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N L Mulambya ^{1, 2, 3}; P Sakubita^{1, 2, 3}; R Hamoonga²; B Mulubwa^{2, 3}; O Namafente⁴; M Mutengo^{3, 5} ; E Yard⁶
1. Field Epidemiology Training Program, Lusaka, Zambia. 
2. Zambia National Public Health Institute, 
3. Ministry of Health
4. Tropical Disease Research Centre, Department of Entomology and Vector Control, Ndola Zambia, 
5. University Teaching Hospital, Department of Pathology and Microbiology, Parasitology Unit, 
6. The US Centres for Disease Control and Prevention 
Corresponding author: Nelia Langa, (nmulambya2000@gmail.com)
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Citation style for this article: Mulambya N L, Sakubita P, Hamoonga R, Mulubwa B, Namafente O, Mutengo M,  Yard E. Tungiasis Outbreak Investigation In Masaiti District, Zambia. Health Press Zambia Bull. 2018 2(9); pp 8-16.

Tungiasis is a neglected tropical disease caused by infestation by the female sand flea Tunga penetrans. Primary reservoirs include livestock such as pigs, goats and cattle. Infection occurs when skin comes into with fleas in soil of floor. The flea burrows in the epidermis of the skin causing local itching and irritation. An outbreak of tungiasis was reported in Njelemani area, Masaiti district of Copperbelt province in October 2017. We investigated to determine the magnitude and geographic spread of the outbreak, and conducted epidemiologic and clinical assessment of cases in the affected communities. 
Key words: Tunga penetrans, tungiasis, jiggers, Zambia
METHODS
We defined a case of tungiasis as any person from Njelemani area with T.penetrans associated lesions (i.e. white patch or black dot with pain and or itching) on any part of the body from 1st August to 13th October 2017. We reviewed records and conducted active case search. We calculated attack rates by using population estimates from central statistical office 2010 census. We interviewed a convenient sample of case-patients using a structured questionnaire and collected data on demographics, tungiasis symptoms, location of lesions and hygiene practices. In addition, eggs and fleas were collected from patients and the environment for microscopic examination. Descriptive analyses were performed using Epi info 7.
RESULTS
We identified 192 tungiasis case-patients during the 1st August to 13th October of which 120 (63%) were male, constituting an attack rate of 16%. Of the 66 cases interviewed, majority (40%) were children aged 0-9 years of which 66% were males. Almost all (91%) lesions were located on the feet. Predominant symptoms were itching 66 (100%) and pain 49 (75%). Although 85% of cases reported having footwear, only 16% wore them regularly. More than half (56%) of case patients had dirty feet and half of the houses in the area were temporary structures with bare earthen floors. Laboratory investigations revealed the presence of T.penetrans eggs from the lesions of eight cases-patients. 
CONCLUSION
An outbreak of tungiasis occurred in Njelemani area of Masaiti district. Interventions aimed at raising awareness, promoting regular use of footwear, hygiene and maintenance of housing floors remains essential in controlling and preventing tungiasis. Furthermore, we recommend strengthening collaboration between the Ministries of Health and Livestock and Veterinary services since tungiasis affects both humans and animals.
INTRODUCTION
Tungiasis is a neglected tropical disease caused by infestation by the female sand flea Tunga penetrans also commonly known as jigger or chigoe [1]. The flea burrows in the epidermis of the skin. While in the epidermis, the flea increases in body volume causing local itching and irritation. Tungiasis is a zoonosis affecting both humans and animals.  Reservoirs for human infection are predominantly pigs and bovines; but may include dogs, cats and rats in resource-poor urban communities [1] [15]. Studies conducted in Brazil have shown high risk of human tungiasis in communities were animal tungiasis is high. [3]. T. penetrans fleas penetrate the skin when it comes into contact with soil or floors which have developed sand fleas [2]. Tungiasis is common in villages and shanty neighborhoods of cities with low economic conditions [3]. A study conducted 
Most (99%) of the lesions occur on the feet although any part of the body can be affected [1]. Tungiasis is a debilitating disease that can lead to restricted mobility especially if one has multiple lesions. Complications of chronic tungiasis may include  bacteria superinfection  of  the lesions resulting in abscesses and lymphangitis [4]. Deformity and mutilation of the feet due to reoccurring infections may lead to impaired mobility and contribute to stigma and absenteeism among school going children [5, 6]. Studies conducted in Africa, Asia and South America have shown that tungiasis is associated with poor housing and low socio-economic status. In Zambia the overall prevalence of human tungiasis is unknown serve for the study conducted in Chipata and Vubwi eastern province in 2015 showed an overall prevalence of 13.5%. 
