among army personnel in Japan. Archives of Dermatology and Syphilology, 57, 128-131. Stockdale, l?. M. (1953). Requirements for the growth and sporulation of Trichophyton persicolor. Journal of General Microbiology, 8,434-441.
Accepted for publication
lOthJanuary,
1980.
Mycoses
AND HYGIENE,
VOL.
in India-study
A. KAMALAM, A. S. THAMBIAH,
75, NO.
in
1, 1981
Madras*
M. BAGAVANDAS
AND S. GOVINDARAJU Dept. of Dermatology, Madras Medical College & Government General Hospital, Dept. qf Statistics, Madras Christian College, Madras, India.
Summary The incidence of mycoses is high in Madras accounting for over 13’z of dermatoses diagnosed in a three-year period. Dermatophytoses (tinea corporis and tinea cruris) and pityriasis versicolor were most common in May and October. A correlation was observed between these infections and environmental temperature, humidity and rainfall. Most cases of all dermatophytoses except tinea capitis were recorded between 10 and 30 years of age but the latter was most common between one and 10 years. Males were predominantly affected with all except tinea axillaris, candidiasis and piedra. The incidence of piedra and deep mycoses was low. Introduction From ancient times to the modern space era, dermatophytoses have been a major public health problem throughout the world, including India. The state of Tamil Nadu has a population of 41,199,168 and its capital, Madras, has a population of 27.88.000 (1975 census). Overcrowding is a , , common feat&e in all cities of the state and is worst in Madras. There are five major general hospitals in the city. Most patients attend the Government General Hospital (GGH), which is the oldest and largest hospital in Madras, serving some 5000 to 6000 patients daily. The mycoses diagnosed at the GGH during 1973 to 1976 were studied and the results are presented here. Materials and Methods Clinical material was collected on alternate days from the Out-Patient Department of Dermatology, GGH between November 1973 and October 1976. Laboratory investigations were done in the Mycology section of the same department. Following a thorough clinical examination, routine wet preparations were made of the diseased tissues in KOH when appropriate preparations were mounts, stained bv Gram and Ziehl Neelsen urocedures. Cultures &ere made in Sabouraud’s dextrose agar with and without cycloheximide and chloramphenicol (EMMONS et al., 1970). Biopsy sections were stained with haematoxylin and eosin and periodic Schiff reagent. Some isolates were sent to Prof. I,. N. Mohapatra, Delhi and Dr. L. Ajello, Atlanta, Georgia, USA for confirmation or identification.
-
~
* This formed part of the thesis submitted for Ph.D. of Madras University in 1977 by A. Kamalam.
and
Data regarding environmental temperature, humidity and rainfall during the period of study were obtained from the Metereological Centre, Nungambakkam, Madras. When quantitative data are arranged in the order of their occurrence, the resulting statistical series is called a time series. The components of a time series are the individual various elements which may be separated from the observed data. These are secular trend, seasonal variation, cyclical fluctuation and random fluctuations. Seasonal variations are those periodic movements which repeat themselves hourly, daily, monthly, quarterly or even annually. These variations can be measured in terms of relative seasonal indices in rates or in percentages. The seasonal indices are calculated as “Ratio to moving average” method. For monthly data, a 12-month moving average completely eliminates the seasonal movements if they are of constant pattern. So, 12-month moving averages were used to calculate the monthly trends. Seasonal indices and trend values were calculated making use of the IBM 370/l% computer at the Indian Institute of Technology Computer Centre, Madras. The relationship of climatic conditions to the various mycoses was studied for a total period of four years by including previous work (KAMALAM & THAMBIAH, 1976) in the present work in order to have a wider duration for correlation. The population census (1975) of Madras city was obtained from the Corporation of Madras for comparative study. Observations During the three-year period there were 104,797 new cases of dermatoses with an average of 34,932 cases yearly. This formed 50”;) of the total dermatoses seen in the department. Among this group 15,082 patients were investigated for evidence of mycoses. A total of 13,724 cases was confirmed by the methods employed in this study (Table I). This represented 13.1 o:, of all dermatoses diagnosed during-the study perio& For individual yea&, the annual incidence of mycoses was 9.96”;, 12.89:‘; and 16.45”. of the total dermatoses. The most common skin disorder was scabies followed by impetigo. Mycoses were the third most common. Fig. 1 illustrates the incidence of mycoses in relation to total dermatoses during the three years of study. Mycoses were diagnosed more frequently during the hot summer months although a rise was also observed during October.
