Memórias do Instituto Oswaldo Cruz Fundação Oswaldo Cruz, Fiocruz ISSN: 1678-8060 EISSN: 1678-8060 Vol. 98, Num. s1, 2003, pp. 173-179

Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 98(Suppl. I), January 2003, pp. 173-179

Louse Infestation of the Chiribaya Culture, Southern Peru: Variation in Prevalence by Age and Sex

Karl J Reinhard/⁺, Jane Buikstra*

School of Natural Resource Sciences, University of Nebraska-Lincoln, 214 Bessey Hall, Lincoln, NE 685-0340 USA *Department of Anthropology, University of New Mexico, Albuquerque, New Mexico, USA
⁺Corresponding author. Fax: +402-472.6858. E-mail: kreinhard1@unl.edu

Received 26 August 2002
Accepted 25 November 2002

Code Number: oc03026

In order to improve the interpretive potential of archaeoparasitology, it is important to demonstrate that the epidemiology of ancient parasites is comparable to that of modern parasites. Once this is demonstrated, then we can be secure that the evidence of ancient parasitism truly reflects the pathoecology of parasitic disease. Presented here is an analysis of the paleoepidemiology of Pediculus humanus infestation from 146 mummies from the Chiribaya culture 1000-1250 AD of Southern Peru. The study demonstrates the modern parasitological axiom that 10% of the population harbors 70% of the parasites holds true for ancient louse infestation. This is the first demonstration of the paleoepidemiology of prehistoric lice infestation.

Key words: Pediculus humanus - pathoecology - paleoepidemiology - archaeoparasitology - Peru

In archaeoparasitology, as with any field of parasitology, interpretive strength is based on reliable analysis of large numbers of observations. For those of us dependent on archaeological excavations, the biggest challenge is obtaining large numbers of observations. Often times factors of preservation, field sampling conditions, and other aspects of archaeology reduce the number of observations to a handful of data points. This in turn limits the strength of interpretations about prehistoric infections, infestations and health.

Dr Jane Buikstra's Programa Contisuyo excavations in the Moquegua Valley of Southern Peru offered the opportunity to collect archaeoparasitology data from a large series of mummies. During dissection of the mummies, we noted the presence of louse nits and eggs in the hair and realized that a survey of the mummies for nits and eggs would provide an unparalleled source of intersite comparative data. We examined 146 mummified or partially mummified individuals from the sites of San Geronimo, Chiribaya Alta, Algodonal, and El Yaral.

MATERIALS AND METHODS

During the month of August, 1990, we collected data on louse parasitism for every individual that had been dissected to date and could be located in the Ilo Programa Contisuyo Laboratory from the sites of Chiriabya Alta, Algodonal, El Yaral and San Geronimo. One problem that we encountered was that many of the mummies had already been dissected and cleaned. Therefore, it was not possible to quantify all of the infestations. Of 164 individuals from all sites, we located 146 and examined them for lice nits/eggs. Not every specimen was acceptable for study. Some individuals had hair or scalp tissue that was too poorly preserved for analysis. These individuals were so noted in the field to prevent their inclusion in later comparative analysis (Table I a, b). Because examination of hair did not require dissection, it was possible to analyze several mummies from El Yaral as they were unwrapped.

The technique improvised for this study was based on the examination of the hair bases at the scalp (referred to subsequently as scalp measurements) and hair shafts located several inches away from the scalp (referred to subsequently as hair measurements). The scalps were examined to identify areas of maximum nit density and minimum nit density. Maximum density usually was on the parietal area, and in the area above and behind the ears. A 2 x 2 cm square was cut into a cardboard strip. The cardboard strip was then placed on the identified areas and all nits/eggs within the 2 x 2 cm area were counted. Three observations were taken for each area of scalp minimum density and scalp maximum density (Table II a, b). The hair was also examined for areas of minimum and maximum nit/egg density. An optimal distance of 5 inches from the scalp was preferred, but in some cases, observations were made 4-6 cm from the scalp when the hair was not well preserved at 10 cm. The cardboard strip was then placed on the identified areas and all nits/eggs within the 2 x 2 cm area were counted.

The family Glycyphagidae comprises a large group associated with nests of small mammals, especially of rodents (Flechtmann 1986). Many lineages invaded stored products (Oconnor 1982) but are also present in house dust (Wooley 1988, Colloff 1998).