The Ministry of Health through the Copperbelt Provincial health office was alerted to an outbreak of tungiasis in Njelemani village in Masaiti District on 21st September 2017. Masaiti is one of the three rural districts on the Copperbelt province. It is located 343 kilometers north of Lusaka. The district has an estimated total population of 118,548 [7]. Njelemani has a population of 6117 [7] and ten (10) neighborhood health committees. The health facility has reported sporadic cases of tungiasis since 2003. However, in August 2017 there was a spike in the number of cases and affected households. To determine the magnitude and the geographic spread of the outbreak, we conducted a descriptive epidemiologic and clinical assessment of the cases in the affected communities.  
METHODS
We defined a case of tungiasis as any person from Njelemani area with T. penetrans associated lesions (i.e. white patch, black dot with pain and itching) on any part of the body from 1st August to 13th October 2017. We reviewed facility records which showed the number of tungiasis cases per year and the villages which were affected. We also conducted active case search for tungiasis cases in affected villages. We interviewed a convenient sample of case-patients using a structured questionnaire and collected geographic coordinates of the area. We collected data on demographics, clinical symptoms, location of lesions, hygiene practices, treatment, housing characteristics, number and type of animals, access to veterinary services and observed animals for lesions. We calculated the attack rate based on the total population in affected villages Clinical assessment and staging was conducted using the Fortaleza classification criteria. The criteria was described by Eisele et al (2003) consisting of five (5) stages. Stage 1 characterized by penetration of skin by flea, stage 2 complete penetration and burrowing of most of the fleas body leaving only hind quarters, stage 3 the flea achieves maximum hypertrophy, the skin layer thins out resulting in the appearance of a white halo around a black dot. Egg release is common at this stage. Stage 4, the flea dies, the lesion shrinks in size, turns brown and appears wrinkled. Stage 4b is characterized by flea elimination through skin repair. Stage 5, the dead flea has been expelled leaving characteristic circular skin residues of infection and brown black appearance.  In addition, eggs and fleas were collected from cases and the environment for laboratory confirmation of T.penetrans. GPS coordinates were also collected to map out the spatial distribution of cases. We also observed the feet of respondents for cleanness using agreed upon rating. We used Epi info 7 to obtain descriptive statistics. 
ETHICAL CONSIDERATION
Since the study was conducted as part of an outbreak response, ethical clearance waiver was obtained from the Tropical Disease Research Centre (TDRC) ethics committee. Consent was obtained from participants aged 18 years and older. We obtained assent from children younger than 18years and consent from their parents and guardians.
RESULTS
As seen in Figure 1, there has been a cumulative 944 of tungiasis cases in Njelemani since 2003. After a peak in 2003, a reduction in the prevalence of tungiasis was noted. However, in 2017, an increase in the number of cases was observed.  Following interventions, the number of cases reduced drastically as noted in (fig. 2).
During the outbreak period, a total of 192 cases of tungiasis were identified of which 63% (120) were males and 38% (72) were females, constituting an attack rate of 16%. A total of 66 cases were interviewed, of these, majority (41%) were children aged 0-9 years. In this age group, 33% were females and 67% were males.  More than 50% of the cases lived in temporary houses while only 10% lived in permanent houses (Table 1). Almost all (91%) lesions were located on the feet and 7% on the fingers. Predominant symptoms were itching 66 (100%), and pain 49(75%). The number of lesions per person ranged from 1 to 20 with a median of 3. About 7% of the cases had severe tungiasis with lesions ranging from 11-20. Fortaleza classification revealed multiple staging with 53% of cases in stage II, 43% stage III (Eisele M et al. 2003) (Table 2).  In relation to foot wear, 85% (56) of the respondents reported having footwear while 15% (10) had no footwear. Although 85% of cases had foot wear, more than half 66% wore them occasionally and only 5% reported wearing them all the time. Hygiene was assessed by observing the feet of the respondents for cleanness, and more than half (57%) of the cases had feet that were classified as dirty. The most common type of animals kept in the community were goats (43%) and pigs (39%). Some of the pigs examined had lesions associated with T. penetrans infestation. 
Table 1: Socio-demographic characteristics of respondents of Njelemani area Masaiti District Zambia August – October,2017 

Table 2: Clinical assessment of tungiasis cases in Njelemani area Masaiti District, Zambia  August – October 2017

 
Table 3  Factors associated with tungiasis in Njelemani area of Masaiti district, Zambia August – October, 2017

Laboratory findings
Although the diagnosis of tungiasis is clinical, samples were collected from 8 patients who had various stages of lesions and were examined microscopically for the presence of T. penetranseggs. In addition, the characteristic adult T. penetransflea was identified on microscopic examination.