A. KAMALAM
Table I-Types 1973-1976
of mycoses
Diseases
diagnosed
between
No. of cases
Dermatophytoses Tinea versicolor Candidiasis Deep mycoses Piedra
10,122 2,252 1,324 20 6
73-75 16.41 9.65 o-15 o-044
Total
13,724
100
The statistical data of monthly mean value with standard deviation of the various entities have been given in Table II. The actual incidence and trend lines are given in Figs. 2a to 2g. Total
Mycoses
The monthly mean value with standard deviation of total mvcoses was 369 * 16 -t 148.63. The highest incidence2 was seen in October (151.77%)-and May(132.707’) and thelowest in January(52.56%). There was a downward trend from 1973 to 1974 with a gradual upward trend during 1975 and 1976 (Fig. 2a). Total mycoses correlated with all types of dermatophytoses, pityriasis versicolor, candidiasis, minimum and maximum temperature and rainfall. Tinea capitis
There were a total of 790 (5.23”:,)
cases of tinea
93
et al.
capitis with monthly mean value with standard deviation of 16-45 f 13.32. The highest incidence was found in August (136.39%) and the lowest in January. Between 1973 and 1976 there was an upward trend (Fig. 2b). The disease was highly correlated with total mycoses, tinea facei, tinea barbae, tinea corporis, tinea cruris, tinea manuum, tinea pedis, tinea unguium, pityriasis versicolor and candidiasis. Correlation with temperature, humidity and rainfall was not marked or was lacking. Tinea facei
There were 673 (4.87%,) cases of tinea facei. The monthly mean value and standard deviation was 17.95 i 6.29. The highest incidence was in October (157.37%) and the lowest in December (61.68’;4) and was highly correlated with total mycoses, tinea corporis, tinea cruris, tinea manuum, tinea pedis, pityriasis versicolor, candidiasis and humidity and rainfall but not with temperature. There was change in trend value from 1972 to 1975 but there was a slight rise in 1976. Tinea barbae
A total of 372 (2.69%) cases were of this type. The monthly mean value with standard deviation was 8.79 & 4.75. The highest incidence was in July (150.56). It was found to be highly correlated with total mycoses, tinea facei, tinea pedis, tinea cruris, tinea corporis, tinea manuum, tinea unguium and pityriasis versicolor but not with temperature, humidity or rainfall. There was a gradual rise in trend value from 1973 to 1976.
4000 I 35oc 1 -
\
DERMATOSES
A
3ooc )250CI2000 / 1500 1000 500 0
Fig. 1. Incidence of total dermatoses, scabies and mycoses from November
1973 to October 1976.
91.34 94.96 94.50 65.14 90.37 88.36 *47 77.28 60.11 64.96
108.10 88.83
mycoses capitis facei barbae corporis cruris axillaris manuum pedis unguium
Total Tinea Tinea Tinea Tinea Tinea Tinea Tinea Tinea Tinea
Tinea versicolor Candidiasis
50.60 84.44
72.57 110.35 61.68 57.97 64.20 64.13 28 74.85 68.13 83-73
Dec.
39.87 90.72
52.56 51.03 81.96 87.35 53.00 46.26 32 87.09 76.01 54.43
Jan.
79-78 87.52
74.21 87.90 85.69 69.46 57.20 65.36 27 105.68 101.02 74.75
Feb.
102.75 102.38
93.31 119.66 124.53 96.20 76.51 85.03 34 97.31 147.31 97.74
Mar.
and mean value with standard
117.88 107.49
111-11 114.88 98.87 125.03 104.92 107.90 35 121.70 148.39 127.22
Apr.
deviation
III-Monthly
Temp. Min. Temp. Max. Hum. 08.30 h Hum. 17.30 h Rainfall
Table
91.56 89.50 107.76 107.80 265 *37
Nov.
Dec.
82.76 86.16 105.70 96.24 12.16
Jan. 86.06 92.36 105.35 96.67 0.21
Feb. 95.55 99.82 105.28 100.68 0.52
Mar.
and mean value with standard
88.59 85.45 104.90 101.62 84.44
incidence
109.20 105.76 99.37 107.40 0.00
Apr.