Species of Blomia are well represented in stored products and Oconnor (1982) suggests that this genus is originally from South America, as evidenced by its abundance and ubiquity in house dust of the neotropical region. The finding of B. tropicalis in the archaeological site of Furna do Estrago corroborates with this assumption due to the antiquity of the studied material.

B. tropicalis is very abundant in tropical and subtropical regions. The climatic conditions in these regions, with mean annual temperature of 28°C and mean relative humidity of 82%, offer a good environment for the growth of this species (Mariana et al. 1996). These observations indicate that the climate in the region was humid and temperate as observed for pyroglyphid mites.

In this work, B. tropicalis was recovered from Felidae coprolites. Probably it was associated with small mammal nest and was ingested by the felid.

According to Colloff (1998) in essence, the pyroglyphids were originally bird-nest dwellers but underwent a shift in habitat to the human nest around the time of the first human settlement, associated with agricultural production, some 10,000 years ago. The glycyphagid inhabitants of human dwellings made a habitat shift from nests of small mammals and likewise encountered similarities with homes, with food resources in the form of seeds, cereals, and other plant materials. Given similarity of trophic niches of human dwellings to those available naturally, it is not surprising that a number of mite species have become associated with human habitations. On basis of the above observations, we can suppose that the actual characterization of some pyroglyphid and glycyphagid species living in anthropic environment has passed through an adaptation period of these mites and their hosts to a sinanthropic environment. This adaptation could have occurred when the subsistence conditions concerning dietary resources in the region become more suitable to human occupation. This fact, according to Lima (1991) occurred between 1,000 and 2,000 yr BP in the archaeological site of Furna do Estrago. The fauna attested by bone artifacts points out a more humid environment that was more favourable to human occupation than the one exploited by the hunter-gatheres around 9,000 yr BP

The Acaridae is a large assemblage of saprophagus, graminivorous, fungivorous and phytophagus species which are frequently found as contaminants of stored and processed food (Krantz 1978). However, they are not restricted to these habitats since they are also found as nidicoles of vertebrates, nidicoles of insects, and in other remains such as organic material, carrion, dung, and decaying matter.

Mites of the species Suidasia pontifica were recovered from Homo sapiens, Felidae and Caviidae coprolites. The most probable hypothesis is that they were carried to fresh feces by coprophilic insects. This supposition is in accordance with the observations of Radovsky (1970) to explain the presence of Acaridae tritonymph in human coprolites and of Kliks (1988) who suggested that the astigmatid mites found in human mummies are ancient or recent pos-mortem invaders.

A similar argument for pyroglyphid and glycyphagid mites could be proposed for species of Suidasia, since they had already been reported in bird nests (Bhattacharyya 1999), and could have substituted their natural habitat by sinanthropic and anthopic habitat. This could have happened as a consequence of human lifestyle favoring the colonization of this mite species. At the present, S. pontifica is more frequently reported as contaminants of stored and processed food (Ho 1996, Sanchez-Borges et al. 1997, Olsen 1998) and at house dust (Galvão & Guitton 1986, Montealegre et al. 1997, Chew et al. 1999).

The importance of species of the families Pyro-glyphidae, Glycyphagidae and Acaridae as allergens causing allergic diseases is noteworthy. This public health hazard is getting worse throughout the years and it is now considered a severe problem of modern humans. Continual investigations in archaeological material will bring, in the future, information about these mites' species allowing the understanding of their interaction with human beings.

From the oribatid mites recovered, the genus Apolohmannia and Aphelacarus had not yet been reported for the neotropical region (Balogh & Balogh 1988), however, Corvarrubias and Toro (1997) reported the species Aphelacarus acarinus in Chile for the first time. The present work confirms the neotropical distribution of this mite species. The genus Apolohmannia was reported in Japan (Balogh 1965). This is the first report of Aphelacarus in Brazil and of Apolohmannia at the American continent.

The species Pterobates incertus was reported in the state of Rio de Janeiro (Balogh & Balogh 1988). Now we are including the state of Pernambuco in the geographical distribution of this species. The genus Eohypochthonius was previously reported to North America and Cir-cumtropical region (Balogh 1961, 1965), and is now reported in Brazil.

The genus Cosmochthonius was previously reported in Europe, Java and neotropical region (Balogh 1961), and the species C. lanatus foveolatus in Chile (Corvarrubias & Toro 1997). We confirm the neotropical distribution of this species and report it for the first time in Brazil.