Fig 4: Sand flea eggs, x40 magnification

Fig 5: Adult T. penetranscollected from the environment of one of the affected communities in Njelemani area of Masaiti
Discussion
In our study, majority of case-patients were males. Similar findings were observed in Haiti, where more males were affected than females [8]. The ages of the case-patients ranged between 1 and 65 years with a median age of 13.5. Most of the respondents were children aged 0-9years, a finding consistent with the study carried out in southern Ethiopia, were most cases were children ages 5-14 years [8-10]. Similar findings were observed in Tanzania and Nigeria, were children were more affected than adults [11][12]. The finding could be due to the fact that children are more likely to be exposed to the sand fleas as they play barefoot. The finding may also be related to selection bias were children are likely to complain about T.penetranssymptoms while adults shy away. Males were more affected due to activities that are more likely to expose them to fleas such as playing football barefoot
With regard to education, only a small percentage of respondents had attained secondary level, a finding which is in tandem with that of a Ugandan study which showed that secondary level education was protective against tungiasis. People with secondary or higher education are more informed and practice high levels of hygiene as compared to those with primary or no education [13]. This finding may also be attributed to the general low number of people with secondary education in the community.  Poor housing, cracked walls, earthen and dusty floors are associated with tungiasis [13]. Similarly our study showed poor housing in the affected area with half of the structures being temporally (Table 1). Furthermore, two thirds of the houses had bare ground or earthen floors a finding which is consistent with studies conducted in Nigeria and Uganda [14], [13]. The high number of houses with earthen dusty floors could be attributed to lack of knowledge on T.penetransprevention among the community members. Dusty earthen floors are very conducive for the fleas.
Although our study findings show that two thirds of the case-patients lacked knowledge on the cause of tungiasis, they were aware of the signs and symptoms, contrary to the findings of Mutebi and others in Uganda[15]. Almost all affected persons preferred self-treatment by extracting embedded fleas using non-sterile sharp instruments such as pins, needles and thorns instead of visiting the health facility similar to the findings in other tungiasis studies[2], [12], [10].
Despite more than three quarters of the case-patients in our study reporting having shoes, only less than a quarter wore them regularly. Regular usage of shoes has been shown to have a protective effect against tungiasis. In a study in Madagascar, the protective effect of shoes from sand fleas was related to the regularity of footwear use [16]. However, it appears that only closed shoes offer some protection.[17]A report from an outbreak investigation in Ethiopia showed that most tourists who had tungiasis wore open shoes [18]. A similar observation was noted in our study were almost half of the case-patients had open shoes. In our study it was noted that close to half of the case-patients who reported having footwear had open shoes. This finding could be due to lack of knowledge on the type of shoes and exposure to fleas.
On removal of T.penetransfleas, nearly all respondents preferred using thorns, razors, pins, chemical pesticides and needles, a finding consistent with studies conducted in Tanzania, Uganda, Kenya and Nigeria [11, 13-15]. However, these are unsafe practices that could lead to transmission of blood-borne pathogens such as hepatitis B and C virus, possibly also HIV [1].
 
Personal hygiene practices such as having dirty feet, and putting on dirty clothes are associated with tungiasis. Dirty feet and clothes provide a conducive environment for T. penetransto survive and hide [11]. This is consistent with our study findings where 55% of the respondents had dirty feet. Several studies have highlighted personal hygiene as an important factor in the control and prevention of T. penetrans [13], [11]. Poor hygiene among our case-patients could also be attributed to distance to water sources in the area. Some villages had unsafe water sources which they shared with animals. Lack of knowledge on hygiene practices therefore remains key in the prevention of tungiasis.
In the present study, most of the pigs in Njelemani area had lesions a finding consistent with other studies which have shown pigs to be the most common animal reservoir of sand fleas [12]. It should be noted that goats were the most common animals in the community but they had no lesions. This could be due to natural resistance to diseases and infection. However, a study conducted in Uganda showed that goats can also be infected by T.penetrans[19]. Limited access to veterinary services in the area could have contributed to the sudden increase in the number of tungiasis cases.
Conclusion
Tungiasis is a common health problem in Njelemani area of Masaiti district. The control of tungiasis requires a one health approach combining efforts and strengthening collaboration between the Ministries of Health and Livestock and Veterinary services since it affects both humans and animals. Interventions aimed at raising awareness and promoting regular use of footwear, hygiene practices and regular maintenance of housing floors remains essential in controlling and preventing tungiasis.
 Limitations: The sample size for this study was small and hence cannot be generalized to a larger population. Furthermore, there was no comparison group which prohibited looking at risk
 