68.96 65.19
90.19 93.22 80.22 92-33 97.67 105.51 67 90.98 89.00 106.68
June
May
113.20 114.25 77.93 81.18 15.78
June
107.12 106.96 93.23 92.14 122.80
July
Aug.
101.44 110.29
105.76 78.28 96.67 102.10 118.33 112.30 89 86.73 77.06 109.35
Sept.
105.40 104.09 98.66 97.83 261.64
Aug.
104.39 102.64 105.60 107.63 90.74
Sept.
and rainfall
98.21 108.16
Ill-49 136.39 114.58 140.83 119.35 120.36 88 113.33 102.80 136.77
humidity
84.43 103.45
108.99 109.63 99.02 150.56 120.98 121.56 77 97.02 98.71 112.90
July
mycoses
of temperature,
165.63 128.91
132.70 110.38 103.97 93.57 131.85 134.00 67 137.30 109.98 127.02
May
of various
115.12 .115.31 85.35 96.60 16.02
deviation
* Values given for tinea axillaris denotes actual incidence. Mean value in all excepting in tinea axillaris is given with standard deviation.
Nov.
incidence
II-Monthly
Table
101.05 97.70 110.85 113.21 290.30
Oct.
182.35 122.62
151*77 93.32 157.37 119.46 165.67 149.17 82 110.67 121.48 104.35
Oct.
30.66 11.40 -
24.17 32.34 77.27 70.62 101.12
& 2.52 + 3.20 zt 7.21 zt 6.54 + 126.61
Mean value
61.10 i. 37.64 &
f 148.63 xt 13.32 zk 6.29 zt 4.75 + 61.19 i 81*21 56 18.00 + 6.22 16-77 * 7.45 24.04 f 17.05
369.16 16.45 17.95 8-79 148.75 171.81
Mean value
5 8 ’ 2 2 5
.,_^...,‘, ,.‘.
J 1975
N .I
I.
I
Fig. 2b
100
200
I\1J 1973
300
NJ 400 7 197_3Fig. 2d
60
N J’ 1973
J
.
0
J 1974
J 1974
.I
J 1975
v
J 1975
J
J 1976
19:s
0
80
Fig. 2e
-
rij 1973
NJ
I.
3
Trend Actual 2 incidence of Incidence of Incidence of Incidence of In’cidence of Incidence of tinea g. Incidence of
Figure a. b. c. d. e. f.
0
1
versicolor candidiasis
J
J 1975
19J75
total mycoses tinea capitis tinea corporis tinea cruris tinea unguium
incidence
Line
j 1974
J
t. _ J NJ 1201 1873 Fig. 2f 1974
20
200 .
J’ 1974
40’
400 ’
80 60,
Fig. 2s
600
800 ’
j 1976
J
J A 1976
0
0
x ?c
96
MYCOSES
Tinea corporis
This was detected in 5,209 (37.6574) cases. The monthly mean value and standard deviation was 148.75 i 61.19. The highest incidence was in October (165*67oj,) and May (131.85%) and the lowest in January (53%). It was highly correlated with total mycoses, tinea cruris, tinea manuum, tinea pedis, tinea unguium, pityriasis versicolor, candidiasis and temperature and rainfall but not with humidity. There was a downward trend from 1973 to 1974 and an upward trend in 1975 and 1976 (Fig. 2~). Tinea cruris
This was the most common expression of dermatophytosis, accounting for 6,388 (46.17%) of the cases diagnosed during the three-year period. This formed 6.10% of all dermatoses seen during this time. The monthly mean value and standard deviation was 171.81 f 81.21. The highest incidence was in October (149.17%) and May (13476) and the lowest in January (46.27”). The disease correlated highly with total mycoses, tinea manuum tinea pedis, tinea corporis, tinea unguium, pityriasis versicolor, candidiasis and temperature and rainfall but not with humidity. The trend line showed a
IN
INDIA
gradual fall in the middle of 1974 with a gradual rise thereafter as in tinea corporis (Fig. 2d). Tinea axillaris
This was detected in 673 (4.87%) cases. The highest incidence was observed during May to October. Incidence was lower during the cooler months from November to March. Tinea manuum
A total of 635 (4.59%) cases were recorded. The monthly mean value with standard deviation was 10.00 + 6.22. The highest incidence was observed in May (137 -30%) and the lowest in December (74.65%). It was highly correlated with tinea pedis, total mycoses, tinea unguium, candidiasis and pityriasis versicolor but not with temperature, humidity or rainfall. A downward trend in 1974 followed by an upward trend in 1975-76 was observed. Tinea pedis
This type was found in 630 (4.55%) cases. The monthly mean value with standard deviation was 16.77 & 7.45. The highest incidence was observed in April (148.390/,) and March (147.31%) and the
6500 6000 5500 5000 4500 44000 3500 3000 2500 2000 I
-
15oc I
-
1000 I
-
500 I
-
Fig. 3. Shows the consolidated incidence of various mycoses in males and females of 13,724 cases of mycoses during November 1976.