Corvarrubias and Toro (1997) studied oribatid species in Chile and concluded that A. acarinus and C. lanatus foveolatus constitute the dominant fauna in ecosystems of prolonged dryness. According to Lima (1991) at the archaeological site of Furna do Estrago, the archaeological evidence reflects rigorous climate conditions - high temperatures and dryness for a long period of time, between 9,000 and 8,000 yr BP This fact is consistent with the finding of these two species of mites.

The findings of Apolohamnnia, Pterobates, Eo-hypochthonius, Cosmochthonius and Aphelacarus are indicative that the neotropical climate with humidity and temperature compatible with the development of these genera was established in the region of the archaeological site.

Members of all the families of the order Oribatida with remains that are known as fossils are still living at the present time. This is indicative of the exceptionally low rates of morphogenesis in Oribatida. Apparently, the cause of the low variability level in Oribatida lies in the stability of the soil as an environment as well as in the diversity of ecological niches available (Krivolusky & Druk 1986). These are the features that explain why a number of extremely archaic forms have survived to the present time. The preliminary results about the finding of oribatid mites in archaeological material reported by Guerra et al. (2001a) and the ones presented in this paper corroborate the observations mentioned above.

Oribatid species and species assemblages offer several advantages for assessing the quality of terrestrial ecosystems (Behan-Pelletier 1999). Therefore they could be used as bioindicators, and in this way help to reconstruct the environment conditions of the past as already demonstrated with other arthropods. Atkinson et al. (1987) reconstructed seasonal temperatures in Britain during the past 22,000 years using radiocarbon-dated beetle remains. Some soil animals, especially those with firm exoskeletons, such as the oribatids, have tendency to fossilize (Krivolusky & Druk 1986) and their remains could be used for the same purpose.

Finally, it is worth mentioning that the genus and species recovered in the present study still exist. We suppose that human action has favored the colonization of domiciliary environments by mites previously associated with animals bringing, as a result, undesired consequences to human beings. This change in habitat could have happened from the moment that human groups become more sedentary. In the archaeological site of Furna do Estrago the diversity and amount of food sources allowed human settlement, population growth, and cultural complexity around 2,000 yr BP (Lima 1991). The population exploited simultaneously the sources of the "caatinga" and of the "mata serrana do Buriti" that made possible a semi-sedentary way of life and a hunting-gathering economy (Lima 1991). This way of life made possible for the population at Furna do Estrago to interact with the region's animals and plants, and consequently with their mites.

RESULTS

Of 146 individuals examined, not all were sufficiently preserved for analysis (Table I a, b). In some cases, the scalp was poorly preserved but the hair was well preserved. More rarely, the hair was poorly preserved or absent, but the scalp was well preserved. A few individuals exhibited poor preservation of scalp and hair. The San Geronimo individuals especially exhibited poor preservation of the hair and scalp tissue. Consequently, this site had to be dropped from comparative study because of poor over-all preservation.

Generally, individuals who had lice nits/eggs on the scalp had louse nits/eggs on the hair. From all 4 sites, 75 mummies had both scalp and hair present. Twenty (27%) individuals had nits/eggs on the hair immediately adjacent to the scalp and on the hair away from the scalp, 4 (5%) had nits/eggs on the hair only, and 9 (12%) had nits/eggs on the scalp hairs only. In general, there was a tendency for maximum density of nits/eggs to decrease from the scalp to the hair away from the scalp. Twenty (27%) individuals had fewer nits/eggs on the hair in comparison to the scalp, and 11 (17%) showed more nits/eggs on the hair than on the scalp.

Only seven individuals from Algodonal were available for field analysis. Of these, 5 (71%) were infested with lice. From El Yaral, 22 individuals were available and were sufficiently preserved for analysis. Of these, 4 (18%) were infested. From Chiribaya Alta, 69 individuals could be studied of which 25 (36%) were infested. Statistical significance in prevalence beyond the 0.05 level is present in El Yaral-Algodonal and Alta-Algodonal comparison (c² = 9.742, 0.005 > P > 0.001 and c² = 4.933, 0.05 > P > 0.025 respectively). Significance at the near 0.05 level is evident in the El Yaral-Chiribaya Alta comparison (c² = 3.403, 0.10 > P > 0.05). Therefore, louse prevalence is significantly variable between sites (Table III). Sex is a variable that can affect parasite prevalence (Table III). The sites were pooled for this comparison. Of 21 women, 8 (38%) were infested. Of 18 men, 10 (56%) were infested. This difference is not statistically different at the 0.05 probability level (c² = 1.995, 0.25 > P > 0.10). There was variation between adults and children. Of 49 subadults from Chiribaya Alta and El Yaral, 12 (24%) show infestation. Of 43 adults, 19 (44%) show infestation. The difference is statistically significant beyond the 0.05 confidence interval (c² = 4.907, 0.05 > P > 0.025).