Figure 1

Fig 2 shows the epi-curve of the tungiasis outbreak in Njelemani area of Masaiti district

Fig 3: Map of Copperbelt province showing Masaiti district 

Fig 4: Map of Njelemani health centre and surrounding villages showing cases of tungiasis (n=66
REFERENCES

1. Feldmeier, H., E. Sentongo, and I. Krantz, Tungiasis (sand flea disease): a parasitic disease with particular challenges for public health.Eur J Clin Microbiol Infect Dis, 2013. 32(1): p. 19-26.
2. Karunamoorthi, K., Tungiasis: a neglected epidermal parasitic skin disease of marginalized populations–a call for global science and policy.Parasitol Res, 2013. 112(10): p. 3635-43.
3. De Avelar, D.M., E.J. Facury Filho, and P.M. Linardi, A new species of Tunga (Siphonaptera: Tungidae) parasitizing cattle from Brazil.J Med Entomol, 2013. 50(4): p. 679-84.
4. Bouree, P., L. Osse, and F. Rabenandrasana, [Tungiasis, an uncommon ectoparisitic disease].Rev Prat, 2009. 59(2): p. 163-5.
5. Wiese, S., et al., Prevalence, intensity and risk factors of tungiasis in Kilifi County, Kenya: I. Results from a community-based study.PLoS Negl Trop Dis, 2017. 11(10): p. e0005925.
6. Ferreira, L.A., et al., Tunga penetrans as a traveler’s disease.Travel Med Infect Dis, 2009. 7(6): p. 381-2.
7. CSO, C.S.O., 2010 Census of population and housing national analytical report. 2012, CSO: Lusaka. p. DF-1.4 .
8. Louis, S.J., et al., Tungiasis in Haiti: a case series of 383 patients.Int J Dermatol, 2014. 53(8): p. 999-1004.
9. Walker, S.L., et al., The prevalence and association with health-related quality of life of tungiasis and scabies in schoolchildren in southern Ethiopia.PLoS Negl Trop Dis, 2017. 11(8): p. e0005808.
10. Kimani, B., J. Nyagero, and L. Ikamari, Knowledge, attitude and practices on jigger infestation among household members aged 18 to 60 years: case study of a rural location in Kenya.Pan Afr Med J, 2012. 13 Suppl 1: p. 7.
11. Dassoni, F., et al., Tungiasis in Northern Tanzania: a clinical report from Qameyu village, Babati District, Manyara Region.J Infect Dev Ctries, 2014. 8(11): p. 1456-60.
12. Ugbomoiko, U.S., et al., Risk factors for tungiasis in Nigeria: identification of targets for effective intervention.PLoS Negl Trop Dis, 2007. 1(3): p. e87.
13. Wafula, S.T., et al., Prevalence and risk factors associated with tungiasis in Mayuge district, Eastern Uganda.Pan Afr Med J, 2016. 24: p. 77.
14. Ugbomoiko, U.S., et al., Prevalence and clinical aspects of tungiasis in south-west Nigerian schoolchildren.Tropical Doctor, 2017. 47(1): p. 34-38.
15. Mutebi, F., et al., Animal and human tungiasis-related knowledge and treatment practices among animal keeping households in Bugiri District, South-Eastern Uganda.Acta Tropica, 2018. 177: p. 81-88.
16. Thielecke, M. and H. Feldmeier, The fate of the embedded virgin sand flea Tunga penetrans: hypothesis, self-experimentation and photographic sequence.Travel Med Infect Dis, 2013. 11(6): p. 440-3.
17. Mwangi, J.N., H.S. Ozwara, and M.M. Gicheru, Epidemiology of tunga penetrans infestation in selected areas in Kiharu constituency, Murang’a County, Kenya.Trop Dis Travel Med Vaccines, 2015. 1: p. 13.
18. Grupper, M. and I. Potasman, Outbreak of tungiasis following a trip to Ethiopia.Travel Med Infect Dis, 2012. 10(5-6): p. 220-3.
19. Mutebi, F., et al., Two Severe Cases of Tungiasis in Goat Kids in Uganda.J Insect Sci, 2016. 16.