1973 to October
0
E-
0
cn s
2l>
0”
8’
2.
T. CORPORIS
T. CAPITIS
op Ei H ul Ei
AGE IN YEARS . 0 m fs 10” s
z
g
g,
g-
2
T. VERSICOLOR
T. MANUUM
%
0” _
98
MYCOSES
lowest in November (60.11%). It was correlated with total mycoses, tinea unguium, pityriasis versicolor and candidiasis but there was no correlation with temperature, humidity and rainfall. The trend value showed a stable line from 1973 to 1975 with a gradual rise in 1976. Tinea unguium
This was detected in 906 (6.56%) cases. The monthly mean value with standard deviation was 24.04 & 17.05. The highest incidence was observed in April (127.22%) and the lowest in January (54.43%). There was significant correlation with total mycoses, candidiasis and pityriasis versicolor but no correlation with temperature, humidity and rainfall. There was a gradual downward trend from 1973 to 1974 and an upward trend from July 1974 to July 1975 followed by a second fall thereafter (Fig. 2~). Pityriasis
versicolor
This was detected in 2,252 (16.29%) cases. The monthly mean value with standard deviation was 61.10 + 30.66. The highest incidence was found in October (182.35%) &-id May (165.63%) and the lowest in January (39.87%). There was a downward trend from 1973 to July 1974 with an upward trend thereafter (Fig. 2f). The diseasewas highly correlated with total mycoses, tinea corporis, tinea cruris, tinea manuum, tinea pedis, tinea unguium, candidiasis, temperature and rainfall. Candidiasis
Candidiasis of the skin, mucous membranes and nails was detected in 1.324 (9 *57%) cases. The monthly mean value with standard’ “deviation was 37.64 -+ 11.40. The highest incidence was in May (128.91%) and October (122.62%) and the lowest in June (65.19%). There was a downward trend value from 1973 to 1974 and an upward trend thereafter (Fig. 2g). The disease was highly correlated with total mycoses, tinea unguium and tinea versicolor, and moderately correlated with all other types of dermatophytoses except tinea barbae. There was no correlation with temperature, humidity and rainfall. Pie&a
The incidence of piedra was the lowest of all mycoses and was found in only six (0.043%) cases. There were four cases of white piedra and two of black piedra. They were all recorded in the cooler months of October (three), November (two) and December (one). Deep Mycoses
A total of 20 (0.14%) cases was diagnosed, 18 with mycetoma and two with entomophthoramycosis. Most were recorded in July. Sex incidence of various mycoses
There were 9254 (66.89%) adult males, 3,963 (28.65%) adult females and 617 (4.46%) children less than 10 years old. Of these children, 326 (52.83%) were male and 291 (47.17%) were female. Fig. 3 shows the consolidated incidence of various mycoses seen in males and females among
IN INDIA
13,834 recorded cases from November 1973 to October 1976. Males were found to be predominantly affected by all but tinea axillaris, candidiasis and piedra. Age incidence of various mycoses
Fig. 4 shows the age incidence. In general, the majority affected were between 10 and 50 years of age. In tinea capitis, maximum cases were seen in the age group of five to 10 years. In all other diseases the incidence was maximum between 10 and 30 years of age. Climatic
conditions
Table III shows the monthly incidence and mean value with standard deviation of temperature, humidity and rainfall. Temperature minimum
The mean value with standard deviation of minimum temperature recorded was 24.17 & 2*52”C. The lowest minimum temperature was recorded in January (82.76%) and the highest in May (115 * 12%) with a straight trend line. The calculated values correlated with the incidence of tinea corporis, tinea cruris, pityriasis versicolor, total mycoses, maximum temperature and humidity. Temperature maximum
The mean value and standard deviation for maximum temperature was 32 a34 It 3.20%. The lowest maximum temperature was in December (85.45%) and the highest in May (115.31%) with a straight trend line. The calculated values correlated with tinea corporis, tinea cruris, pityriasis versicolor, total mycoses, minimum temperature and humidity. Humidity
at 08.30 hours