The scalp maximum nit/egg densities (column 1 in Table II a, b) are insightful with regard to parasitism at or around the time of death for the individuals under study. We believe that this provides a better idea of how many active louse infestations occurred in the population as opposed to measurements from the hair shafts which infestations represent several months before death. An examination of the distribution of infection (Fig. 1) shows that the louse nits/eggs are not evenly distributed in the human host population. Most individuals were not infected or had small numbers of eggs/cm² of scalp. Only a few individuals were heavily infected. For all of the sites, 194 nits/eggs were observed. Of these, 118 (61%) were observed on 5 (6%) of the mummies. For the site with the largest sample size, Chiribaya Alta, 95 nits/eggs were observed. Of these, 70 (74%) were found on 5 (4%) of the mummies.

The mean maximum louse density also varied per site. The highest mean maximum density of 8.9 nits/eggs/cm² was found for Algodonal. The mean maximum density for Chiribaya Alta and El Yaral were 1.7 and 1.73 nits/eggs/cm² respectively. The value for all sites was 2.28 nits/eggs/cm². The mean maximum nit/egg density varied between children, men and women. Children had a mean maximum value of 0.8 nits/eggs/cm² as opposed to 2.6 for women and 3.5 for men.

The highest concentrations occurred among adults. Among the adults, infestation was limited to 31 (34%) of 92 people in the sample. Of those people infested, most have a mean maximum scalp value of 1 nit/cm² or less. We consider a mean maximum density of 5 nits/eggs/cm² or more to represent heavy infestations. Only 8 individuals had heavy infestations which ranged from mean maximum scalp value of 5 nits/eggs/cm² to 22 nits/eggs/cm². Of the total number of nits/eggs counted in the study, 69% were found on these eight individuals who make up only 9% of the 92 individuals studied.

DISCUSSION

In modern parasitology, it is axiomatic that 10% of the hosts will harbor 70% of the parasites. These numbers are approximated in the data for El Yaral and Chiribaya Alta. For El Yaral, 84% of the parasites found in the 2 (10%) of the most heavily infested mummies. For Chiribaya Alta, 74% of the parasites were observed on 5 (9%) of the most heavily infested mummies (Figs 1, 2). Statistically, these are the most important points that come from this analysis. This demonstrates that it is possible to retrieve paleoepidemiological data from archaeoparasitology studies that approximate the modern world. This is an essential basis for going on to more fine-tuned paleoepidemio-logical interpretations.

Several basic points can be distilled from Table III. First of all, there is significant variation between the sites in the percentage of mummies infested (Fig. 3). This indicates that the pathoecology of the sites was variable. Second, males are more commonly infested than females at all sites. At Chiribaya Alta, adult females are more commonly infested than children. At El Yaral, children are more often infested than women.

Lice are easily transmitted from person to person and crowding results in higher prevalence. Therefore, Pediculus humanus tells us something of the nature of the life conditions between the two villages of Chiribaya Alta and El Yaral. The prevalence per site for P. humanus is plotted in Fig. 3. The prevalence is markedly different between Yaral and Chiribaya Alta. This indicates that the inhabitants of Chiribaya Alta were more crowded and therefore at greater risk of exposure and reexposure than those of El Yaral.

The Chiribaya were certainly host to head lice. The lice must have been a source of considerable discomfort. P. humanus is a species of anopluran lice, commonly called sucking lice. The common name refers to their mode of feeding which is by ingesting blood. Their mode of obtaining a blood meal is termed solenophagia. Solenophagic arthropods push their mouth parts directly into blood vessels to obtain blood. The mouth parts are modified into piercing stylets which work in a way analogous to a hypodermic needle. The bites of the louse cause a localized, pruritic response which in turn elicits scratching. The scratching can lead to dermatitis. Secondary infestation could also be a problem. After years of exposure, the scalp becomes thickened and discolored. This condition is commonly known as vagabond's disease. Further examination of Chiribaya crania may show that many individuals suffered from dermatitis.

Individual 802-1371 may reflect the extreme development of pediculosis: plica polonica. In the case of plica polonica, the hair becomes matted with exudate and fungus grows in the mass. Individual 802-1371 exhibited hair that was matted in scab-like material and perhaps was badly effected by lice.

