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In its long and eventful history, the Roman Curia has repeatedly undergone organizational changes. At first, the Latin term curia, of Etruscan origin, means a subdivision of the tribe, then the deliberation room of the Senate and then the Senate itself.

Like every bishop, the pope was surrounded by a college of priests. The college met regularly to form councils to lead his diocese. Its function also extended a calling to the universal Church, and for matters relating to it, the Pope surrounded himself with other bishops around Rome to hear their advice. Gradually, these consistories took an almost permanent presence: the word "curia" is first used in the Church by a papal document in 1089, during the reign of Pope Urban II. Meetings were held three times a week under Pope Innocent III.Outside the presbyteries, which dealt with general topics, the pope set up specialized committees of Cardinals on particular topics. These commissions, first in temporary mandate, became more and more important and stable. Gradually, consistories lost their effectiveness and started to look like meetings apparatus. The real work was done within the congregations.

In 1542, the first congregation, the Holy Office was established by Pope Paul III to fight against Protestantism and other heresies. Then other congregations were created on this model: one after the Council for the Interpretation of the Decrees of the Council of Trent in 1561, and one for the Index in 1571.

After the Council of Trent, Pope Sixtus V reorganized it on 22 January 1588 with the bull Immensa Aeterni Dei. There was another general reorganization under Pope Pius X, which took into account the concentration on ecclesiastical matters alone that resulted from the loss of the Papal States in central Italy.

While the Pope was sovereign of that region, the Curia had both religious and civil functions. The latter were lost when the Kingdom of Piedmont-Sardinia, expanding to include the greater part of Italy, seized most of the Papal States in 1860 and the city of Rome itself and its surrounding area in 1870, thus ending the Papacy's temporal power. The Curia was from then on dedicated in practice entirely to the Pope's ecclesiastical responsibilities. When the Holy See concluded the Lateran Pacts with the Italian State in 1929, the Holy See recognized the annexation by Italy of the Papal States, and Vatican City State was created. The Curia has continued to devote itself exclusively to ecclesiastical affairs, and a distinct body, not considered part of the Curia, was established for the governance of the minuscule state.

The Second Vatican Council was followed by further changes. Some offices ceased to exist, because their former functions were abolished, as happened with the Dataria. The functions of some others were transferred to another office, as the remaining functions of the Apostolic Chancery and those of the Secretariate of Briefs were transferred to the Secretariat of State, and those of the Congregation of Ceremonies to the Prefecture of the Pontifical Household. Others were split into separate offices, as the Congregation of Rites became the Congregation for the Causes of Saints and the Congregation for Divine Worship, the latter of which later became, by fusion with another office, the Congregation for Divine Worship and the Discipline of the Sacraments. Others again were simply given a new name.

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