Humidity
at 17.30 hours
The mean value and standard deviation was 77.27 & 7.21. The lowest was in June (77.93%) and the highest in October (110*85?L) with a straight trend line. The calculated -v&es correlated with minimum and maximum temperature, humidity at 17.30 hours and rainfall. The mean value and standard deviation was 70.62 f 6.54. The lowest was in June (81.18%) and the highest in October (113 -21%). The trend line was straight. The calculated values correlated with tinea facei, pityriasis versicolor, maximum temperature, humidity at 08.30 hours and rainfall. Rainfall
The monthly mean value and standard deviation was 101.12 f 126.61. The lowest was in April (0.00%) and highest in October (290.30%). The trend line showed a tendency to rise during 1975 to 1976. The calculated values showed correlation with tinea facei, tinea corporis, tinea cruris, pityriasis versicolor, total mycoses and humidity at 08.30 hours and at 17.30 hours. Comment
The incidence of mycoses was 13.2%. They were the third most common disease diagnosed in skin
A. KAMALAMet al. clinics in Madras. Such a high incidence of mvcoses has also been found in Hvderabad (NAGABHUSHANAMet al., 1969) and -Bombay (DESAI & BJSAT, 1961). Higher incidences of mycoses, particularly dermatophytoses, pityriasis versicolor and candidiasis have been reported in areas which are situated at sea level where hot humid weather prevails (CANIZARES,1973). This climate prevails in Madras and when combined with a high population density these infections are likely to be prevalent. Such high incidences have also been found in Nigeria (SHRANK. 1965) \ -, and Japan (SIGEL, 1948). Mycoses, particularly dermatophytoses and pityriases versicolor were most common during May when the temperature is highest and in October the temperature is lower but when humidity and rainfall are highest. Such seasonal incidence has been similar over the preceding 12 years. Regions such as Mexico, Puerto Rico, certain Latin American countries, Nigeria and Philippines have a high incidence of mycoses (RIPPON, 1974; SHRANK, 1965; REVES& JACALNE,1962) as does India, suggesting that latitude and climatic conditions play a role in these infections. Temoerature. rainfall and humiditv recorded during-the present work have shown* a definite correlation with mycoses, particularly the major portions of dermatophytoses like tinea corporis, tinea cruris and pityriasis versicolor which were found collectively in 83.82% of patients. Humidity and rainfall were highly correlated to tinea facei. These tropical environmental conditions are comparable with the known favourable temperature of 25°C to 30°C and high humidity of 95% to 100% (COCHRANE, 1958; STOCKDALE, 1953) that are necessary for optimal growth of dermatophytes. Another contributory factor to high prevalence is the increased sweating in tropical environments which, in turn, would raise the pH of sweat from 4.5-5.5 to 7 (PILLSBURYet al., 1956) which is a known optimum pH for the growth of many dermatophytes. The incidence of other dermatophytoses such as tinea barbae, tinea manuum, tinea pedis and tinea unguium was found to be low. Correlation with temperature and humidity and rainfall were less striking in these types and there was no correlation between climatic conditions and tinea capitis. The incidence of piedra was very low, but its occurrence in cooler months with heavy rainfall and high humidity suggested that the disease might be associated with cooler and wet conditions. The incidence of deep mycoses was low (0.14%) and it would be erroneous to infer from this number any seasonal incidence since all reported caseswere either from outside Madras city or from the southern districts of Tamil Nadu such as Ramanathapuram, Tirunelveli and Madurai and had reported for treatment months or years after the onset of the disease. However, the incidence of deep mycoses in southern districts is known to be high and 266 cases had been previously recorded during 1959 to 1966 (Asirvatham, personal communication). These districts are in the same latitude as countries such as Sudan, Nigeria, Puerto Rico and certain Latin American countries