Unfortunately, the hair was so matted on this individual that it was impossible to examine the scalp for the proliferation of lice that accompany plica polonica without destroying the integrity of the specimen.

Men had a higher infestation prevalence than women. This is because men more commonly had elaborate hair styles that covered the scalp in braids (Fig. 4). Shielded by these hair styles, the lice might find more hospitable hosts on men. The men's braided hair was remarkably clean. It is likely that Chiribaya men had more lice for the same reasons as modern girls who are more commonly infested because long, clean hair promotes louse infestation.

Considering the annoyance lice must have caused to Chiribayans, they must have had some technological and hygienic tools to minimize louse proliferation. It is possible that the lice were controlled by mutual grooming accompanied by eating the lice, as is common among many tribal peoples. Artifactual evidence bears on the question. We noticed comb-like tools buried with some individuals (Fig. 5). These may have been used for weaving. However, the presence of these artifacts shows that the Chiribaya had the technology to make combs. A few individuals had a decreased density of scalp nits/eggs in comparison to hair measurements. This suggests that louse infestation could be controlled and decreased by hygienic measures. Individuals 901-2059, 14-175, 21-46, 850-1391, and 4-1700 show decreasing louse density from the hair to the scalp. This indicates that these individuals were reducing their louse infestations. When louse infestation became extreme, a technique of last resort must have been cutting off the hair. One male, 317-1173, had an amazing density of louse nits/eggs. He did not exhibit the highest maximum density of lice, but he did exhibit a relatively high minimum density. Every square centimeter of scalp had louse nits or eggs. The range of maximum density was 7-13 nits/eggs/cm² with a mean of 9/cm². The range of minimum densities was 1-6.5 nits/eggs/cm² with a mean of 4/cm². This individual must have been suffering severely from louse infection and his hair was shorn off between 1 and 2 inches from the scalp. This individual also suffered from an infestation of the mucocutaneous tissue of the nose and mouth, probably as a result of leishmaniasis. The facial disfigurement of this individual was profound and probably inspired avoidance by other members of the village. Such avoidance and fear is common in areas with endemic leprosy which produces similar soft tissue lesions. In the case of individual 317-1173, it appears that the lice proliferated in a weakened individual who may not have been able to gain hygienic aid from anyone else beyond a hair cut. Several individuals show pronounced densities of lice at the scalp with lower densities in the hair. This may indicate a similar proliferation of lice in sick and dying individuals (407-1304, 10-147, and 211-2225). Therefore, declining individual health status may have allowed lice to proliferate when individual care could not be easily rendered.

The fact that children were least often infested is interesting. In modern societies, children are most often infested (Mellanby 1942, Ibarra 1989, Mumcuoglu et al. 1990, Ibarra & Hall 1996, Ibarra et al. 2000). Children from large families are more likely to be infested than children from small families. Child cares, schools, and preschools in the modern world promote social interaction between children and louse infestation. The low prevalence of infestation among Chiribaya children suggest that children were not associated in the same social settings as modern children. The contrast between Chiribaya louse prevalence between the Chiribaya children and modern children highlights the importance of schools and other child-centered social activities in promoting infestation.

Of all the areas of archaeoparasitology, we believe that the study of lice has the greatest potential for providing real epidemiological data regarding past populations. When large numbers of mummies are examined, it is relatively effortless to collect sufficient observations for interpretation. In this study, only San Geronimo had such poor preservation that it could not be used. The poor preservation of mummies from the site of San Geronimo is due to it beach location and association with moisture. Of the remaining three sites, Chiribaya Alta and El Yaral provide the best insights into louse paleoepidemiology due to the relatively large numbers of mummies for which age and sex was determined. The analysis of these mummies shows how aspects of hairstyle and other behavior effected louse distribution among the Chiribaya.

REFERENCES

• Ibarra J 1989. Head lice in schools. Health at School 4: 147151.
• Ibarra J, Hall DMB 1996. Head lice in schoolchildren. Arch Dis Child 75: 471473.
• Ibarra J, Fry F, Wickenden C 2000. Treatment of head lice. Lancet 356: 2007.
• Mellanby K 1942. Natural population of the head louse (Pediculus humanus capitis: Anoplura) on infected children in England. Parasitology 34: 180184.
• Mumcuoglu KY, Miller J, Gofin R, Adler B, BenIshai F, Almog R, Kafka D, Klaus S 1990. Epidemiological studies on head lice infestation in Israel. Int J Dermatol 29: 502506.

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