99
where the prevailing temperature and rainfall is similar, namely, between 25 and 50 mm per year. In these areas the incidence of dermatophytoses is also high, relative humidity, temperature and rainfall being the main factors contributing to the epidemiological incidence of mycoses. Sex
A preponderance of males has been observed. This could be internreted in two wavs. One is the larger male populatibn of the city. Secondly not all the affected females report for treatment since they are commonly confined to the house by social practice. However, the difference in sex ratio of the affected subjects is too great to ignore the male preponderance, and the difference in the sex ratio of the population is not marked. A definite female preponderance has been observed in tinea capitis, iinea axillaris, candidiasis and niedra. The clothing: habit of close fitting blouse in females gives a local&ed tropical environment in the axillae which would explain this higher incidence for tinea axillaris. Occupational factors and the wet long hair in females could explain the higher incidences of candidiasis and piedra. Children below 10 years have shown a predominance of tinea capitis and candidiasis. For the former disease 47.03% of cases occurred in children. However, when the study population is compared, the ratio of children to adults is approximately 6 : 19 suggesting a definite age proneness. In general all other dermatophytoses showed a sudden increase after 10 years of age. This raises questions on the fungistatic activity of sebum secreted more during summer and after puberty, and suggests that further evaluation of the-role of skin li$ds in dermatoohvtoses is reauired. The higher incidence of &yriasis versicblor, a lipid dependent disease, between 10 and 30 years and in summer correlates with increased sebaceousactivity in this age group and during the summer months. A second peak incidence in October with lower temperature and highest rainfall and humidity may denote a species difference in causal agent of these diseases. Acknowledgement
We gratefully acknowledge the help given by the authorities, Meteorological Centre, Nungambakkam, Madras, Indian Institute of Technology Computer Centre, Madras and Corporation of Madras. We are also grateful to Prof. L. N. Mohapatra, Delhi and Dr. L. Ajello, Atlanta, USA, for help in culture work. References
Canizares, 0. (1973). Epidemiology of the dermatoses of Latin America. In: Essays of Tropical Dermatology. Marshall, J. (Editor). Amsterdam: Excerpta Medica, pp. 427-431. Cochrane, V. W. (1958). Cultivation and growth. In: Physiology of Fungi. New York: John Wiley & Sons, p. l-34. Desai, S. C. & Bhat, M. L. A. (1961). Dermatomycoses in Bombay. Indian Journal of Medical Research, 49, 662-671.
100
MYCOSES
Emmons, C. W., Binford, C. H. & Utz, J. P. (1970). Culture Media. In: Medical Mycology. Philadelphia: Lea & Febiger, pp. 464-468. Kamalam, A. & Thambiah, A. S. (1976). A study of 3891 cases of mycoses in the tropics. Sabouraudia, 14, 129-148. Nagabhushanam, P., Thirumala Rao, R. & Patnaik, R. (1969). Dermatomycoses in Hyderabad Area. Indian Journal of Dermatology and Venereology, 35, 120-123. Pillsbury, D. M., Shelley, W. B. & Kligman, A. M. (1956). The glands of the skin. In: Dermatology. Philadelphia: W. B. Saunders, pp. 52-66. Reyes, A. C. & Jacalne, A. V. (1962). As quoted by Kalique, A. et al., (1974). Incidence and types of Dermatomycoses in Aurangabad. Indian Journal of Dermatology and Venereology, 40,66-72.
IN
INDIA
Rippon, J. W. (1974). Dermatophytosis and Dermatomycosis. In: Medical Mycology. Philadelnhia. London & Toronto: W. B. Saunders, pp.- 96-174. Shrank, A. B. (1974). A field survey in Nigeria. Transactions of the St. Yohn’s HosPital Dermatological Society; 451, 85.” * Sigel, H. (1948). Cutaneous diseases among army personnel in Japan. Archives of Dermatology and Syphilology, 57, 128-131. Stockdale, l?. M. (1953). Requirements for the growth and sporulation of Trichophyton persicolor. Journal of General Microbiology, 8,434-441.
Accepted for publication
lOthJanuary,
1980.